What’s next? The release of exotic pets continues virtually unabated 7 years after enforcement of new legislation for managing invasive species

Abstract

There are many pathways by which invasive species are introduced and become established, with the exotic pet trade becoming an increasingly important route. The abandonment of pets is a growing problem, which has been recognized widely and that has provoked some legislative responses. We developed an approach to deal with the abandonment issue that is more comprehensive than existing frameworks. We analyzed a substantial data set on exotic fish, crayfish and herptiles in northeastern Spain to illustrate the approach and its rationale. Spanish legislation mirroring the recently enforced European Strategy to control invasive species was introduced in 2011, and we analyzed information from 2009 to 2018 to assess the effectiveness of the legislation. The 2011 legislation was intended to ban the sale of a prioritized list of invasive species in retailers, which aimed to reduce the release of exotic species into recipient ecosystems. We did not see any prohibited species for sale in retailers after 2011. However, 60,753 exotic animals from 4 classes, 10 orders, 47 families and 139 species were recorded in Barcelona and elsewhere in northeastern Spain, including 134 species other than the 5 prioritized invasive species. We found little evidence of a change in exotic pet releases into urban lakes after 2011. Invasive terrapins (Trachemys spp.) were captured in urban lakes and were the most prevalent taxon in a herptile rescue centre with increased numbers after 2011. We advocate a four-tier approach to deal more effectively with the pet-abandonment issue, which includes: (1) better understanding of uncertainties in the listing of potentially invasive species; (2) allowing would-be owners to seek accreditation (through training); (3) pit-tagging to ensure that animals can be associated with registered owners, including species now prohibited but that had been traded for decades; and (4) ensuring that adults of low-cost, small-size-at-purchase species are present at the point-of-sale to ‘warn against’ the consequences of impulsive purchases.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Almeida D, Ribeiro F, Leunda PM, Vilizzi L, Copp GH (2013) Effectiveness of FISK, an invasiveness screening tool for non-native freshwater fishes, to perform risk identification assessments in the Iberian Peninsula. Risk Anal 33:1404–1413

    Article  PubMed  Google Scholar 

  2. Auliya M, Altherr S, Ariano-Sanchez D, Baard EH, Brown C, Brown RM et al (2016) Trade in live reptiles, its impact on wild populations, and the role of the European market. Biol Conserv 204:103–119

    Article  Google Scholar 

  3. Axelrod (2007) Atlas of freshwater aquarium fishes. 11th revised edn. TFH Publications,U.S.

  4. Banha F, Gama M, Anastácio PM (2017) The effect of reproductive occurrences and human descriptors on invasive pet distribution modelling: Trachemys scripta elegans in the Iberian Peninsula. Ecol Model 360:45–52

    Article  Google Scholar 

  5. Beck AM, Katcher AH (1996) Between pets and people: The importance of animal companionship. Purdue University Press, Purdue

    Google Scholar 

  6. Bush ER, Baker SE, Macdonald DW (2014) Global trade in exotic pets 2006-2012. Conserv Biol 28:663–676

    Article  PubMed  Google Scholar 

  7. Caiola N, Sostoa AD (2002) First record of the Asiatic cyprinid Pseudorasbora parva in the Iberian Peninsula. J Fish Biol 61:1058–1060

    Article  Google Scholar 

  8. Chao NL, Prang G, Petry P (2001) Project Piaba–maintenance and sustainable development of ornamental fisheries in the Rio Negro basin, Amazonas, Brazil. In: Chao NL, Petry P, Prang G, Sonneschien L, Tlusty M (eds) Conservation and management of ornamental fish resources of the Rio Negro Basin, Amazonia, Brazil–Project Piaba. Chao, NL, pp 3–6

  9. Chapman FA, Fitz-Coy SA, Thunberg EM, Adams CM (1997) United States of America trade in ornamental fish. J World Aquacult Soc 28:1–10

    Article  Google Scholar 

  10. Chardonnet P, Clers BD, Fischer J, Gerhold R, Jori F, Lamarque F (2002) The value of wildlife. Rev Sci Tech-Off Int Epizoot 21:15–52

    Article  Google Scholar 

  11. Chomel B, Belotto A, Meslin FX (2007) Wildlife, exotic pets, and emerging zoonoses. Emerg Infect Dis 13:6–11

    Article  PubMed  PubMed Central  Google Scholar 

  12. Chucholl C (2013) Invaders for sale: trade and determinants of introduction of ornamental freshwater crayfish. Biol Invasions 15:125–141

    Article  Google Scholar 

  13. Clavero M (2011) Assessing the risk of freshwater fish introductions into the Iberian Peninsula. Freshwater Biol 56:2145–2155

    Article  Google Scholar 

  14. Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Phil Trans R Soc Lond B 345:101–118

    Article  CAS  Google Scholar 

  15. Conrad K (2012) Trade bans: a perfect storm for poaching? Trop Conserv Sci 5:245–254

    Article  Google Scholar 

  16. Courtenay WR Jr, Stauffer JR Jr (1990) The introduced fish problem and the aquarium fish industry. J World Aquacult Soc 21:145–159

    Article  Google Scholar 

  17. DAISIE (2009) Handbook of alien species in Europe. Springer, Dordrecht, p 381

    Google Scholar 

  18. Demkowska-Kutrzepa M, Studzińska M, Roczeń-Karczmarz M, Tomczuk K, Abbas Z, Różański P (2018) A review of the helminths co-introduced with Trachemys scripta elegans—a threat to European native turtle health. Amphib - Reptil 39:177–189

    Article  Google Scholar 

  19. Duggan IC, Rixon CA, MacIsaac HJ (2006) Popularity and propagule pressure: determinants of introduction and establishment of aquarium fish. Biol Invasions 8:377–382

    Article  Google Scholar 

  20. Essl F, Nehring S, Klingenstein F, Milasowszky N, Nowack C, Rabitsch W (2011) Review of risk assessment systems of IAS in Europe and introducing the German-Austrian black list information system (GABLIS). J Nat Conserv 19:339–350

    Article  Google Scholar 

  21. EU Regulation No 338/2013 of 9 December 1996 in relation to the protection of species of animals and plants through the control of their trade

  22. EU Regulation No 139/2013 of 7 January 2013 laying down animal health conditions for imports of certain birds into the Union and the quarantine conditions thereof Text with EEA relevance

  23. EU Regulation No 1143/2014 of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species

  24. Fowler AJ, Lodge DM, Hsia JF (2007) Failure of the lacey act to protect US ecosystems against animal invasions. Front Ecol Environ 5:353–359

    Article  Google Scholar 

  25. Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks CA

    Google Scholar 

  26. Franch N, Clavero M, Garrido M, Gaya N, López V, Pou-Rovira Q, Queral JM (2008) On the establishment and range expansion of oriental weatherfish (Misgurnus anguillicaudatus) in NE Iberian Peninsula. Biol Invasions 10:1327–1331

    Article  Google Scholar 

  27. Fujisaki I, Hart KM, Mazzotti FJ, Rice KG, Snow S, Rochford M (2010) Risk assessment of potential invasiveness of exotic reptiles imported to south Florida. Biol Invasions 12:2585–2596

    Article  Google Scholar 

  28. Gante HF, Moreira da Costa L, Micael J, Alves MJ (2008) First record of Barbonymus schwanenfeldii (Bleeker) in the Iberian Peninsula. J Fish Biol 72:1089–1094

    Article  Google Scholar 

  29. García-Díaz P, Ross JV, Woolnough AP, Cassey P (2017) The illegal wildlife trade is a likely source of alien species. Conserv Let 10:690–698

    Article  Google Scholar 

  30. Genovesi P, Carboneras C, Vila M, Walton P (2015) EU adopts innovative legislation on invasive species: a step towards a global response to biological invasions? Biol Invasions 17:1307–1311

    Article  Google Scholar 

  31. Gisbert E, López MA (2007) First record of a population of the exotic mummichog Fundulus heteroclitus (L., 1766) in the Mediterranean Sea basin (Ebro River delta). J Fish Biol 71:1220–1224

    Article  Google Scholar 

  32. Howeth JG, Gantz CA, Angermeier PL, Frimpong EA, Hoff MH, Keller RP, Mandrak NE, Marchetti MP et al (2016) Predicting invasiveness of species in trade: climate match, trophic guild and fecundity influence establishment and impact of non-native freshwater fishes. Divers Distrib 22:148–160

    Article  Google Scholar 

  33. Hulme PE (2015) Invasion pathways at a crossroad: policy and research challenges for managing alien species introductions. J Appl Ecol 52:1418–1424

    Article  Google Scholar 

  34. Hulme PE, Bacher S, Kenis M, Kühn I, Pergl J, Pyšek P, Roques A, Vilà M (2017) Blurring alien introduction pathways risks losing the focus on invasive species policy. Conserv Let 10:265–266

    Article  Google Scholar 

  35. IDESCAT (2019) Institute d’Estadística de Catalunya (in Catalan). https://www.idescat.cat/. Accessed 25 Feb 2019

  36. Johnson ML, Speare R (2003) Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerg Infect Dis 9:922–925

    Article  PubMed  PubMed Central  Google Scholar 

  37. King W, Krakauer T (1966) The exotic herpetofauna of southeast Florida. Quart J Florida Acad Sci 29:144–154

    Google Scholar 

  38. Lafuente S, Bellido JB, Moraga FA, Herrera S, Yagüe A, Montalvo T, de Simó M, Caylà JA (2013) Salmonella paratyphi B and Salmonella litchfield outbreaks associated with pet turtle exposure in Spain. Enferm Infecc Microbiol Clin 31:32–35

    Article  PubMed  Google Scholar 

  39. Leprieur F, Beauchard O, Blanchet S, Oberdorff T, Brosse S (2008) Fish invasions in the world’s river systems: when natural processes are blurred by human activities. PLoS Biol 6:e28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Living Planet Report (2018) https://wwf.panda.org/knowledge_hub/all_publications/living_planet_report_2018/. Accessed 25 Feb 2019

  41. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. T Ecol Evol 20:223–228

    Article  Google Scholar 

  42. Luque GM, Bellard C, Bertelsmeier C, Bonnaud E, Genovesi P, Simberloff D, Courchamp F (2014) The 100th of the world’s worst invasive alien species. Biol Invasions 16:981–985

    Article  Google Scholar 

  43. Maceda-Veiga A (2013) Towards the conservation of freshwater fish: Iberian Rivers as an example of threats and management practices. Rev Fish Biol Fisher 23:1–22

    Article  Google Scholar 

  44. Maceda-Veiga A, Escribano-Alacid J, de Sostoa A, García-Berthou E (2013) The aquarium trade as a potential source of fish introductions in southwestern Europe. Biol Invasions 15:2707–2716

    Article  Google Scholar 

  45. Maceda-Veiga A, Domínguez-Domínguez O, Escribano-Alacid J, Lyons J (2016) The aquarium hobby: can sinners become saints in freshwater fish conservation? Fish Fish 17:860–874

    Article  Google Scholar 

  46. Masin S, Bonardi A, Padoa-Schioppa E, Bottoni L, Ficetola GF (2014) Risk of invasion by frequently traded freshwater turtles. Biol Invasions 16:217–231

    Article  Google Scholar 

  47. Miller ML (2011) Laws, Federal and State. In: Simberloff D, Rejmánek M (eds) Encyclopedia of biological invasions, pp 430–436

  48. OATA (2015) Ornamental aquatic association code of conduct. https://ornamentalfish.org/wp-content/uploads/2015/10/CODE-OF-CONDUCT-FINAL-OCT-2015.pdf. Accessed 25 Feb 2019

  49. OATA (2018). Ornamental aquatic association annual report. https://ornamentalfish.org/read-our-annual-report-2018/. Accessed 25 Feb 2019

  50. Padilla DK, Williams SL (2004) Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Front Ecol Environ 2:131–138

    Article  Google Scholar 

  51. Pârâu LG, Strubbe D, Mori E, Menchetti M, Ancillotto L, Kleunen AV et al. (2016) Rose-ringed parakeet Psittacula krameri populations and numbers in Europe: a complete overview. Open Ornithol J 9(1):1–13

    Article  Google Scholar 

  52. Pasmans F, Bogaerts S, Cunningham AA, Braeckman J, Hellebuyck T, Griffiths RA, Sparreboom M, Schmidt BR, Martel A (2017) Future of keeping pet reptiles and amphibians: towards integrating animal welfare, human health and environmental sustainability. Vet Rec 181:264

    Article  Google Scholar 

  53. Perret N, Joly P (2002) Impacts of tattooing and PIT-tagging on survival and fecundity in the alpine newt (Triturus alpestris). Herpetologica 58:131–138

    Article  Google Scholar 

  54. Perrings C, Dehnen-Schmutz K, Touza J, Williamson M (2005) How to manage biological invasions under globalization. T Ecol Evol 20:212–215

    Article  Google Scholar 

  55. R Core Team (2013) R: a language and environment for statistical computing

  56. Raghavan R, Dahanukar N, Tlusty MF, Rhyne AL, Kumar KK, Molur S, Rosser AM (2013) Uncovering an obscure trade: threatened freshwater fishes and the aquarium pet markets. Biol Conserv 164:158–169

    Article  Google Scholar 

  57. Real Decreto 1628/2011 de 14 de noviembre, por el que se regula el listado y catálogo español de especies exóticas invasoras (in Spanish)

  58. Real Decreto 630/2013 de 2 de agosto, por el que se regula el Catálogo español de especies exóticas invasoras (in Spanish)

  59. Real Decreto 216/2019 de 29 de marzo, por el que se aprueba la lista de especies exóticas invasoras preocupantes para la región ultraperiférica de las islas Canarias y por el que se modifica el Real Decreto 630/2013, de 2 de agosto, por el que se regula el Catálogo español de especies exóticas invasoras (in Spanish)

  60. Reino L, Figueira R, Beja P, Araújo MB, Capinha C, Strubbe D (2017) Networks of global bird invasion altered by regional trade ban. Sci Adv 3:e1700783

    Article  PubMed  PubMed Central  Google Scholar 

  61. Rixon CA, Duggan IC, Bergeron NM, Ricciardi A, Macisaac HJ (2005) Invasion risks posed by the aquarium trade and live fish markets on the Laurentian Great Lakes. Biodivers Conserv 14:1365–1381

    Article  Google Scholar 

  62. Rowan AN (1992) Shelters and pet overpopulation: a statistical black hole. Anthrozoös 5(3):140–143

    Article  Google Scholar 

  63. Schloegel LM, Picco AM, Kilpatrick AM, Davies AJ, Hyatt AD, Daszak P (2009) Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and Ranavirus infection in imported North American bullfrogs (Rana catesbeiana). Biol Conserv 142:1420–1426

    Article  Google Scholar 

  64. Seebens H, Blackburn TM, Dyer EE, Genovesi P, Hulme PE, Jeschke JM et al (2017) No saturation in the accumulation of alien species worldwide. Nat Commun 8:14435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Shine C, Kettunen M, Genovesi P, Essl F, Gollasch S, Wolfgang R, Scalera R, Starfinger U, ten Brink P (2010) Assessment to Support Continued Development of the EU Strategy to Combat Invasive Alien Species. Final Report for the European Commission. Institute for European Environmental Policy (IEEP), Brussels, Belgium

    Google Scholar 

  66. Stringham OC, Lockwood JL (2018) Pet problems: biological and economic factors that influence the release of alien reptiles and amphibians by pet owners. J Appl Ecol 55:2632–2640

    Article  Google Scholar 

  67. Tapley B, Bradfield KS, Michaels C, Bungard M (2015) Amphibian conservation and breeding programmes: do all threatened amphibians belong on the ark? Biodivers Conserv 24:2625–2646

    Article  Google Scholar 

  68. Weyl OLF, Daga VS, Ellender BR, Vitule JRS (2016) A review of Clarias gariepinus invasions in Brazil and South Africa. J Fish Biol 89:386–402

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to two anonymous referees and the associated editor Ronaldo Sousa for their useful suggestions. We also thank to J.D. Lyons, O. Domínguez-Domínguez, O. Cano-Rocabayera and S. Vargas-Amengual for inspiring discussions on the issue of unwanted exotic aquatic pets and to ‘Fomento de Contratas y Construcciones’ and the Galanthus Association, especially to G. Pascual-Pijoan, for providing data on Barcelona’s urban lakes. Data collection and necropsies at CRARC were funded by ‘Fundació Barcelona Zoo-Ajuntament de Barcelona’ and additional technical support and authorizations were provided by Aïda Tarragó, Francesc Mañas and Ricard Casanovas from ‘Generalitat de Catalunya’.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Alberto Maceda-Veiga.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 250 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Maceda-Veiga, A., Escribano-Alacid, J., Martínez-Silvestre, A. et al. What’s next? The release of exotic pets continues virtually unabated 7 years after enforcement of new legislation for managing invasive species. Biol Invasions 21, 2933–2947 (2019). https://doi.org/10.1007/s10530-019-02023-8

Download citation

Keywords

  • Keyword exotic pet trade
  • Introduction pathways
  • Legislation
  • Policy
  • Biosecurity
  • Propagule pressure