The relationship between artificial food supply and natural food selection in two troops of commensal Hamadryas Baboons Papio hamadryas (Mammalia: Primates: Cercopithecidae) in Saudi Arabia

 

 

 

ARTICLE

INTRODUCTION

 

Hamadryas Baboons range throughout the horn of Africa (in parts of Ethiopia, Eritrea, Djibouti, Sudan, and Somalia) and the Arabian Peninsula in Saudi Arabia and Yemen (Kummer 1968; Biquand et al. 1992; Al-Safadi 1994; Zinner et al. 2001). In fact, the Hamadryas Baboon is the only nonhuman primate species to inhabit the Arabian Peninsula. In Saudi Arabia, hamadryas are found along the Sarawat mountains which run parallel to the west coast of the Arabian Peninsula and the Red Sea (Biquand et al. 1992).

Hamadryas Baboons are known to have among the longest daily path lengths of all primate species, and a unique multi-level social organization in which large groups (troops and bands) break into smaller foraging parties (one-male units and clans) during daily travel. These ranging and social patterns have often been attributed to the scarce and widely dispersed distribution of food resources in their semi-desert habitats (Kummer 1968; Sigg & Stolba 1981; Swedell 2002, 2006; Schreier 2010; Schreier & Swedell 2012a). Hamadryas Baboons rely on Acacia species for subsistence throughout their range (Kummer 1968; Nagel 1973; Kummer et al. 1981; Al-Safadi 1994; Schreier 2010). In Ethiopia, Nagel (1973) reported that Hamadryas Baboons at the Awash River most commonly fed on the flowers, seeds, and fresh shoots of Acacia senegal, A. nubica, A. tortilis, and A. clavigera, and appeared to prefer the flowers when they were available. At Erer Gota, Acacia species comprised the majority of the diet across seasons, and the Baboons preferred Acacia flowers and grass seeds when they were available (Kummer 1968). At Filoha, Hamadryas Baboons predominantly fed on A. senegal and A. nubica (Swedell et al. 2008; Schreier 2010). Saudi Arabian hamadryas populations also feed primarily on Acacia trees and other semi-desert plants such as Grewia spp. and Dobera glabra (Kummer et al. 1981; Al-Safadi 1994).

Seasonal dietary patterns are common, with hamadryas feeding on items such as flowers, young leaves and grass seeds when they are available, and switching to less preferred items during the dry season (Kummer 1968). Band 3 at Filoha, Ethiopia consumed fewer food species during the dry season months and a greater number of species in the wet season (Swedell et al. 2008). The baboons at Filoha also fed predominantly on Doum Palm Fruit Hyphaene thebaica—a high quality food source not available elsewhere in hamadryas range—when it was available, and they preferred A. senegal flowers to leaves (Schreier 2010).

In addition to feeding on natural plant resources, some Hamadryas Baboons also rely on human food, via crop raiding or being directly fed by humans (i.e., commensalism). For example hamadryas in Awash National Park, Ethiopia were known to occasionally raid crops both outside and within the park (Nagel 1973). Raiders and commensal baboons account for 35% of the entire estimated Arabian hamadryas population (Biquand et al. 1992). Crop raiders in agricultural areas were much more common than were commensal groups (Biquand et al. 1992). Baboon reliance on human food, however, conflicts with both urban and agricultural activities throughout their entire range in Saudi Arabia (Kamal & Brain 1989; Biquand et al. 1992), increasing human-wildlife conflicts.

Feeding on human foods, by either raiding or being provisioned, has been proposed to be the major cause of population increase in non-human primate troops that frequent human settlements (Sugiyama & Ohsawa 1982; Fa 1988; Kurita et al. 2008). No free-ranging primates, however, have been reported to cease feeding on natural foods after starting to consume human foods (Iwamoto 1988; Boug 1995; Saj et al. 1999).

Based on their extensive surveys on the distribution of Hamadryas Baboons in Saudi Arabia, Biquand et al. (1992) found that few cases of raiding were observed where the availability of natural foods was high, especially where perennial species remained rich on the ground. Specifically, Baboons seldom raided crops in Acacia woodlands and wadis where vegetation was rich. In contrast, crop-raiding frequency was high in certain dry regions as well as in areas where the natural vegetation did not include plant species in the Baboons’ diet. Baboons tended to raid crops and houses and to be provisioned in the extreme case of when their habitat was severely destroyed by overgrazing (Biquand et al. 1992).

The purpose of this study is to investigate whether Biquand et al.’s (1992) findings apply to two local Saudi Arabian Hamadryas Baboon populations. We seek to gain a better understanding of hamadryas feeding strategy by attempting to clarify the relationship between the level of artificial food supply and natural food selection in two troops of commensal Hamadryas Baboons living in different habitats in Saudi Arabia. One site had higher amounts of natural plant foods and was a less damaged habitat overall. We predicted that baboons at the site with richer vegetation would spend less time feeding than those in the damaged habitat. We also predicted that baboons at both sites would spend more time feeding when provisioning was highest and that they would consume less natural food during these periods. Conversely, we predicted that dependency on human foods would decrease during periods of high natural food availability.

 

 

METHODS

Study sites

Alhada: Alhada is a mountainous area located 18km northwest of Taif City, which is the most famous recreation site in southwestern Saudi Arabia. It is a part of the Sarawat range (Fig. 1), and the mountains’ peak elevation reaches 2,100m. At the escarpment facing the Red Sea, a road crosses the area connecting Taif and Makkah (the holy place of Islam).

During the study period at Alhada (September 1990 to August 1991) the baboon troop (Image 1) living at the top of the escarpment was composed of 220 individuals who shared a sleeping site. For most of the year people using the road connecting Taif and Makkah presented food (e.g., bananas, carrots) to the baboons (Boug 1995). In January and February 1991, however, the road was closed for maintenance construction, and thus significantly fewer people visited this area, resulting in a dramatic decrease in provisioning level. This provided the opportunity to study the effects of reduced provisioning on the foraging strategy of this baboon troop (Boug et al. 1994).

Alhada and the Dam Site (see below) have no weather stations, and as a result, we employed meteorological data for the relevant study periods from the Taif airport located 40km east of the escarpment. It is important to note that the weather data may not always represent the exact conditions of the Alhada habitat. The temperatures for the study period at Alhada varied between a maximum of 36.10C in August and a minimum of 40C in January, with monthly averages ranging from 9.2–24.3 0C (Fig. 2). Annual rainfall during the study period was 158.1mm, but intra-annual variation was great (Fig. 2). An analysis of 14 years (1990–2003) of rainfall data from the meteorological station at Taif airport shows that the highest and most stable peak occurs in April with frequent additional peaks occurring in August and November at two to three year intervals.

Like other mountainous areas facing the Red Sea, the considerable variation in daily temperature causes frequent fog to develop, which adds moisture to the area and creates favorable conditions for varied plant growth. For example, these weather conditions permit Juniperus forest to grow at high altitudes of 1,800m (Biquand et al. 1992). Juniperus spp. are the dominant species here, followed by several Acacia species, such as A. origena. This area is considered to be representative of west Sarawat mountain habitat.

Dam Site: The Dam Site—a hilly and wadi area called Al Ruddaf—is located 7km southeast of the Taif City center (25km southeast of Alhada) and is known as the city’s recreational site (Fig. 1). We carried out our field studies at the Dam Site from January to December 2000. It is located in the rain shadow of the eastern Sarawat mountains, where the western cliff facing the Red Sea is the side of Alhada. The elevation is 1,500m.

During the study period, the baboon troop here was composed of 475 individuals who shared a sleeping site beside the Wadi Liyah Dam (Mori et al. 2007). From 1998–2000 this Baboon troop was intensively studied through a collaborative project of the Saudi Wildlife Authority of Saudi Arabia (SWA), Kyoto and Miyazaki Universities, and Kitakyushu Municipal Museum, Japan. People who visited the Dam Site area (including the Al Ruddaf Park) during the study period often presented food to the Baboons. The level of provisioning was influenced by school and national vacations. For example, during summer vacation (June–September) people from nearby cities visit the area to watch the baboons and feed them fruit and vegetables.

The temperature at the Dam Site varied from a maximum of 37.30C in August 2000 to a minimum of 7.30C in January 2000, with monthly averages ranging from 16.2–30.4 0C (Fig. 2). The cumulative rainfall for 2000 was 136.9mm. Inter-annual variation over a 14-year period (1990–2003) at Taif airport ranged between 78.7–360.3 mm, with an average of 200mm. The location of this site as a rain shadow causes a much drier environment than that of Alhada. Two Acacia species are dominant in this area: A. asak in the hilly part of the area and A. gerrardii in the wadi. This area is representative of habitat in the east Sarawat mountain area. Housing, roads, cultivation, and overgrazing associated with the significant human population in this area have disturbed the habitat of the hamadryas here. The Dam site is, therefore, a more damaged site than Alhada.

 

 

 

Vegetation cover

We assessed habitat quality by estimating the coverage of different vegetation types at each study site. We set transects across different topographical features at each site, i.e., three transects each in slope and wadi at the Dam Site, and two transects each in flat, slope and wadi in the Alhada area, for a total of six transects at each site. Each transect was 180x10 m, providing a total area of 1,800m2. We measured the diameter at breast height (DBH) and crown size (the longest and the shortest diameter) of each tree/shrub for all plants within the area located within 5m of each side of the transect line. We also recorded the phenology status for each plant, and that include flowers, fruits, seeds and green leaves. In addition, we set quadrats 3x3 m in size (9m2) every 30m along the transect line to measure the coverage of ground vegetation, such as small shrubs, grasses and herbs. We estimated the percentage of plant cover of each species in these quadrats by eye. We developed a computer program to calculate the coverage of tree/shrub layers in each transect, considering the projection of slopes onto the map and parts of tree crowns that should be excluded from the coverage calculation. Based on the home range area drawn on the 1:50,000 scale map, we assessed the vegetation richness for each troop as the total coverage of tree/shrub layer and herb/grass layer.

 

 

Observations and analyses

We followed the baboons from sunrise to sunset, and determined activity profiles by scan sampling of all visible animals (Altmann 1974), based on scans taken at 15 min intervals over a period of five full days each month. In Alhada we conducted 720 hours of observations and 2,880 scans. As we defined one activity record as the activity of each individual, we obtained 40,536 activity records in Alhada. We also recorded the plant species and part ingested when Baboons were feeding. We conducted the same number of hours of observation at the Dam Site, obtaining a total of 75,915 activity records during 720 hours of observation.

We calculated the following variables to determine the monthly changes and relationships among vegetation, feeding and weather data:

1) The percentage of the number of feeding records to total activity records (time spent feeding; Feed_Total)

2) The percentage of the number of records feeding on natural foods to total activity records (Nat_Total)

3) The percentage of the number of records feeding on natural foods to the total feeding records (Nat_Feed)

4) The diversity index for natural foods calculated by the Shannon-Weiner’s equation (Nat_Div_Index)

We determined diet composition from the activity scan data. We established a checklist of plant species, and calculated the relative contribution of each food item/species eaten to total feeding records to compare feeding habits at the two study sites. We statistically compared monthly changes in feeding profiles in both study sites by Spearman’s rank correlation and Wilcoxon sign test for the level of significance. Significance level was set at p<0.05. For Alhada, we carried out the analyses for two sets of data, one for 12 months (September 1990–August 1991) and another for 10 months (September–December 1990 and March–August 1991) to measure the effect of the road closing in January and February on the baboons’ dietary patterns.

 

 

RESULTS

 

Plant availability

Plant coverage was higher in sloped regions in Alhada compared to the Dam Site. The percentages of trees and shrubs in two slope transects in Alhada were 10.5% and 14.2% (mean=12.3%), while in three slope transects at the Dam Site the percentages were 4.7%, 13.6% and 4.7% (mean=7.6 %; Table 1). Ground cover (i.e., grass/herb percentages) in slopes was also higher in Alhada than in the Dam Site. In two slope transects in Alhada the percentages of grass and herb cover were 53.3% and 27.2% (mean=40.25), while in three slope transects at the Dam Site the percentages were 18.3%, 15.0%, and 15.0% (mean=16.1). In wadi areas, the percentages of trees and shrubs were 14.2% and 16.7% (mean=15.4%) in Alhada, and 15.9 %, 21.9%, and 47.4% (mean=28.4%) at the Dam Site. Despite the higher tree/shrub coverage in wadis at the Dam Site, ground cover in these areas was higher in Alhada (mean 5.85%) than at the Dam Site (mean=1.67%). Considering that the home ranges of both troops were mainly sloped, Alhada has denser vegetation cover than the Dam Site.

We also estimated total vegetation cover in both tree/shrub and grass/herb layers for the two sites from the size of each geographical feature in the baboon home ranges (Alhada, 6.69km2; Dam Site, 6.70km2). The tree/shrub layer covers 10.6% and 9.4%, and the grass/herb layer covers 21.7% and 14.2% in Alhada and the Dam Site, respectively. These data confirm that the Alhada habitat provides richer vegetation cover than the Dam Site.

At both sites there was one major plant emergence corresponding with the first period of heavy rainfall that took place during March–April. The second period of heavy rainfall (July–August) had a more moderate effect on plant emergence and growth. Plant species included annuals, biennials and perennials. Most plants were herbaceous and a few were woody. Leafing, flowering, and fruiting periods varied among species; however, these plant parts including leaves, flowers, and fruits were most prevalent from March to November. Growth of most species was minimal during winter.

 

 

 

Diet composition

Hamadryas Baboons in the study areas showed a wide range of dietary selection. We recorded a total of 65 plant species consumed by the baboons; 42 in Alhada and 23 at the Dam Site (Appendix 1). Baboons chose one to seven plant parts (bark, flowers, fruit, stems, seeds, roots, gum) depending on the species (Acacia gerrardii and A. asak at the Dam Site, and Juniperus and Ficus species at Alhada).

The flowering, fruiting and seeding season of preferred species played a strong role in the food choice and feeding strategy of the Hamadryas Baboons in this study (Fig. 3). The Alhada troop depended on the seeds of A. gerrardii for 50% and 24.7% of its natural foods diet during January and February, respectively (Fig. 3). Baboons in Alhada ate fruits of J. phoenicia intensively, accounting for 47% and 31% of the feeding records in April and May, respectively. As the dominant plant species in Alhada, its bark accounted for 59.6% of the feeding records in February and its leaves for 26.2% in August. They ate fruits of Ficus carica during June (12.8%), July (16.7%) and August (14.5%). Ingestion of F. ingens fruits made up 45.5%, 14.5%, and 28.6% of feeding records in June, July and August, respectively.

The Dam Site troop fed mainly on the flowers of A. gerrardii, making up 60.9%, 47.8% and 22.4% of the total natural feeding records collected in June, July and August, respectively (Fig. 3). They also depended heavily on fruits making up 78.4% and 40.4% of the total feeding records in September and October, respectively. The Dam Site troop fed on flowers of A. asak in 11% of the feeding records in August and on its fruits for 26.8% of the records in November. This species is dominant on the slope areas at the Dam Site.

It is clear that preferred plant species play an important role in the food choice of Hamadryas Baboons and their feeding strategy. Both troops fed heavily on ground vegetation sprouting shortly after rainfalls in spring; however, once the young plants on the ground were depleted, baboons in the richer/less damaged habitat (Alhada) shifted their main diet to parts of Juniperus and Ficus trees in spite of an abundance of Acacia trees, while those in the less rich/more damaged habitat (Dam Site) changed their diet mainly to Acacia parts.

 

 

 

 

Feeding Activity

H Feeding activity records accounted for 18% and 33% of the total activity records collected in Alhada and the Dam Site, respectively (Fig 4a). Baboons at the Dam Site spent significantly more time feeding than those at Alhada (Wilcoxon sign test, p=0.003). The curve trends of monthly change were different (Spearman rank correlation, r=0.194611, p=0.547) between sites.

The Baboons at Alhada spent less time feeding in January and February (13.4% and 15.0% of the activity records) than did the Baboons at the Dam Site (22.5% and 33.9%). These months were when the road connecting Taif and Makkah was closed for maintenance, preventing provisioning by people at Alhada. During this time, provisioning at the Dam Site was high.

At both sites, the baboons spent the most time feeding during summer, which corresponds to school vacation and thus higher numbers of visitors and increased provisioning. In Alhada the Baboons spent 25.0% of their time feeding in July and 24.1% in August. At the Dam Site, the baboons spent 32.7% of the time feeding in June, 37.6% in July, and 39.9% in August. Here these summer months also coincided with the flowering season of A. gerrardii, a preferred plant species. The next highest levels of feeding at both sites corresponded with when availability of natural plants was high due to peaks in monthly rainfall (Fig. 2). Baboons at Alhada spent 22.5% of activity records feeding in May, while baboons at the Dam Site spent 30.6% of activity records feeding in April.

The largest difference in monthly feeding time between the two sites occurred in December when the Alhada baboons spent 17.9% of the time feeding while those at the Dam Site spent 43.0% of their time feeding. This difference can be attributed to an increased number of visitors to the Dam Site associated with a delayed Islamic vacation season in 2000.

The monthly patterns of feeding on natural foods were similar across sites (Fig. 4b; Spearman rank correlation (correlation coefficient) r=0.668521102, p=0.018), and there is no significant difference in the position (Wilcoxon signed rank test, p=0.433). In Alhada, the peaks in feeding on natural foods during January (51.3%) and February (45.6%) are likely due to a reduction of provisioning during these months when the road was closed. In contrast, feeding on natural food was relatively low at the Dam Site at this time of the year (28.7% of feeding records in January and 23.4% in February). Baboons at both sites consumed high percentages of natural foods in April (42.2% in Alhada, 46.5% at Dam Site) which may be related to the increased rainfall during this time. In September, natural food feeding was high at the Dam Site (30.3%) due to the fruiting season of preferred plant species A. gerrardii. In June, July and August, dependency on natural plants was considerably lower at both sites likely due to the low natural plant availability during the hot summer season and low rainfall.

There was no significant difference between the mean monthly values of diversity index for natural foods across sites (Wilcoxon signed rank test, r=0.014751, p=0.424; Fig. 4c). The diversity index peaked at both sites in March and April (3.4–3.6). The lowest diversity index occurred in October at Alhada (1.5) and in September at the Dam Site (1.5). There were higher diversity values during autumn and winter (October to February, range 2.8–3.3) at the Dam Site compared to Alhada (1.5–2.6). Baboons at the Dam Site fed on many food items (mainly fruits) from Acacia species during October to December, and fallen Acacia seeds and food items from the herb/grass layer in January and February. During these months, the diversities are high despite the lower dependency on natural foods during this period (Fig. 4b).

 

 

Analysis of factors influencing feeding activities

We examined the relationships among several variables (rainfall, Feed_Total, Nat_Total, Nat_Feed and Nat_Div_Index) employing Spearman’s rank correlation coefficients analysis (Table 2). Both Nat_Feed and Nat_Total for Baboons in Alhada showed significant positive correlations with rainfall in both the 12-month and 10-month analyses (rs=0.615 and 0.603, respectively; p<0.05). Feed_Total and Nat_Feed were negatively correlated (rs=-0.643; p<0.05) in Alhada only in the 12-month analysis, indicating that the Baboons spent less time feeding overall when a higher proportion of their diet came from natural foods. In January and February, baboons at Alhada were forced to collect a lot of Acacia fruits and seeds (Fig. 3) because provisioning by humans was very limited. There were, however, no statistically significant correlations between Nat_Feed and Feed_Total at the Dam Site or for the 10-month analysis in Alhada.

When excluding January and February in Alhada, Nat_Div_Index showed significant positive correlations to both rainfall (0.621; p<0.05) and Nat_Total (0.661; p<0.05). This suggests that natural food diversity rose with both increasing rainfall and time spent feeding on natural foods under regular provisioned conditions. There were no significant correlations among those variables at the Dam Site, however. These results suggest a clear relationship between feeding activities and natural food conditions at Alhada but not the Dam Site.

 

DISCUSSION

 

Our results suggest that three variables influence the baboons’ feeding behavior at our study sites and affect their dependency on natural plant foods: (1) level of natural plant availability, (2) level of provisioning, and (3) seasonality of preferred food species. As predicted, the baboons at Alhada (where there is more dense vegetation) spent less time feeding than those at the Dam Site (the less dense habitat). Furthermore, as expected the troops at both sites spent more time feeding during periods of the year when provisioning by humans was highest. Moreover, the baboons spent more time feeding on natural foods when numbers of human visitors were low. In fact, the greatest difference between the two troops in the percentage of feeding on natural foods occurred in January and February, when humans were precluded from visiting Alhada because of road closure. These were the two months of the year that the Alhada baboons spent the most time feeding on natural foods. With respect to seasonality, fresh shoots of ground vegetation that sprouted after prominent spring rainfall resulted in high levels of feeding at both sites.

A molecular genetic study by Winney et al. (2004) revealed that the ancestor of present Hamadryas Baboons might have immigrated to Saudi Arabia passing a southern bridge between the horn of Africa and Arabian Peninsula that was available during an interglacial age. The baboons’ inhabitation of this peninsula might have been guided by the relatively rich ground (perennial and bushy) and arboreal (Juniperus, Ficus and Acacia) vegetation formed by the cooler and wetter climate due to high altitude, as observed at our study sites. The Baboons’ preferred habitat, however, is also favored by humans. Presently, the Sarawat mountain region has high human population density (General Statistic Commission of Saudi Arabia 2013) and the area therefore suffers from severe degradation of the natural environment due to cultivation, nomadism and urbanization. The grazing of ground vegetation by cattle is responsible for high levels of degradation in this area.

Following their extensive surveys throughout Saudi Arabia, Biquand et al. (1992) concluded that the degree of interaction between baboons and humans, such as raiding and commensalism, is closely related to the preservation status of the natural habitat, especially with respect to ground vegetation. Our study confirms that their findings also apply to two nearby troops living in different habitats, namely, the feeding behavior of baboons living in the denser habitat (Alhada) reflected the natural food resources, but this was not the case for Baboons living at the Dam Site. The more commensal troop lived in the less dense habitat and heavily depended on artificial foods.

Sugiyama & Ohsawa (1982) reported that an artificially provisioned troop of Japanese macaques showed a higher birth rate, earlier primiparous age, and lower infant mortality rate resulting in a larger troop size compared to a natural troop. Iwamoto (1988) analyzed nutritional content of both natural and artificial foods, and reported that many artificial foods given to Japanese macaques contained more soluble carbohydrates than natural foods. Monkeys can readily convert carbohydrates into energy. Provisioned foods thus appear to provide high energy content but they are not nutritionally balanced (Iwamoto 1988; Saj et al. 1999). This may explain why the baboons in our study sites continued to spend a substantial amount of time feeding on natural foods, despite the high availability of artificial foods. In other words, baboons need a nutritional balance even under energetically rich food conditions, which may prevent them from relying solely on human foods. For example, the baboons appear to depend on natural foods for protein. Fresh grass and herb shoots are likely rich in protein, as are Acacia fruits and flowers, fruits, and leaves of Juniperus and Ficus, all preferred foods by the Baboons (Hausfater & Bearce 1975; Wrangham & Waterman 1981; Isbell et al. 2012; Rothman et al. 2012). Natural foods may also provide baboons with many kinds of minerals, vitamins, and sometimes medicinal chemicals (Hausfater & Bearce 1975; Wrangham & Waterman 1981; Isbell et al. 2012; Rothman et al. 2012). We suggest that the need for a nutritionally balanced diet has kept the baboons from becoming completely dependent on human foods.

Interestingly, the proportion of time spent feeding on artificial foods is almost the same for the two troops, despite the significant difference in total feeding time. The only differences between the Alhada and Dam Site troops in time spent feeding on artificial foods appeared in January and February, when the main road in Alhada was closed and provisioning was limited, and in September and October when the Dam Site troop preferred Acacia fruits to human foods. The percentages of the diet from natural and artificial foods were almost identical across sites for the other months of the year. We also found the same pattern of seasonal trends in natural diet diversity across the two sites. The similarity in findings for the two troops suggests that the baboons used a strategy of balancing their feeding on natural and artificial foods that prevents them from becoming too dependent on human diets.

Our results suggest that baboons favor natural foods over artificial foods if they can freely choose their diet under free ranging conditions. Considering their evolutionary radiation (Kummer 1968), Hamadryas Baboons might have initially adapted to an environment that was basically arid but locally covered by highland Juniperus, Acacia and Ficus forests with richer ground vegetation than at the present time. This characteristic hamadryas habitat is much harsher than that typical of most primates in the tropics; Hamadryas Baboons have been able to cope with the limited food availability throughout their range by employing large home ranges and long daily paths, as well as by altering group size in response to different levels of food availability (Kummer 1968; Swedell 2006; Mori et al. 2007; Schreier & Swedell 2009, 2012a,b). In these environments, they particularly require foods containing low fiber and high soluble carbohydrates (Hausfater & Bearce 1975; Wrangham & Waterman 1981; Isbell et al. 2012; Rothman et al. 2012). It is likely that the Saudi Arabian Hamadryas Baboons discovered that artificial foods provide them with ready energy, providing another means to overcome the low abundance of food resources in typical hamadryas habitat. Commensal and crop-raiding baboon troops frequenting urbanized areas are virtually guaranteed access to such high energy foods.

The fundamental problem in places like Alhada and the Dam Site is that human and baboon activities overlap. The baboons enter human-inhabited areas in order to obtain human food, which can lead to human-baboon conflict. Furthermore, eating human foods has been proposed to be the major cause of population increase in non-human primate troops that frequent human settlements (Sugiyama & Ohsawa 1982; Fa 1988; Kurita et al. 2008). The Saudi Wildlife Authority (SWA) developed a management plan to reduce the number of conflicts caused by baboon commensalism (Boug et al. 1991). Several projects have been implemented in various areas of the country to test the feasibility of the management plan (Boug et al. 1991, 1994), however, urban and cultivated areas still suffer from raiding and crop damaging by baboons. Our study suggests that in order to satisfy their particular nutritional needs, Hamadryas Baboons are unlikely to completely abandon feeding on natural foods in favor of artificial foods. Thus, it seems possible for the baboons to revert to natural and healthy populations with lower densities. This can be realized by restricting provisioning by tourists of ready to use human foods during the severe periods in summer and winter, when natural food availability is low and provisioning level is high, ultimately decreasing human-wildlife conflict.

 

 

REFERENCES

 

 

Al-Safadi, M.M. (1994). The Hamadryas Baboon, Papio hamadryas (Linnaeus, 1758) in Yemen (Mammalia: Primates: Cercopithecidae). Zoology in the Middle East 10: 5–16.

Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour 49: 227–267.

Biquand, S., V. Biquand-Guyot, A. Boug & J.P. Gautier (1992). The distribution of Papio hamadryas in Saudi Arabia: Ecological correlates and human influences. International Journal of Primatology 13: 223–234.

Boug, A. (1995). Studies on ecological behaviour of baboon Papio hamadryas in Alhada mountain in Saudi Arabia. MSc Thesis. Biological Sciences - Faculty of Science, King Abdulaziz University, Jeddah.

Boug, A., S. Biquand & V. Biquand-Guyot (1991). An example of management of best baboons around urban areas, pp. 39–40. In: Ehara A., T. Kimura, O. Takenaka & M. Iwamoto (eds.). Primatology Today. Elsevier, New York.

Boug, A., S. Biquand, V. Biguand-Guyot & K. Kamal (1994). The response of commensal Hamadryas Baboons to seasonal reduction in food provisioning. Revue d’Ecologie (Terre Vie) 49: 307–319.

Fa, J.E. (1988). Supplemental food as an extranormal stimulus in Barbary Macaques Macaca sylvanus at Gibraltar its impact on activity budgets, pp. 53–78. In: Fa, J.E. & C.H. Southwick (eds.). Ecology and Behavior of Food Enhanced Primate Groups. Alan R. Liss, New York.

General Statistic Commission of Saudi Arabia (2013) Human Population in Saudi Arabia - report.

Hausfater, G. & W.H. Bearce (1976). Acacia tree exudates: their composition and use as a food source by baboons. East African Wildlife Journal 14: 241–243.

Isbell, L.A., J.M. Rothman, P.J. Young & K. Rudolph (2012). Nutritional Benefits of Crematogaster mimosae Ants and Acacia drepanolobium Gum for Patas Monkeys and Vervets in Laikipia, Kenya. American Journal of Physical Anthropology 150(2): 286–300; http://doi.org/10.1002/ajpa.22205

Iwamoto, T. (1988). Food and energetics of provisioned wild Japanese Macques Macaca fuscata, pp 79–94. In: Fa, J.E. & C.H. Southwick (eds.). Ecology and Behavior of Food Enhanced Primate Groups. Alan R. Liss, New York.

Kamal, K., & P.F. Brain (1989). An extension of the range of Hamadryas Baboon in central western Saudi Arabia. Journal of Saudi Arabian Natural History Society 2(9): 14–20

Kummer, H. (1968). Social Organization of Hamadryas Baboons. Basel, Karger.

Kummer, H., A.A. Banaja, A.N. Abo-Khatwa & A.M. Ghandour (1981). Mammals of Saudi Arabia: Primates: a survey of Hamadryas Baboons in Saudi Arabia. Fauna Saudi Arabia 3: 441–471.

Kurita, H., Y. Sugiyama, H. Ohsawa, Y. Hamada & T. Watanab (2008). Changes in demographic parameters of Macaca fuscata at Takasakiyama in relation to decrease of provisioned foods. International Journal of Primatology 29: 1189–1202.

Mori, A., A. Yamane, H. Sugiura, T. Shotake, A. Boug & T. Iwamoto (2007). A study on the social structure and dispersal patterns of Hamadryas Baboons living in a commensal group at Taif, Saudi Arabia. Primates 48: 179–189.

Nagel, U. (1973). A comparison of Anubis Baboons, Hamadryas Baboons and their hybrids at a species border in Ethiopia. Folia Primatologica 19: 104–165.

Rothman, J.M., C.A. Chapman & P.J. van Soest (2012). Methods in primate nutritional ecology: a user’s guide. International Journal of Primatology 33: 542–566.

Saj, T., P. Sicotte & J.D. Paterson (1999). Influence of human food consumption on the time budget of vervets. International Journal of Primatology 20(6): 977–994.

Schreier, A.L. (2010). Feeding ecology, food availability, and ranging patterns of wild Hamadryas Baboons at Filoha. Folia Primatologica 81: 129–145.

Schreier, A.L. & L. Swedell (2009). The fourth level of social structure in a multi-level society: ecological and social functions of clans in Hamadryas Baboons. American Journal of Primatology 71: 948–955.

Schreier, A.L. & L. Swedell (2012a). Ecology and sociality in a multilevel society: ecological determinants of social cohesion in Hamadryas Baboons. American Journal of Physical Anthropology 148: 580–588.

Schreier, A.L. & L. Swedell (2012b). The socioecology of network scaling ratios in the multilevel society of Hamadryas Baboons. International Journal of Primatology 33: 1069–1080.

Sigg, H. & A. Stolba (1981). Home range and daily march in a Hamadryas Baboon troop. Folia Primatologica 26: 40–75.

Sugiyama, Y. & H. Ohsawa (1982). Population dynamics of Japanese monkeys with special reference to the effect of artificial feeding. Folia Primatologica 39: 238–263.

Swedell, L. (2002). Ranging behavior, group size and behavioral flexibility in Ethiopian Hamadryas Baboons (Papio hamadryas hamadryas). Folia Primatologica 73: 95–103.

Swedell, L. (2006). Strategies of Sex and Survival in Hamadryas Baboons: Through a Female Lens. Upper Saddle River, NJ, Prentice Hall College Division.

Swedell, L., G. Hailemeskel & A. Schreier (2008). Composition and seasonality of diet in wild Hamadryas Baboons: Preliminary findings from Filoha. Folia Primatologica 79: 476–490.

Winney, B.J., R.L. Hammond, W. Macasero, B. Flores, A. Boug, V. Biquand, S. Biquand & M.W. Bruford (2004). Crossing the Red Sea: phylogeography of the Hamadryas Baboon, Papio hamadryas hamadryas. Molecular Ecology 13: 2819–2827.

Wrangham, R.W. & P.G. Waterman (1981) Feeding behaviour of vervet monkeys on Acacia tortilis and Acacia xanthophloea with special reference to reproductive strategies and tannin production. Journal of Animal Ecology 50: 715–731.

Zinner, D., F. Peláez & F. Torkler (2001). Distribution and habitat associations of Baboons (Papio hamadryas) in central Eritrea. International Journal of Primatology 22: 397–413.