Red List of South African Species

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Least Concern (LC)
Assessors: Birthe Linden Kirsten Wimberger Yvette Ehlers-Smith Matthew Child
Contributors: Lizanne Roxburgh Caroline Howlett
Reviewers: Birthe Linden Kirsten Wimberger Yvette Ehlers-Smith Matthew Child

Rationale

Samango Monkeys are restricted to a variety of forest habitats and comprise three subspecies within the assessment region: Samango Monkey (C. a. labiatus), Stair’s White-collared monkey (C. a. erythrarchus), and Schwarz’s White-collared Monkey (C. a. schwarzi). While C. a. labiatus is endemic to the assessment region, C. a. erythrarchus occurs throughout southern Africa and it is uncertain whether C. a. schwarzi is endemic due to lack of sampling in suitable extra-regional habitats. However, according to current data the latter subspecies is, at this point in time, most likely completely isolated with no rescue effect from neighbouring countries possible. Furthermore, given historical and ongoing forest habitat loss and fragmentation, all three subspecies exist in isolated or semi-isolated forest fragments with a suspected low rate of dispersal. Although the estimated extent of occurrence for all subspecies is > 20,000 km2, area of occupancy was calculated as the amount of remaining natural habitat within forest patches greater than 1.5 km2 in extent (below which, forest patches are generally unoccupied by Samangos), which yielded 870 km2, 692 km2 and 340 km2 for C. a. labiatus, C. a. erythrarchus and C. a. schwarzi respectively.

For all three subspecies, there is an inferred continuing decline in area of occupancy due to ongoing forest habitat loss across the country, a suspected continuing decline in habitat quality from commercial forestry reducing food resources, and a suspected continuing decline in mature individuals from frequent reports of mortality from road collisions, electrocutions, snaring and hunting for traditional medicine. This results in the listings of Vulnerable B2ab(ii,iii,v) for both C. a. labiatus and C. a. erythrarchus, and Endangered B2ab(ii,iii,v) for C. a. schwarzi. Although the extra-regional habitat of C. a. erythrarchus is similarly fragmented, and we do not yet understand the dispersal capacity of Samango Monkeys, its core range is protected by the Lubombo Transfrontier Conservation Area (established in 2000), which has secured corridors between Swaziland, South Africa and Mozambique. Thus, because these northern forests of the South African range of C. a. erythrarchus are formally protected and there is at least the potential for dispersal across boundaries, we down-list C. a. erythrarchus to Near Threatened B2ab(ii,iii,v). Although the minimum estimated population sizes fall below 10,000 mature individuals, and C. a. labiatus and C. a. schwarzi have lower estimates for the largest subpopulation size below 1,000 mature individuals, the huge range in possible population sizes was deemed too great to realistically apply the C criterion without more recent density and occupancy estimates from field surveys.

Although preliminary studies suggest that Samango Monkeys adapt to human-modified habitat by being able to eat exotic plant species planted by people, core forest patches are needed by the species for successful reproduction, recruitment and viability. Extinction risk is thus entirely dependent upon effective management of the Forest Biome. Key interventions correspondingly include enforcement of penalties for forest-related transgression, protected area expansion and the establishment and/or maintenance of corridors between forest patches. Critically, distribution data from the literature need to be collated and surveys of all suitable habitats need to be performed to more accurately delineate range boundaries and occupancy in remaining forest patches. This current assessment should therefore be revised once a more complete dataset is available.

Regional population effects: While C. a. labiatus is confirmed to be endemic to South Africa, and C. a. schwarzi is assumed to be endemic until further research shows otherwise, C. a. erythrarchus is presumably connected to extra-regional subpopulations through the Lubombo Transfrontier Conservation Area and thus we assume rescue effects are possible. Future research should, however, confirm dispersal between countries.

Distribution

Cercopithecus albogularis is distributed from Ethiopia to South Africa and also occurs in southern and eastern Democratic Republic of the Congo and northwestern Angola (Groves 2001, 2005). The current South African Samango Monkey populations are relicts of the repeated historical (Pleistocene and Holocene) expansion and contraction of forests. They are naturally fragmented and, as a result, often isolated. This natural fragmentation is exacerbated by human population expansion and development. Where there might have been connections and dispersal corridors between subpopulations in the past (for example, through riverine corridors), these have been increasingly lost to development and agriculture.

Cercopithecus a. labiatus is endemic to South Africa and has been separated from populations further north in the assessment region for ~1.7 million years (Dalton et al. 2015). The southern limit of C. a. labiatus is the Pirie Forest in the Eastern Cape, it is not found in the evergreen Knysna and Tsitsikamma forests further south (Lawes 1990), and it extends northeastwards to the midlands of the KwaZulu-Natal Province. Its present distribution is closely correlated with the distribution of Afromontane forests within the assessment region (Lawes 1990). It seems to occur in Scarp and Indian Ocean Coastal belt forests, as well as Pondoland forests (Hayward et al. 2005). However, identification of the subspecies there is unknown, and needs to be done via genetic analyses. The boundary between C. a. labiatus and C. a. erythrarchus is currently suspected to be the St. Lucia and Umfolozi River systems (Lawes 1990; Dalton et al. 2015), where apparently neither subspecies are found in the dune forest south of the St. Lucia estuary (Lawes 1992).

Accordingly, C. a. erythrarchus occurs from northern KwaZulu-Natal Province, possibly along southern Mpumalanga Province (Figure 1), through Zimbabwe and Mozambique (although the coastal limits are uncertain) up to Malawi. While this subspecies has been described to extend as far as Malawi, their forest habitat is fragmented (both naturally and through human expansion and development), and thus it is unlikely that there is significant immigration from outside the region, especially as not enough is known yet about individuals’ (especially male) dispersal abilities. In Swaziland they have been recorded from forest patches in Mlawula and Muti Muti Nature Reserves and in some of the larger forested gorges in the eastern Lubombos (for example, Mnyame Gorge) (Monadjem et al. 2003) (Table 1).

The area bordering Swaziland to the north and the area just north of the Umfolozi River and west to the confirmed C. a. erythrarchus range (in the past assigned to C. a. labiatus) are both confirmed C. a. albogularis distribution records. However, at this stage it is not known to which subspecies these distribution records belong (Dalton et al. 2015). For the purposes of this assessment, we have assigned the record to C. a. erythrarchus.

The distribution of C. a. schwarzi comprises Mariepskop in the Pilgrims Rest District, north to the Magoebaskloof area including Woodbush (Mpumalanga Province) (Roberts 1951; Groves 2001), as well as the Soutpansberg mountains (Dalton et al. 2015). It is unknown whether the subspecies is endemic, as possibly suitable locations in the Afromontane forests further north (Eastern Highlands in Zimbabwe and Gorongoza in Mozambique) have not yet been sampled. Consequently, genetic data on subpopulations further north are unavailable for comparison. The Soutpansberg C. a. schwarzi subpopulations are currently most likely isolated from the escarpment C. a. schwarzi subpopulations further south due to a lack of suitable connecting habitat and extensive human-induced landscape change. For this assessment, the area south of Mariepskop along the escarpment to Swaziland has been assigned to C. a. schwarzi. However, future sampling of those populations and genetic analysis will need to be undertaken in order to make a definite assignment to which subspecies they belong.

Samango Monkeys are mostly restricted to intact forest habitat although they will traverse other habitats while foraging or moving between forest patches (Skinner & Chimimba 2005; Linden et al. in prep.(a); Wimberger et al. in prep.), such as pine and blue gum plantations and residential gardens, but patch occupancy seems unaffected by land-use type of the surrounding matrix (Lawes et al. 2000). As such, we construe intact forest patches as a measure of core area of occupancy. Estimating extent of occurrence (EOO) and area of occupancy (AOO) is challenging as the precise range delimitations and current forest patch occupancy has not been determined. However, based on available data and information from the literature (for example, Lawes 1990, 1992; Lawes et al. 2000; Dalton et al. 2015), the estimated EOO is between 21,605 and 90,412 km2 (Table 2). The AOO can be estimated according to all forest patches available (based on the Mucina & Rutherford 2006 vegetation types) within the EOO or from forest patches with current confirmed presence, which, for C. a. labiatus, ranges from 1,109–1,400 km2 (depending on more or less conservative forest patch inclusion) to 702 km2 respectively. The minimum critical forest patch size has been calculated as 0.44 km2 and forest patches < 1.5 km2 were never occupied by Samango Monkeys (Lawes et al 2000). By including only patches above the 1.5 km2 threshold, AOO is estimated to be between 382 and 989 km2 (all available patches). Finally, using current (2014) land-cover satellite data (GeoTerraImage 2015), we estimated the effective AOO as the amount of remaining natural habitat within forest patches, which was 88–89% of the habitat (11–12% modified), which yielded revised AOO estimates of 340 km2, 692 km2 and 870 km2 for C. a. schwarzi, C. a. erythrarchus and C. a. labiatus respectively (Table 2).

The effective AOO is likely to be less when dispersal distances (3.7 km) between known occupied forest patches are taken into consideration (Lawes et al. 2000). Indeed, Lawes et al. (2000) found that only 7% of forest patches were occupied in the Balgowan and Karkloof districts of KwaZulu-Natal Province. Similarly, only 11–17% of the forest patches are above the 1.5 km2 threshold for the various subspecies and thus suspected to be occupied by viable subpopulations (Table 2).

Population trend

Trend

The population density of C. albogularis varies greatly with the habitat type occupied, but they can be common in suitable habitat. In South Africa, lowest densities are found in swamp, sand and riverine forests (< 30 individuals / km2), medium densities in Afromontane forests (44–83 individuals / km2) and highest densities in coastal forests (200 individuals / km2) (Lawes 1992). C. a. labiatus in general have lower population densities than C. a. erythrarchus (Lawes 1992). Home range size varied from 0.46 km2 for C. a. schwarzi in the Soutpansberg (Limpopo Province) (Heikamp 2008) to 0.22 km2 and 0.27 km2 for C. a. labiatus in Hogsback (K. Wimberger unpubl. data) to 0.15 km2 for C. a. erythrarchus in Cape Vidal (KwaZulu-Natal Province), with densities of between 145 individuals / km2 and 202 individuals / km2 (Lawes & Henzi 1995). Table 3 shows the population and largest subpopulation estimates (using the largest forest patch per subspecies as a proxy) for the three subspecies based on maximum and minimum densities using the effective AOO estimates listed in Table 2. The number of mature individuals per troop varies from 40–50% (Friedmann & Daly 2004; Linden et al. 2015). Although the minimum estimates are below 10,000 mature individuals, and two subspecies contain lower estimates of < 1,000 mature individuals in the largest subpopulation, the range in mature individuals is too great to estimate a population size of <10,000 mature individuals for any subspecies. Further surveying will help to refine occupancy of forest patches and subsequently subpopulation sizes.

For the subspecies with the largest AOO, C. a. labiatus, Table 4 shows the probable subpopulation sizes in various forest types for currently occupied forest patches above the 1.5 km2 threshold. The analysis still yields over 10,000 mature individuals within the assessment region. However, this approach should be replicated when new density estimates become available for the various forest types within the subspecies’ ranges, especially for the largest forest patches, and when current occupancy of forest patches is more comprehensively mapped.

Small forests are generally unable to support a troop of Samango Monkeys; thus they are generally absent from forests smaller than 1.5 km² (Swart et al. 1993; Lawes 2002) (Table 2). Although it may be simplistic to define a subpopulation as a forest patch, Samango Monkeys are poor dispersers, in comparison to other forest-dwelling mammals, such as Blue Duiker, Philantomba monticola and Southern Tree Hyrax, Dendrohyrax arboreus, and are reluctant to disperse over open ground (Lawes et al. 2000). As such, most forest patches where they occur can be considered isolated or semi-isolated subpopulations. For example, nearly half (42%, N = 22) of the known (currently occupied) subpopulations of Samango Monkeys (for both erythrarchus and labiatus subspecies) in KwaZulu-Natal Province are found in forests patches smaller than 4 km2 (Lawes 1992; Lawes et al. 2000). Based on estimates of mean density (59 individuals / km2, Lawes 1992) this would mean that a large number of subpopulations contain fewer than 250 individuals and thus probably contain fewer than 100 mature individuals (based on 40–50% mature subpopulation structure). Such small subpopulations are vulnerable to demographic and environmental stochasticity facing a high risk of losing genetic diversity and thus adaptability through breeding of closely related individuals and are seldom recolonised (Swart & Lawes 1996). They exist in transient, non-equilibrium or declining metapopulations vulnerable to local extinctions as a result of diminishing forest areas and decline in habitat quality (Lawes 2002). Thus, the long-term viability of these small subpopulations is threatened if further habitat loss or a reduction in their population density occurs. Swart et al. (1993) found that if the density of this species falls below 30–40 individuals / km2 they are at risk of local extinctions within 50 years as they are unable to withstand a further 30–35% reduction in size.

Threats

The major threat to the species is deforestation and resulting habitat fragmentation, especially as Samango Monkeys are poor re-colonisers and are susceptible to local extinction within small forest fragments (Lawes et al. 2000; Lawes 2002). Although forests are currently well-protected in some areas, there is a continuing loss of forest habitat and habitat quality across the assessment region (see current habitat trend below). For instance, loss of habitat and habitat disturbance caused by selective logging of forests for timber and firewood, mainly in the Eastern Cape; and charcoal production and the medicinal plant trade in Maputaland. Coastal development through residential and industrial expansion is a major threat to the coastal forest habitats of both C. a. labiatus and C. a. erythrarchus, while expanding human settlements on the Pongola Floodplain may have led to the extirpation of the riverine subpopulations of C. a. erythrarchus in the area. Further south in the region, strip mining (between St Lucia and Sodwana) is a threat to C. a. erythrarchus and possibly C. a. labiatus. Extensive commercial afforestation in mistbelt regions of South Africa has resulted in the loss of small forests and reduction in area of some of the larger forests (Armstrong et al. 1998), which may specifically threaten C. a. schwarzi (Armstrong & van Hensbergen 1996). Indeed, in Limpopo’s Soutpansberg Mountains, ongoing habitat loss and degradation of riverine vegetation, which are possible corridors between forest patches, are the greatest threats to C. a. schwarzi (B. Linden pers. obs. 2012).

The effects of forest loss and fragmentation include an increase in edge effects on forest patches and abundance of exotic plant species and availability of “human food” (for example, bread) and bring Samango Monkeys into more frequent contact with human settlements and infrastructure, which may lead to increased rates of morbidity and mortality. These deaths and injuries can be caused by bushmeat hunting, collection for the muthi trade, intentional or incidental snaring and hunting by dogs (which are possibly directed at other forest species; for example, antelope), attacks by residential dogs, direct persecution as pests, road collisions and electrocution when using power lines to cross roads and/or properties (especially in the eastern Soutpansberg, B. Linden et al. unpubl. data; in the Haenertsburg and Magoebaskloof areas, M. Harman pers. comm 2013; in Hogsback, K. Wimberger pers. obs. 2010–2012). It seems that adult males (lone or bachelor males not associated with troops) are particularly vulnerable to being road killed in certain areas in the Soutpansberg where they have been found to move out of forests through highly transformed landscapes (B. Linden et al. unpubl. data). In addition to being persecuted as pests when foraging for food in people’s homes (K. Wimberger pers. obs. 2010–2015; B. Linden pers. obs. 2012), and in campsites (Chapman et al. 1998), they may become pests in large-scale and subsistence fruit orchards or pine plantations surrounding natural forest remnants as they sometimes strip the bark to eat the sap (Droomer 1985; von dem Bussche & van der Zee 1985; B. Linden unpubl. data).

Uses and trade

Samango Monkeys are mainly used in the local trade for traditional medicine (Table 5). Samango Monkey skins and carcasses have been found to be traded illegally at South Africa’s largest traditional medicine market, the Faraday market in Johannesburg (Whiting et al. 2011). Anecdotal evidence suggests they are used in traditional medicine if caught, as skins and hands were found near human settlements (Soutpansberg: J. Linden pers. obs. 1998; Hogsback: K. Wimberger pers. obs. 2011) and requests to researchers for Samango skulls and hands by traditional healers were also experienced in the Soutpansberg area (B. Linden unpubl. data). They are possibly used on a subsistence level for bushmeat according to anecdotal reports, snares found intact on Samango Monkeys and an infant Samango Monkey being sold (for example, Hogsback K. Wimberger pers. obs. 2011). The effects of this trade are suspected to be minimal because they are infrequently captured and not a targeted species in cultural hunts.

Conservation

We argue for separate conservation management of the three distinct genetic entities defined by Dalton et al. (2015), as subspecies need to be conserved to prevent the loss of genetic diversity in the species, which is an essential part of biodiversity conservation. This needs to apply in the wild as well as in captivity (zoological gardens and primate rehabilitation facilities). In particular, rehabilitation facilities which aim at establishing troops and releasing them in the wild must ensure that different subspecies are not mixed and able to interbreed in captivity and that individuals from any of the three subspecies are not reintroduced into another subspecies range resulting in interbreeding in the wild. Similarly, if wild troops are relocated, such as when provincial conservation authorities conducted relocation programmes for monkeys causing damage to plantations (Droomer 1985; von dem Bussche & van der Zee 1985), they should be translocated to the correct area for the subspecies. Strict guidelines are therefore needed for zoological gardens, rehabilitation centres and provincial conservation authorities in order to conserve the genetic distinctness of the three subspecies and even that within metapopulations of the same subspecies.

Protected area expansion and proper management of indigenous forests are the primary interventions for this species. The various subspecies occur in protected areas across their range. For example, C. a. labiatus in Hogsback Forest Reserve; C. a. schwarzi in Happy Rest Provincial Nature Reserve, Entabeni and Ratombo parts declared Forest Reserves, and Luvhondo Private Nature Reserve in the Soutpansberg; and C. a. erythrarchus in the Lubombo Transfrontier Conservation Area. Protected area expansion could focus on reclaiming and restoring non-viable or cleared commercial forest plantation areas, particularly those that had been planted in areas conducive to indigenous forest growth including riparian forests along streams and rivers (for example, southern mountain slopes). Samango Monkey life-history traits necessitate large forest areas, which means identifying large habitat patches that are close to one another and minimising disturbance in and on the edge of these patches as a key management strategy (Lawes et al. 2000). Conservation planning should thus continue to connect forest fragments to create viable subpopulations and ensure the persistence of metapopulations (Swart & Lawes 1996), especially in Afromontane and Scarp forests (Eeley et al. 1999). For example, in Maputaland, a new transfrontier landscape is being designed that will, amongst other species, presumably benefit C. a. erythrarchus immensely by extending the existing Lubombo Transfrontier Conservation Area to the south (Smith et al. 2008). For C. a. schwarzi, forest patches in the eastern Soutpansberg (e.g. Entabeni and Thathe Vondo) are key areas to ensure the Samango’s long term persistence in the eastern part of the mountain range as they are naturally larger in size than the patches in the western Soutpansberg but are under highest pressure from human development. On the escarpment, Woodbush and Magoebaskloof forests are important sites as they are both large, continuous indigenous forest patches.

Effective forest management is also crucial. Forest guards should be trained to reduce poaching and disturbances within forests. Human-wildlife conflict could be reduced by educating surrounding communities on proper waste and refuse control in residential areas, as well as securing potential attractants such as vegetable gardens, subsistence farming and chicken coops with monkey-proof enclosures or by physically chasing the monkeys away. Intentional feeding of monkeys should be prevented. Communities should also be encouraged to plant indigenous garden trees rather than planting exotic ones to make gardens only as attractive to Samango Monkeys as the surrounding indigenous forest habitat. Indigenous species often have less attractive fruit and flowers than those offered by exotic plants (for example, protein and fat rich acorns, such as in Hogsback, K. Wimberger et al. unpubl. data).

In general, conservationists should identify road collision hotspots for this species and erect monkey bridges to ensure safe crossing in those areas. Conservationists should also trial other interventions to encourage monkeys to use specific locations to cross over roads. Raising public awareness about Samango Monkeys is also being trialled through bumper stickers (“I brake for Samango Monkeys”) and road signs (“Samangos crossing”), in conjunction with local newspaper articles informing people about the problem (B. Linden unpubl. data) Similarly, power line infrastructure should be secured so as to reduce electrocution incidents.

Recommendations for land managers and practitioners:
  • Captive breeding programmes are not needed for the species if the long-term persistence of Samangos throughout their current range is ensured through proper management. In situ conservation is the only logical approach for ensuring long-term Samango Monkey persistence in the country. An important part of ensuring the latter is the identification and creation of corridors linking local subpopulations as well as proper management and protection of their forest habitat.
  • Managers should develop a Biodiversity Management Plan for this species to sustain a genetically diverse, resilient metapopulation amongst remaining forest patches. Engagement with the private sector will be key in this regard.
  • Managers should continue to monitor the cutting down of trees and hunting within or on the edge of forest patches, and enforce penalties.
  • Due to the differing landownership types in the range of the Samango Monkey (private, communal, state) different management approaches have to be formulated and areas should ideally be managed by one entity only to ensure the appropriate management strategies.

Research priorities: Research is currently being undertaken in the Soutpansberg on the distribution, population status and conservation of Samangos (University of Venda) which partly falls under the Samango Monkey Working Group (SMWG, http://www.nzg.ac.za/research/samango.html, https://www.facebook.com/groups/samango/) which collaboratively investigates phylogeographic and taxonomic questions about the species. Current research questions include:
  • Collection and collation of all Samango Monkey distribution data (including from the literature) and analysis of specimens to delineate boundaries and/or hybrid zones between the subspecies.
  • Surveys to determine current distribution and density across forest fragments, including demographic research.
  • Further taxonomic resolution of the Cercopithecus complex is needed. For example, are the South African Samango Monkeys a different species (C. albogularis) to the rest of the African Blue Monkeys (C. mitis) or a subspecies? Genetic data are needed. For C. a. erythrarchus, further research is needed to identify the extent of occurrence, especially further south along the South African coast (and especially around the Umfolozi area) and also whether they occur in Scarp and Afromontane forests inland (South Africa, Zimbabwe and Mozambique). For C. a. schwarzi, further research is needed to identify the extent of occurrence, southern limits in South Africa and northern limits outside of the country, especially further north (Mozambique and Zimbabwe) to clarify endemism.
  • Behaviour of lone males (for example, how far they disperse) is important for generating parameters relevant to metapopulation persistence (such as gene flow rates and effects of fragmentation on population stability).
  • Reproduction and breeding success of each subspecies in different habitat types
  • Development of human-wildlife conflict mitigation measures such as adequate bridge designs for Samango troops to use to cross roads. Starting with erecting these in the Soutpansberg, with possible roll out throughout the country.

Encouraged citizen actions:
  • Read the brochures developed by K. Wimberger on how to understand and live with Samango monkeys (http://imfene.org/resources).
  • For property owners and tourists, ensure no feeding is done either directly or indirectly (for example, leaving fruit out for birds to eat or badly managed bins and rubbish dumps).
  • Plant indigenous garden species so that your garden is only as enticing as the surrounding indigenous forest.
  • Report sightings on virtual museum platforms (for example, iSpot and MammalMAP).
  • Contact the Samango Monkey Working Group (Bibi Linden at bibi@lajuma.com) if Samango Monkeys are found on private land. Please collect faecal samples for genetic analyses, note any injuries/deaths of individuals and possible causes, and estimate number of individuals in troops and the types of habitat in which they are found.

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 year = {2003}
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,@phdthesis{4221,
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 school = {University of Würzburg},
 title = {The role of cheek pouches in seed dispersal: An analysis of dispersal methods within a free ranging group of Sykes’ monkeys (<i>Cercopithecus albogularis</i>) in the Western Soutpansberg, South Africa. M.Sc.Thesis},
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 volume = {48},
 year = {1987}
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 volume = {9},
 year = {1988}
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 volume = {224},
 year = {1991}
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 volume = {14},
 year = {2000}
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 volume = {59},
 year = {1992}
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,@article{4221,
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 year = {2014}
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,@book{4221,
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 publisher = {Kluwer Academic Publishers},
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 year = {2002}
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,@article{4221,
 author = {Rycroft HB},
 journal = {Journal of the South African Forestry Association },
 pages = {14–25},
 title = {The Karkloof Forest, Natal},
 volume = {11},
 year = {1944}
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,@article{4221,
 author = {von dem Bussche GH, van der Zee D},
 journal = {South African Forestry Journal},
 pages = {43–48},
 title = {Damage by Samango monkeys, <i>Cercopithecus (mitis)</i> albogularis, to pine trees in the Northern Transvaal.},
 volume = {133},
 year = {1985}
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,@article{4221,
 author = {von Maltitz G, Geldenhuys CJ, Lawes MJ, Eeley H, Aidie H, Vink D, Fleming G, Bailey C},
 title = {Classification system for South African indigenous forests. An objective classification for the Department of Water Affairs and Forestry. ENV-P-C 2003-017.},
 year = {2003}
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,]
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