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Abstract

Diet and feeding behavior data are crucial to a deep understanding of the behavioral response and adaptation of primates to a high-altitude environment. From August 2019 to June 2021, we collected data on the feeding behavior of a high-altitude rhesus macaque Macaca mulatta group from Yajiang County, Western Sichuan Plateau, which has an altitude of over 3,500 m. The results showed that feeding (33.0 ± 1.8%) and moving (28.3 ± 2.6%) were the dominant behavior of rhesus macaques. Macaques ate 193 food items, comprising 11 food categories from 90 species. Our study found that plant roots (30.9 ± 30.1%) and young leaves (28.0 ± 33.1%) were the main foods eaten by macaques. The preferred foods of rhesus macaques were young leaves, fruits, and seeds, and the consumption of these items was positively correlated with its food availability. When the availability of preferred foods was low, macaques took plant roots, barks, and fallen leaves as fallback foods. In particular, roots were a dominant food item in winter, and this way of feeding became a key survival strategy. Our results suggest that, facing the relative scarcity and strong seasonal fluctuations of food resources in high-altitude habitat, macaques adopt active foraging strategies, relying on a variety of food species and adjusting flexibly their food choices based on food availability, which may help to maximize the energy efficiency of high-altitude macaques.

Diet has a strong influence on primate fitness (Altmann 1991), and the employment of flexible foraging strategy is an important way for primates to adapt to different environments (Cui et al. 2019; Green et al. 2020). Researchers have proposed a variety of foraging strategies to explain which foods animals choose and the consumption of each food (Felton et al. 2009). Energy maximization and minimization strategies are commonly used to explain primate foraging strategies (Schoener 1971; Dasilva 1992; Felton et al. 2009). An energy maximization strategy is generally considered as individuals attempting to maximize the amount of energy gain per unit of feeding time (Schoener 1971). When resource availability is low, energy maximizers spend more time foraging, depend on more patches, and spend less time resting than energy minimizers (Schoener 1971; Hixon and Carpenter 1988). Therefore, energy maximizers are expected to have similar feeding patterns between food-rich and food-lean seasons, whereas minimizers spend less time foraging and more time resting during lean periods (Schoener 1971; Lambert and Rothman 2015; Nagy-Reis and Setz 2017). It is generally believed that frugivorous primates tend to adopt an energy maximizing strategy, as fruits are considered as higher-quality food items because they are richer in sugar than leaves, easier to digest, and rapidly converted into energy (Richard 1985; Lambert and Rothman 2015). However, as fruits are generally available in clumps and are unevenly distributed, frugivores must spend more time moving and traveling between food patches while searching for fruits, and relatively less time resting than those who rely on leaves (Rosenberger and Strier 1989; Korstjens et al. 2010). Therefore, the energy benefit of eating fruits is often greater than the expenditure during moving longer distances to find fruits. By contrast, folivores are generally considered to adopt an energy minimization strategy (Dasilva 1992; Rangel-Negrín et al. 2018). As leaves are generally evenly distributed, folivores can spend less time moving and searching for food. In addition, leaves contain a higher amount of fiber, which has a lower energy density and requires a longer time to digest than fruits; correspondingly, folivores require a long mandatory resting time for digestion (Richard 1985; Lambert and Rothman 2015).

Although these general patterns exist between folivores and frugivores, the opportunity for primates to balance their diet is usually limited by seasonal fluctuations and the distribution of major food types (Hemingway and Bynum 2005; Dunbar et al. 2009; Green et al. 2020). The same species displays an energy maximization strategy in one habitat and an energy minimization strategy in another, or even showing different strategy across seasons (Owens et al. 2015; Rangel-Negrín et al. 2018). Specifically, primates adjust their time budget and diet composition in response to fluctuations in food abundance (Guan et al. 2018; Cui et al. 2019). The way individuals respond to a reduction in the availability of preferred foods varies dramatically: they may decrease their moving time and traveling distance to save energy or increase their traveling distance in search of more food (Felton et al. 2009; Lambert and Rothman 2015). For instance, the Assamese macaques Macaca assamensis spend more time moving and travel longer during fruit-rich seasons than the fruit-lean ones (Li et al. 2020).

When there is a shortage of preferred foods, the adjustment of food selection is usually to consume the fallback foods (Hemingway and Bynum 2005; Hohmann 2009; Lambert and Rothman 2015). Fallback foods can be defined as "foods whose use is negatively correlated with the availability of preferred foods" (Marshall and Wrangham 2007; Lambert and Rothman 2015) and are represented by various forms, according to the primate taxon and environment, usually including herbs, seeds, lianas, lichens, invertebrates, roots, barks, fungi, and others (Grueter et al. 2009; Hohmann 2009; Lambert and Rothman 2015). For instance, black-and-white snub-nosed monkeys Rhinopithecus bieti rely on fruticose lichens as a fallback food to buffer winter in the high-altitude forests of China (Grueter et al. 2009).

Most primates live in tropical and subtropical areas, and only a few primates inhabit temperate and high-altitude regions (Myers et al. 2000; Grueter et al. 2009). Temperate and high-altitude habitats are characterized by more intense periods of resource scarcity than others (Barry 2008; Tsuji et al. 2013). In particular, areas in high-altitude alpine forests tend to be less productive than neighboring areas at lower elevations, with decreased plant and animal densities, lower temperature and atmospheric pressure, and increased ultraviolet radiation (Lomolino 2001; Barry 2008). In addition, in high-altitude alpine forests the availability of high-quality food (e.g. fruits) is relatively low and the climate is relatively seasonal (Xiang et al. 2007); moreover, primates may be acutely impacted by winter conditions, which present the challenge of food shortages for several months (Grueter et al. 2009). In response, primates should evolve behavioral strategies to enable them to make the best use of food sources (Grueter et al. 2009; Tsuji et al. 2013), and the way they have done so is highly enlightening (Grow et al. 2014).

The rhesus macaques Macaca mulatta are generally considered frugivores; however, the proportion of fruits in their diet varies among populations (Tsuji et al. 2013). This dietary flexibility allows them to survive in habitats spanning temperate and tropical latitudes and a series of altitude gradients (0 up to 4,000 m) (Fooden 2000). However, the mechanism of diet selection in plateau macaques adapted to high-altitude habitats remains unclear. The wild rhesus macaques in the Western Sichuan Plateau are a potentially ideal research subject for diet adaptation in primates. The Western Sichuan Plateau is part of the southeast edge of the Qinghai-Tibet Plateau and Hengduan Mountains, with an average altitude exceeding 3,000 m. Rhesus macaques are widely distributed throughout the temperate-alpine forest areas of the Western Sichuan Plateau, indicating that macaques have adapted to the high-altitude environment (Yao et al. 2014; Zhao et al. 2018). Like other temperate-alpine forest primates, their manner of dealing with the shortage of food resources and seasonal changes should be flexible. For example, black-and-white snub-nosed monkeys feed on lichen as an important food (Grueter et al. 2009; Tsuji et al. 2013; Cui et al. 2019). The study on the dietary flexibility of macaques at high-altitude will help us to understand more deeply the potential mechanism of adaptation of this species adaptation to the plateau environment. However, at present there are few studies on plateau macaque populations, with only preliminary reports on habitat selection (Li et al. 2012), feeding ecology (Goldstein and Richard 1989), and intestinal microbial diversity (Zhao et al. 2018). The diet characteristics and foraging strategies of plateau macaques to adapt to high-altitude environments remain unclear (Goldstein and Richard 1989; Garber et al. 2018).

To better understand feeding ecology and adaptation to extreme environments in rhesus macaques, we present a general description of wild rhesus macaques activity patterns and diet composition based on study conducted over 20 months in Yajiang County, which has an altitude over 3,500 m in the Western Sichuan Plateau, China. Firstly, we describe the activity pattern and diets as well as their seasonal changes in rhesus macaques. Secondly, we analyze the relationship between food composition and food availability and determine the preferred and fallback foods of macaques. Finally, we discuss the flexibility of foraging strategy of high-altitude macaques by testing the following predictions:

  • 1) Macaques prefer fruits and young leaves and are affected by seasonal fluctuations in food resources (Tsuji et al. 2013; Tang et al. 2016). We predict that the consumption of fruits and young leaves increases with their availability.

  • 2) When preferred foods are scarce, primates usually consume fallback foods (Marshall and Wrangham 2007). Primates in temperate-alpine forests rely mainly on mature leaves and lichens as fallback foods (Grueter et al. 2009; Tsuji et al. 2013). We predict that the consumption of fallback foods, especially mature leaves and/or lichens, will be inversely proportional to the availability of preferred foods.

Materials and Methods

Study site and animals

This study was conducted in Yajiang County, Ganzi Tibetan Autonomous Prefecture, Sichuan Province, China (Figure 1). Yajiang County is located in the hilly and mountainous area of western Sichuan, with an average altitude of over 3,000 m, ranging between 2,266 and 5,252 m. Yajiang County belongs to the sub-humid climate area of the Qinghai-Tibet Plateau, and has distinct seasonality. Our study site was at the junction of Honglong Township, Kela Township, and Decha Township in Yajiang County (29°51ʹ–29°57ʹN, 100°38ʹ–100°44ʹE) (Figure 1). We selected a group of wild rhesus macaques (Western China Rhesus monkey, M. m. lasiotis) from this region as our target group. The target group was composed of 34–36 individuals (4 adult males, 12 adult females, 6–8 subadults, 8 juveniles, 4 infant). Based on previous observations since July 2019, the subject group used an elevational zone between 3,500 and 4,300 m A.S.L.

Figure 1.

The study area information. (A) The location of study site in Yajiang County, Sichuan, China (red triangle). (B) The habitat of the target macaque group, mainly covered by alpine vegetation. The map quoted from the Ministry of Natural Resources of the People's Republic of China, No. GS (2019) 1673.

The study area information. (A) The location of study site in Yajiang County, Sichuan, China (red triangle). (B) The habitat of the target macaque group, mainly covered by alpine vegetation. The map quoted from the Ministry of Natural Resources of the People's Republic of China, No. GS (2019) 1673.

There is a township road in the study site. The main activities of local residents are grazing, picking Cordyceps, macro-fungi, and digging for medicinal materials, without crop cultivation. The study area is covered by alpine vegetation, mainly temperate-alpine forests, such as coniferous broad-leaf mixed forest, evergreen sclerophyllous forest, evergreen coniferous shrubs, deciduous broad-leaf shrubs, and meadows (Zhang et al. 2016). We investigated and collected climate and vegetation structure data on the study site, and we describe them in detail below.

Climate

We collected rainfall/snowfall data using a rain gauge (20 cm diameter) and used an electronic automatic temperature logger (SSN-22, YOWEXA Sensing systems LTD) to collect temperature and humidity data from August 2019 to June 2021. Data showed that the mean monthly temperature was 6.9 °C (range from −1.8 °C in December to 13.4 °C in June). The annual average humidity was 54.4% (28.9–84.4%). The annual rainfall/ Snowfall was 1,677.5 mm, and the average monthly rainfall was 139.8 mm (range from 32 mm in January to 290 mm in June) (Figure 2). Based on temperature and rainfall, we divide the whole year into 4 seasons: spring (April–June), summer (July–September), autumn (October–November), and winter (December–March).

Figure 2.

Monthly temperature, relative humidity and rainfall during the study period. MHT: mean highest temperature; MLT: mean lowest temperature; MT: mean temperature; RH: mean relative humidity.

Monthly temperature, relative humidity and rainfall during the study period. MHT: mean highest temperature; MLT: mean lowest temperature; MT: mean temperature; RH: mean relative humidity.

Vegetation composition and food availability

We set up 25 forest quadrats (20 m × 20 m) at the main research site to investigate the vegetation composition. Combined with the growth characteristics of woody plants in high-altitude habitats, if the plant height is ≥2m, measuring its diameter at breast height; and if the plant height is <2m, measuring its diameter at the ground. We did not record woody plants with a diameter at the ground <2 cm. We also set up three 2 m × 2 m herb quadrats along the diagonal in the forest quadrat to investigate the species and average height of herbs. In addition, we set up 45 2 m × 2 m quadrats on the grassland for herb investigation. We calculated the density (numbers of individuals/ ha) of different plant species and used relative density (%), relative frequency (%), relative base area (%), and relative height (%) to calculate the dominance of different vegetation layers (tree layer, shrub layer, and herb layer). According to the plant sample survey, the dominant species in our study area were Picea asperata, Quercus pannosa, Rhododendron capitatum, Spiraea schneideriana, Lonicera microphylla, Berberis diaphana, Ptilagrostis mongholica, Potentilla fruticosa, Ligularia tongolensis, Astragalus sinicus, Saussurea tatsienensis, and Carex spp.

We set up twelve 150–200 m transects (5 m wide) for vegetation phenology monitoring, and those transects covered all habitat types in the macaques home range. In the middle of each month, we recorded the available food items (young leaves, mature leaves, flowers, fruits, and seeds) of the woody and herbaceous species that we could observe and identify in the transect and recorded the number of macro-fungi visible on the transect. We scored an abundance of various food parts on a scale from 0 to 5, based on coverage, i.e., 0 = absence, 1 = 1–10%, 2 = 11–25%, 3 = 26–50%, 4 = 51–75%, and 5 = 76–100%. The monthly food availability index (FAI) for the young leaves, mature leaves, flowers, fruits, and seeds were calculated by integrating the density, average basal area, average height, and phenology score of the sampled trees. Where possible, we monitored at least 15 trees for each species on the sample line. The calculation formula is as follows: F A I = ∑ i = 1 n B H i D i P i ⁠, where BHi denotes the average basal area of tree species i (m2/ha) or the average height (m/ha) of herb species i, Di denotes the density of species i, and Pi represents the assignment values of different food parts of species i (Albert et al. 2013, Huang et al. 2015; Campera et al. 2021). In addition, the total number of macro-fungi recorded by 12 splines represent the availability index of macro-fungi in that month.

Behavioral data collection

The sampling period for observation was from July 2019 to June 2021, of which the first month was a preliminary survey. In addition, from February to April 2020, we failed to track and observe macaque behavior; thus, a total of 20 months of data were collected. We used instantaneous scan sampling (Altmann 1974) to collect macaques' feeding behavior data. Each scan period was 15 min and lasted for 5 min, with a 10-min interval until the next scan began (Huang et al. 2015; Zhang et al. 2021). We recorded the main behaviors of the macaques, classified into 6 categories: resting, feeding, moving, grooming, playing, and other (Li et al. 2020; Zhang et al. 2020). We observed each individual for 5 s and then regarded the individual's behavior lasting more than 3 s within 5 s as the main behavior (Zhang et al. 2020). When the scanned individual fed, we recorded the food species and parts (young leaves, mature leaves, flowers, fruits, invertebrates, seeds, roots, macro-fungi, barks, fallen leaves, and others) (Tsuji et al. 2013; Huang et al. 2015; Cui et al. 2019).

During the 20-month study period, the macaque group were directly observed for 1,506 h over 178 d (8.9 ± 2.3 d per month, range 6–14 d), resulting in 6,024 scans (301.2 ± 112.2 scans per month, range 163–603) and 91,193 individual behavior records (4,559.6 ± 2,949.0 per month, range 1,872–13,709), which included 37,168 feeding records (1,858.8 ± 1,190.6 per month, range 740–5,673) ( Supplementary Table S1).

Data analysis

The activity budget was expressed as the percentage of time spent on a particular activity (Fan et al. 2012; Li et al. 2020). First, we took each scan as the calculation unit, and the time proportion of the behavior in the current scan is expressed by the proportion of the number of individuals with certain behavior to the total number of individuals recorded in the scan. Second, we took the average of the data scanned 4 times per hour, and then generated an hourly time budget. Third, we averaged the hourly data (7:00–19:00) to calculate the average monthly activity budget, effectively avoiding the deviation caused by uneven data collection over time (Fan et al. 2012; Zhang et al. 2020). We used a similar approach to generate statistics on dietary data, calculating the diet composition as percentages of specific food species or types consumed within the feeding time (Huang et al. 2015).

We used the Shannon–Wiener Index to calculate the monthly food diversity index (FDI), and the calculation formula as follows: H ″ = − ∑ i = 1 n P i × l n P i ⁠, where P i is the percentage of food species i in the monthly diet based on time spent feeding (Huang et al. 2015).

Following Ganas et al. (2008) and Arseneau-Robar et al. (2021), we divided the preferred foods of macaques by calculating the preference scores (EI). We used Ivlev's electivity index to calculate EI (Ma et al. 2017; Miller et al. 2020), according to the following formula: EI = (R d i – N a i)/ (R d i + N a i), where R d i is the monthly rank of the food item i in the diet composition, and N a i is the monthly rank of availability of item i. The preferred food is divided according to the EI score, where −1 to 0 indicate that a food was not preferred, a score of 0 signified neutrality, and a score 0 to 1 indicate that it was preferred. We selected the food species each accounting for >0.5% of all feeding records to calculate the preference score, which, combined, accounted for 94.1% of all feeding records (Table 1). When the selection index of a certain food part is >0 and its seasonal consumption is positively correlated with availability, we regard it as the preferred food for macaques. We classified fallback foods as those food species or categories whose consumption increases when the availability of preferred foods or preferred food categories decreases (Grueter et al. 2009; Lambert and Rothman 2015; Miller et al. 2020).

Table 1.

Important species in the diet of high-altitude rhesus macaques

Species Food type Parts eaten Annual feeding months % of feeding time Preference selection times Average preference score (EI) Preferred parts eaten
Epilobium tibetanum H 1,2,5,6 12 9.56 5 0.27 5
Carex brunnea H 1,2,6,9 12 8.07
Carex obscuravar H 1,2,6,9 12 7.79
Kobresia pygmaea H 1,2,6,9 12 7.49
Berberis diaphana B 1,2,3,4,9 12 6.89 10 0.44 1,3
Poa annua H 1,2,6,9 12 6.68 3 0.20 1
Lonicera tangutica B 1,2,3,8,9 12 5.32 9 0.31 1,3
Salix cupularis B 1,2,4 5 4.01 3 0.24 1
Invertebrate I 11,12 8 3.67
Lonicera japonica B 1,2,3,8,9 12 2.89 8 0.30 1,3
Astragalus mongholicus H 1,6 11 2.81
Marco-Fungi M 10 10 2.68 6 0.20 10
Ligularia tongolensis H 1,2,7 7 2.28
Berberis dictyophylla B 1,2,3,8,9 12 2.26 9 0.39 1,3
Saussurea japonica H 6 7 1.78
Astragalus sinicus H 1,6 9 1.75
Rubus stans var Stans B 1,2,3,4,7 12 1.74 8 0.15 1,3
Allium macranthum H 5 6 1.54 3 0.08 5
Moss spp O 13 3 1.36
Vicia sepium H 1,2,5,6 10 1.30 8 0.39 5
Quercus pannosa T 1,3,5 5 1.20
Astragalus lucidus H 1,2,6 9 1.12
Avena fatua H 1,2,6 8 1.02
Ribes nigrum H 1,8 8 0.98
Polygonum viviparum H 1,4,6 7 0.86 1 0.16 1
Gramineae spp2 H 1,6 9 0.83
Potentilla chinensis H 1,2,5,6 11 0.79
Unidentified spp4 H 1 3 0.78 3 0.35 1
Heracleum hemsleyanum H 1,7 7 0.76 2 0.12 1
Galium spurium H 1,2 7 0.76 1 0.04 1
Nepeta cataria H 5,6 9 0.75 5 0.13 5
Gramineae spp3 H 1,6 11 0.71
Sinopodophyllum hexandrum H 3,5 4 0.63 2 0.15 3
Aconitum carmichaeliDebx H 1,7 3 0.57 3 0.19 1
Roegneria kamoji H 1,6 7 0.55
Species Food type Parts eaten Annual feeding months % of feeding time Preference selection times Average preference score (EI) Preferred parts eaten
Epilobium tibetanum H 1,2,5,6 12 9.56 5 0.27 5
Carex brunnea H 1,2,6,9 12 8.07
Carex obscuravar H 1,2,6,9 12 7.79
Kobresia pygmaea H 1,2,6,9 12 7.49
Berberis diaphana B 1,2,3,4,9 12 6.89 10 0.44 1,3
Poa annua H 1,2,6,9 12 6.68 3 0.20 1
Lonicera tangutica B 1,2,3,8,9 12 5.32 9 0.31 1,3
Salix cupularis B 1,2,4 5 4.01 3 0.24 1
Invertebrate I 11,12 8 3.67
Lonicera japonica B 1,2,3,8,9 12 2.89 8 0.30 1,3
Astragalus mongholicus H 1,6 11 2.81
Marco-Fungi M 10 10 2.68 6 0.20 10
Ligularia tongolensis H 1,2,7 7 2.28
Berberis dictyophylla B 1,2,3,8,9 12 2.26 9 0.39 1,3
Saussurea japonica H 6 7 1.78
Astragalus sinicus H 1,6 9 1.75
Rubus stans var Stans B 1,2,3,4,7 12 1.74 8 0.15 1,3
Allium macranthum H 5 6 1.54 3 0.08 5
Moss spp O 13 3 1.36
Vicia sepium H 1,2,5,6 10 1.30 8 0.39 5
Quercus pannosa T 1,3,5 5 1.20
Astragalus lucidus H 1,2,6 9 1.12
Avena fatua H 1,2,6 8 1.02
Ribes nigrum H 1,8 8 0.98
Polygonum viviparum H 1,4,6 7 0.86 1 0.16 1
Gramineae spp2 H 1,6 9 0.83
Potentilla chinensis H 1,2,5,6 11 0.79
Unidentified spp4 H 1 3 0.78 3 0.35 1
Heracleum hemsleyanum H 1,7 7 0.76 2 0.12 1
Galium spurium H 1,2 7 0.76 1 0.04 1
Nepeta cataria H 5,6 9 0.75 5 0.13 5
Gramineae spp3 H 1,6 11 0.71
Sinopodophyllum hexandrum H 3,5 4 0.63 2 0.15 3
Aconitum carmichaeliDebx H 1,7 3 0.57 3 0.19 1
Roegneria kamoji H 1,6 7 0.55

Important species: foods with proportions of ≥1% as staple foods, and foods with proportions of 0.5% < X < 1% as secondary foods.

Food type: T: trees; B: bushes; H: herbs. I: invertebrates; M: macro-fungi; O: others.

Food parts: 1: young leaves; 2: mature leaves; 3: fruits; 4: flowers; 5: seeds; 6: roots; 7: stems; 8: barks; 9: fallen leaves; 10: macro-fungi; 11: larvae/adults; 12: eggs; 13: others.

Preference selection times: The number of preference score (EI) > 0 over the study period.

Table 1.

Important species in the diet of high-altitude rhesus macaques

Species Food type Parts eaten Annual feeding months % of feeding time Preference selection times Average preference score (EI) Preferred parts eaten
Epilobium tibetanum H 1,2,5,6 12 9.56 5 0.27 5
Carex brunnea H 1,2,6,9 12 8.07
Carex obscuravar H 1,2,6,9 12 7.79
Kobresia pygmaea H 1,2,6,9 12 7.49
Berberis diaphana B 1,2,3,4,9 12 6.89 10 0.44 1,3
Poa annua H 1,2,6,9 12 6.68 3 0.20 1
Lonicera tangutica B 1,2,3,8,9 12 5.32 9 0.31 1,3
Salix cupularis B 1,2,4 5 4.01 3 0.24 1
Invertebrate I 11,12 8 3.67
Lonicera japonica B 1,2,3,8,9 12 2.89 8 0.30 1,3
Astragalus mongholicus H 1,6 11 2.81
Marco-Fungi M 10 10 2.68 6 0.20 10
Ligularia tongolensis H 1,2,7 7 2.28
Berberis dictyophylla B 1,2,3,8,9 12 2.26 9 0.39 1,3
Saussurea japonica H 6 7 1.78
Astragalus sinicus H 1,6 9 1.75
Rubus stans var Stans B 1,2,3,4,7 12 1.74 8 0.15 1,3
Allium macranthum H 5 6 1.54 3 0.08 5
Moss spp O 13 3 1.36
Vicia sepium H 1,2,5,6 10 1.30 8 0.39 5
Quercus pannosa T 1,3,5 5 1.20
Astragalus lucidus H 1,2,6 9 1.12
Avena fatua H 1,2,6 8 1.02
Ribes nigrum H 1,8 8 0.98
Polygonum viviparum H 1,4,6 7 0.86 1 0.16 1
Gramineae spp2 H 1,6 9 0.83
Potentilla chinensis H 1,2,5,6 11 0.79
Unidentified spp4 H 1 3 0.78 3 0.35 1
Heracleum hemsleyanum H 1,7 7 0.76 2 0.12 1
Galium spurium H 1,2 7 0.76 1 0.04 1
Nepeta cataria H 5,6 9 0.75 5 0.13 5
Gramineae spp3 H 1,6 11 0.71
Sinopodophyllum hexandrum H 3,5 4 0.63 2 0.15 3
Aconitum carmichaeliDebx H 1,7 3 0.57 3 0.19 1
Roegneria kamoji H 1,6 7 0.55
Species Food type Parts eaten Annual feeding months % of feeding time Preference selection times Average preference score (EI) Preferred parts eaten
Epilobium tibetanum H 1,2,5,6 12 9.56 5 0.27 5
Carex brunnea H 1,2,6,9 12 8.07
Carex obscuravar H 1,2,6,9 12 7.79
Kobresia pygmaea H 1,2,6,9 12 7.49
Berberis diaphana B 1,2,3,4,9 12 6.89 10 0.44 1,3
Poa annua H 1,2,6,9 12 6.68 3 0.20 1
Lonicera tangutica B 1,2,3,8,9 12 5.32 9 0.31 1,3
Salix cupularis B 1,2,4 5 4.01 3 0.24 1
Invertebrate I 11,12 8 3.67
Lonicera japonica B 1,2,3,8,9 12 2.89 8 0.30 1,3
Astragalus mongholicus H 1,6 11 2.81
Marco-Fungi M 10 10 2.68 6 0.20 10
Ligularia tongolensis H 1,2,7 7 2.28
Berberis dictyophylla B 1,2,3,8,9 12 2.26 9 0.39 1,3
Saussurea japonica H 6 7 1.78
Astragalus sinicus H 1,6 9 1.75
Rubus stans var Stans B 1,2,3,4,7 12 1.74 8 0.15 1,3
Allium macranthum H 5 6 1.54 3 0.08 5
Moss spp O 13 3 1.36
Vicia sepium H 1,2,5,6 10 1.30 8 0.39 5
Quercus pannosa T 1,3,5 5 1.20
Astragalus lucidus H 1,2,6 9 1.12
Avena fatua H 1,2,6 8 1.02
Ribes nigrum H 1,8 8 0.98
Polygonum viviparum H 1,4,6 7 0.86 1 0.16 1
Gramineae spp2 H 1,6 9 0.83
Potentilla chinensis H 1,2,5,6 11 0.79
Unidentified spp4 H 1 3 0.78 3 0.35 1
Heracleum hemsleyanum H 1,7 7 0.76 2 0.12 1
Galium spurium H 1,2 7 0.76 1 0.04 1
Nepeta cataria H 5,6 9 0.75 5 0.13 5
Gramineae spp3 H 1,6 11 0.71
Sinopodophyllum hexandrum H 3,5 4 0.63 2 0.15 3
Aconitum carmichaeliDebx H 1,7 3 0.57 3 0.19 1
Roegneria kamoji H 1,6 7 0.55

Important species: foods with proportions of ≥1% as staple foods, and foods with proportions of 0.5% < X < 1% as secondary foods.

Food type: T: trees; B: bushes; H: herbs. I: invertebrates; M: macro-fungi; O: others.

Food parts: 1: young leaves; 2: mature leaves; 3: fruits; 4: flowers; 5: seeds; 6: roots; 7: stems; 8: barks; 9: fallen leaves; 10: macro-fungi; 11: larvae/adults; 12: eggs; 13: others.

Preference selection times: The number of preference score (EI) > 0 over the study period.

We used the one-sample Kolmogorov–Smirnov test to examine the normality of variables. We used a Kruskal–Wallis test to examine seasonal variations of time budget and diet composition. We used Spearman rank correlation to test the relationship between diet composition and food availability and to examine feeding time on potential fallback foods changed in accordance with availability of preferred foods FAI. We conducted all data analyses using SPSS 26 and R 4.1.1 software. All tests were 2-tailed, with significance levels of 0.05.

Results

Phenological patterns and resource availability

The results showed that during our study period, food availability index varied across the year (Figure 3). There were significant seasonal differences in the FAI of different food parts, young leaves FAI (χ 2 = 17.134, df = 3, P = 0.001), mature leaves FAI (χ 2 = 14.699, df = 3, P = 0.002), flowers FAI (χ 2 = 18.351, df = 3, P < 0.001), fruits FAI (χ 2 = 16.083, df = 3, P = 0.001), seeds FAI (χ 2 = 15.373, df = 3, P = 0.002), macro-fungi FAI (χ 2 = 9.160, df = 3, P = 0.027).

Figure 3.

Monthly food availability index during the study period. YL-FAI: food availability index for the young leaves; ML-FAI: food availability index for the mature leaves; FL-FAI: food availability index for the flowers; FR-FAI: food availability index for the fruits; S-FAI: food availability index for the seeds; M-FAI: food availability index for the macro-fungi.

Monthly food availability index during the study period. YL-FAI: food availability index for the young leaves; ML-FAI: food availability index for the mature leaves; FL-FAI: food availability index for the flowers; FR-FAI: food availability index for the fruits; S-FAI: food availability index for the seeds; M-FAI: food availability index for the macro-fungi.

Feeding activity patterns

Results shows that the macaques spent the largest part of their daily activity time feeding (33.0 ± 1.8%), followed by moving (28.3 ± 2.6%), resting (24.9 ± 3.7%), grooming (9.0 ± 1.4%), playing (3.4 ± 0.9%), and other activities (1.4 ± 0.9%). Observational data showed that active behavior (feeding + moving) was the dominant behavior of macaques (53.4–68.2%). There was no significant seasonal difference in the dominant behavior of rhesus macaques (feeding: χ 2 = 3.990, df = 3, P = 0.262; moving: χ 2 = 5.663, df = 3, P = 0.129).

Diet

Food species

During the study period, we identified at least 90 food species and 193 food items. The number of consumed food species and dietary diversity differed by month. The monthly diversity index was 3.99 ± 0.19, ranging from 3.68 to 4.36. The food species of rhesus macaques come from different food types; specifically, herbs were the most common type consumed (n = 53, 58.9% of food species), followed by bushes (n = 15, 16.6%), macro-fungi (n = 9, 10%), trees (n = 5, 5.6%), invertebrates (n = 5, 5.6%), others (n = 2, 2.2%), and vines (n = 1, 1.1%). It should be noted that due to the problem of field identification, the feeding proportion of 9 species of macro-fungi (7 identified and 2 unidentified) and 5 species of invertebrates (5 unidentified) cannot be accurately determined. Therefore, in the food composition, we have made statistical analysis according to 2 categories: macro-fungi and invertebrates.

Diet composition

We found that plant roots were the main food type of macaques, accounting for 30.9 ± 30.1% of the total feeding time, followed by young leaves (28.0 ± 33.1%), fallen leaves (7.8 ± 9.3%), mature leaves (7.5 ± 13.3%), seeds (7.1 ± 12.2%), invertebrates (3.9 ± 4.4%), others (3.7 ± 1.9%), macro-fungi (3.6 ± 5.5%), fruits (2.5 ± 4.3%), barks (2.4 ± 4.5%), and flowers (2.4 ± 3.0%) ( Supplementary Table S2).

Seasonal variations in diet

The diets for rhesus macaques in Yajiang County changed seasonally ( Supplementary Table S2, Figure 4). There were significant differences in the feeding proportion of each food items in different seasons, young leaves (χ 2 = 15.246, df = 3, P = 0.002), mature leaves (χ 2 = 12.498, df = 3, P = 0.006), flowers (χ 2 = 16.704, df = 3, P = 0.001), fruits (χ 2 = 15.197, df = 3, P = 0.002), invertebrates (χ 2 = 11.521, df = 3, P = 0.009), seeds (χ 2 = 11.051, df = 3, P = 0.011), roots (χ 2 = 15.364, df = 3, P = 0.002), fungi (χ 2 = 9.942, df = 3, P = 0.023), barks (χ 2 = 11.801, df = 3, P = 0.008), fallen leaves (χ 2 = 10.837, df = 3, P = 0.013), and others (χ 2 = 8.968, df = 3, P = 0.030). Rhesus macaques mainly consumed young leaves in spring; young leaves and mature leaves in summer; roots, seeds, and mature leaves in autumn; roots and fallen leaves in winter. The feeding peak of macaques for fruits, invertebrates, and macro-fungi was in summer; the peak for flowers was in spring, the peak for barks was mainly in winter. In addition, we found that there was a significant difference in the monthly number of food species consumed between seasons (χ 2 = 8.489, df = 3, P = 0.037), but the seasonal difference in the food diversity index was not significant (χ 2 = 3.649, df = 3, P = 0.302).

Figure 4.

Annual diet composition of high-altitude rhesus macaques.

Annual diet composition of high-altitude rhesus macaques.

Food choice and preferred and fallback foods

Among the 90 food species, in total 35 species each accounted for ≥0.5% of the annual diet, accounting for 94.1% of the annual diet altogether. Among them, 23 species each accounted for ≥1% of the annual feeding records, accounting for 85.2% of the total feeding records. We regarded foods with proportions of ≥1% as staple foods for the year, and foods with proportions of 0.5% < X < 1% as secondary foods.

The preference selection analysis of 35 food species (each with a feeding proportion >0.5%) showed that 23 parts of 18 food species had a preference score of >0, including young leaves, fruits, macro-fungi, and seeds (Table 1). In addition, the consumption of young leaves, fruits, and seeds increased with their availability ( Supplementary Table S3). These results showed that young leaves, fruits, and seeds were the preferred food for macaques.

The consumption of mature leaves was positively correlated with the availability of mature leaves, fruits, and seeds ( Supplementary Table S3), indicating that mature leaves were unlikely to become fallback foods. The consumption of roots, barks, and fallen leaves was negatively correlated with the FAI of young leaves and fruits ( Supplementary Table S3). Therefore, our results suggested that roots, bark, and fallen leaves are fallback food for macaques.

Discussion

Our study reported the feeding ecology data for the rhesus macaque population at high-altitude (above 3,500 m), enriching basic research on this species and high-altitude primates. We found that macaques mainly fed on roots during the autumn-winter and young leaves during the spring-summer of plants. Their preferred foods were young leaves, fruits, and seeds, which strongly supports prediction 1. Plant roots, barks, and fallen leaves were their fallback food, and prediction 2 was not supported.

The results show that the main behaviors of rhesus macaques living in high-altitude habitat were feeding and moving, indicating that they were extremely active, which may be to maximize energy benefits. This is consistent with other primate studies in high-altitude or temperate-alpine forests, including, black-and-white snub-nosed monkeys, whose spent more time on foraging (feeding 49.1% + moving 20.4%) than on resting (17.7%) (Xiang et al. 2010) and Japanese macaques, who spent 38.0% of the daytime feeding, 16.0% traveling, and 32.0% resting (Hanya 2004). By comparison, the wild rhesus macaque population at low altitude in Nonggang, Guangxi, China spent more time resting (42.1%) and tended to adopt passive foraging strategies to cope with the shortage of food resources (Tang et al. 2017). These may be related to the shortage of resources and their uneven distribution in the plateau area, especially that of high-quality food such as fruit (Hanya 2004; Xiang et al. 2010; Albert et al. 2018). Macaques need to spend a long time moving to find food and a long time eating to meet their energy requirements. However, we found that the seasonal variation in the feeding and moving time of high-altitude macaques were not significant; they maintained a stable rhythm of feeding, which seemed to be to save energy. This was related to the lack of resources and their low-quality diets. We found that the food composition of high-altitude macaques contains a large number of roots, mature leaves, fallen leaves, and bark. Similarly, other studies found that high-altitude and temperate forest primates rely on low-quality food, such as mature leaves, buds, barks, and lichens (Grueter et al. 2009; Xiang et al. 2010; Tsuji et al. 2013). Subsequent studies need detailed nutritional energy intake data to verify the energy strategy of rhesus macaques.

Our results show that the number of foods utilized by rhesus macaques at high-altitude is notably high, indicating that feeding on a variety of food species and parts is an effective strategy for rhesus macaques to adapt to food shortages in high-altitude habitats. Macaques ate 193 food items, comprising 11 food categories from 90 food species, with high food diversity. This is similar to observations in other primates in high-altitude and temperate regions (Grueter et al. 2009; Tsuji et al. 2013). For example, black-and-white snub-nosed monkeys consume >165 food items comprising 94 species in Samage (3,500–4,250 m ASL, Grueter et al. 2009), Pan troglodytes consume >167 food items comprising 102 species in Kibale National Park (2,700–3,400 m ASL, Watts et al. 2012), and Japanese macaques use 147 food items comprising 93 species in Yakushima (Hill 1997). Due to the shortage of food resources in high-altitude habitats, macaques must rely on a variety of food types to meet their needs. Researchers have found that primates respond to food shortages by increasing the number of types of food they eat (Hemingway and Bynum 2005). For example, rhesus macaques in the limestone forest of northern Guangxi increased the number of food types they consumed in winter (Zhou et al. 2009), and primates can benefit from high food diversity (Fan et al. 2015; Zhang et al. 2021).

During the study, we observed that the main food of rhesus macaques was roots and young leaves, followed by fallen leaves, mature leaves, seeds, invertebrates, other parts, macro-fungi, fruits, flowers, and barks ( Supplementary Table S2). In terms of food types, this is consistent with the reported feeding strategy of macaques in temperate-alpine forests, who tend to eat more leaves and other items, such as bark and fungi (Tsuji et al. 2013). However, fruits only contributed 2.5% of the total diets of high-altitude macaques, far lower than the average value for Asian macaques (48.0%) and even lower than the average value for Asian colobus monkeys (29.0%) (Tsuji et al. 2013). This is similar with an early study of a high-altitude macaque population in Pakistan (over 2,000 m ASL), who were found to consume fruits in a proportion of 8.5% of their total diet, whereas leaves, stems, and other vegetative plant parts made up 84.4% of their diet (Goldstein and Richard 1989). These differences may be due to the difference in fruit availability. Fruits are unevenly distributed and scarce in high-altitude habitats, whereas leaves are a uniformly distributed resource (Richard 1985; Xiang et al. 2010; Tsuji et al. 2013). Thus, macaques fed less on fruit and rely more on leaves. Similar studies have found that macaques in karst limestone forests with shortages of fruit are generally more folivorous and less frugivorous when compared with other species living in tropical forests, and reliance on leaves is an important strategy for them to adapt to the limestone habitat (Huang et al. 2015; Tang et al. 2016). Dependence on leaves may have been an important strategy used by macaques to survive temperate forests (Hanya et al. 2011). In addition, our study found that high-altitude macaques eat a large number of young leaves, were the main food in spring (71.0%) and summer (38.3%). This is different from most other high-altitude and temperature primates. Young leaves are available only during a particular period of time in temperate forests (Hanya et al. 2013). Therefore, usually, young leaves do not become the most important food for temperate-living primates (Grueter et al. 2009; Tsuji et al. 2013). The phenological pattern in our study area is consistent with the trend in temperate forests, that is, with larger seasonal fluctuations in fruits and leaves and the duration of the rich season is shorter (Figure 3). However, food is scarce at high altitudes. Young leaves have a high protein and low cellulose content (Richard 1985), and their rich period appears earlier than that of other high-quality foods. Macaques eat a lot of young leaves in spring, which can make up for the energy deficit in the long winter. Similar studies have found that Sichuan snub-nosed monkeys (Rhinopithecus roxellanae) in Shennongjia were also quite dependent on young leaves, which account for 28.7% of the feeding records (Li 2006). Therefore, we believe that consuming large amounts of leaves, especially young leaves, is an important foraging strategy for macaques to adapt to the high-altitude habitat.

Consistent with prediction 1, fruits and young leaves are the preferred food for rhesus macaques in high-altitude forests, even though fruits represent only a small proportion of their diet (2.5%). This preference is evidenced by the correlation between the consumption and availability of fruits and young leaves ( Supplementary Table S3); moreover, the preference score (EI) of rhesus macaques for fruits and young leaves of various species is >0 (Table 1). This is consistent with other studies showing that fruit and young leaves are high-quality foods and are the first choice for many primates (Richard, 1985; Hemingway and Bynum 2005; Tsuji et al. 2013). Young leaves are also the preferred food for R. bieti in the Samage forest, western Yunnan (Grueter et al. 2009). The results showed that in addition to fruits and young leaves, rhesus macaques showed a preference for seeds, and their consumption was also significantly positively correlated with availability. Although we do not have accurate invertebrate availability data to confirm that invertebrates are the preferred food. We observed that macaques actively search and feed on invertebrates, so invertebrates can be classified as the preferred food for discussion. Seeds and invertebrates have high nutritional value (high in protein, fat, and metabolizable energy) (Rothman et al. 2014; Lambert and Rothman et al. 2015; Cui et al. 2019), are high-quality foods, and have become the preferred food for some primates. For example, seeds are the preferred food for Taihangshan macaques in autumn, accounting for 89.2% of their diet, and play an important role in balancing seasonal feeding intake (Cui et al. 2019). Follow up work requires detailed food nutritional characteristics and intake data for further verification to help us understand why macaques can adapt to high-altitude environment.

We provide evidence that plant roots, barks, and fallen leaves constitute as fallback food for rhesus macaques in high-altitude habitats as they are not preferred, and consumption is negatively correlated with the availability of preferred food, in line with the definition of fallback food (Marshall and Wrangham 2007). Contrary to prediction 2, neither mature leaves nor lichens are a fallback food for macaques, which is positively correlated with the availability of preferred foods (fruits and seeds) ( Supplementary Table S3). This is because the availability of mature leaves also fluctuates seasonally in high-altitude habitats (Figure 3), and they are, therefore, not a stable food source. By contrast, roots, barks, and fallen leaves (dry mature leaves) are continuously available in winter and become fallback food for macaques. Similar to other studies, temperate primates may feed on bark and herbs as fallback food in winter. For example, Japanese macaques living in Kinkazan ate more barks and herbs when the temperature was low (Agetsuma and Nakagawa 1998; Tsuji et al. 2006); the rhesus macaques in northwest Pakistan were strongly dependent on herbs and roots account for 23.7% of their winter food composition (Goldstein and Richard 1989). Lichen is a stable resource; some primates eat lichens seasonally, and lichens occupy an important part of their diet (Tsuji et al. 2013). For instance, lichens play a prominent role in the annual diet of R. bieti (67.0% of their annual diet) and become the dominant food item in winter when resources are scarce, and ultimately a key survival strategy (Grueter et al. 2009); fruticose lichens were fallback food for Rwenzori colobus (Colobus angolensis ruwenzorii) and allow them to sustaining the supergroup during periods of reduced food availability (Miller et al. 2020); Barbary macaques (Macaca sylvanus) consumed lichens as a "staple", not as a "filler" fallback food, in Morocco and Algeria (Ménard and Vallet 1986). However, we did not observe the consumption of lichens by macaques during this study, consistent with other Asian macaque studies: lichens are not a food of Asian macaques (Tsuji et al. 2013). In contrast, macaques in high-altitude habitats use the roots, barks, and fallen leaves as fallback food. Among them, roots play a prominent role in macaques annual food consumption and become the dominant food item in winter (63.4% of their winter diet). During this study, we observed that all the roots consumed by macaques came from herbs (Table 1). In addition to the lack of resources in the habitat itself, it may also be related to the high intensity of local grazing (mainly by yaks and horses). For macaques eating plants roots may help to save energy (without long travel distances) and reduce interspecific food competition with livestock and wild herbivores (e.g. tufted deer, Elaphodus cephalophus), which needs further verification. Studies have found that rhesus macaques in northwest Pakistan were strongly dependent on herbs due to habitat destruction by logging and cattle grazing (Goldstein and Richard 1989). Also affected by overgrazing of sika deer (Cervus Nippon Temminck), the Japanese macaques in Kinkazan relied more heavily on herbs than those at Yakushima (Tsuji and Takatsuki 2004). We believe that, similarly to the strategy of R. bieti relying on lichens, using roots is a way for macaques in the Western Sichuan Plateau to regulate the seasonal lack of palatable foods and ultimately a key survival strategy (Xiang et al. 2007; Grueter et al. 2009).

In summary, the dominant behavior of rhesus macaques was feeding and moving, and remains stable throughout the year, with a long duration of daily feeding activities. They adjust their food composition according to seasonal fluctuations in food availability; young leaves, fruits, and seeds are their preferred food; and when the preferred food is in short supply, they eat roots, bark, and fallen leaves as fallback foods. Among these, the roots of herbaceous plants are the key food for them to survive through the winter and occupy a prominent position in the food composition of the whole year. Rhesus macaques in the Western Sichuan Plateau choose active feeding methods, broaden recipes, and flexibly adjust food composition, possibly to maximize energy efficiency to adapt to the shortage and strong fluctuation of food resources in high-altitude habitats. These observations highlight that these rhesus macaques may have adapted well to the high-altitude environment.

Acknowledgements

We are very grateful to the Yajiang Forestry and Grassland Administration for permitting us to conduct our research. We are also grateful to Fei Zhou, Duo Ma, Danzhen Tu-Deng, Ma Ni, and Wei Jiang for their logistical assistance.

Funding

This study was supported by the National Natural Science Foundation of China (31870355; 31960106).

Ethical Statement

Permission to conduct fieldwork in the Yajiang area was granted by the Yajiang Forestry and Grassland Administration. All data collection was noninvasive.

Author Contributions

H.L.X. and Z.H.H. designed the research. K.C.Z., Z.X.J., Q.Y.N., Y.F.Y., H.T.X, B.J.L., and W.J.P.C. collected data. K.C.Z. and F.K. analyzed the data and wrote the manuscript. H.L.X., F.K., and Z.H.H. revised the manuscript. All authors read and approved the final manuscript.

Conflict of Interest

The authors have no conflicts of interest to declare.

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Author notes

These authors contributed equally to this work.

© The Author(s) 2022. Published by Oxford University Press on behalf of Editorial Office, Current Zoology.

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