Research Article |
Corresponding author: Adam Toomes ( adam.toomes@adelaide.edu.au ) Academic editor: Daniel Sol
© 2020 Adam Toomes, Oliver C. Stringham, Lewis Mitchell, Joshua V. Ross, Phillip Cassey.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Toomes A, Stringham OC, Mitchell L, Ross JV, Cassey P (2020) Australia’s wish list of exotic pets: biosecurity and conservation implications of desired alien and illegal pet species. NeoBiota 60: 43-59. https://doi.org/10.3897/neobiota.60.51431
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Globalisation of the live pet trade facilitates major pathways for the transport and introduction of invasive alien species across longer distances and at higher frequencies than previously possible. Moreover, the unsustainable trade of species is a major driver for the over-exploitation of wild populations. Australia minimises the biosecurity and conservation risk of the international pet trade by implementing highly stringent regulations on the live import and keeping of alien pets beyond its international CITES obligations. However, the public desire to possess prohibited alien pets has never been quantified and represents a number of species that could be acquired illegally or legally under different future legislative conditions. As such, highly desirable species represent an ongoing conservation threat and biosecurity risk via the pet-release invasion pathway.
We aimed to characterise the Australian desire for illegal alien pets and investigate potential sources of external information that can be utilised to predict future desire. Using public live import enquiry records from the Australian Commonwealth Department of Agriculture, Water and the Environment as a proxy for alien pet desire, we tested for differences in the proportion of species with threatened listings and records of invasions, after accounting for taxonomy. Additionally, we used a United States of America (U.S.) live imports dataset to infer pet demand in another Western market with less stringent regulations and determined whether species highly desired in Australia had higher U.S. trade demand than would be expected by chance.
The Australian public desire for alien pets is heavily and significantly biased towards species threatened with extinction, species popular in the U.S. trade and species with a history of successful invasions. Not only does this indicate the potential impacts of pet desire on invasion risk and the conservation of threatened species, but we also highlight the potential role of the U.S. trade as an effective predictor for Australian desire. Our research emphasises the value of novel datasets in building predictive capacity for improved biosecurity awareness.
alien, invasive species, non-native, smuggling, wildlife trade
Globalisation of trade and tourism has led to substantial changes in the international trade of live pets (
Australia has experienced an increased rate of IAS incursions over the last two decades, particularly from species prominent in the international pet trade, such as rose-ringed parakeets (Psittacula krameri), corn snakes (Pantherophis guttatus) and red-eared sliders (Trachemys scripta elegans) (
Australia implements wildlife trade restrictions beyond its’ CITES obligations (
While it is important to consider Australia’s acquisition of alien pets from the perspective of biosecurity risk, there are also potentially serious conservation implications. The unsustainable harvest and trade of species at rates exceeding their reproductive output can be a major driver of biodiversity loss (
Quantifying and characterising public demand for alien wildlife is extremely difficult given that the keeping of most alien pets in Australia is illegal or unregulated by any domestic permit system (
The Australian Department of Agriculture, Water and the Environment (DAWE) maintains a hotline for people to enquire about the legality of importing or owning a particular species in Australia. A DAWE policy officer answers and responds to the enquiry and records non-identifiable information about each request. The information recorded by the officer, if supplied by the caller, includes: (i) the date the enquiry occurred; (ii) the location of the enquirer (city or State/Territory); (iii) the species enquired about; (iv) the action (importing, keeping/owning, breeding); and (v) whether the action was for private or commercial reasons. We acquired this dataset for all enquires lodged from October 2017 to April 2019, which contained a total of 150 phone calls. We acknowledge that the sample size of this dataset is relatively small; however, as we are using the data to identify broad-scale biases, we assumed the data to be sufficiently representative of highly-desired alien pets. Moreover, as enquiries are free and anonymous, we assumed the set of anonymous callers to be an unbiased representation of pet keepers/traders with an interest in importing alien pets.
We categorised the stated use of the animal into six categories: (i) pet (private use); (ii) zoo (commercial use for display in a zoo/wildlife park); (iii) exhibitor (commercial use for exhibition/show); (iv) breeding pets (commercial use to breed as pet); (v) breeding food (commercial use to breed as food); (vi) other (not otherwise specified). If an enquirer specified multiple intended uses, all use types were recorded. We referenced species and common names against the Global Biodiversity Information Facility (
The U.S. maintains a database of imports/exports of live organisms and wildlife products, called the Law Enforcement Management Information System (LEMIS), which is maintained by the U.S. Fish and Wildlife Service (see
We compared four metrics between species in DAWE enquiries and U.S. imports: (i) popularity in the trade; (ii) the proportion of threatened taxa; (iii) the proportion of taxa with international trade restrictions; and (iv) the proportion of species known to be invasive species elsewhere. To compare the proportion of threatened taxa, we matched each species from DAWE enquiries and LEMIS imports to their IUCN Red List designations: Data Deficient (DD), Least Concern (LC), Near Threatened (NT), Vulnerable (VU), Endangered (EN) and Critically Endangered (CR) (IUCN 2019). For the purpose of our analysis, we re-categorised the Red List designation into a binary variable: Not Threatened (LC and NT) and Threatened (VU, EN and CR). Species listed as “Data Deficient” were excluded from our analysis. We created a binary variable because we had small sample sizes for some IUCN designations. To compare proportions of trade-restricted taxa, we recorded whether species were listed in the Appendices of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) (UNEP-WCMC 2019). Finally, we used the Global Invasive Species Database (GISD) to determine if a species has a history of successful invasions (ISSG 2019). We supplemented this dataset to include species known to the authors as being considered invasive in peer-reviewed scientific literature, for example, established populations of Argentine black and white tegus (Salvator merianae) in Florida (
We performed four analyses comparing the species in the phone enquiries with the species in exotic pet trade at large (i.e. species from U.S. imports). First, we compared the popularity (see U.S. imports of live animals) of the species in the phone enquiries to the overall popularity of species in the exotic pet trade at large. Next, we compared whether the proportion of threatened species (i.e. species listed in the IUCN Red List) in the phone enquiries differs from the proportion of threatened species in the exotic pet trade at large. Then, we tested whether the proportion of species with trade restrictions (i.e. species listed in CITES appendix) in the phone enquiries differs from the proportion of species with trade restrictions in the exotic pet trade at large. Finally, we tested whether the proportion of species known to be invasive species elsewhere (whether or not in a GISD database) in the phone enquiries differs from the proportion of species known to be invasive species elsewhere in the exotic pet trade at large.
To test these hypotheses, we performed a series of empirical hypothesis tests (analogous to two-tailed t-tests but for ranked data; also known as bootstrap hypothesis testing) by randomly sampling from the U.S. imports dataset and comparing this to what was observed in the DAWE phone enquiries. To obtain the popularity of pets in the overall exotic pet trade, we uniformly randomly sampled species from the U.S. import records and calculated their collective median rank. To obtain the proportion of species threatened, with trade restrictions or invasive in the overall exotic pet trade, we randomly sampled species from the U.S. import records and recorded their collective proportions (respectively). The sample size of this sampling procedure was set to the total number of phone enquiries and was stratified by taxonomic class to account for taxonomic bias. For example, for the species popularity test, there was a total of 79 phone enquiries corresponding to species or subspecies, of which 42 enquiries were mammals (class Mammalia), 24 were birds (class Aves), 14 were reptiles (class Reptilia) and nine were fish (class Actinopterygii or Chondrichthyes). Therefore, for each iteration of sampling, we randomly sampled from the U.S. imports 42 mammals, 24 birds, 14 reptiles and nine fish. We repeated this sampling for 10,000 iterations for each analysis, with replacement. The sample size, stratified by taxonomic class, differed slightly for the proportion threatened (IUCN) test since some species are not yet evaluated by the IUCN or designated as Data Deficient and therefore excluded from analysis. We then compared the phone enquiry median rank or proportion (i.e. observed rank/proportion) with the resulting distribution of rank or proportions from sampling of the U.S. imports. P-values were calculated as the proportion of sampling iterations that were more extreme than the observed rank or proportion. For these analyses, we only considered taxa that were resolved to the taxonomic level of species (i.e. no genus, family etc.).
In total, there were 196 enquiries from 150 phone calls. Most enquiries were related to the private keeping of pets (n = 180), followed by breeding for food (n = 11; Fig.
The stated use and purpose of public import enquiries recorded by the Australian Government Department of Agriculture, Water and the Environment. Use was categorised using enquiry notes (Pet = private use of the animal as a pet; breeding food = commercial use of the animal to be bred as food; breeding pets = commercial use of the animal to breed and sell as pets; zoo = commercial use for display in a zoo/wildlife park; exhibitor = commercial use for exhibitions/shows; research = use of the animal for scientific research; other = use not stated).
The number of unique taxa (a) and total enquiries (b) according to taxonomic classification rank for enquiries relating the private use of keeping or importing pets. We resolved the species or common names mentioned by the enquirers to the most specific possible taxonomic rank. Here, species refers to both species and subspecies. Genus – family corresponds to taxonomic ranks in between genus and family (i.e. tribe, subfamily) and family – order corresponds to taxonomic ranks in between family and order (i.e. infra-order). Colours correspond to the taxonomic class, where fish includes Chondrichthyes and Actinopterygii. Other taxonomic class refers to taxa not in vertebrate (Vertebrata) classes.
The number of enquiries by taxonomic class (a) and order (b) and highest taxa specified (c), excluding invertebrates. The subfamily Erinaceinae includes hedgehogs, Vulpes zerda is the fennec fox, Psittacus erithacus is the African grey parrot, order Simiiformes refers to monkeys, Cebuella pygmaea is the pygmy marmoset, Scelropages formosus is the Asian arowana, Chinchilla lanigera is the long-tailed chinchilla, Tribolonotus gracilis is the red-eyed crocodile skink, Testudo horsfieldii is the Russian tortoise, the family Testudinidae includes tortoises, the family Lutrinae include otters, Atelerix albiventris is the four-toed hedgehog and Ara ararauna is the blue-and-yellow macaw.
We found that enquired species were more popular than expected by chance compared to species in the U.S. exotic pet trade (p = 0.007, Fig.
Empirical hypothesis tests comparing: (a) enquired species popularity; (b) proportion of threatened species; (c) proportion of international trade-restricted species; and (d) proportion of invasive species, to the overall exotic pet trade. Each histogram represents 10,000 iterations of random sampling from the U.S. Fish and Wildlife imports dataset from 1999–2016 (representative of the Western exotic pet trade), stratified by taxonomic class. Red lines correspond to the ‘observed’ median rank or proportion from the enquired species. P-values are calculated as the proportion of sampling iterations that fall to the left or right of the observed rank or proportion. Non-vertebrate taxa were not included in these analyses.
Australia imposes strict legislation to prevent the importation of alien vertebrate species (
Our findings that desired species were more likely to be IUCN-listed and CITES-listed compared to overall trade are consistent with the Anthropogenic Allee Effect, a process in which the trade and harvest of a species increases with rarity due to its effect on perceived value (Courchamp et al. 2006;
In addition to conservation indicators, we found that desired species were much more likely to be invasive than expected by chance. Unlike the Anthropogenic Allee Effect, we are not aware of any study that shows a correlation between desirability of a species and their invasion status. This novel finding is of great concern for biosecurity agencies because it suggests that a filtering process is occurring where illegally smuggled animals may already be “pre-selected” to have the characteristics that are correlated with invasive species. For instance, traits closely associated with successful invasions include high fecundity and broad climatic tolerances (Herrel and van der Meijden 2014; Capellini et al. 2015; Howeth et al. 2016). In addition, the most desired taxa (mammals and birds) are considered ‘charismatic’, meaning people prefer them due to their appearance, behaviour or function (Beeves et al. 2019). These charismatic taxa may present an additional challenge to biosecurity because, if they become introduced or established, the general public may oppose eradication efforts (e.g. free-roaming horses in Australia, monk parakeets in the U.S. (
Our analysis relied on information collected in the style of a self-selecting survey from people interested in acquiring alien species, particularly pets. This does not necessarily represent actual intentions to illegally acquire alien pets and it remains unknown how desirability and introduction efforts are correlated. Given the records of illegally smuggled animals and illegally kept pets in Australia (
The legislative framework surrounding the import of alien pets, to which our enquiry data pertain, has a number of shortcomings that need to be addressed in order for the threat of alien imports to be reduced. In particular, there are discrepancies between what can be legally imported into Australia and what can be legally kept in domestic captivity as part of the national permitted list (Part 13A of the EPBC 1999) or State/Territory legislation. A large number of species are not permitted for live import, yet possession of live individuals within Australia is not necessarily a prosecutable offence unless evidence can be provided that the individuals have an illegal origin (
Using U.S. import frequency, we have demonstrated that Australian import enquiries are heavily biased towards species popular in an overseas western market. The underlying process behind this observation deserves more investigation. We hypothesise that both U.S. legal trade and Australian demand for alien pets are driven by the same underlying processes, facilitated by the emergent role of social media in providing access to and awareness of available pets (
Invasive alien species have the potential to be introduced into Australia despite substantial investment in border and post-border biosecurity. We characterised a subset of domestic desire for alien pets via public import enquiries and identified several biases pertinent to both biosecurity and the conservation of threatened species. Specifically, desired species are more likely to be threatened by extinction and be invasive species elsewhere compared to species in the overall pet trade. Moreover, we emphasise the need for modifications to Australia’s live import list in order to maintain relevance with a rapidly changing international pet trade. Finally, the utility of the U.S. pet demand as a predictor of Australian desire for alien pets needs to be investigated further and for other regional pet markets, in order to foster greater biosecurity preparedness.
We would like to thank Jo Beath, Julie Quinn and Alex Blander from the Australian Government Department of Agriculture, Water and the Environment for providing access to de-identified digitised public enquiry data. This research was funded by the Centre for Invasive Species Solutions (Project PO1-I-002). The authors have declared that no competing interests exist.