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Article

The Potential of Foraging Chacma Baboons (Papio ursinus) to Disperse Seeds of Alien and Invasive Plant Species in the Amathole Forest in Hogsback in the Eastern Cape Province, South Africa

by
Lwandiso Pamla
1,
Loyd R. Vukeya
2,* and
Thabiso M. Mokotjomela
2,3
1
Scientific Services Unit, Eastern Cape Parks and Tourism Agency, 17–25 Oxford Street, East London 5200, South Africa
2
Centre for Invasion Biology, South African National Biodiversity Institute, Free State National Botanical Garden, Rayton Rd., Dan Pienaar, P.O. Box 29036, Bloemfontein 9310, South Africa
3
School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg 3209, South Africa
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(3), 168; https://doi.org/10.3390/d16030168
Submission received: 9 January 2024 / Revised: 20 February 2024 / Accepted: 27 February 2024 / Published: 6 March 2024
(This article belongs to the Special Issue Emerging Alien Species and Their Invasion Processes)

Abstract

:
The invasion of alien and invasive plants into the threatened Amathole Forest in Hogsback, Eastern Cape Province (South Africa) is an emerging priority conservation issue. The objective of this pilot study was to document and compare the foraging visits of two chacma baboon (Papio ursinus) troops in their natural and human habitats and their foraging behavioural activities to understand their potential to disperse ingested alien seeds in Hogsback. We also estimated the number of seeds per faecal sample collected from the foraging trails of the two troops of baboons, and determined potential dispersal distances using allometric equations. Since the focal troops used preferred sleeping and foraging sites, we predicted that these sites would have a high concentration of propagules. We applied the normalised difference vegetation index (NDVI) to discern possible vegetation cover changes. Overall, the two chacma baboon troops showed a similar number of daily foraging visits, although they preferred to forage more in human-modified than natural habitats. Their feeding and moving activities were significantly greater than other activities recorded during the study. There were significant differences in the numbers of seeds of six different fruiting plant species: 82.2 ± 13.3% (n = 284) for Acacia mearnsii; 78.9 ± 12.1% (n = 231) for Pinus patula, and 64.0 ± 20.0% (n = 108) for Solanum mauritianum. The two baboon troops could transport about 445 536 seeds from the six focal fruiting plant species considered in this study. Baboons’ seed dispersal distances were long at > 5 km per daily foraging activity. The NVDI vegetation cover analysis (i.e., 1978–2023) shows that the dense vegetation cover expanded by 80.9 ha, while the moderate and sparse vegetation cover collectively decreased by 10.3 ha. Although the seed dispersal pattern was neither clumped nor displayed any recognisable pattern, against our prediction, the number of faecal samples containing alien seeds and the observed foraging movement patterns suggest that chacma baboons disperse alien plant seeds that may establish and facilitate the deterioration of the natural forest. Further quantitative studies investigating the diversity of the plant species dispersed, their germination rates after ingestion by baboons, and their seasonal patterns are required to understand the baboon seed dispersal systems in the Amathole forests of Hogsback.

1. Introduction

It is estimated that more than 95% of tropical seeds are dispersed by animals [1] and that between 30% and 50% of temperate tree species [2] are dispersed largely by birds [3,4,5] and primates [6]. The role of primates in seed dispersal is well documented [6,7]. Globally, more than 380 primate species feed on fruits and disperse seeds [8,9], and they represent 25–40% of the frugivore biomass in tropical forests [10,11,12]. For example, baboons are omnivorous and opportunistic feeders with diverse dietary material, depending on the nature of the prevailing environment [13,14]. They may eat large quantities of fruit, and either defecate or spit out large numbers of viable seeds [15,16,17,18,19,20] while a certain portion can be destroyed [21]. Owing to their mobility, baboons may contribute to long-distance seed dispersal [22,23,24], and thus potentially influence local vegetation population and community dynamics. Several studies have investigated primate frugivory and seed dispersal in Africa [6,15,18,20,25,26,27,28], but seed dispersal by baboons in South Africa and its ecological implications for natural vegetation (e.g., indigenous forest) dynamics have received little attention [23,29,30]. Animal-mediated seed dispersal processes are essential in maintaining plant communities [4,31,32] as well as the associated ecosystem goods and services.
Studies have revealed that fruiting invasive alien plants may out-compete indigenous plant species for pollination and seed dispersal services [33,34,35,36]. Thus, recently introduced fruiting plants may exploit the baboons’ dispersal services to the detriment of the indigenous plant species that have co-existed over long periods, thereby creating an ecological imbalance. Much as alien fruits are important food resources for many native animals, there is indeed evidence that invasive alien plants disrupt the animal–plant dispersal mutualisms [34,36,37], thus negatively impacting local vegetation dynamics. However, undisturbed continental tropical areas with the highest abundance (e.g., 80%) of fleshy fruits [5] reportedly experience relatively lower alien plant invasion threats than extra-tropical habitats owing to the absence of empty and colonisable niches [38,39]. For example, it has been argued that a counter-competition by 65 native plant species bearing fleshy fruits for vertebrate seed dispersal agents may have prevented the spread of the recognised 19 alien fleshy-fruited species in Montpellier, France [40]. Preliminary field observations of the black wattle’s (Acacia mearnsii) invasion patterns show that the indigenous forest fringes pose some natural resistance [38,41], which is, however, continually weakened by anthropogenic physical disturbance that facilitates colonisation by alien plants. Indeed, the introduction of alien invasive plants has profoundly altered the state of natural habitats worldwide [42]. We speculate that, with the increasing number of alien species, the negative impacts may also increase, since management efforts are also limited.
Habitat fragmentation is another major conservation threat to vertebrate dispersal mutualisms [43]. The fragmented habitats are impoverished of natural resources and animal movements are restricted [44]. Mucina and Rutherford [45] indicated that indigenous forests support a large proportion of South Africa’s biodiversity, although the forest biome is the smallest and most severely fragmented by anthropogenic developments in South Africa, particularly in the Eastern Cape Province [46,47,48,49,50]. Therefore, the fragmented state of the patches of Amathole indigenous forests in the Eastern Cape Province may increase certain species’ vulnerability to extinction [45,51]. In addition, the invasion of alien and invasive plant species is an emerging conservation issue, and needs urgent attention, since invasive plants alter the structure and functionality of the habitat [52,53]. Consequently, understanding the role of baboons in the seed dispersal of alien and invasive plants is important for the conservation of the threatened indigenous Amathole Southern Mistbelt forest fragments in Hogsback in the Eastern Cape Province of South Africa. For example, alien and invasive plants will potentially pose a threat to indigenous keystone plant species such as yellowwood (Podocarpus latifolius), white stinkwood (Celtis africana), cape chestnut (Calodendrum capense), and forest knobwood (Zanthozylum davyi) [54].
While the main study was centred around the human–wildlife conflict phenomenon in the Hogsback village, the foraging range of the studied chacma baboon troops also covered human-modified habitats in Hogsback (e.g., orchards and gardens) [55], which are deemed to be a major source of alien plant propagules [50,56,57,58]. We therefore predicted that foraging by the chacma baboons in the human-modified habitat would increase the transfer of seeds from alien and invasive plants into the natural forest, thereby compounding the forest’s vulnerability to the reported extinction threat. The objective of this pilot study was to document and compare the foraging visits of two baboon troops in the natural and human-modified habitats and to determine their foraging behavioural activities (i.e., feeding and moving) related to the spread of the ingested alien seeds. We also estimated the number of intact seeds per faecal sample collected from the foraging trails of the two troops of baboons in Hogsback, and generated seed dispersal distances using allometric equations. Since the troops used preferred sleeping and foraging sites, we also predicted that these sites would have a high concentration of propagules. Finally, we applied the normalised difference vegetation index (NDVI) to discern possible vegetation cover changes owing to the invasion of alien plants.

2. Material and Methods

2.1. Study Site

The study was conducted in Hogsback (GPS location: 32.5833° S, 26.9500° E), located in the Amathole Mountains of the Eastern Cape Province, South Africa (Figure 1). The area comprises human-modified and natural habitats dominated by indigenous Afromontane forest (i.e., Southern Mistbelt) vegetation, including the alpine grasslands of the Maputaland–Pondoland–Albany key biodiversity conservation area [45,59], and covers a total area of 13.78 km2 at an altitude of 1200–1300 m. Hogsback village is situated about 40 km from the town of Alice, and was established in the 19th century as a hill station for the families of British soldiers [60]. The village has many large gardens and farms that cover extensive areas [55]. Hogsback residents often favour woody alien plants bearing fruit and berries, which are visited by the primates, causing the animals to be regarded as pests. Hogsback also has relatively high levels of human disturbance, as it attracts tourists [45]. Furthermore, Hogsback has been one of the centres of the South African timber industry for more than 100 years, and the area hosts several commercial pine plantations. Alien timber plantations cover 1.2% of the total area of South Africa [61,62], comprising 50% pine (pine plantations including other conifers such as Cedrus, Widdringtonia, and Cupressus species), 43% Eucalyptus (eucalypt, poplar, oak, and other hardwood plantations), and 7% wattle (commercial plantations of Acacia mearnsii with small areas of other Acacia species) [61,63]. A serious threat is posed by alien tree plantations, where herbicides and fertilisers are used to the detriment of indigenous species [64] and contaminate the forest ground cover [65,66].
Ambient temperatures in Hogsback range from below freezing between June and August to more than 30 °C on hot summer days in February [45]. The area receives an average annual rainfall of 974 mm, with most of the rain falling in summer, often accompanied by thunderstorms. Temperature and rainfall have a pervasive effect on animals, not only directly but also indirectly by affecting food production, which, if reduced, can lead to increased intraspecific and interspecific competition [67]. The availability of food and water influences home range size, and thus lower levels of food resources in the local forest mean that the wild animals must be more adventurous to meet their nutritional needs [67].

2.2. Study Species

The Hogsback baboons have been around for a long time; long enough, according to [68], at least to have already impacted the distribution of the plants they disperse. Chacma baboons live in various habitats, and can survive under difficult environmental conditions [69]. Slater [70] has described baboons as some of the most flexible, opportunistic, and adaptable animals on earth (Figure 2). They are also among the primate taxa that exhibit the greatest degree of spatial overlap with humans [71]. Baboons are a highly mobile species, enhancing their value to ecosystem seed dispersal [24]. Home range, troop size, and travel patterns are influenced mainly by the distribution of food resources, water sources, and suitable sleeping sites [14,70,72]. The daily travel distances of chacma baboons ranges from 1.7 to 11.7 km [73,74].

2.3. Data Collection: Foraging Visits, Occurrence of Alien Plant Species, and Faecal Sampling

The two troops of Hogsback baboons were tracked on foot over six months [55]; we monitored troop sizes, composition, and foraging behaviour, using both scan and focal animal sampling ([75]; Figure 2). The troops were followed weekly from October 2014 to May 2015 (i.e., the optimal growing season) from 6:30 a.m. until either the troop was settled in its sleeping site at the end of the day or tracking was no longer possible. Data collection was not conducted on days of heavy rain because of poor global positioning system (GPS) functioning and low visibility. A total of 306 scans were collected for Nola’s troop and 228 scans for Evie’s troop, yielding 15 and 13 days of data, respectively, owing to human–primates conflict. The shooting of baboons by humans made locating the troops on a daily basis difficult. The home range sizes of the troops were determined by recording GPS data points at 15 min intervals using a handheld device (Garmin eTrex 10, New York, NY, USA). The type of habitat used by each troop was also recorded (e.g., whether it occupied a natural habitat or a human-modified habitat), and whether the baboons were feeding or moving, among other activities. Since the foraging visits frequency of vertebrate frugivores is proportional to fruit removal and subsequent seed dispersal [76,77,78], we determined the number of visits and their distribution at each site (Figure 3).
To determine which alien plant species are potentially dispersed by the chacma baboons in Hogback, we also recorded the fruiting alien plant species in their preferred foraging sites for both troops, which was the area in which their home ranges overlapped. We walked transects of varying lengths through the major foraging area, and recorded each fruiting plant species at 10 m intervals [79]. Because of limited accessibility in the Hogsback landscape owing to the fencing of private properties, a limited number of transects were sampled.
To assess seed dispersal patterns, faecal samples containing seeds were collected in the most preferred sleeping and foraging sites [80,81]. We also followed the baboon troops’ paths to and from the foraging sites, as documented by Pamla [5]. Any faecal samples encountered were processed on the spot (see Figure 4 below). Each faecal sample, either fresh or dry, was carefully crushed with a wooden rod to expose the components of the ingested material. This allowed for the separation of masticated seeds (identified by their coats) from those that were intact. Only intact seeds were counted and recorded for each faecal sample; the intact seed load represented a conglomerate of different plant species consumed during foraging.
To determine potential seed dispersal distances, we used allometric (i.e., as a function of animal body mass [BM]) mechanistic models to predict gut retention time (GRT) in hours for ingested seeds, and movement capacity (MC) in kilometres (km) for potential dispersal range of the chacma baboons that might influence plant recruitment processes.
Since the selected mammals were non-ruminant species (hindgut fermenters), we estimated the GRT (in hours), using the allometric equation from Steuer et al. [82], as follows:
GRT = 31.0 {BM}0.01 (31.0 and 0.01 are allometric constants)
Although the MC is not consistent because of seasonality, age and sexual dimorphism, dietary type, body mass, and local availability of survival resources [83,84,85], the MC (in km) was estimated using appropriate equations that were derived and modified from Du Toit [86]:
MC = 0.024 {BM}0.18 (0.024 and 0.18 are allometric constants)
To differentiate the land use in the habitats that the two troops targeted for their foraging movements, we applied NDVI measurements to determine the vegetation types and level of environmental disturbance in such patches. High-resolution images were generated for the area of interest—the study site—over 45 years (1978–2023); the year 1978 was used as a baseline. The pre-processed satellite images—Landsat Collection 2 Level-2 imagery for Landsat 4/5 TM (1978), Landsat 7 ETM (2002), and Landsat 8–9 OLI/TIRS (2023)—of the study area (path 171/row 80) were acquired using the United States Geological Survey (USGS) Earth Explorer (http://earthexplorer.usgs.gov). The USGS platform provides ready-to-use surface reflectance Landsat data processed by the Earth Resources Observation and Science (EROS) Science Processing Architecture’s (ESPA) on-demand interface, the Landsat Surface Reflectance Code (LaSRC) [87]. Extra care was taken in selecting the images in the same season/month–date range (February to March, i.e., growing season) to increase the accuracy of the research results and the vegetation reflection data with a cloud cover of less than 10%. The shapefile was imported to ArcGIS Pro software. To scale the data to reflectance, the data were processed using Modelbuilder and iterators raster tools in ArcGIS Pro, and each raster image was multiplied by the scaling factor of 0.0000275 + −0.2 using the raster calculator.
The NDVI image set was used to classify the Landsat satellite pattern and to determine the change in the vegetation cover distribution of the study area. The NDVI remote sensing method displays the health and greenness (relative biomass) of the vegetation and measures the state of the plants’ health based on the plants’ reflection of light at certain frequencies. The band combination of channels that are used to obtain coverage of the vegetation indices’ characteristics was selected. The NDVI is calculated as the ratio of the difference between the red and near-infrared signal of the electrometric spectrum divided by the sum of both, which refers to the spectral bands 4 and 5. The NDVI value ranges between −1.0 and +1.0, and reflects the health of plants (greens). An NDVI value of 0.6 to 1 represents dense vegetation cover, 0.4 to 0.6 represents moderate vegetation cover, 0.2 to 0.4 represents sparse vegetation cover, 0.1 to 0.2 shows grass cover with bare space, and −1 to 0.1 represents no vegetation, i.e., water cover [88].

3. Statistical Analysis

We derived the numbers of foraging visits of the two troops from the total observations of the troops in the field, as seen either in the natural or the human-modified habitat. A count data statistical model, the generalised linear model (GLM) with Poisson errors, was used to compare the overall number of foraging visits to human-modified and natural habitats by the two baboon troops. All statistical analyses were conducted in SPSS v. 28 (IBM, New York, NY, USA). The number of foraging visits in each environment was fitted as the response variable, while the troop names and types of habitats were the categorical variables.
Another GLM was run to compare the frequency of observations in which the baboon troops were seen feeding and moving. The predictor variables entailed baboon activities (i.e., feeding and moving) while their frequencies were fitted as the response variable. Because of high data variance, negative binomial errors were used.
For the six dominant fruiting plant species, we compared the number of intact seeds obtained from the faecal samples using GLM. The plant species were fitted as the predictor variables, while the numbers of seeds were the response variables.
The potential seed dispersal distances for the baboons were determined using allometry equations (after [78]) in combination with the actual distances measured from the sleeping sites of each baboon troop to the furthest location reached during foraging. The average distance was calculated from the above two values.
The number of seeds likely to be transported by the baboons was estimated as a product of the average seed load per faecal sample, the total number of adult baboons, and the number of monitoring days in which the troops foraged at the site during the study.
To analyse the NDVI trends during the study period (1978–2023), different proportions of vegetation cover class in hectares and converted to percentages were used to quantify the potential vegetation cover change in the study site.

4. Results

The two troops of baboons showed significantly a greater foraging frequency in human-modified than in natural habitats (Wald χ2 = 70.0; df = 1; p < 0.001), and the pattern was similar for both of the baboon troops: Evie (Wald χ2 = 19.7; df = 1; p < 0.0001; Nola (Wald χ2 = 49.0; df = 1; p < 0.0001). Overall, the two chacma baboon troops were not significantly different in their number of daily foraging visits (Wald χ2 = 0.27; df = 1; p = 0.603; Figure 5).
Both baboon troops displayed a significantly greater frequency of feeding activity (Person χ2 = 29.6; df = 1; p < 0.0001; 330 out of 534) and moving activity than other activities recorded during the study (Person χ2 = 287.7; df = 1; p < 0.0001; 474 out of 534).
Overall, eighteen fruiting shrubs/trees were observed in the study area. There were significant differences in the numbers of intact seeds among the six different fruiting plant species recorded in the areas visited by the baboon troops (Wald χ2 = 217.4; df = 5; p < 0.0001; Table 1). They entailed five alien shrubs and one indigenous shrub species. The estimated number of seeds of fruiting species exploited by the baboons in Hogsback were 82.2 ± 13.3% (n = 284) for Acacia mearnsii; 78.9 ± 12.1% (n = 231) for Pinus patula, and 64.0 ± 20.0% (n = 108) for Solanum mauritianum.
Based on the total troop size and the number of observation days, it was estimated that the two baboon troops could transport 445,536 seeds of the six focal fruiting plant species documented during the study period.
It was also estimated that the baboons could disperse seeds over an average distance >5 km for each daily foraging activity (Table 2).
The overall NDVI shows that the change in vegetation cover is the result of bush encroachment in the study areas between 1978 and 2023. The predominant vegetation in the forest biome’s ‘dense vegetation cover’ has expanded by 80.9 ha over 45 years (88.8 to 97.4%; Figure 6). Conversely, the moderate vegetation and sparse vegetation covers have collectively decreased by 10.3 ha (Figure 6).

5. Discussion

The baboons’ foraging preference for domestic gardens creates human–wildlife conflict and accounts for a significant decline in species that were once abundant [55]. In this study, we show that chacma baboons also have the potential to spread the ingested seeds of fleshy-fruited alien and invasive plant species consumed in domestic gardens, although alien plant resources are important food supplements [76]. This may deprive indigenous plant species of reproductive ecological services (i.e., pollination and seed dispersal [50]) that are essential for plant recruitment and the maintenance of the threatened Amathole forest in Hogsback, Eastern Cape Province.
Because the foraging visits frequencies of vertebrates on fruit resources influence seed dispersal effectiveness [76,77], the significantly high foraging preference of chacma baboons towards the human-modified habitats of Hogsback supports the prediction that baboons may transport the seeds of invasive alien plant species. The orchards and gardens are reportedly a major source of alien plant propagules [55,56,57,89,90], and are indeed a major resource for native animals where indigenous forests have been cleared [76]. In the absence of the rare and large indigenous fruits preferred by large mammal frugivores [57,91,92,93,94], the baboons may opt for the large fruit crops of the alien plant species in gardens [35], which deprives the natural vegetation of seed dispersal services. This is concerning, since invasive plant species are known to alter habitat functionality and damage biodiversity [52,53].
Primates (e.g., Papio species) are known to be effective dispersal vectors, transporting huge seed loads in Africa [23,94,95,96]. Our consistent finding that the chacma baboon troops may transport many intact seeds from the six fruiting plant species is likely a result of the prevalence of these species in the human-modified habitat of Hogsback and on forest edges where they become established over time. We argue that baboons might effectively disperse seeds from the fleshy-fruited S. mauritianum and Rubus cuneifolius in Hogsback, as suggested by Kunz and Linsenmair [21], since they often eat the ripe and colourful fruits in the forest [94,97,98]. Lotter et al. [99] also associated the infestation of the invasive Opuntia stricta in Kruger National Park, South Africa with seed dispersal due to the foraging of chacma baboons. In contrast, chacma baboons are partly seed predators that depend on the nature of the fruits [14,25,96], and Kunz and Linsenmair [21] reported that predation effects are suffered by dry seeds while fleshy fruits with smaller seeds can be effectively dispersed. Since the foraging site was mainly dominated by invasive A. mernsii and P. patula (i.e., having dry seeds), we suggest that significant proportions of their seeds were likely to be masticated by the baboons, which could suppress their dispersal as soft-coated seeds and their establishment, leading to the further invasion of hard-coated seeds. In addition, the asynchronous fruiting pattern of S. mauritianum, which concurrently keeps many unripe and immature and a few ripe fruits/berries in the infructescence for foraging frugivores [34,58], can reduce seed dispersal effectiveness, since immature seeds will not geminate [58,98,100]. A similar phenomenon has been previously reported for baboons feeding on the fruits of the Baobab (Adansonia digitata) in South Africa [99].
It has been proposed that large mammal vectors are likely to produce clumped dispersal patterns [81] because of their constant daily foraging movement patterns in combination with the use of permanent sleeping sites in a particular landscape [101]. We argue that an absence of clumped seed dispersal, against the study’s prediction and the report by Kunz [28], is likely to be physiologically driven by laxative alkaloids in the foliage and the fruits of alien plant species, especially S. mauritianum [102,103,104]. This finding was unexpected, since, during the study, the baboons spent 38% of their time eating and because the fruit resources were abundant. It seems that the baboons intermittently defecate as they traverse the habitat. Also, we speculate that the rugged terrain of the study site allows floods to wash away some dispersed/defecated seeds during the rainy season, and thus conceal clear patterns, although this may provide secondary dispersal services. Nevertheless, the seeds that are retained in the gut are likely dispersed over long distances (>5 km), and this is known to facilitate the establishment of new alien plant populations [105]. In combination with biophysical disturbance and the arrival of new alien plant propagules [106], there is a high possibility of alien plant invasion occurring in the Amathole forest, and infiltration by alien and invasive plant species may result in the deterioration of forest resilience. We consistently observed an increase in woody vegetation cover and a decrease in sparse vegetation spatial coverages, which supports our proposal that new-recruiting alien plant species are likely to drive change in the forest’s integrity. In addition, the observed change may be expedited by the local timber plantations that have transformed the native forest’s ecological supporting vegetation units that reportedly bolster the resilience of critical biodiversity areas in South Africa [88,107].
In conclusion, we have shown that the foraging of chacma baboons in domestic gardens encourages the spread of alien and invasive plants’ seeds in Hogback, and that this is a conservation threat to the protection of the Amathole forest in South Africa. We recommend eradicating the alien and invasive plants and rehabilitating the areas that will be cleared to allow for the regrowth of indigenous species. Alternatively, baboons in the African savanna and forest habitats masticate dry seeds [93,97,108,109], and the foraging of partially ripe fruits of S. mauritianum may result in the dispersal of immature seeds that do not germinate, which would thwart the effective seed dispersal. Since fruit resource distribution influences foraging movement patterns [109], we suggest that the observed foraging movement patterns of the chacma baboons during this study were skewed by the availability of food resources in the human-modified habitat, which may greatly reduce seed dispersal services for indigenous plants in the threatened Amathole forest. While the contribution of the baboons to the seed dispersal of alien and invasive plants was not known in Hogsback, we acknowledge that the prevalence of the invasive A. mernsii, P. patula, and S. mauritianum in the local habitat could be partly driven by the bird-mediated dispersal of highly viable seeds (i.e., greater than 80% [110,111,112,113]). According to the South African National Regulations for Biological Invasions (the National Environmental Management: Biodiversity Act [NEM:BA, Act 10 of 2004] and the Alien and Invasive Species Regulation of 2014 revised in 2020), S. mauritianum and R. cuneifolius are habitat transformers, and thus must be controlled and, where possible, removed and destroyed; trade or planting is also strictly prohibited. Lesica and Shelly [113] reported that the continuous removal of the invasive Arabis fecunda improved the survival and population performance of the native fruiting species in the northwestern USA. Further, quantitative studies investigating the diversity of the plant species dispersed, their germination rates after ingestion by baboons, and their seasonal patterns are required to understand the baboon seed dispersal systems in the Amathole forests of Hogsback.

Author Contributions

Conceptualization, L.P. and T.M.M.; methodology, L.P., T.M.M. and L.R.V.; software, T.M.M. and L.R.V.; validation, T.M.M., L.R.V. and L.P.; formal analysis, T.M.M. and L.R.V.; investigation, L.P., T.M.M. and L.R.V.; resources, L.P. and T.M.M.; data curation, T.M.M. and L.R.V.; writing—original draft preparation, L.P. and T.M.M.; writing—review and editing, LR, visualization, T.M.M. and L.R.V.; supervision, T.M.M.; project administration, L.P. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by National Research Foundation grant 92541 awarded to J.C. Masters. The late Prof. J.C. Masters and Dr. F. Génin provided insightful comments on the MS drafts, and this MS is dedicated to them. The Centre for Invasion Biology partly funded the field trips for the study.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data available on request.

Acknowledgments

Ken Harvey contributed field visuals to the study.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Terborgh, J.; Pitman, N.; Silman, M.; Schichter, H.; Nunez, P.V. Maintenance of tree diversity in tropical forests. In Seed Dispersal and Frugivory: Ecology, Evolution and Conservation; Levey, D.J., Silva, W.R., Galetti, M., Eds.; CABI Publishing: New York, NY, USA, 2002; pp. 351–364. [Google Scholar]
  2. Howe, H.F.; Smallwood, J. Ecology of Seed Dispersal. Annu. Rev. Ecol. Syst. 1982, 13, 201–228. [Google Scholar] [CrossRef]
  3. Gómez, J.M.; Verdú, M. Mutualism with plants drives primate diversification. Syst. Biol. 2012, 61, 567–577. [Google Scholar] [CrossRef] [PubMed]
  4. Herrera, C.M. Seed dispersal by vertebrates. In Plant-Animal Interactions: An Evolutionary Approach; Herrera, C.M., Pellmyr, O., Eds.; Blackwell Publishing: Oxford, UK, 2003; pp. 185–208. [Google Scholar]
  5. Jordano, P. Fruits and frugivory. In Seeds: The Ecology of Regeneration in Natural Plant Communities; Fenner, M., Ed.; CABI Publishers: Wallingford, UK, 2000; pp. 125–166. [Google Scholar]
  6. Bufalo, F.S.; Galleti, M.; Culot, L. Seed Dispersal by Primates and Implications for the Conservation of a Biodiversity Hotspot, the Atlantic Forest of South America. Int. J. Primatol. 2016, 37, 333–349. [Google Scholar] [CrossRef]
  7. Chapman, C.A.; Russo, S.E. Primate seed dispersal. In Primates in Perspective; Oxford University Press: New York, NY, USA, 2007; pp. 510–525. [Google Scholar]
  8. Sengupta, A.; McConkey, K.R.; Radhakrishna, S. Primates, provisioning and plants: Impacts of human cultural behaviours on primate ecological functions. PLoS ONE 2015, 10, e0140961. [Google Scholar] [CrossRef] [PubMed]
  9. Sengupta, A.; Radhakrishna, S. Fruit trait preference in rhesus macaques (Macaca mulatta) and its implications for seed dispersal. Int. J. Primatol. 2015, 36, 999–1013. [Google Scholar] [CrossRef]
  10. Chapman, C.A. Primate seed dispersal: Coevolution and conservation implications. Evol. Anthropol. Issues News Rev. 1995, 4, 74–82. [Google Scholar] [CrossRef]
  11. Chaves, O.M.; Bicca-Marques, J.C.; Chapman, C.A. Quantity and quality of seed dispersal by a large arboreal frugivore in small and large Atlantic forest fragments. PLoS ONE 2018, 3, e0193660. [Google Scholar] [CrossRef]
  12. Johnson, C.E.; Tafoya, K.A.; Beck, P.; Concilio, A.; White, K.E.; Quirós, R. Primate richness and abundance is driven by both forest structure and conservation scenario in Costa Rica. PLoS ONE 2023, 18, e0290742. [Google Scholar] [CrossRef]
  13. Reed, K.E.; Bidner, L.R. Primate communities: Past, present, and possible future. Am. J. Phys. Anthropol. 2004, 125, 2–39. [Google Scholar] [CrossRef]
  14. Swedell, L. Baboon Ecology. Available online: http://www.imfene.org/baboon-biology/baboon-ecology (accessed on 7 July 2017).
  15. Tew, E.; Landman, M.; Kerley, G.I.H. The Contribution of the Chacma Baboon to Seed Dispersal in the Eastern Karoo, South Africa. Afr. J. Wildl. Res. 2018, 48, 1–8. [Google Scholar] [CrossRef]
  16. Bueno, R.S.; Guevara, R.; Ribeiro, M.C.; Culot, L.; Bufalo, F.S.; Galetti, M. Functional redundancy and complementarities of seed dispersal by the last neotropical megafrugivores. PLoS ONE 2013, 8, e56252. [Google Scholar] [CrossRef] [PubMed]
  17. Julliot, C. Impact of seed dispersal by red howler monkeys Alouatta seniculus on the seedling population in the understory of tropical rain forest. J. Ecol. 1997, 85, 431–440. [Google Scholar] [CrossRef]
  18. Lambert, J.E. Seed handling in chimpanzees (Pan troglodytes) and redtail monkeys (Cercopithecus ascanius): Implications for understanding hominoid and cercopithecine fruit-processing strategies and seed dispersal. Am. J. Phys. Anthropol. 1999, 109, 365–386. [Google Scholar] [CrossRef]
  19. Stevenson, P.R. Estimates of the number of seeds dispersed by a population of primates in a lowland forest in western Amazonia. In Seed Dispersal: Theory and Its Application in a Changing World; Dennis, A.J., Schupp, E.W., Green, R.J., Westcott, D.A., Eds.; Biddles Ltd.: King’s Lynn, UK, 2007; pp. 340–362. [Google Scholar]
  20. Wrangham, R.W.; Chapman, C.A.; Chapman, L.J. Seed dispersal by forest chimpanzees. J. Trop. Ecol. 1994, 10, 355–368. [Google Scholar] [CrossRef]
  21. Kunz, B.K.; Linsenmair, K.E. Fruit Traits in Baboon Diet: A comparison with plant species characteristics in west Africa. Biotropica 2010, 42, 363–371. [Google Scholar] [CrossRef]
  22. Schurr, F.M.; Spiegel, O.; Steinitz, O.; Trakhtenbrot, A.; Tsoar, A.; Nathan, R. Long-distance seed dispersal. Annu. Plant Rev. 2009, 38, 204–237. [Google Scholar] [CrossRef]
  23. Segal, C. Foraging Behaviour and Diet in Chacma Baboons in Suikerbosrand Nature Reserve. Master’s Thesis, University of the Witwatersrand, Johannesburg, South Africa, 2008. [Google Scholar]
  24. Slater, K.; du Toit, J.T. Seed dispersal by chacma baboons and synoptic ungulates in southern African savannas. South Afr. J. Wildl. Res. 2002, 32, 75–79. [Google Scholar]
  25. Albert, A.; Savini, T.; Huynen, M.C. The role of Macaca spp (primates Cercopithecidae) in seed dispersal networks. Raffles Bull. Zool. 2013, 61, 423–434. [Google Scholar]
  26. Gautier-Hion, A. La dissemination des graines par les cercopithecides forestiers Africains. Terre Vie 1984, 39, 159–165. [Google Scholar] [CrossRef]
  27. Gautier-Hion, A.; Duplantier, J.M.; Quris, R.; Feer, F.; Sourd, C.; Decous, J.P.; Doubost, G.; Emmons, L.; Erard, C.; Hecketsweiler, P.; et al. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 1985, 65, 324–337. [Google Scholar] [CrossRef]
  28. Kunz, B.K. Frugivory and Seed Dispersal: Ecological Interactions between Baboons, Plants, and Dung Beetles in the Savanna-Forest Mosaic of West Africa. Ph.D. Thesis, University of Würzburg, Würzburg, Germany, 2008. [Google Scholar]
  29. Barnes, M.E. Seed predation, germination and seedling establishment of Acacia erioloba in northern Botswana. J. Arid. Environ. 2001, 49, 541–554. [Google Scholar] [CrossRef]
  30. Linden, B.; Linden, J.; Fischer, F.; Linsenmair, K.E. Seed dispersal by South Africa’s only forest-dwelling guenon, the samango monkey (Cercopithecus mitis). Afr. J. Wildl. Res. 2015, 45, 88–99. [Google Scholar] [CrossRef]
  31. Spennemann, D.H.R. Frugivory and seed dispersal revisited: Codifying the plant-centred net benefit of animal-mediated interactions. Flora 2020, 263, 151534. [Google Scholar] [CrossRef]
  32. Chave, J.; Muller-Landau, H.C.; Levin, S.A. Comparing classical community models: Theoretical consequences for patterns of diversity. Am. Nat. 2002, 159, 1–23. [Google Scholar] [CrossRef] [PubMed]
  33. Bitani, N.; Shivambu, T.C.; Shivambu, N.; Downs, C.T. An impact assessment of alien invasive plants in South Africa generally dispersed by native avian species. NeoBiota 2022, 74, 189–207. [Google Scholar] [CrossRef]
  34. Mokotjomela, T.M.; Musil, C.F.; Esler, K.J. Do frugivorous birds concentrate their foraging activities on those alien plants with the most abundant and nutritious fruits in the South African Mediterranean-climate region? Plant Ecol. 2013, 214, 49–59. [Google Scholar] [CrossRef]
  35. Trakhtenbrot, A.; Nathan, R.; Perry, G.; Richardson, D.M. The importance of long distance dispersal in biodiversity conservation. Divers. Distrib. 2005, 11, 173–181. [Google Scholar] [CrossRef]
  36. Traveset, A.; Richardson, D.M. Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol. Evol. 2006, 21, 208–216. [Google Scholar] [CrossRef]
  37. Richardson, D.M.; Pyšek, P.; Rejma’nek, M.; Barbour, M.G.; Panetta, F.D.; West, C.J. Naturalization and invasion of alien plants—Concepts and definitions. Divers. Distrib. 2000, 6, 93–107. [Google Scholar] [CrossRef]
  38. Rejmanek, M. Species richness and resistance to invasions. In Biodiversity and Ecosystem Processes in Tropical Forests; Orians, G.H., Dirzo, R., Cushman, J.H., Eds.; Springer: Berlin/Heidelberg, Germany, 1996; pp. 153–172. [Google Scholar]
  39. Rejmanek, M.; Richardson, D.M.; Pysek, P. Plant invasions and invasibility of plant communities. In Vegetation Ecology; van der Maarel, E., Ed.; Oxford: Blackwell, UK, 2005; pp. 332–355. [Google Scholar]
  40. Debussche, M.; Isenmann, P. Fleshy fruit characters and the choices of bird and mammal seed dispersers in a Mediterranean region. Oikos 1989, 56, 327–338. [Google Scholar] [CrossRef]
  41. Richardson, D.M.; Rejmánek, M. Trees and shrubs as invasive alien species—A global review: Global review of invasive trees & shrubs. Divers. Distrib. 2011, 17, 788–809. [Google Scholar] [CrossRef]
  42. Pebsworth, P. Feeding ecology of chacma baboons (Papio ursinus) living in a human-modified environment. Afr. J. Ecol. 2020, 58, 319–326. [Google Scholar] [CrossRef]
  43. Muller-Landau, H.C.; Hardesty, B.D. Seed dispersal of woody plants in tropical forests: Concepts, Examples, and Future Directions. In Biotic Interactions in the Tropics: Their Role in the Maintenance of Species Diversity; Burslem, D., Pinard, M., Hartley, S., Eds.; Cambridge University Press: Cambridge, UK, 2005; pp. 267–309. [Google Scholar]
  44. Fleming, T.H.; Kress, W.J. The Ornaments of Life: Coevolution and Conservation in the Tropics; The University of Chicago Press: Chicago, IL, USA, 2013; p. 588. [Google Scholar]
  45. Mucina, L.; Rutherford, M.C. (Eds.) The Vegetation of South Africa, Lesotho and Swaziland; Strelitzia 19; South African National Biodiversity Institute: Pretoria, South Africa, 2006. [Google Scholar]
  46. Leaver, J.; Cherry, M.I. Forest product harvesting in the Eastern Cape, South Africa: Impacts on habitat structure. S. Afr. J. Sci. 2020, 116, 1–9. [Google Scholar] [CrossRef]
  47. Chapman, C.A.; Lawes, M.J.; Eeley, H.A.C. What hope for African primate diversity? Afr. J. Ecol. 2006, 44, 116–133. [Google Scholar] [CrossRef]
  48. Eeley, H.A.C.; Lawes, M.J.; Piper, S.E. The influence of climate change on the distribution of indigenous forest in KwaZulu-Natal, South Africa. J. Biogeogr. 1999, 26, 595–617. [Google Scholar] [CrossRef]
  49. Lawes, M.J.; Mealin, P.E.; Piper, S.E. Patch occupancy and potential metapopulation dynamics of three forest mammals in fragmented Afromontane forest in South Africa. Conserv. Biol. 2000, 14, 1088–1098. [Google Scholar] [CrossRef]
  50. Mokotjomela, T.M.; Vukeya, L.R.; Pamla, L.; Scott, Z. The critical role of coastal protected areas in buffering impacts of extreme climatic conditions on bird diversity and their ecosystem services’ provisioning in the Eastern Cape Province, South Africa. Ecol. Evol. 2023, 13, e10452. [Google Scholar] [CrossRef] [PubMed]
  51. von Maltitz, G.; Mucina, L.; Geldenhuys, C.J.; Lawes, M.; Eeley, H.; Aidie, H.; Vink, D.; Fleming, G.; Bailey, C. Classification System for South African Indigenous Forests. An Objective Classification for the Department of Water Affairs and Forestry; Report ENV-P-C 2003-017; Environmentek, CSIR: Pretoria, South Africa, 2003. [Google Scholar]
  52. Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES). Summary for Policymakers of the Thematic Assessment Report on Invasive Alien Species and Their Control of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. IPBES Secretariat. 2023. Available online: https://zenodo.org/records/10521002 (accessed on 22 December 2023).
  53. Van Wilgen, B.W.; Zengeya, T.A.; Richardson, D.M. A review of the impacts of biological invasions in South Africa. Biol. Invasions 2022, 24, 27–50. [Google Scholar] [CrossRef]
  54. Mucina, L.; Geldenhuys, C.J. (Eds.) Afrotemperate, subtropical and azonal forests. In The Vegetation of South Africa, Lesotho and Swaziland; Strelitzia 19; South African National Biodiversity Institute: Pretoria, South Africa, 2006; pp. 585–614. [Google Scholar]
  55. Pamla, L. The Importance of Habitat Use in the Foraging Behaviour of Village Chacma Baboons (Papio Ursinus, Cercopithecidae: Primates) in Hogsback, Eastern Cape. Master’s Thesis, University of Fort Hare, Alice, South Africa, 2016. [Google Scholar]
  56. Richardson, D.M. Forestry trees as invasive aliens. Conserv. Biol. 1998, 12, 18–26. [Google Scholar] [CrossRef]
  57. Quix, J.C. The role of alien plants in the composition of fruit-eating bird assemblages in Brazilian urban ecosystems. Orsis 2007, 22, 87–104. [Google Scholar]
  58. Mokotjomela, T.M. A Comparison of Bird Foraging Preferences for Fruits of Indigenous and Alien Shrubs and Seed Dispersal Potentials in the Cape Floristic Region. Ph.D. Thesis, Stellenbosch University, Stellenbosch, South Africa, 2012. [Google Scholar]
  59. Driver, A.; Sink, K.J.; Nel, J.N.; Holness, S.; Van Niekerk, L.; Daniels, F.; Jonas, Z.; Majiedt, P.A.; Harris, L.; Maze, K. National Biodiversity Assessment 2011: An assessment of South Africa’s Biodiversity and Ecosystems. Synthesis Report; South African National Biodiversity Institute and Department of Environmental Affairs: Pretoria, South Africa, 2011. [Google Scholar]
  60. Webster, J.P.; Gower, C.M.; Knowles, S.C.; Molyneux, D.H.; Fenton, A. One health–an ecological and evolutionary framework for tackling Neglected Zoonotic Diseases. Evol. Appl. 2016, 9, 313–333. [Google Scholar] [CrossRef]
  61. Xulu, S.; Peerbhay, K.; Gebreslasie, M. Remote sensing of forest health and vitality: A South African perspective. South. For. A J. For. Sci. 2018, 81, 91–102. [Google Scholar] [CrossRef]
  62. Dye, P.; Versfeld, D. Managing the hydrological impacts of South African plantation forests: An overview. For. Ecol. Manag. 2007, 251, 121–128. [Google Scholar] [CrossRef]
  63. Scott, D.F.; Le Maitre, D.C.; Fairbanks, D.H.K. Forestry and streamflow reductions in South Africa: A reference system for assessing extent and distribution. Water SA 1998, 24, 187–199. [Google Scholar]
  64. Yeiser, J.L.; Ezell, A.W. Competition control in slash pine (Pinus ellliottii Engelm) plantations. In Slash Pine: Still Growing and Growing! Proceedings of the Slash Pine Symposium. United States, Department of Agriculture, Forest Service; Dickens, E.D., Barnett, J.P., Hubbard, W.G., Jokela, E.J., Eds.; Southern Research Station: Asheville, NC, USA, 2004; pp. 23–25. [Google Scholar]
  65. Tudi, M.; Daniel Ruan, H.; Wang, L.; Lyu, J.; Sadler, R.; Connell, D.; Chu, C.; Phung, D.T. Agriculture development, pesticide application and its impact on the environment. Int. J. Environ. Res. Public Health 2021, 18, 1112. [Google Scholar] [CrossRef]
  66. Rad, S.M.; Ray, A.K.; Barghi, S. Water pollution and agriculture pesticide. Clean Technol. 2022, 4, 1088–1102. [Google Scholar] [CrossRef]
  67. Owen-Smith, N. Foraging responses of kudus to seasonal changes in food resources: Elasticity in constraints. Ecology 1994, 75, 1050–1062. [Google Scholar] [CrossRef]
  68. Kerr, R. The Animal Kingdom or Zoological System of the Celebrated Sir Charles Linnaeus; John Murry: London, UK, 1792. [Google Scholar]
  69. Chowdhury, S.; Brown, J.; Swedell, L. Anthropogenic effects on the physiology and behaviour of chacma baboons in the Cape Peninsula of South Africa. Conserv. Physiol. 2020, 8, coaa066. [Google Scholar] [CrossRef]
  70. Slater, K. Home range utilization by chacma baboon (Papio ursinus) troops on Suikerbosrand Nature Reserve, South Africa. PLoS ONE 2018, 13, e0194717. [Google Scholar] [CrossRef]
  71. Hill, C.M. People, crops, and primates: A conflict of interests. In Commensalism and Conflict: The Human–Primate Interface; Paterson, J.D., Wallis, J., Eds.; The American Society of Primatologists: Norman, OK, USA, 2005; pp. 40–59. [Google Scholar]
  72. Stone, O.M.; Laffan, S.W.; Curnoe, D.; Herries, A.I. The spatial distribution of chacma baboon (Papio ursinus) habitat based on an environmental envelope model. Int. J. Primatol. 2013, 34, 407–422. [Google Scholar] [CrossRef]
  73. Pebsworth, P.A.; MacIntosh, A.J.; Morgan, H.R.; Huffman, M.A. Factors influencing the ranging behavior of chacma baboons (Papio hamadryas ursinus) living in a human-modified habitat. Int. J. Primatol. 2012, 33, 872–887. [Google Scholar] [CrossRef]
  74. McCann, R.; Bracken, A.M.; Christensen, C.; Fuertbauer, I.; King, A.J. The relationship between GPS sampling interval and estimated daily travel distances in chacma baboons (Papio ursinus). Int. J. Primatol. 2021, 42, 589–599. [Google Scholar] [CrossRef]
  75. Altmann, J. Observational study of behaviour: Sampling methods. Behaviour 1974, 49, 227–265. [Google Scholar] [CrossRef] [PubMed]
  76. Mokotjomela, T.M.; Musil, C.F.; Esler, K.J. Frugivorous birds visit fruits of emerging alien shrub species more frequently than those of native shrub species in the South African Mediterranean climate region. S. Afr. J. Bot. 2013, 86, 73–78. [Google Scholar] [CrossRef]
  77. Vazquez, D.P.; Morris, W.F.; Jordano, P. Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecol. Lett. 2005, 8, 1088–1094. [Google Scholar] [CrossRef]
  78. Vukeya, L.R.; Mokotjomela, T.M.; Powrie, L.W.; Nenungwi, L. Determining the critical recruitment needs for the declining population of Olea europaea subsp. africana (Mill.) PS Green in Free State, South Africa. Ecol. Evol. 2023, 13, e10177. [Google Scholar] [CrossRef] [PubMed]
  79. Hill, D.; Tucker, G.; Fasham, M.; Shrewry, M.; Shaw, P. Handbook of Biodiversity Methods: Survey, Evaluation and Monitoring; Cambridge University Press: New York, NY, USA, 2005. [Google Scholar]
  80. Hamilton, W.J. Baboon Sleeping Site Preferences and Relationships to Primate Grouping Patterns. Am. J. Primatol. 1982, 3, 41–53. [Google Scholar] [CrossRef] [PubMed]
  81. Howe, H.F. Scatter-and clump-dispersal and seedling demography: Hypothesis and implications. Oecologia 1989, 79, 417–426. [Google Scholar] [CrossRef]
  82. Steuer, P.; Südekum, K.; Müller DW, H.; Franz, R.; Kaandorp, J.; Clauss, M.; Hummel, J. Is there an influence of body mass on digesta mean retention time in herbivores? A comparative study on ungulates. Comp. Biochem. Physiol. A 2011, 160, 355–364. [Google Scholar] [CrossRef]
  83. McQualter, K.; Chase, M.; Fennessy, J.; McLeod, S.; Leggett, K. Home ranges, season alranges and daily movements of giraffe (Giraffa camelopardalis giraffa) in Northern Botswana. Afr. J. Ecol. 2015, 54, 99–102. [Google Scholar] [CrossRef]
  84. Msweli, L. Role and Effects of Wild Southern African Ungulates on Seed Dispersal of Selected Alien Invasive Plants. Ph.D. Thesis, University of KwaZulu-Natal-Afrique du Sud, Durban, South Africa, 2021. [Google Scholar]
  85. Saïd, S.; Servanty, S. The influence of landscape structure on female roe deer home-range size. Landsc. Ecol. 2005, 20, 1003–1012. [Google Scholar] [CrossRef]
  86. du Toit, J. Homerange-body mass relations: A field study on African browsing ruminants. Oecologia 1990, 85, 301–303. [Google Scholar] [CrossRef]
  87. Urban, M.; Berger, C.; Mudau, T.E.; Heckel, K.; Truckenbrodt, J.; Onyango Odipo, V.; Smit, I.P.; Schmullius, C. Surface moisture and vegetation cover analysis for drought monitoring in the southern Kruger National Park using Sentinel-1, Sentinel-2, and Landsat-8. Remote Sens. 2018, 10, 1482. [Google Scholar] [CrossRef]
  88. Vukeya, L.R.; Mokotjomela, T.M.; Malebo, N.J.; Smith, D.A.E.; Oke, S. The vegetation cover dynamics and potential drivers of habitat change over 30 years in the Free State National Botanical Garden, South Africa. Reg. Environ. Chang. 2023, 23, 24. [Google Scholar] [CrossRef]
  89. Takahashi, M.Q.; Rothman, J.M.; Cords, M. The role of non-natural foods in the nutritional strategies of monkeys in a human-modified mosaic landscape. Biotropica 2023, 55, 106–118. [Google Scholar] [CrossRef]
  90. Mokotjomela, T.M.; Nemurangoni, T.; Mundalamo, T.; Jaca, T.P.; Kuhudzai, A.G. The value of dump sites for monitoring biological invasions in South Africa. Biol. Invasions 2022, 24, 971–986. [Google Scholar] [CrossRef]
  91. Martínez, I.; García, D.; Obeso, J.R. Differential seed dispersal patterns generated by a common assemblage of vertebrate frugivores in three fleshy-fruited trees. Ecoscience 2008, 15, 189–199. [Google Scholar] [CrossRef]
  92. Sobral, M.; Larrinaga, A.R.; Guitian, J. Fruit-size preferences in wild and naive Eurasian blackbirds (Turdus merula) feeding on one seed hawthorn (Crataegus Monogyna). Auk 2010, 127, 532–539. [Google Scholar] [CrossRef]
  93. Sebastián-González, E.; Pires, M.M.; Donatti, C.I.; Guimarães, P.R., Jr.; Dirzo, R. Species traits and interaction rules shape a species-rich seed-dispersal interaction network. Ecol. Evol. 2017, 7, 4496–4506. [Google Scholar] [CrossRef]
  94. Hill, R.A. Ecological and Demographic Determinants of Time Budgets in Baboons: Implications for Cross-Populational Models of Baboon Socioecology. Ph.D. Thesis, University of Liverpool, Liverpool, UK, 1999. [Google Scholar]
  95. Kunz, B.K.; Linsenmair, K.E. The role of the olive baboon (Papio anubis, Cercopithecidae) as seed disperser in a savannah-forest mosaic of West Africa. J. Trop. Ecol. 2008, 24, 235–246. [Google Scholar] [CrossRef]
  96. Lambert, J.E. Exploring the link between animal frugivory and plant strategies: The case of primate fruit processing and post-dispersal fate. In Seed Dispersal and Frugivory: Ecology, Evolution and Conservation; Levey, D.J., Silva, W.R., Galetti, M., Eds.; CAB International: Wallingford, UK, 2002; pp. 365–379. [Google Scholar]
  97. Lambert, J.E.; Garber, P.A. Evolutionary and Ecological Implications of Primate Seed Dispersal. Am. J. Primatol. 1998, 45, 9–28. [Google Scholar] [CrossRef]
  98. Altmann, S.A. Foraging for Survival; University of Chicago Press: Chicago, IL, USA, 1998. [Google Scholar]
  99. Lotter, W.D.; Thatcher, L.; Rossouw, L.; Reinhardt, C.F. The influence of baboon predation and time in water on germination and early establishment of Opuntia stricta (Australian pest pear) in Kruger National Park. Koedoe 1999, 42, 43–50. [Google Scholar] [CrossRef]
  100. Venter, S.M.; Witkowski, E.T.F. Baobab (Adansonia digitata L.) fruit production in communal and conservation land-use types in Southern Africa. For. Ecol. Manag. 2011, 261, 630–639. [Google Scholar] [CrossRef]
  101. Kleyheeg, E.; van Dijk, J.G.; Nolet, B.A.; Tsopoglou-Gkina, D.; Woud, T.; Boonstra, D.; Soons, M.B. Daily movement distances and home range sizes of mallards (Anas platyrhynchos) are strongly affected by landscape configuration. Seed Dispersal A Gen. Duck 2017, 101. [Google Scholar]
  102. Cowie, B.W. Bugweed Biocontrol: New Insights into the Biological Control Agents of Solanum Mauritianum, Gargaphia Decoris and Anthonomus Santacruzi. Master’s Thesis, University of Witwatersrand, Johannesburg, South Africa, 2016. [Google Scholar]
  103. Cipollini, M.L.; Levey, D.J. Secondary metabolites of fleshy vertebrate-dispersed fruits: Adaptive hypotheses and implications for seed dispersal. Am. Nat. 1997, 150, 346–372. [Google Scholar] [CrossRef]
  104. Mokotjomela, T.M.; Downs, C.T.; Esler, K.; Knight, J. Seed dispersal effectiveness: A comparison of four bird species feeding on seeds of invasive Acacia cyclops in South Africa. S. Afr. J. Bot. 2016, 105, 259–263. [Google Scholar] [CrossRef]
  105. Vukeya, L.R.; Mokotjomela, T.M.; Malebo, N.J.; Saheed, O. Seed dispersal phenology of encroaching woody species in the Free State National Botanical Garden, South Africa. Afr. J. Ecol. 2022, 60, 723–735. [Google Scholar] [CrossRef]
  106. Le Roux, J.J.; Clusella-Trullas, S.; Mokotjomela, T.M.; Mairal, M.; Richardson, D.M.; Skein, L.; Wilson, J.R.; Weyl, O.L.; Geerts, S. Biotic interactions as mediators of biological invasions: Insights from South Africa. Biol. Invasions S. Afr. 2020, 35, 387–427. [Google Scholar]
  107. Tolley, K.A.; Da Silva, J.M.; Jansen van Vuuren, B.; Bishop, J.; Dalton, D.; Du Plessis, M.; Labuschagne, K.; Kotze, A.; Masehela, T.; Suleman, E. South African National Biodiversity Assessment 2019: Technical Report Volume 7: Genetic Diversity. Available online: http://researchspace.csir.co.za/dspace/handle/10204/11471 (accessed on 22 December 2023).
  108. Perry, G.L.; Enright, N.J.; Miller, B.P.; Lamont, B.B. Do plant functional traits determine spatial pattern? A test on species-rich shrublands, Western Australia. J. Veg. Sci. 2013, 24, 441–452. [Google Scholar] [CrossRef]
  109. Bunney, K. Seed dispersal in South African Trees: With a Focus on the Megafaunal Fruit and Their Dispersal Agents. Master’s Thesis, University of Cape Town, Cape Town, South Africa, 2014. [Google Scholar]
  110. Corlett, R.T. Frugivory and seed dispersal by vertebrates in tropical and subtropical Asia: An update. Glob. Ecol. Conserv. 2017, 11, 1–22. [Google Scholar] [CrossRef]
  111. Webster, J. Ethical and animal welfare considerations in relation to species selection for animal experimentation. Animals 2014, 4, 729–741. [Google Scholar] [CrossRef] [PubMed]
  112. Witkowski, E.T.F.; Garner, R.D. Seed production, seed bank dynamics, resprouting and long-term response to clearing of the alien invasive Solanum mauritianum in a temperate to subtropical riparian ecosystem. S. Afr. J. Bot. 2008, 74, 476–484. [Google Scholar] [CrossRef]
  113. Lesica, P.; Shelly, J.S. Competitive effects of Centaurea maculosa on the population dynamics of Arabis fecunda. Bull. Torrey Bot. Club 1996, 123, 111–121. [Google Scholar] [CrossRef]
Figure 1. Map of Hogsback study site (red box) in Eastern Cape, South Africa (A). (B) shows the vegetation types, and (C) shows the natural and human environments within the study site.
Figure 1. Map of Hogsback study site (red box) in Eastern Cape, South Africa (A). (B) shows the vegetation types, and (C) shows the natural and human environments within the study site.
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Figure 2. Male chacma baboon on the edge of the mountain, Hogsback in Eastern Cape Province, South Africa (picture: Ken Harvey).
Figure 2. Male chacma baboon on the edge of the mountain, Hogsback in Eastern Cape Province, South Africa (picture: Ken Harvey).
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Figure 3. Foraging paths of the focal baboon troops. The red colour shows Nola’s troop’s range, and the blue colour shows Evie’s troop’s range. The orange polygon shows the overlap between the foraging home ranges of the two troops.
Figure 3. Foraging paths of the focal baboon troops. The red colour shows Nola’s troop’s range, and the blue colour shows Evie’s troop’s range. The orange polygon shows the overlap between the foraging home ranges of the two troops.
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Figure 4. Chacma baboon faecal sample that is not crushed (above) and crushed with a stick (below) containing seeds processed during foraging.
Figure 4. Chacma baboon faecal sample that is not crushed (above) and crushed with a stick (below) containing seeds processed during foraging.
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Figure 5. Daily mean foraging visits frequency of Evie’s and Nola’s troops in the human-modified and natural habitats. The standard error is represented by the bars.
Figure 5. Daily mean foraging visits frequency of Evie’s and Nola’s troops in the human-modified and natural habitats. The standard error is represented by the bars.
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Figure 6. Variation in the normalised difference vegetation index for Hogsback areas (the study site) between 1978 and 2023.
Figure 6. Variation in the normalised difference vegetation index for Hogsback areas (the study site) between 1978 and 2023.
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Table 1. Significant differences between the number of intact seeds of fruiting alien plants preferentially consumed by the chacma baboons in Hogsback shown by the generalised linear models (GLMs). Superscript “a” represents a parameter that was selected as a reference for comparison of the significance. *** native plant species.
Table 1. Significant differences between the number of intact seeds of fruiting alien plants preferentially consumed by the chacma baboons in Hogsback shown by the generalised linear models (GLMs). Superscript “a” represents a parameter that was selected as a reference for comparison of the significance. *** native plant species.
Plant Species Hypothesis Test
χ2Dfp-Value
Overall test model217.32850.000
BStd. Error
Rubus cuneifolius−0.9200.108971.35810.000
Cotoneaster pannosus−1.0080.112480.43610.000
Sersia trilobata ***−1.2240.1220100.80810.000
Pine patula−0.0410.08310.24810.618
Solanum mauratianum−0.2480.08787.97610.005
Acacia mearnsii0 a----
Table 2. Potential seed dispersal distances for chacma baboons in Hogsback: Predicted distances were generated using allometry equations, while actual distances were measured over the foraging trails from sleeping sites to the furthest location reached by each troop during foraging.
Table 2. Potential seed dispersal distances for chacma baboons in Hogsback: Predicted distances were generated using allometry equations, while actual distances were measured over the foraging trails from sleeping sites to the furthest location reached by each troop during foraging.
Troop Predicted Distance in km [78]Actual Distance (km)Average (km)
Evie4.47.145.8
Nola4.46.335.4
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Pamla, L.; Vukeya, L.R.; Mokotjomela, T.M. The Potential of Foraging Chacma Baboons (Papio ursinus) to Disperse Seeds of Alien and Invasive Plant Species in the Amathole Forest in Hogsback in the Eastern Cape Province, South Africa. Diversity 2024, 16, 168. https://doi.org/10.3390/d16030168

AMA Style

Pamla L, Vukeya LR, Mokotjomela TM. The Potential of Foraging Chacma Baboons (Papio ursinus) to Disperse Seeds of Alien and Invasive Plant Species in the Amathole Forest in Hogsback in the Eastern Cape Province, South Africa. Diversity. 2024; 16(3):168. https://doi.org/10.3390/d16030168

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Pamla, Lwandiso, Loyd R. Vukeya, and Thabiso M. Mokotjomela. 2024. "The Potential of Foraging Chacma Baboons (Papio ursinus) to Disperse Seeds of Alien and Invasive Plant Species in the Amathole Forest in Hogsback in the Eastern Cape Province, South Africa" Diversity 16, no. 3: 168. https://doi.org/10.3390/d16030168

APA Style

Pamla, L., Vukeya, L. R., & Mokotjomela, T. M. (2024). The Potential of Foraging Chacma Baboons (Papio ursinus) to Disperse Seeds of Alien and Invasive Plant Species in the Amathole Forest in Hogsback in the Eastern Cape Province, South Africa. Diversity, 16(3), 168. https://doi.org/10.3390/d16030168

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