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.
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References
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
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
Axelrod (2007) Atlas of freshwater aquarium fishes. 11th revised edn. TFH Publications,U.S.
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
Beck AM, Katcher AH (1996) Between pets and people: The importance of animal companionship. Purdue University Press, Purdue
Bush ER, Baker SE, Macdonald DW (2014) Global trade in exotic pets 2006-2012. Conserv Biol 28:663–676
Caiola N, Sostoa AD (2002) First record of the Asiatic cyprinid Pseudorasbora parva in the Iberian Peninsula. J Fish Biol 61:1058–1060
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
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
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
Chomel B, Belotto A, Meslin FX (2007) Wildlife, exotic pets, and emerging zoonoses. Emerg Infect Dis 13:6–11
Chucholl C (2013) Invaders for sale: trade and determinants of introduction of ornamental freshwater crayfish. Biol Invasions 15:125–141
Clavero M (2011) Assessing the risk of freshwater fish introductions into the Iberian Peninsula. Freshwater Biol 56:2145–2155
Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Phil Trans R Soc Lond B 345:101–118
Conrad K (2012) Trade bans: a perfect storm for poaching? Trop Conserv Sci 5:245–254
Courtenay WR Jr, Stauffer JR Jr (1990) The introduced fish problem and the aquarium fish industry. J World Aquacult Soc 21:145–159
DAISIE (2009) Handbook of alien species in Europe. Springer, Dordrecht, p 381
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
Duggan IC, Rixon CA, MacIsaac HJ (2006) Popularity and propagule pressure: determinants of introduction and establishment of aquarium fish. Biol Invasions 8:377–382
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
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
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
EU Regulation No 1143/2014 of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species
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
Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks CA
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
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
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
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
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
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
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
Hulme PE (2015) Invasion pathways at a crossroad: policy and research challenges for managing alien species introductions. J Appl Ecol 52:1418–1424
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
IDESCAT (2019) Institute d’Estadística de Catalunya (in Catalan). https://www.idescat.cat/. Accessed 25 Feb 2019
Johnson ML, Speare R (2003) Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerg Infect Dis 9:922–925
King W, Krakauer T (1966) The exotic herpetofauna of southeast Florida. Quart J Florida Acad Sci 29:144–154
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
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
Living Planet Report (2018) https://wwf.panda.org/knowledge_hub/all_publications/living_planet_report_2018/. Accessed 25 Feb 2019
Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. T Ecol Evol 20:223–228
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
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
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
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
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
Miller ML (2011) Laws, Federal and State. In: Simberloff D, Rejmánek M (eds) Encyclopedia of biological invasions, pp 430–436
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
OATA (2018). Ornamental aquatic association annual report. https://ornamentalfish.org/read-our-annual-report-2018/. Accessed 25 Feb 2019
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
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
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
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
Perrings C, Dehnen-Schmutz K, Touza J, Williamson M (2005) How to manage biological invasions under globalization. T Ecol Evol 20:212–215
R Core Team (2013) R: a language and environment for statistical computing
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
Real Decreto 1628/2011 de 14 de noviembre, por el que se regula el listado y catálogo español de especies exóticas invasoras (in Spanish)
Real Decreto 630/2013 de 2 de agosto, por el que se regula el Catálogo español de especies exóticas invasoras (in Spanish)
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)
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
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
Rowan AN (1992) Shelters and pet overpopulation: a statistical black hole. Anthrozoös 5(3):140–143
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
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
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
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
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
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
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’.
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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
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DOI: https://doi.org/10.1007/s10530-019-02023-8