ORIGINAL RESEARCH

 

Impact of poaching on the population structure and insect associates of the Endangered Encephalartos eugene-maraisii from South Africa

 

 

P.D. Janse van Rensburg^I; H. Bezuidenhout^{II, III}; J. van den Berg^I

^IUnit of Environmental Sciences and Management, North-West University, Private Bag X6001, Potchefstroom 2520, South Africa
^IIArid Ecosystems Research Unit, Conservation Services, SANParks, P.O. Box 110040, Hadison Park, Kimberley 8306, South Africa
^IIIApplied Behavioural Ecology and Ecosystem Research Unit, University of South Africa, Private Bag X6, Florida Campus, 1717, South Africa

Correspondence

 

 

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ABSTRACT

BACKGROUND: South Africa is an important centre of cycad diversity in Africa, however, the country's cycads face extinction. Among the primary causes is the poaching of plants from the wild, even within protected areas.
OBJECTIVES: This study examined poaching patterns in a local population of the Endangered Encephalartos eugene-maraisii I.Verd. and how it might affect the population structure, sex ratios, as well as interactions with associated insects.
METHODS: The population was surveyed in 2008 and 40% of this population was resurveyed between 2021 and 2022. We mapped missing cycads and generated heatmaps. Lastly, we investigated whether the proportion of stems from different size classes, sex ratios and abundance of insect associates varied between areas with a high and low poaching incidence.
RESULTS: Poaching, defined as the illegal removal of individuals from the wild, occurred 1.5 times more frequently along the border fence line than areas further away. Medium-sized stems (21-80 cm) are primarily targeted (likely as they can be carried more easily) and low proportions of these stems remain in areas with a high poaching incidence. While E. eugene-maraisii exhibits some resilience against poaching through basal suckering, it takes several decades for suckers to mature and replace harvested stems. No effect on sex ratios were recorded in areas with a high poaching incidence, suggesting poachers have not deliberately selected female or male cycads at this site. No pollinating insects were detected on E. eugene-maraisii, and no seedlings were observed
CONCLUSION: Cone production may be too rare in diminished populations to support pollinators that utilise cones as brood sites. The presence of insects that use other plant parts, including leaves, dried leaf stalks and cycad trunks, in the larger population suggests that they are more resilient to diminishing host populations. However, these insects were absent in smaller populations, and their abundances were lower in low-density sites and smaller clump sizes of their host in the larger population. This suggests these insects may be vulnerable to the decline of their host populations due to poaching.

Keywords: cycads, conservation areas, herbivore-plant interactions, population decline, impact.

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Introduction

South Africa is a major centre of cycad diversity in Africa, with the monotypic Stangeria eriopus (Kunze) Baill. and 37 species of Encephalartos Lehm., of which 29 species are endemic to South Africa (Calonje et al. 2023). However, South Africa's cycads face extinction. Many species have limited distributions and small populations, and their numbers are continually declining (Table 1). South African species include four that are already Extinct in the Wild, 11 that are Critically Endangered, four that are Endangered, 11 that are Vulnerable, and five that are Near Threatened (IUCN 2023). Relatively more cycads in South Africa are Extinct in the Wild or Critically Endangered than in other centres of cycad diversity (Donaldson 2008).

In most regions of the world, the primary cause of the decline in cycad numbers is habitat loss, but in South Africa the poaching of wild plants has played an even greater role, affecting nearly all species (Okubamichael et al. 2016; Table 1). Established cycads from the wild are targeted because cycads are notoriously slow growing and can take decades to reach desirable sizes (Donaldson 2003). Consequently, many plants have been collected for botanical gardens and private collections (Osborne 1995). Those that become rare increase in value, making them even more desirable to collectors and increasing the pressure on species in the wild (Courchamp et al. 2006; Okubamichael et al. 2016). Some species have suffered dramatic declines; for example, in Kaapsehoop, 1 700 Encephalartos laevifolius Stapf & Burtt Davy plants were present in the 1970s, but there are now fewer than five remaining (Government Gazette 2017). Despite various conservation measures, restrictive legislation, and the use of novel technologies (such as microchips and microdots), poaching continues relentlessly because large, rare specimens are in high demand (Donaldson 2003).

South African cycads are also harvested for traditional medicine (Ravele & Makhado 2010; Cousins et al. 2011, 2012, 2013; Williamson et al. 2016; Ndou et al. 2021). Traditional medicine has experienced significant commercialisation in recent years and there has been an increase in the sale of stem sections and bark strips of Encephalartos species at traditional markets, which puts more pressure on wild Encephalartos populations (Cousins et al. 2011). Intensive harvesting of bark strips and stem sections can be destructive and often result in the death of plants (Donaldson 2003; Bamigboye & Tshisikhawe 2020).

Other threats include the destruction of habitats and invasive plant species. Historically, habitat destruction has contributed to a decline in South African cycad populations. For example, the clearing of dune thicket for agriculture directly reduced E. arenarius R.A.Dyer populations (Donaldson 2003). Alien plants such as Lantana camara L. have invaded the habitat of cycads such as E. princeps R.A.Dyer and E. lebomboensis I.Verd. and can potentially affect recruitment by smothering young plants (Donaldson 2003; Government Gazette 2017).

Those involved in illicit trade with cycads often claim that their goal is conservation, even though the illicit collection is the main threat (Torgersen 2017). It is important to conserve cycads not only as part of South Africa's natural heritage but also as a component of ecosystem function. They provide food and shelter for birds and animals (Donaldson 2008), host complex mutualistic relationships with insects (Toon et al. 2020), and host arbuscular mycorrhizae that shape biogeo-chemical processes in their microhabitats (Marler & Calonje 2020).

Cycads recover slowly from poaching due to their slow growth (Raimondo & Donaldson 2003). Poaching can affect the size of the cycad population, age structure and sex ratio. For example, Cycas circinalis L. populations subjected to pith harvesting completely lacked individuals greater than 50 cm tall (Krishnamurthy et al. 2013). The expected sex ratio for a healthy cycad population is 1:1 but in small populations, male-biased sex ratios are often observed, and it has been speculated that this results from selectively harvesting female plants since they produce seeds (Donaldson 2008). The rarest species are now often represented only by small populations, making them vulnerable to stochastic events (e.g., drought, fire), inbreeding depression and reduced natural recruitment (Donaldson 2003). Cycads and their pollinators exhibit brood-site mutualism, making them vulnerable to coextinction (Toon et al. 2020). There may be too few cones produced by diminished cycad populations to support insect pollinators (Oberprieler 1995). South African species of Encephalartos also have a high diversity of other specialised insects, for example, female cone specialists and leaf consumers, which are also threatened by declining host populations (Oberprieler 1995).

Encephalartos eugene-maraisii I.Verd. is listed as Endangered under Red List criteria A2ad + 4ad; B1ab(v) (IUCN 2023). This species has a limited distribution in the Waterberg range and lacks natural recruitment, making it extremely vulnerable to poaching (Bezuidenhout et al. 2020). The impact of poaching on this cycad has not been studied before. A lack of scientific information constrains decision support systems and the development of management decisions that can effectively ensure the survival of E. eugene-maraisii in the wild (Bezuidenhout et al. 2020). This study aimed to 1) identify poaching patterns of E. eugene-maraisii in one of its last remaining populations, 2) assess its impact on the size class structure and sex ratio of the population, and 3) how this might impact insects closely linked with E. eugene-maraisii.

 

Materials and methods

Study site

Encephalartos eugene-maraisii is endemic to the Waterberg range in Limpopo, South Africa (Bezuidenhout et al. 2020). The majority of individuals remain in two main conservation areas, located at either end of its geographical range. Marakele National Park (Marakele) is located at the southwestern extreme of the Waterberg cycad distribution. The Entabeni Safari Conservancy (Entabeni) is at the northeastern edge of its range, where the majority of E. eugene-maraisii plants still exist. There have been no reports of cycad poaching in Marakele since its proclamation in 1994 (Bezuidenhout et al. 2020). However, at that time, very few plants (< 50) remained in Marakele and they are extremely difficult to reach (Bezuidenhout et al. 2017). We have also failed to record the presence of any cycad-associated insects in Marakele. Therefore, sampling was confined to Entabeni where the majority of plants remain.

Most plants grow on the rocky mountain plateaus and scarps in the Waterberg-Magaliesberg Summit Sourveld (Gm 29) at high altitudes (1500-1750 m.a.s.l.) (Mucina et al. 2006). The vegetation is characterised by patches of open woodland of Protea caffra Meisn. and open shrubland of Englerophytum magalismontanum (Sond.) T.D.Penn. and Ancylobotrys capensis (Oliv.) Pichon (Steyn & Bezuidenhout 2020). The climate is warm in summer and cold and prone to frost in winter. Historically, fires were frequent in the study areas due to the very high frequency of lightning strikes, and fire scars were visible on the cycads in both populations.

Study species

Encephalartos eugene-maraisii has aerial stems (up to 4 m long) that become procumbent as they age. Individual plants are multi-stemmed through the production of basal suckers (Figure 1). Individual plants can persist over long periods of time due to vegetative production of suckers and stem longevity. Like all cycads, E. eugene-maraisii is dioecious although cones are produced infrequently.

Patterns of poaching

Poaching was assessed in Entabeni, where the majority of plants remain. The main driver behind the poaching in Entabeni is the horticultural trade, which requires that whole stems are removed. We did not find evidence that plant parts are being harvested for the traditional medicinal trade. This is also supported by previous authors (Bezuidenhout et al. 2020). Encephalartos eugene-maraisii has also not been recorded in traditional medicine markets (Cousins et al. 2011, 2012, 2013).

In 2008, Entabeni conducted a cycad census on its property to determine the population size and distribution within the reserve (De Klerk, 2008). GPS coordinates were provided to facilitate the retracing of individual plants. Given the scattered distribution of plants, it was unlikely to mistake them for those in similar locations. The original census took months to complete and many of the plants are in areas difficult to reach. Given time limitations, we only re-surveyed the most densely populated area between 2021 and 2022. Approximately 40% of the plants identified in the original census (De Klerk 2008) were revisited. The studied plants occurred in a small area (~8 km²), which accounted for approximately 30% of the total area. We recorded plants as present, dead or missing. Remains of dead cycads are visible for a very long period. It was rarely possible to determine the cause of mortality, but common causes include stems falling over, baboon damage and poachers damaging and excavating large stems to get to smaller stems that they could carry. If no remains were found they were classified as missing. Missing cycads were mapped and heatmaps produced. We recorded the number of stems for the plants present, and for each individual stem, we measured its height. The survey areas were also searched for seedlings to confirm the presence or absence of natural recruitment.

Impact of poaching

The plants grew in areas along the fence line and areas further from the fence. The fence stretches over a distance of approximately 3 km over rocky terrain that is difficult to patrol. Other areas are more easily visible and accessible from roads within the reserve. It appears that plants have been poached from across the entire population. However, poaching has historically been more intense along the fence line (Entabeni reserve manager, pers. comm.). Therefore, analyses were conducted by categorising areas along the fence line as 'high poaching incidence' and areas further from the fence line as 'low poaching incidence'. A ridgeline divides the two areas. The high poaching incidence area consists of plants along the fence line and the western slope of the ridgeline, which faces the fence. The low poaching incidence area consists of plants on the eastern slope of the ridgeline and further away.

All analyses were done using SPSS version 28 (IBM Corp 2021). To assess the impact of poaching on the size structure of the population we compared the distribution of stem height of individual stems in areas with high and low poaching incidence using the Kolmogorov-Smirnov test for goodness of fit (e.g., Botha et al. 2004a, 2004b). The studied plants occurred in a small area and experienced similar climatic conditions and fire regimes. Additionally, cycad stem growth is positively correlated with stem height, therefore shrinkage of stems is ruled out (Griffiths et al. 2005; Marler et al. 2020).

Medium-sized stems seemed to be primarily targeted because large stems may be too heavy to carry over the large distances that poachers need to cover over neighbouring properties (Entabeni reserve manager, pers. com.). To test this, we investigated whether the proportion of stems from different size classes varied between areas with high poaching incidence and low poaching incidence. We classified all stems into five size classes based on their length: suckers (no visible stem); visible stems (> 0 cm); small stems (1-20 cm); medium-sized stems (21-80 cm) and large stems (> 80 cm). The proportion of each size class in the areas of high and low poaching incidence was compared using Chisquare analyses (χ²). Finally, to show how the clump size of individual plants might be affected by poaching we tested for significant differences with a Kruskal-Wallis test, between the mean number of stems per plant for each category in areas with high vs low poaching incidence.

During the 2008 census, a small proportion of plants were sexed. To gather more data, we examined cycad plants for cone material to determine the sex of the plants. A binomial test was conducted to see if the proportion of male and female plants are different from the expected 1:1 sex ratio in cycads. To test whether poaching affects the sex ratio through selective harvesting of female plants, we compared the proportions of male and female plants between areas with a high poaching incidence and low poaching incidence using Chisquare analysis. We also tested for significant differences in the mean number of stems between male and female plants using a Kruskal-Wallis test.

Insect abundance

We recorded three insect species associated with E. eugene-maraisii in Entabeni (Figure 2), but, as per previous extensive surveys, none of these are pollinators. Reference collections (accession numbers: PDJVR Morpho 6 and 7) are stored at the Biosystematics Division, South African National Collection of Insects (SANC), Agricultural Research Council, Pretoria, South Africa.

Amorphocerus cf. setosus Boheman, 1838 (Coleoptera: Curculionidae) bore into the trunk of E. eugene-maraisii. The trunks exhibit characteristic emergence holes made by beetles. All stems except those out of reach or pinned between rocks were assessed for beetle emergence holes. This was done by placing a 10 cm wide piece of clear plastic, from top to bottom on each stem and counting the number of exit holes made by A. cf. setosus adults. The number of holes per square centimetre was calculated by dividing the number of holes by the area recorded (the length of the stem x 10 cm).

Apinotropis verdoornae Jordan, 1945 (Coleoptera: Anthribidae) breed in dead leaf stalks of E. eugenemaraisii. It has overlapping life history stages and so it is usually possible to find adults and larvae within the same leaf stalk at any time of the year (personal observations). If dead leaf stalks were present, five dead leaves were randomly selected from each stem, cut off and dissected after which the numbers of larvae and adults were determined.

Larvae of Zerenopsis lepida (Walker, 1854) (Lepidoptera: Geometridae) consume new leaf flushes (Janse van Rensburg et al. 2023). Herbivory damage was used as an estimate of the abundance of Z. lepida. To determine the level of damage, the percentage of leaf area removed for each leaf was visually estimated using different damage classes: 0%, 1-25%, 26-50%, 51-75%, and > 75%. We calculated the percentage of leaf area consumed by larvae by multiplying the number of leaves from each damage class with the midpoint of each damage class category, e.g., 13% for the 1-25% class. The values of all classes were then summed and divided by the total number of leaves per stem. Only new leaf flushes are damaged and only a small portion of plants flush leaves each season. For a more complete sample of the entire population, we combined leaf damage estimates from consecutive years, 2021 and 2022.

Kruskal-Wallis tests were used to determine whether there were significant differences in mean insect abundances between plant sex, altitude and aspect. Additionally, we recorded whether the stems had fire scars and tested for significant differences between the abundance of insects on the burned and unburned stems. To assess the potential impacts of poaching we compared insect abundance between high poaching incidence and low poaching incidence areas. Also, because poaching can lead to lower plant densities and smaller clump sizes due to removed stems, we compared insect abundance between different densities of E. eugene-maraisii and analysed correlations between the abundance of insects and the clump size (number of visible stems) of E. eugene-maraisii using Spearman rank correlation analysis. Using heat maps of existing plants, we rated areas with dense plant density (dark spots on the heatmap), sparse plant density (light spots on the heatmap), and intermediate plant density (areas between dense and sparse areas).

Ethical considerations

Ethics approval (no.: NWU-01552-20-A9) for this study was granted by the North-West University, Faculty of Natural and Agricultural Sciences Ethics Committee (FNASREC). A permit (no.: ZA/LP/111179) to do research on plants in the Limpopo province of South Africa was granted by the Limpopo Department of Economic Development, Environment and Tourism (LEDET).

 

Results

Patterns of poaching

We were unable to find any seedlings in the survey areas. A total of 297 plants recorded in 2008 were revisited. Out of those, 246 (83%) plants were still present, eight (~3%) plants were dead and 43 (~14%) plants could not be relocated. This represents a reduction of ~17% (51 plants) in 14 years, equivelant to an annual intrinsic population growth rate of -0.013. The estimation is based only on completely missing plant individuals and does not include missing stems from plant individuals that were still present. Most of the missing plants were those that occurred adjacent to the border fence of the conservation area and are assumed to have been removed from the wild by poachers (Figure 3).

Impact of poaching

The Kolmogorov-Smirnov test for goodness of fit only indicated a marginally significantly different stem size distribution between areas with high poaching incidence (n = 70) and low poaching incidence (n = 176) (K-S = 1.443, p = 0.031). Chi-square analysis indicated that there was a higher proportion of stemless suckers in areas with high poaching incidence (35.8%) compared to areas with low poaching incidence (24.3%) (χ² = 10.457, df = 1, p = 0.001) (Table 2). There was a higher proportion of visible stems (> 0 cm) in the areas with low poaching incidence (75.7%) than areas with a high poaching incidence (64.2%) (χ² = 10.805, df = 1, p = 0.001). Of the visible stems, the frequency of medium-sized stems was lower in the areas with a high poaching incidence (18.7%) compared to areas with a low poaching incidence (28.5%) ( χ² = 5.596, df = 1, p = 0.018). The proportions of small stems (χ² = 0.454, df = 1, p = 0.500) and large stems (χ² = 0.006, df = 1, p = 0.937) did not differ significantly between areas.

This was further reflected by a significantly higher mean number of medium-sized stems (21-80 cm) and lower stemless suckers (0 cm) per plant in areas with a low poaching incidence (Table 2).

Sex ratios

We were able to determine the sex of 90 (39.3%) of the remaining plants, of which 52 were male and 38 were female. A two-tailed binomial test indicated that the observed proportion of female plants did not differ significantly from the expected value 0.50 (p = 0.142). There were no differences in the frequency of male and female plants between areas (χ² = 0.552, p = 0.457). We found no difference between the mean number of visible stems and suckers between female (2.83) and male plants (2.85) (H = 0.029, p = 0.865) and the mean numbers of medium-sized stems (primarily targeted for harvesting) between female (0.33) and male plants (0.69) (H = 1.216, p = 0.270).

Insect abundance

There was no significant association between the abundance of insects and aspect, altitude and the sex of plants (Tables S1, S2; Supplementary material). A total of 78% of stems had visible fire scars. This did not significantly affect the abundance of A. verdoornae or herbivory by Z. lepida. However, the mean number of A. cf. setosus exit holes was significantly higher on burned stems (0.018 holes/cm²) than on unburned stems (0.005 holes/cm²) (p < 0.001).

The mean number of A. verdoornae individuals were higher in areas with a low poaching incidence, but not significantly so (Table 3). The abundance of A. verdoornae was significantly lower in areas with low plant density, and plants with smaller clump sizes also had a lower abundance of A. verdoornae (Table 3). The level of herbivory from Z. lepida was significantly higher in areas with a low poaching incidence and decreased significantly with decreasing plant density and decreasing clump sizes of E. eugene-maraisii (Table 3). We did not record any significant difference in the number of exit holes of A. cf. setosus between the areas nor any correlation with the density or clump sizes of E. eugene-maraisii (Table 3).

 

Discussion

This is the first investigation into poaching patterns in a local population of the Endangered E. eugene-marai-sii and how it might affect its population structure and interactions with associated insects. Supporting the observations made by the reserve manager, a slightly higher intensity of poaching was observed along the border fence line of the conservation area. Areas along the border fence line had a low proportion of medium-sized stems (21-80 cm), which seems to be the primary target for poachers. We found no difference in the sex ratios between areas with high poaching incidence and low poaching incidence and found no evidence for selective harvesting of female plants. The abundance of A. verdoornae and herbivory by Z. lepida decreased in lower densities and clump sizes of E. eugene-maraisii, indicating they may be sensitive to the decline of their host plant.

Poaching of E. eugene-maraisii has been a major problem for the past 30 years, with estimates suggesting a 50% reduction in the population (Government Gazette 2017). As a result, the distribution has shrunk, and the remaining subpopulations can be found mostly in Entabeni and Marakele (formally protected area managed by SANParks) (Bezuidenhout et al. 2020). There have been no reports of cycad poaching in Marakele since its proclamation in 1994 (Bezuidenhout et al. 2020). There were, however, very few plants left by then. Entabeni's plants were some of the most difficult to reach. The eradication of cycads in most areas in the Waterberg, caused by poaching, has led to an increase in poaching incidents in Entabeni.

Although sampling only 40% of the population was a limitation, we concentrated on the locations with the highest density of plants that were most often targeted by poachers. Other plants on the reserve are more randomly distributed and harder to reach. In this study, a slightly higher poaching rate (1.5 times) was observed along the border fence line. Besides being the first cycads encountered, it also falls in a difficult-to-patrol area with many places for poachers to hide. The majority of medium-sized stems (21-80 cm) had been intensively harvested. Cycads are generally removed indiscriminately of size (Okubamichael et al. 2016). While larger stems fetch higher prices, smaller stems are also targeted because they are easier to transport (Okubamichael et al. 2016). The reason for targeting medium-size stems in Entabeni may be case specific.

To reach cycads, poachers must walk long distances (up to 12 km) through neighbouring properties, and larger stem sizes are often too heavy to carry. However, large stems are sometimes damaged or excavated to reach the smaller stems that can be carried with relative ease (Figure 4).

The selective harvesting of medium-sized stems, in this case, has led to significantly different size class distribution of stems between areas with a high poaching incidence and low poaching incidence. Poachers often only target a subset of individuals in a population, for example, individuals with the largest tusks in the case of elephants (Chiyo et al. 2015) or selective harvesting of certain tree species in higher size classes (e.g., Botha et al. 2004a, 2004b). Selective harvesting may result in changes to the population structure, possibly causing declines. Poaching is the main threat to cycads in South Africa (Table 1); however, it is also very difficult to detect in populations that are not closely monitored. The stem size structure may potentially be used as a flexible and cost-effective indicator to track changes in wild populations of cycads and provide insight into the status of poaching. For example, C. circinalis populations subjected to pith harvesting have resulted in a complete absence of plant individuals taller than 50 cm (Krishnamurthy et al. 2013).

As evidenced by the large number of stemless suckers produced by plants in the areas targeted by poachers, E. eugene-maraisii has been able to survive despite severe poaching pressures and the absence of natural recruitment because it reproduces vegetatively. Cycads grow extremely slowly, with reports generally indicating around 1-3 cm per year (Vovides 1990; Cabrera-Toledo et al. 2019; Marler et al. 2020). Consequently, cy-cads are not particularly resistant to poaching because suckers will take a long time to reach the size of their poached counterparts. Modelling different poaching scenarios for two South African species with contrasting life histories revealed that poaching even small numbers of adult plants can cause rapid population declines (Raimondo & Donaldson 2003).

Moreover, E. eugene-maraisii lacks natural recruitment and has a complete lack of subadults, which suggests that the absence of natural recruitment has been a long-standing problem. Even in the presence of natural recruitment, species such as E. cycadifolius (Jacq.) Lehm. that have highly persistent adult plants and infrequent recruitment events are unable to recover within a reasonable time frame (< 100 years) even from small losses of adult plants (Raimondo & Donaldson 2003). Reinforcement (adding individuals to an existing population) efforts have been made in a proactive attempt to limit the decline of E. eugenemara-isii (Bezuidenhout 2019; Bezuidenhout et al. 2020). However, rare opportunities to hand-pollinate female cones and the slow growth of reintroduced seedlings have not been able to stem the tide of poaching (Bezuidenhout et al. 2020).

Limited conclusions can be drawn on the sex ratios because only 39% of the plants could be sexed. The sex ratio was slightly male-biased; however, female plants are less likely to be identified because they cone less frequently. If a larger proportion of the population was sexed the sex ratio may have been closer to 1:1. We found no evidence that female plants are selectively harvested. Due to the slow coning rate of E. eugene-maraisii, there is little material (live cones, dry cone material and seeds) poachers can use to sex plants. The destruction of cones, especially female cones, by baboons also removes evidence of coning. Moreover, individual stems are usually harvested rather than whole multi-stemmed plants, which will maintain the sex ratio.

No pollinators have been recorded on E. eugene-mara-isii despite extensive surveys. Cycad pollinators are dependent on cones for reproduction and the time between coning events can become too long for pollinators to be sustained in diminished host populations (Oberprieler 1995). The presence of other insects on E. eugene-maraisii may indicate higher resilience to decreasing host populations because they depend on more abundant plant parts (Figure 2). However, herbivory by Z. lepida and abundance of A. verdoornae decreased at lower plant densities and smaller clump sizes of E. eugene-maraisii, indicating that they are still sensitive to the decline of their host. South Africa hosts a rich diversity of insects associated with cycads (Oberprieler 1995). However, several cycad species are now only represented by single populations containing few individuals (Table 1). Several cycad species also exhibit reduced reproductive success, which might indicate rarity or absence of their pollinators (Table 1). Specialist herbivores are often absent in small host populations due to the higher probability of herbivore extinction (Kéry et al. 2001; Colling & Matthies 2004). Chance events (droughts, floods, fires, etc.) puts small insect populations at greater risk of extinction (Thomas & Jones 1993). Smaller ranges have fewer patches (refuges) that escape disturbance from where insect populations can recolonise cycad host plants.

Apinotropis verdoornae is of particular interest. It is a detritivore that feeds on dead leaf stalks and dried cone material. It is the only genus of Anthribidae exclusively associated with cycads (Oberprieler 1999). Entabeni is the only known locality where A. verdoornae occurs, as we have not recorded it from other E. eugene-maraisii population or closely related species such as E. middelburgensis Vorster, Robbertse & S.van der Westh. and E. dyerianus Lavranos & D.L.Goode. To conserve E. eugene-maraisii and its associated insects, it is crucial to maintain as many refuges of suitable habitat as possible.

 

Conclusion

This study examined poaching patterns in one of the last remaining populations of E. eugene-maraisii and its impact on population structure and insect interactions. Higher poaching incidence was observed along the border fence line, primarily targeting medium-sized stems. These findings can inform decision making processes, helping determine areas that require increased patrolling and prioritise stem sizes for interventions like micro-dotting. Lower insect abundance in areas with lower host densities and smaller clump sizes of their host highlights the potential impact of poaching, emphasising the need for protection against poaching. Conserving E. eugene-maraisii in the wild will require several actions that may include increased protection from poaching, species recovery techniques (reinforcement and reintroductions), identifying other threats (e.g., climate change) and further research on the disappearance and reintroduction of pollinators.

 

Acknowledgements

The Wild Cycad Conservancy contributed funding to the project. We are thankful to Simphiwe Dubazane for assisting us during field surveys. Beetle identifications were carried out by R.G. Oberprieler (Australian National Insect Collection) and R. Stals (South African National Collection of Insects (SANC)) and reference collections are stored at SANC.

Author contributions

All authors contributed to the study's conception and design. Data collection and analysis were performed by PDJvR with assistance from JvDB and HB. The first draft of the manuscript was written by PDJvR and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Disclaimer

The views expressed in the submitted article are our own and not an official position of the institution or funder.

 

References

Bamigboye, S.O. & Tshisikhawe, M.P, 2020, 'The impacts of bark harvesting on a population of Encephalartos transvenosus (Limpopo cycad), in Limpopo Province, South Africa', Biodiversitas 21, 8-13, https://doi.org/10.13057/bio-div/d210102.         [ Links ]

Bezuidenhout, H., 2019, 'Supplementation of the Encephalartos eugene-maraisii populations in Marakele National Park', Internal report 02/2019, Scientific Services, Kimberley, SANParks.         [ Links ]

Bezuidenhout, H., Steyn, T., Van Staden, W., Hofmeyr, M. & Froneman, W., 2017, 'Monitoring the cycad population in Marakele National Park', Internal report 27/2017, Scientific Services, Kimberley, SANParks.         [ Links ]

Bezuidenhout, H., Steyn, T., Mamatsharaga, T., Froneman, W., Rodgers, S., Lessing J., Van den Berg, J. & Van Eeden, W., 2020, 'Management plan for the Encephalartos eugene-maraisii (Waterberg cycad)', Internal report 08/2020, Scientific Services, Kimberley, SANParks.         [ Links ]

Botha, J., Witkowski, E.T.F. & Shackleton, C.M., 2004a, 'Harvesting impacts on commonly used medicinal tree species (Catha edulis and Rapanea melanophloeos) under different land management regimes in the Mpumalanga Lowveld, South Africa', Koedoe 47(2), https://doi.org/10.4102/koe-doe.v47i2.77.         [ Links ]

Botha, J., Witkowski, E.T.F. & Shackleton, C.M., 2004b, 'The impact of commercial harvesting on Warburgia salutaris ('pepperbark tree') in Mpumalanga, South Africa', Biodiversity and Conservation 13, 1675-1698, https://doi.org/10.1023/B:BIOC.0000029333.72945.b0.         [ Links ]

Cabrera-Toledo, D., González-Astorga, J., Vovides, A.P, Casa, A., Vargas-Ponce, O., Carrillo-Reyes, P., Nolasco-Soto, J. & Vega, E., 2019, 'Surviving background extinction: inferences from historic and current dynamics in the contrasting population structures of two endemic Mexican cycads', Population Ecology 61, 62-73, https://doi.org/10.1002/1438-390X.1008.         [ Links ]

Calonje, M., Stevenson, D.W. & Osborne, R, 2023, 'The world list of cycads, online edition', http://www.cycadlist.org, date accessed: 7 July 2023.         [ Links ]

Chiyo, PI., Obanda, V. & Korir, D.K., 2015, 'Illegal tusk harvest and the decline of the tusk size in the African Elephant', Ecology and Evolution 5, 5216-5229, https://doi.org/10.1002/ece3.1769.         [ Links ]

Colling, G. & Matthies, D., 2004, 'The effects of plant population size on the interactions between the endangered plant Scorzonera humilis, a specialised herbivore, and a phytophagous fungus', Oikos 105, 71-78, http://www.jstor.org/stable/3547885.         [ Links ]

Courchamp, F., Angulo, E., Rivalan, P., Hall, R.J., Signoret, L., Bull, L. & Meinard, Y., 2006, 'Rarity value and species extinction: the anthropogenic Allee effect', PLoS Biology 4, 2405-2410, https://doi.org/10.1371/journal.pbio.0040415.         [ Links ]

Cousins, S.R., Williams, V.L. & Witkowski, E.T.F., 2011, 'Quantifying the trade in cycads (Encephalartos species) in the traditional medicine markets of Johannesburg and Durban, South Africa', Economic Botany 65, 356-370, https://doi.org/10.1007/s12231-011-9173-0.         [ Links ]

Cousins, S.R., Williams, V.L. & Witkowski, E.T.F., 2012, 'Uncovering the cycad taxa (Encephalartos species) traded for traditional medicine in Johannesburg and Durban, South Africa', South African Journal of Botany 78l, 129-138, https://doi.org/10.1016/j.sajb.2011.06.001.         [ Links ]

Cousins, S.R., Williams, V.L. & Witkowski, E.T.F., 2013, 'Sifting through cycads: a guide to identifying the stem fragments of six South African medicinal Encephalartos species', South African Journal of Botany 84, 115-123, https://doi.org/10.1016/j.sajb.2012.10.004.         [ Links ]

De Klerk, G.J., 2008, 'Report on the census of Waterberg cycad on the Entabeni Safari Conservancy', An internal report by Envirodel, Polokwane for Entabeni Safari Conservancy.         [ Links ]

Donaldson, J.S., 2003, 'Regional overview: Africa', in J.S. Donaldson (ed.), Cycads, status survey and conservation action plan, pp. 9-19, IUCN/SSC Cycad Specialist Group: Gland, Switzerland and Cambridge, UK.         [ Links ]

Donaldson, J.S., 2008, 'South African Encephalartos species', NDF workshop case studies: Case Study 4: Encephalartos, Mexico.         [ Links ]

Government Gazette, 2017, 'Biodiversity management plan for 11 Critically Endangered and 4 Endangered Enceph-alartos species (Notice 315 of 2017)', Government Gazette 40815, 28 April 2017.         [ Links ]

Griffiths, A.D., Schult, H.J. & Gorman, J., 2005, 'Wild harvest of Cycas arnhemica (Cycadaceae): impact on survival, recruitment and growth in Arnhem Land, northern Australia', Australian Journal of Botany 53,771-779, https://doi.org/10.1071/BT04123.         [ Links ]

IBM Corp., 2021, 'IBM SPSS statistics for windows, version 28.0', Armonk, NY: IBM Corp.         [ Links ]

IUCN, 2023, 'The IUCN Red List of threatened species', https://www.iucnredlist.org, viewed 21 January 2023.         [ Links ]

Janse van Rensburg, P.D., Bezuidenhout, H. & Van den Berg, J., 2023, 'Impact of herbivory by Zerenopsis lepida (Lepidoptera: Geometridae) on the Endangered Encephalartos eugene-maraisii under field conditions', Biodiversity and Conservation 32, 2451-2468, https://doi.org/10.1007/s10531-023-02612-z.         [ Links ]

Kéry, M., Matthies, D. & Fischer, M., 2001, 'The effect of plant population size on the interactions between the rare plant Gentiana cruciate and its specialized herbivore Maculinea rebeli', Journal of Ecology 89, 418-427, https://doi.org/10.1046/j.1365-2745.2001.00550.x.         [ Links ]

Krishnamurthy, V., Mandle, L., Ticktin, T., Ganesan, R., Saneesh, C.S. & Varghese, A., 2013, 'Conservation status and effects of harvest on an endemic multi-purpose cycad, Cycas circinalis L., Western Ghats, India', Tropical Ecology 54, 309-320.         [ Links ]

Marler, T.E. & Calonje, M., 2020, 'Two cycad species affect the carbon, nitrogen and phosphorus contents of soil', Horticulture 6, 24, https://doi.org/10.3390/horticultur-ae6020024.         [ Links ]

Marler, T.E., Griffith, M.P. & Krishnapillai, M.V., 2020, 'Height increment of Cycas micronesica informs conservation decisions', Plant Signaling and Behavior 15: e1830237, https://doi.org/10.1080/15592324.2020.1830237.         [ Links ]

Mucina, L., Hoare, D.B., Lötter, M.C., et al., 2006, 'Grassland Biome', in L. Mucina & M.C. Rutherford (eds), The vegetation of South Africa, Lesotho and Swaziland, Strelitizia 19, 349-437, South African National Biodiversity Institute, Pretoria.         [ Links ]

Ndou, T.M., Stam, E.M., Tshisikhawe, M.P., Alabi, M.A. & Adeeyo, A.O., 2021, 'Poaching of Encephalartos transvenosus, in the Limpopo Province, South Africa', Resources 10, 119, https://doi.org/10.3390/resources10120119.         [ Links ]

Oberprieler, R.G., 1995, 'The weevils (Coleoptera: Curculionoidea) associated with cycads. 2. Host specificity and implications for cycad taxonomy', in P. Vorster (ed.), Proceedings of the Third international Conference on Cycad Biology, pp. 335-365, Cycad Society of South Africa: Stellenbosch, South Africa.         [ Links ]

Oberprieler, R.G., 1999, 'Systematics and evolution of the cycad-associated weevil genus Apinotropis Jordan (Coleoptera: Anthribidae)', African Entomology 7, 1-33, https://hdl.handle.net/10520/AJA10213589_385.         [ Links ]

Okubamichael, D.Y., Jack, S., Bösenberg, J.D., Hoffmann, M.T. & Donaldson, J.S., 2016, 'Repeat photography confirms alarming decline in South African cycads', Biodiversity Conservation 25, 2153-2170, https://doi.org/10.1007/s10531-016-1183-x.         [ Links ]

Osborne, R., 1995, 'The world cycad census and a proposed revision of the threatened species status for cy-cad taxa', Biological Conservation 71, 1-12, https://doi.org/10.1016/0006-3207(95)91086-D.         [ Links ]

Raimondo, D.C. & Donaldson, J.S., 2003, 'Responses of cycads with different life histories to the impact of plant collecting: simulation models to determine important life history stages and population recovery times', Biological Conservation 111, 345-358, https://doi.org/10.1016/S0006-3207(02)00303-8.         [ Links ]

Ravele, A.M. & Makhado, R.A., 2010, 'Exploitation of Encephalartos transvenosus outside and inside Mphaphuli Cycads Nature Reserve, Limpopo Province, South Africa', African Journal of Ecology 48, 105-110, https://doi.org/10.1111/j.1365-2028.2009.01086.x.         [ Links ]

Steyn, T. & Bezuidenhout, H., 2020, 'Entabeni biodiversity and conservation value', Internal report for Entabeni Safari Conservancy, Scientific Services, Kimberley, South African National Parks.         [ Links ]

Thomas, C.D. & Jones, T.M., 1993, 'Partial recovery of a skipper butterfly (Hesperia comma) from population refuges: lessons for conservation in a fragmented landscape', Journal of Animal Ecology 62, 472-481, https://doi.org/10.2307/5196.         [ Links ]

Toon, A., Terry, L.I., Tang, W., Walter, G.H. & Cook, L.G., 2020, 'Insect pollination of cycads', Austral Ecology 45, 1033-1058, https://doi.org/10.1111/aec.12925.         [ Links ]

Torgersen, J.S., 2017, 'Crime, culture and collecting: the illicit cycad market in South Africa', Unpublished MSc dissertation, University of Cape Town, South Africa.         [ Links ]

Vovides, A.P., 1990, 'Spatial distribution, survival, and fecundity of Dioon edule (Zamiaceae) in a tropical deciduous forest in Veracruz, Mexico, with notes on its habitat', American Journal of Botany 77, 1532-1543, https://doi.org/10.1002/j.1537-2197.1990.tb11394.x.         [ Links ]

Williamson, J., Maurin, O., Shiba, S.N.S., Van der Bank, H., Pfab, M., Pilusa, M., Kabongo, R.M. & Van der Bank, M., 2016, 'Exposing the illegal trade in cycad species (Cyca-dophyta: Encephalartos) at two traditional medicine markets in South Africa using DNA barcoding', Genome 59, 771-781, https://doi.org/10.1139/gen-2016-0032.         [ Links ]

 

 

Correspondence:
P.D. Janse van Rensburg
e-mail: pjvrensburg18@gmail.com

Submitted: 24 January 2023
Accepted: 12 July 2023
Published: 13 September 2023

 

 

Supplementary Data

The supplementary data is available in pdf: [Supplementary data]