South Africa as a Donor of Its Native and Exotic Species to the International Pet Trade

Abstract

The global pet trade is a thriving multibillion-dollar industry, involving the international exchange of various species and regulated by the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). South Africa plays a significant role as both an importer and exporter within this market. By analysing over 13 million records from the CITES database, spanning from 1975 to 2023, we aimed to access South Africa’s role in the international pet trade and to analyse trade volume and trends over time. Our findings indicate that alien species dominate exports, particularly birds and mammals, while native species are traded in lower volume, involving only a few species. The top 10 traded species for birds and mammals belong to the genera Agapornis and Callithrix, while 80% of reptile exports were native, with Stigmochelys pardalis being the most exported species. Bird and mammal exports are primarily composed of captive-bred individuals, whereas both captive-bred and wild-sourced individuals contribute to reptile exports. Approximately 100 countries import various species from South Africa, with Asia and Europe as major importers of birds. The extensive exportation of South Africa’s native species, particularly reptiles, raises significant conservation concerns regarding the potential impact on local biodiversity.

1. Introduction

The pet trade is a global phenomenon which involves the exchange of species across international borders [1,2,3,4,5]. About 184 countries are signed as members of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), these countries trade exotic pet species, either as importers, exporters or transit points facilitating the movement of species [6,7,8]. As a result, the pet trade sector has evolved into a multibillion-dollar enterprise, reflecting the demand for exotic pets worldwide [7,9,10]. The demand for these animals has raised ethical, conservation and welfare concerns [11,12,13]. Moreover, the pet trade can drive unsustainable species harvest, resulting in some species becoming critically endangered [14,15]. In addition, some species have become invasive due to intentional release and accidental escapees from captivity [4,10]. Studies have also identified exotic pets as one of the major sources of emerging infectious diseases [16,17].

The heightened impacts and scrutiny of the pet trade industry have resulted in governments taking regulatory actions, e.g., the CITES convention [2,18,19,20]. Efforts to address these concerns have focused on promoting sustainable trade practices, enhancing animal welfare, and implementing measures to mitigate the spread of invasive species and zoonotic diseases [16,21,22]. The CITES has played an important role in implementing these initiatives, although some countries still face challenges associated with illegal trade and poaching [23,24,25]. South Africa, for example, has been identified as one of the countries facing ongoing illegal trafficking of species and unsustainable trade practices [23,26,27].

South Africa joined the CITES treaty in November 1976 and has since played a major role in the international pet trade, both as an importer and exporter of different animal species [28,29,30]. The country’s pet trade involves the sale of different taxa, including amphibians, birds, fish, mammals, and reptiles which are either native or alien [31,32,33,34,35,36]. Over the years, South Africa has gained recognition for its expertise in captive breeding [36,37]. As a result, the country has been re-exporting species that are not native to its territory to other countries. For example, South Africa has gained a prominent role as one of the significant players in the global parrot trade, serving as both the importer and exporter to the markets in Western and Southeast Asia [34,36].

This study aimed to determine South Africa’s role in the international pet trade, focusing on its involvement as both an importer and exporter of various animal species. We also aimed to understand the trade volume and analyse temporal trends of South Africa’s contribution to the pet trade industry. Through this investigation, we aim to shed light on the implications of South Africa’s involvement in the pet trade for conservation efforts and the sustainable management of species.

2. Materials and Methods

2.1. Data Collection

We gathered pet trade data from the CITES trade database (https://trade.cites.org/, accessed on the 13 June 2024), which contains over 13 million records covering 34,000 species of fauna and flora. Previous research has utilized this database to analyse legal international trade, animal welfare, and conservation issues [38]. The database is maintained by the United Nations Environment Programme World Conservation Monitoring Centre (UNEP-WCMC) on behalf of the CITES Secretariat. It includes trade data from 1975 to the present, spanning 49 years. For this study, we downloaded import and export trade data for native and alien species of amphibians, birds, mammals, reptiles, and other taxa (invertebrates) traded from South Africa (Table S1). We only included taxa recorded as live from 1975 to 2023 (48 years). The information collected comprised: (1) import and export data, (2) taxa and species, (3) year, (4) quantity (total number of import and export), (5) source of trade (C and D (Appendix I): captive-bred, F: born in captivity, I: confiscations/seizures, W: wild), and (6) purpose of trade (T: commercial, P: personal, B: breeding in captivity). We define “captive-bred” as a lineage of animals bred in captivity over multiple generations, and “born in captivity” refers to animals born in captivity regardless of whether their parents were wild-caught or captive-bred, and it focuses on the location of birth rather than breeding process [39]. To verify if the selected species on CITES are traded as pets, we searched for their use and trade on the International Union for Conservation of Nature (IUCN) (https://www.iucnredlist.org/, accessed on the 13 May 2024). If the use and trade are indicated as pets or display animals, we concluded that the species are traded as pets.

2.2. Data Analysis

All statistical analyses were performed using the R statistical software version 4.3.2 [40], covering data from 1975 to 2023. We employed Pearson’s Chi-squared test to assess the differences in the number of native and alien species exported by South Africa. Additionally, a paired t-test was conducted to compare the export volumes of alien versus native taxa over the years. To analyse differences in the sources of trade, we performed the Kruskal-Wallis Chi-squared test, followed by the Pairwise Wilcoxon test with Bonferroni-adjusted p-values.

3. Results

3.1. Number of Species Exported

Our results showed that South Africa is involved in the international pet trade of both native and alien species. We found that there was a significant difference between the number of alien and native species exported from South Africa to other countries (X² = 13.61, df = 3, p < 0.05) (Figure 1). South Africa exports 77% (n = 385) of alien species compared to 23% (n = 114) of native species. The most significant difference is observed in birds’ exports, followed by reptiles and mammals (Figure 1). South Africa exports 298 alien species of birds compared to 83 native species. In the case of mammals, 26 alien species are exported versus only three native species (Figure 1). South Africa exports 50 alien species of reptiles compared to 28 native species (Figure 1). In other taxa, none of the South African native species are exported. This includes species from the following taxa: Anthozoa (two species), Amphibia (two species), Arachnida (four species), Actinopterygii (two species), and Insecta (one species) (Figure 1 and Figure 2).

3.2. Temporal Trend Analysis

The trend analysis over the years (1981–2022) showed that individuals of alien birds and mammals were mainly exported when compared to reptiles, where native species were mostly exported (Figure 3). We found that there was a significant difference between the volume of alien bird exports over the years when compared to the volume of native bird exports (t (40) = 4.9753, p < 0.0001) (Figure 3a). A paired t-test showed that the mean difference between alien and native bird exports was 105,227.5, with a 95% confidence interval ranging from 62,481.48 to 147,973.45 (Figure 3a). This indicates that alien bird exports have been substantially higher than native bird exports over the years, with a notable surge since the mid-2000s (Figure 3a). Similarly, alien mammal exports were significantly higher than native mammal exports over the years (t (41) = 5.304, p < 0.0001) (Figure 3b). The mean difference in export volumes was 464.1905, with a 95% confidence interval ranging from 287.4472 to 640.9337 (Figure 3b).

Alien mammal exports have increased markedly since the mid-1990s, with notable peaks (1998–2003, 2009–2014, 2017–2019), whereas native mammal exports have risen more gradually, particularly from 2014 (Figure 3b). Conversely, we found that native reptiles were exported in higher volumes when compared to alien reptiles (t (41) = −5.0638, p < 0.0001) (Figure 3c). The mean difference in export volumes was −447.7073, with a 95% confidence interval ranging from −626.3979 to −269.0168 (Figure 3c). Reptile exports showed a considerable fluctuation, especially for native species, with noticeable peaks around certain years (1992–1994, 2009, 2010, 2012–2014, 2020), while alien reptile exports remain relatively low but slightly increasing (Figure 3c). The export volume of other alien species has remained minimal until a sharp rise around 2018 (Figure 3c). Overall, more birds were exported from South Africa than any other taxa (trade volume up to half a million). This was followed by mammals and reptiles (Figure 3c). Other taxa were, however, exported in hundreds (Figure 3d).

3.3. Top Ten Exported Species

The analysis of export volumes for the top 10 bird species exported from South Africa revealed that all exported bird species, except Agapornis roseicollis were alien. Order Psittaciformes dominated the trade (Figure 4a). The genus Agapornis was most frequently exported, with A. fischeri leading the trade at approximately 900,000 individuals (Figure 4a). This was followed by A. personatus, with around 800,000 birds exported. Species such as Psittacus erithacus, Aratinga solstitialis, and A. roseicollis were exported in the tens of thousands (Figure 4a). Other species such as Pyrrhura molinae, A. nigrigenis, A. lilianae, Amazona aestiva, and Myiopsitta monachus had export volumes ranging from 25,000 to 194,897 birds (Figure 4a).

Similarly, for mammals, only alien species were major exports from South Africa. The trade was dominated by two orders, Carnivora (three species) and Primates (seven species), with the genus Callithrix comprising a significant portion (Figure 4b). The most exported species included Callithrix jacchus, with 15,199 individuals exported, followed by Callithrix penicillata, with 4878 individuals (Figure 3b). Species such as Cebus apella, Vulpes zerda, Saguinus oedipus, Cebus olivaceus, Callithrix geoffroyi, Panthera tigris, and Saimiri boliviensis had export volumes of less than 1000 (Figure 4b).

In contrast, for reptile exports, the majority (80%) of species were native to South Africa, including three endemic species (Figure 4c). The trade was dominated by three genera, Sauria, Serpentes, and Testudines, with most species belonging to Sauria. Stigmochelys pardalis was the most exported species, with approximately 13,500 individuals traded (Figure 4c). This was followed by Chersina angulate and Python regius, each with over 2000 individuals exported (Figure 4c). Species such as Varanus albigularis, Smaug giganteus, Bradypodion transvaalense, Smaug warreni, Bradypodion thamnobates, Centrochelys sulcata, and Homopus areolatus had export volumes of less than 1000 individuals (Figure 4c).

3.4. Rare and Threatened Species

Our analysis revealed that 65 species are classified as threatened and confined to a single geographical range (

Table 1. Number of rare and threatened species exported by South Africa to other countries.

Class	Near Threatened	Vulnerable	Endangered	Critically Endangered
Birds	12	17	16	5
Mammals	0	1	3	1
Reptiles	1	2	0	4
Other	0	1	1	1

). Among birds, many are categorized as vulnerable, endangered, or near threatened. Critically endangered bird species include Ara glaucogularis, A. rubrogenys, Cyanoramphus malherbi, Lathamus discolor, and Zanda baudinii (Table S1). The first three bird species are endemic to Bolivia, while L. discolor is endemic to New Zealand, and Z. baudinii endemic to Australia (Table S6). A total of 56 countries participate in the import of threatened bird species, with Portugal and Spain being the leading importers (Figure S2). The trade also includes A. fischeri, one of the top 10 most traded birds, which is listed as near threatened and traded by 28 countries (Table S6). The trade of threatened mammals includes one vulnerable species (Eulemur fulvus), three endangered species (Callithrix aurita, Chinchilla lanigera, and Lemur catta), and one critically endangered species, S. Oedipus, which is one of the top 10 exported mammal endemic to Colombia. Callithrix aurita is endemic to Brazil, while C. lanigera is endemic to Chile, and L. catta is endemic to Madagascar (Table S6). Countries involved in the trade of mammals include the United Arab Emirates, Namibia, and Thailand (Figure S3). The trade of reptiles includes one near-threatened species, Calumma parsonii endemic to Madagascar, and two vulnerable species, S. giganteus (one of the top 10 traded), and Zonosaurus quadrilineatus. These species are endemic to South Africa and Madagascar, respectively (Table S6). Critically endangered traded reptiles include Astrochelys radiata, Geochelone platynotan, Pyxis arachnoides and P. planicauda. All these four species are endemic to Madagascar. Twelve countries participate in the trade of these reptiles, and the USA is the largest importer (Figure S4). Other species traded include two arachnids and one amphibian, with the arachnid species listed as near threatened (Brachypelma smithi), and the amphibian species endangered (Mantella aurantiaca) and critically endangered (Ambystoma mexicanum). Brachypelma smithi and Ambystoma mexicanum are endemic to Mexico, while Mantella aurantiaca is endemic to Madagascar. Only Botswana and the UK are involved in importing these species (Table S6, Figure S5).

3.5. Sources of Trade

The total export of live animals between 1981 and 2022 predominately consisted of captive-bred animals for all the taxa, followed by those born in captivity, wild-sourced, and confiscated (Figure 5). We found that there was a significant difference between the sources of trade for pet birds, with the majority being captive-bred (χ² = 86.34, df = 3, p < 0.05) (Figure 5a). The export of captive-bred birds significantly increased from the mid-2000s, peaking around 2018 and 2020 (Figure 5a). Birds born in captivity contributed less to the total exports, while wild-caught and confiscated birds constituted a small proportion of the total exports (Figure 5a). Captive-bred birds were exported to 142 countries, birds born in captivity to 46 countries, while wild and confiscated birds were exported to 54 and four countries, respectively (Table S2).

Similarly, for mammals, there was a significant difference between the sources of trade, with captive-bred individuals being the primary source (χ² = 73.89, df = 3, p < 0.05) (Figure 5b). The export of captive-bred mammals increased from the early 2000s, peaking in the mid-2010s (Figure 5b). Mammals born in captivity, wild-caught, and confiscated represented minimal contributions to the overall trade volume (Figure 5b). A total of 104 countries imported captive-bred mammals, while mammals born in captivity were exported to 46 countries. Additionally, 31 and three countries imported wild-caught and confiscated mammals, respectively (Table S3).

In the case of reptiles, we found that there was a significant difference between trade sources (χ² = 138.49, df = 3, p < 0.05) (Figure 5c). The Wilcoxon Pairwise test indicated that reptiles born in captivity and confiscated were exported in significantly lower volumes when compared to wild-sourced and captive-bred individuals (Figure 5c). Most traded reptiles were from captive-bred sources, with an increase observed in the late 2000s (Figure 5c). Wild-sourced reptiles had higher export volumes, particularly in the late 1990s and early 2000s, whereas those born in captivity and confiscated made minimal contributions to the total exports (Figure 5c). A total of 44 countries imported captive-bred reptiles, while 19 countries imported reptiles born in captivity, and 30 countries imported wild-sourced reptiles. Three countries imported confiscated reptiles (Table S4). Other taxa were predominantly associated with the export of animals born in captivity (eight countries) and wild-sourced (one country) individuals (Figure 5d; Table S5).

3.6. Importing Countries

We found that 100 countries import different species from South Africa (Figure S1). Birds were identified as the most imported taxa, followed by mammals and reptiles (Figure 6 and Figure S1). Regarding regional trends, Asia and Europe were the major importers of birds, with countries such as Oman, Qatar, Malaysia, Spain, Belgium, Czech Republic, France, and Germany importing significant volumes (Figure 6 and Figure S1). North America and South America also contributed significantly to bird imports, with Mexico and the United States of America (USA) contributing the most (Figure 6). Asia imports birds and mammals in large quantities; for example, Japan imports 11,781 birds and 416 mammals, while China imports 111 mammals and 109 birds in total volume over the years (Figure 6 and Figure S1). Some countries import a variety of species; for example, Indonesia is the major importer of birds, mammals, and reptiles (Figure S1). However, a country like Kenya imports few birds and mammals but more reptiles, indicating a focus on reptiles (Figure S1). Certain countries specialize in specific taxa; for instance, Madagascar imports a significant number of reptiles compared to other species (Figure S1). Kuwait shows a particular interest in reptiles and birds. Many countries import relatively small volumes of species, suggesting either niche markets or less emphasis on wildlife trade (Figure S1). Examples include Luxembourg (one bird), Iceland (30 birds), and Croatia (three birds) (Figure S1). Only three countries import other species; this includes Botswana, Eswatini, the United Kingdom, and the USA (Figure S1).

4. Discussion

The pet trade is one of the growing businesses in South Africa, generating revenue and creating job opportunities. For example, there are over 100 pet shops across South Africa, and different breeders specializing in specific taxa (invertebrates, birds, and mammals) [41,42,43,44]. The country has become an active consumer as an exporter of alien live species traded internationally for the pet industry [29,30,34,36,37]. This study provides an important insight into the scope and scale of CITES-listed species exported from South Africa to different parts of the world. We found that alien birds, mammals and reptiles were mainly exported compared to native species. Conversely, only alien species were exported for the following taxa, Anthozoa, Amphibia, Arachnida, Actinopterygii, and Insecta. This trend may be due to the conservation status of native species, which often restricts their trade. For example, it is illegal to keep, collect, and trade some of the native species in most South African provinces (https://cer.org.za/virtual-library/legislation, accessed on 23 July 2024). In addition, the CITES may impose stricter controls on the trade of native species to protect biodiversity and prevent over-exploitation [45,46].

Our temporal analysis from 1981 to 2022 reveals dynamic trends in species export volumes, particularly highlighting the dominance of alien species in the trade. The main volume of bird and mammal exports were alien species. This suggests a sustained demand for alien birds and mammals over the years. None of the top ten exported birds and mammals were native to South Africa. This is unsurprising, especially for birds, as certain species are preferred in the international pet trade. For example, parrots are the most traded group, favoured for their ability to mimic voice, vibrant colours, and adaptability [30,37,47]. Notably, Psittaciformes, particularly species such as Agapornis fischeri and Agapornis personatus were exported in high volumes, highlighting their popularity in the global pet trade. South African native birds are not common in the international pet trade; hence, we found that none of them are in the top 10 most commonly traded species. Given this, several breeding facilities in South Africa breed parrots for export to different parts of the world, particularly Western and Southeast Asia markets [34,36].

South African native mammalian species are not commonly traded as pets, as documented in Shivambu et al. [35]. Primates and carnivores were the most traded groups, with primate species such as C. jacchus and C. penicillata traded in large volumes. Primates are often used in biomedical research and testing due to their physiological similarities to humans [48,49]. As a result, the demand for primates in the pet trade and research sectors contributes to their significant presence in international trade. None of the South African primates and carnivores are common as pets in the global pet trade. As a result, it is not surprising that the country does not export most of its native primates and carnivores. However, for reptiles, the main volume of reptile exports were native species, this raises concerns about the possible impact on the state of biodiversity. Furthermore, the trade of the top ten reptile species included endemic species. Species such as S. pardalis and Chersina angulata dominated the trade. Consequently, S. pardalis has been overexploited for the pet trade and is considered threatened in some regions of the country [50]. The fact that South African native species make up the trade for the most exported volume is concerning, given that some species are endemic and have restricted geographical distribution. These species may be threatened as they are restricted to small areas. For example, H. areolatus is only found in the Western Cape, Northern Cape, and Eastern Cape provinces, while B. thamnobates is restricted to KwaZulu-Natal province and S. giganteus in Free State and Mpumalanga provinces.

The findings of this study highlight the significant pressures faced by a select group of species within the global trade network, particularly those restricted to a single geographical range. The inclusion of A. fischeri, a near-threatened species traded by 28 countries and ranked among the top 10 most traded birds, raises concerns about the sustainability of such practices. In the case of mammals, the data reveal a more concentrated trade network, with only two countries involved, yet the impact on species is severe. The United Arab Emirates’ role as the main importer of endangered mammals is particularly concerning, as it includes the critically endangered S. oedipus, which is among the top 10 most exported mammals. This suggests a high demand for species that are already on the brink of extinction, posing a significant risk to their survival. Reptiles, on the other hand, present a different challenge. The fact that the majority of traded reptiles are critically endangered, with the USA leading as the top importer, points to a potentially unsustainable demand for these species. The vulnerability of S. giganteus, a top 10 traded reptile species, further emphasizes the precarious state of reptilian conservation. The trade in other species, including arachnids and amphibians, while less extensive, still raises important conservation concerns. The involvement of Botswana and the UK in importing these species indicates that even less prominent taxa are not prone to the pressures of international trade. The near-threatened status of the arachnid species and the critically endangered status of the amphibian species highlight the need for vigilant monitoring and regulation of this trade to prevent further declines. Overall, this analysis sheds light on the complex and often alarming dynamics of species trade, where the demand for certain species, particularly those that are threatened, endangered, or critically endangered, poses a significant threat to global biodiversity. The concentrated nature of this trade, with specific countries acting as major importers, highlights the need for targeted conservation efforts and stricter regulation of international wildlife trade to protect these vulnerable species from further exploitation.

The trade sources for all the taxa species reveal a significant reliance on captive breeding, especially for birds and mammals, indicating efforts to meet market demand while reducing pressure on wild populations sustainably. Our analysis showed that the shift towards captive breeding has occurred since the early 2000s, aligning with global conservation initiatives aimed at curbing illegal wildlife trade and promoting sustainable practices. Wild-sourced and confiscated individuals contributed minimally to export volumes, suggesting effective enforcement of wildlife regulations in exporting countries, particularly for birds and mammals. However, wild-sourced reptiles had higher export volumes than those born in captivity and confiscated. Consequently, some reptile species’ populations may decline as they are sourced directly from the wild. For example, in 2018, species such as H. areolatus, S. warren, C. angulate and S. pardalis were sourced directly from their natural habitats. Removing these species from the wild is not defensible because captive-bred individuals existed before 2018, demonstrating the presence of breeding facilities in the country for these species. Given this, it is important for regulatory bodies in different countries to be stringent enough to control the import of wild-sourced reptiles.

We found that 100 countries import native and alien species from South Africa. Countries in Asia and Europe emerged as major import hubs for birds, mammals, and reptiles. North America also imports large volumes of birds. The substantial importation of these species could indicate that these countries have large pet markets. For example, Germany plays a role in the European Union as the hub and destination for exotic pets from different countries [51]. On the other hand, the USA has been identified as one of the largest consumers of wildlife for pet trade purposes [52]. Germany, the USA, Japan, France, the United Kingdom, and Hong Kong emerged as the top South African endemic reptile species importers. Consequently, the demand for unique exotic pets drives illegal wildlife trade, further impacting biodiversity [53]. For example, we found that some bird and reptile species were confiscated, and the top importing countries included the USA, Czech Republic, and Portugal.

5. Conclusions

In conclusion, South Africa plays a pivotal role in the global pet trade, with alien species, particularly birds and mammals, exported to different countries in large volumes compared to native species. The substantial increase in export volumes of alien birds and mammals in recent decades points to the growing demand and South Africa’s expertise in captive breeding. In contrast, the export of native reptiles remains significant, with a notable contribution from both captive-bred and wild-sourced individuals. The diverse range of importing countries, predominantly in Asia and Europe, highlights the global reach and impact of South Africa’s pet trade. As the international pet trade continues to evolve, it is crucial for policymakers and conservationists to work together to ensure sustainable practices that protect biodiversity. Future efforts should strengthen regulations, enhance public awareness, and promote sustainable trade practices to safeguard native and alien species involved in the global pet trade.