The threats posed by the pet trade in alien terrestrial invertebrates in South Africa

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Abstract

The pet trade has been a major pathway for the introduction of vertebrate invaders, but little is known about its role in invertebrate invasions. Here we assess the trade in terrestrial invertebrates (excluding spiders) in South Africa and the potential of this trade to result in biological invasions and impacts. Pet stores, websites, and expositions were visited, and a list of the taxa traded was compiled. DNA barcoding was used to determine if the species were correctly identified in the trade. Information on invasion history and impact elsewhere was used to assess the potential for species to become invasive and have impact in South Africa. We found 53 alien terrestrial invertebrate taxa that were traded, although only 36 of these matched a valid species name. Of 11 species tested using DNA barcoding nine were correctly identified. Species accumulation curves were produced, but did not reach an asymptote, suggesting there are many species in the trade that were not recorded. The most common species were used as food for pets, rather than as pets themselves. None of the species were reported to be invasive elsewhere, and few had records of causing negative impacts (the exception being moderate impacts to human health caused by venomous scorpions). Therefore, there is little evidence that the invertebrates traded pose a significant threat to South Africa. However, given uncertainties in which taxa are traded and the lack of data on invasiveness and impact, there might be a significant invasion debt. We recommend continued monitoring and engagement with the industry.

Introduction

Every year, billions of live animals are transported around the world as part of the pet trade (Broad, Mulliken, & Roe, 2003; Karesh, Cook, Bennett, & Newcomb, 2005; Kopecky, Patoka, & Kalous, 2016). Species are traded for ornamental (Ng et al., 2016) and recreational purposes (Cambray, 2003), and as food for pets (Haggett, 2013). Once these species are in the pet trade, they could be released by humans or escape from captivity (Cadi & Joly, 2003; Faulkes, 2010). Those individuals or populations of introduced species that are able to survive and reproduce can become invasive (Ernst & Lovich, 2009). For example, in South Africa, the common myna (Acridotheres tristis) was introduced into the pet trade, later escaped, and has subsequently spread throughout southern Africa (Peacock, van Rensburg, & Robertson, 2007). The increased popularity of alien pets has led to more species being introduced globally, making the pet trade a significant pathway for introducing new species (van Wilgen et al., 2010; Papavlasopoulou, Vardakas, Perdikaris, Kommatas, & Paschos, 2013; Mori et al., 2017; Lockwood et al., 2019).

There are many different sources (e.g. pet stores and internet) from which people can obtain pets. As with the trade in other commodities, there has been an increasing amount of trade in pets over the internet (Kikillus, Hare, & Hartley, 2012; Derraik & Phillips, 2010). For example, over 500 terrestrial invertebrate species are offered for sale on one website alone (https://www.bugzuk.com; accessed: 4 June 2017). The internet has thus increased accessibility to more species from a range of taxa (Bush, Baker, & Macdonald, 2014).

The likelihood that species sold in the pet trade will establish is affected, in part, by the number of different species introduced (i.e., the colonisation pressure) and the number of individuals of a specific species introduced in combination with the number of introduction events (i.e., the propagule pressure) (Lockwood, Cassey, & Blackburn, 2009). The more species introduced into a single area, the higher the likelihood that one of these species will be able to establish and become invasive. Similarly, the higher the propagule pressure of a specific species, the more likely that species will establish and become invasive. The size of the trade, in terms of the number of species and the number of individuals of those species traded, therefore determines colonisation and propagule pressure (Marr et al., 2017). Moreover, humans also directly influence the probability of an invasion by either keeping specimens in captivity (and so, to various degrees, limiting the likelihood of an unintentional escape) or by intentionally releasing individuals (Maceda-Veiga et al., 2019).

In South Africa, the role of the pet trade as a pathway for the introduction of species has been studied for reptiles (van Wilgen et al. 2010), amphibians (Measey et al., 2017), and tarantulas (Shivambu, 2018). But there has not been a general assessment of the terrestrial invertebrate trade. However, at least one traded terrestrial invertebrate species has escaped from captivity and established. The Indian walking stick insect (Carausius morosus) was introduced to South Africa for research purposes and as a pet species, and subsequently established a population in the Cape Floristic Region (Picker & Griffiths, 2011; Picker, Griffiths, & Weaving, 2002). After the species established, the whole order Phasmatodea was regulated in South Africa under the Alien and Invasive Species Regulations of the National Environmental Management: Biodiversity Act [NEM:BA A&IS Regulations (DEA, 2016)] — however there has not been a detailed risk analysis conducted for any of the species in this group to date.

If an invasion does occur, it can cause devastating environmental and socio-economic impacts (Olson, 2006; Vila et al., 2011). Invasive species can outcompete native species (Cadi & Joly, 2004; Polo-Cavia, Lopez, & Martın, 2008), cause biodiversity loss (Wan, Guo, & Wang, 2002), and spread diseases and pathogens that are harmful to humans or native species (Haenen, Way, Bergmann, & Ariel, 2004; Weir et al., 2012). For example, the red imported fire ant (Solenopsis invicta), which is native to south America, is invasive in Texas and has reduced the diversity of native ants in areas where it has invaded (Porter & Savignano, 1990). In order to address these impacts, Aichi Biodiversity Target 9 specifies that damaging alien species should be identified and prioritised for management (CBD, 2013).

Countries, therefore, need to compile an inventory of alien species as it serves as a first reference point in the management of biological invasions (Roy et al., 2014). These inventories are needed in order to know which species are present and potentially harmful, and which species require management (Latombe et al., 2016; McGeoch, Spear, Kleynhans, & Marais, 2012; Regan, Colyvan, & Burgman, 2002). Accurate and taxonomically correct lists are also important because they can help inform the prevention of future invasions. However, even lists of supposedly well-known groups contain many errors and inconsistencies (e.g., Magona, Richardson, Le Roux, Kritzinger-Klopper, & Wilson, 2018). This is particularly an issue in the pet trade where valid scientific names are not consistently used (Bartlett, Griswold, & Bartlett, 2001) and species are misidentified (Petersen et al., 2007).

Once an inventory of alien species is compiled, one of the most common approaches to identify the taxa that could cause harm is to estimate the likelihood and consequence of an invasion by a particular species by assessing its history of invasion and impact elsewhere in its introduced range (Hulme, 2012; Kulhanek, Ricciardi, & Leung, 2011; Weber, Panetta, Virtue, & Phelong, 2009). To facilitate such analyses, various impact scoring schemes have been developed in order to assess the impact of alien species and facilitate their prioritisation for management, for example the Environmental Impact Classification for Alien Taxa (EICAT) and Socio-Economic Impact Classification for Alien Taxa (SEICAT) (Bacher et al., 2018; Hawkins et al., 2015).

The aims of this study were to: 1) determine the size of the trade (number of species and their availability) in alien terrestrial invertebrates in South Africa; 2) test the accuracy of the identification of the traded terrestrial invertebrates using DNA barcoding; 3) assess the uses of the traded species; and 4) assess the potential of the traded species to become invasive and cause negative impacts.

Section snippets

Data collection

We considered three main ways in which alien terrestrial invertebrates are sold as part of the pet trade – in pet stores; at expositions (large public exhibitions where breeders, pet stores owners and hobbyists gather to sell and buy a variety of species); and over the internet (both dedicated commercial sites and sales offered on general sites). A total of 64 pet stores, 12 websites, and 18 breeders (from five different expositions) were visited. As there are a large number of tarantula

Results

We recorded 60 names of terrestrial invertebrate taxa in the pet trade, of which seven correspond to species native to South Africa (Scorpiones; Parabuthus capensis, Parabuthus transvaalicus, Hadogenes troglodytes, Blattodea; Oxyhaloa deusta, Coleoptera; Anisorrhina flavomaculata, Rhabdotis aulica and Pachnoda sinuata). These native species were excluded from further analysis. Of the other 53 taxa, 36 names (i.e. 64 %) corresponded to species alien to South Africa while 17 names could not be

Discussion

Terrestrial invertebrates have been introduced for many purposes (Kumschick et al., 2016) including for: animal feed (Kenis et al., 2014), pets (Edward & Hibbard, 1999), food for pets (Haggett, 2013), habitat and soil improvement (Baker, Brown, Butt, Curry, & Scullion, 2006), live exhibits (Boppre & Vane-Wright, 2012), conservation purposes (Winston et al., 2014), the silk production (Murakoshi, Chang, & Tamura, 1972), and ornamental trade (New, 2008). We found that the pet trade in South

Declaration of conflicting interest

There is no conflict of interest from all authors

Acknowledgements

The South African Department of Forestry, Fisheries, and the Environment (DFFtE) are thanked for funding noting that this publication does not necessarily represent the views or opinions of DFFtE or its employees. We also acknowledge the DSI-NRF Centre of Excellence for Invasion Biology for their support. We thank two anonymous referees for comments which helped to improve the manuscript.

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      Citation Excerpt :

      In South Africa, the trade of wildlife as pets is relatively young but has increased as they have become a popular hobby (van Wilgen et al., 2010; Nelufule et al., 2020; Shivambu et al., 2021a). The trade of wildlife in South Africa involves a range of taxa, including amphibians, reptiles, birds, fishes, invertebrates, small mammals, and birds (van Wilgen et al., 2008; Symes, 2014; Marr et al., 2017; Measey et al., 2017; Nelufule et al., 2020; Shivambu et al., 2021a). Some of these animals have established, spread, and become invasive, for example, frogs (Lithobates catesbeianus and Xenopus laevis) (Measey et al., 2017), rose-ringed parakeets (Psittacula krameri) (Hart & Downs, 2015; Shivambu et al., 2020d), and red-claw crayfishes (Cherax quadricarinatus) (Nunes et al., 2017).

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