Humans have kept animals as pets since ancient times (Hughes, 2003), an activity that has persisted in all societies throughout history (Williams, 1956; Ucko & Dimbleby, 1969, Driscoll & Macdonald, 2010). In the last century, a rise in the pet trade and in the use of wildlife products, illegal and legal, has dramatically boosted animal movements across frontiers (Oldfield, 2003). Such trade, if uncontrolled, can directly threaten biodiversity (Rosen & Smith, 2010; Phelps et al., 2016), may cause the spread of zoonotic diseases (Smith et al., 2012; Mazza et al., 2014) as well as open the gateway for biological invasions (Reino et al., 2017).
Populations of numerous vertebrate taxa from fish to mammals are legally caught alive from the wild and are sold as exotic pets or for exhibition (Kisling, 2000; Natusch & Lyons, 2012; Bush et al., 2014). Birds, most often traded for pets, are also among the most successful invaders; many species becoming naturalised in many countries in which they can cause extensive damage to agriculture and natural environments (Hulme et al., 2009; Simberloff, 2014; Turbé et al., 2017). Parrots (Psittaciformes), one of the most popular birds to be traded for pets, are known to success- fully become established in new environments as a result of accidental escapes or deliberate releases (Abellán et al., 2017; Cardador et al., 2017; Mori et al., 2017).
In the last decade, almost 63% of all known parrot species have been imported into Spain, especially for pets (BirdLife International, 2016; CITES, 2016). This group, together with ducks and geese (Anseriformes) and perching birds (Passeriformes), are the most traded bird orders in the Iberian Peninsula (Abellán et al., 2016). Among the imported parrot species, the Monk Parakeet Myiopsitta monachus and the Ring-necked Parakeet Psittacula krameri have become rapidly naturalised across the country and beyond (Cardador et al., 2016; Molina et al., 2016; Somoza et al., 2018). It has been demonstrated that these feral populations negatively affect native wildlife, including other avian species (Yosef et al., 2016) and mammals (Hemández-Brito et al., 2014).
In this study, we examined the trends in the number of individuals of the Monk Parakeet and the Ring-necked Parakeet, which entered Spain legally. We compared the growth in this trade with the known establishment and increase of feral populations in the country. In particular, we addressed the following questions: (i) What is the volume of parakeets imported over time? (ii) Where did these individual animals originate and what was the purpose of their import? (iii) How have feral populations evolved in the study period regarding the number of imported individuals? (iv) How have regulatory changes modified the evolution of imports in the study period? and (v) How can our observations for these species help us manage other potential invasive taxa?
The Monk and Ring-necked Parakeets, native to South America and Central Africa-Asia respectively, have been popular pets since before the 1970s (Bull, 1973). Millions of individuals of these two species have been captured and bred for export worldwide, and introduced into different parts of the world (Muñoz & Real, 2006; Russello et al., 2008; Strubbe & Matthysen, 2009a; Pârâu et al., 2016; Postigo et al., 2016). Both species share a powerful and unpleasant yell, which is often the reason why many owners may have released birds (Muñoz & Real, 2006, Strubbe & Matthysen, 2009a).
Feral populations of these two species are known to pose threats to a country's economy (Davis, 1974; Avery et al., 2002; Stafford, 2003; Tala et al., 2005) and biodiversity (Strubbe & Matthysen, 2007; 2009b; Czajka, 2011; Hernández-Brito et al., 2014; Menchetti & Mori, 2014; Menchetti et al., 2014; Peck et al., 2014). The Ring-necked Parakeet, in particular, is amongst the top 100 most problematic alien species in Europe (DAISIE, 2009).
The first record of a free-living Monk Parakeet in Spain dates back to 1975, when two individuals were seen in Barcelona and Murcia urban areas (Molina et al., 2016). Evidence of the presence of feral Ring-necked Parakeets is even earlier: a specimen was hunted in Caceres province in 1970 (Pérez - Chiscano, 1971). Since then, both species have expanded their range throughout Spain, especially in and around large cities (Batllori & Nos, 1985; De Juana, 1985, 1989; Sol et al., 1997; Muñoz & Real, 2006; Somoza et al., 2018) and have the potential for spreading even more widely (Real et al., 2008; Muñoz, 2016; Muñoz et al., 2018).
We consulted the trade database from the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) to obtain data on the number of Psittaciformes legally imported into Spain during 1975–2015. The use and treatment of the data followed the guidelines set in CITES (2013). Three types of import/export data can be found in the CITES (2016) database: comparative tabulation reports, gross reports and net reports. We used data in the comparative tabulation reports because they provide information on origin, source and purpose of imported animals. We examined the total annual number of reported Monk and Ring-necked Parakeets in Spain, their origin, whether they were wild caught or bred in captivity, and the reason for the importation. Data suspected to be duplicate according to CITES guidelines (2013) were removed. CITES trade database only considers data at the country level, which precludes further analysis on smaller territorial units.
We also gathered information on known population numbers for both species in the wild. Three population estimates were obtained from the literature for 1997, 2002, and 2015. Data for 1997 and 2002 were compiled from information contained in the Ornithological News published by SEO/BirdLife in the scientific journal Ardeola and published atlases of breeding birds in Spain (Purroy, 1997; Martí & del Moral, 2003), as well as from local bird reports. For 2015, we used data from the latest wild population standardized national censuses carried out in 2015 (Molina et al., 2016; Somoza et al., 2018).
Numbers, countries and destination of imported birds
Between 1978 and 2015, more than 1 million parrots of 252 species were legally imported into Spain. Most birds belonged to three genera: Agapornis (409,417 individuals), Myiopsitta (194,086 individuals) and Psittacula (62,799 individuals, 95% of these being Ring-necked Parakeets). Monk and Ring-necked Parakeets were the second and fifth-most imported species respectively (Figure 1).
The most common country of origin for the Monk Parakeet was Uruguay (87%), followed by Argentina (13%). In the case of the Ring-necked Parakeet, the main exporting countries were Pakistan (77%) and Senegal (20%) (Figure 2). Most birds imported of both species were wild caught, though a large proportion of individuals (24% for the Monk Parakeet and 46% for the Ring-necked Parakeet) were declared of unknown origin (Figure 3). Most individuals (99.9%) were imported as pets, the rest being imported for research purposes or exhibition in zoos.
The first declared importations of Monk Parakeets and Ring-necked Parakeets occurred in 1986 and 1987, respectively. The last recorded importations in our database date from 2005 for both species. Peak importations for the Monk Parakeet occurred mainly during the period 1989–1995, while the Ring-necked Parakeet was mostly imported over the period 1998–2001 (Figure 4).
Feral population numbers
Monk and Ringed-necked Parakeet feral populations grew exponentially since first breeding populations were detected, after an establishment phase of approx. 10–20 years since initial observations. Original population estimates for Monk Parakeet in Spain were of around 1,300 individuals in 1997 (Muñoz & Ferrer, 1997), almost doubling by 2002 (Muñoz, 2003a). In 2015, the population size was 18,980–21,455 individuals throughout Spain (Molina et al., 2016). For the Ring-necked Parakeet, the first population estimate was about 150 birds in 1997, tripled in 2002, and had multiplied by approximately 20 by 2015, with 3,005–3,115 estimated individuals (Muñoz, 2003b; Somoza et al., 2018).
Relationship between imports and wild populations
Population increases in the wild were later than peak importation periods (1989–1995 for the Monk Parakeet, and 1997–2001 for the Ring-necked Parakeet). Feral populations of the two species grew exponentially throughout the study period, with the population peaks in both cases occurring after importations ceased. The average annual growth rate (AAGR) between 1997 and 2002 for the Monk Parakeet was 167 animals per year. This number increased by a factor of almost 8 during the next 13 years, with an AAGR of 1,276 birds per year between 2002 and 2015. For the Ring-necked Parakeet, the AAGR between 1997 and 2002 was 26 animals per year, and again around 8 times higher, 206 animals, between 2002 and 2015.
The magnitude of Monk and Ring-necked Parakeets trade in Spain
Monk and Ring-necked Parakeets are abundant in their original ranges, and considered agricultural pests in some areas (Mott, 1973; Khan et al., 2004; Volpe & Aramburú, 2011). This has enabled the collection and export of thousands of birds during decades. Both parakeet species have been the commonest and cheapest parrots available in pet shops in Spain until 2013, before the law prohibited their sale. In just 19 years, more than 190,000 birds of Monk and almost 63,000 Ring-necked Parakeets were legally imported into Spain, mostly to meet the demand for pet animals. This means that one in every four parrots that entered Spain belonged to these two mentioned species. These numbers are much higher than previously thought, however, this amount should be considered a minimum figure, since parrots are attractive in the black market and a huge unreported number could have entered the country (Weston & Memon, 2009; Pires, 2012; Tella & Hiraldo, 2014). In addition, according to the net import CITES report, 258,273 Monk and 80,000 Ring-necked Parakeets were brought into Spain during 1975–2015, a higher figure than the reported numbers in the CITES comparative tabulation reports (see above).
Origin of parakeets
Our findings support recent genetic studies for both species in Spain (Edelaar et al., 2015; Jackson et al., 2015) that Ring-necked Parakeets in Spain comprised birds originating mostly from Asia (Muñoz, 2003a), as is the case for the UK (Pithon & Dytham, 2002) and the United States (Juniper & Parr, 1998). However, according to the CITES trade data base, we show that most birds (77%) came from Asia (P. k. borealis), but 20% of individuals had an African origin, belonging to the subspecies P. k. krameri. This is interesting, since there are hardly any wild African Ring-necked Parakeets in the naturalised populations in Spain. Cardador et al. (2016) suggested that the lack of wild-origin African individuals in comparison to their Asian counterparts may be due to the poor suitability of the Spanish environments, which would not allow them to adapt and establish successfully. For the Monk Parakeet, nonetheless, our findings reaffirm that most feral individuals are M. m. monachus, a subspecies native to the South America region, between Uruguay and eastern Argentina. This is consistent with the genetic analyses by Rusello et al. (2008). Uruguay and Argentina are the main exporters for this species worldwide (Edelaar et al., 2015).
Why are Monk and Ringed-necked Parakeets so successful?
According to our results, imported Monk and Ringed-necked Parakeets in Spain were mostly captured from the wild, with a significant percentage of individuals with an unknown origin, being potentially wild-caught as well (Figure 3). It is well known that birds, which have been captured from the wild, are more adaptable and have higher success for establishing in case of release (Cabezas et al., 2013; Abellan et al., 2017). In contrast, animals which have been born into a controlled environment have difficulty in adapting to the wild if released or escaped, because they have not learnt the most important skills for surviving in nature and its ability to fly long distances may be reduced (Cabezas et al., 2013; Carrete & Tella, 2016). The genus Agapornis (lovebirds) is one of the most demanded Psittaciformes in Spain, with three species being imported even in larger numbers than Monk and Ring-necked Parakeets (Figure 1). However, almost 99% of the imported lovebirds were captive-born, which could be the main cause why these species have failed to establish themselves successfully in nature, even when the propagule pressure could have been larger.
The evolution of Monk and Ring-necked Parakeets trade and feral populations in Spain
According to the existing records both species in Spain date back to the 1970s (Perez-Chiscano, 1971; Clavell et al., 1991). Although it is indicative of an international trade at that time, it is not possible to quantify Monk and Ring-necked Parakeets imported before that date, as CITES was not implemented in Spain yet. Even so, the great popularity of these parakeets as pets in Spain was later compared to other regions of Europe and America, where self-sustaining populations were recorded during the 1960s and 1970s (Bull, 1973; Butler, 2003). Besides CITES, there are different regulations concerning the traffic of exotic birds, European and national, which have influenced trade for years (Santos, 2012). The tightening of the laws for the trade of Monk and Ring-necked Parakeets has been noteworthy. Monk Parakeets were popularized as pets in Spain during the 1980s–1990s (Santa-Olalla et al., 2014), when laws were more permissive than today. The highest peaks occurred between 1989– 1995, with almost 20,000 imported birds reported per year (Figure 4). In 1997, there was a strong importation decrease that coincided with the first wild population estimate (>1.300 established birds) (Marti & del Moral, 2003). Importations were affected by the European Law “On the protection of species of wild fauna and flora by regulating trade therein” (Council Regulation —EC338/97), which, in the article 4.6.d imposed “Limitations on live specimens of species for which it has been established that their introduction into the natural environment of the Community presents an ecological threat to wild species of fauna and flora indigenous to the Community”. When Monk Parakeet imports decreased, they were shortly after replaced in the market with the Ring-necked Parakeet (Figure 4).
The avian influenza crisis in the earlier 2000s severely affected the trade of domestic and exotic birds because of health alert worldwide (Van Borm et al., 2005; Karesh et al., 2005; Karesh et al., 2007; Van den Berg, 2009). The European Union temporally banned the entrance of wild birds in 2005, and this measure became permanent in 2007 (Carrete & Telia, 2008). In Spain, more restricted laws were implemented in the following years regarding invasive species, banning completely the trade and possession of Monk and Ring-necked Parakeets (Real Decreto 630/2013). Even so, the last imported Monk Parakeet was reported in 2008.
Although there have been practically no imports of both species in 16 years, wild populations have grown in such a way that they can sustain themselves through breeding without the need of new introductions. There was an exponential growth of Monk Parakeet wild populations between 2002 and 2015, increasing from 2,300 to almost 18,000 birds. The growth was also significant for the Ringnecked Parakeet, which increased from 467 birds to over 3,000 in 13 years (SEO/BirdLife, 2016a, b).
In both cases, intentional or accidental releases currently play a key role in the appearance of new populations. The fear of possible fines regarding bird possession, as a result of the new regulatory restrictions, may have played a role in it. This situation would be an example of how more tightening laws regarding to the control of the wildlife trade could paradoxically increase the problem of invasive species if they are not properly applied (Carrete & Telia, 2008).
The wildlife trade of other Psittaciformes species in Spain and the hazard of introducing new potential invasive species
Many other parrot species were and are imported to Spain with not many restrictions regulating their trade. The high demand in highly populated cities facilitates the presence of these birds in pet stores throughout the country (Gulx et al., 1997; Weston & Memon, 2009). Several species of genera such as Aratinga, Poicephalus and Nandayus, have been seen in the wild in different parts of Spain, and some of them may be considered as potential breeders, although still in low numbers (Martínez-Santos & Grupo de Aves exóticas, 2012). The Senegal Parrot Poicephalus senegalus was the seventh most imported species in Spain, indicative of its commercial interest (Figure 1). Although it is not considered invasive in Spain and there are no specific laws prohibiting its possession and trade, it starts to appear as a breeding species in different parts of Spain as the Canary Islands, Valencia, Barcelona (Grupo de Aves exóticas, 2016) and Málaga (unpublished data). This species, probably in its first steps of the invasion process, could be another example of how legal wildlife trade in large scales facilitates the establishment of exotic and potentially invasive species. More preventive measures must be added regarding the trade of certain potentially invasive taxa, restricting (even banning) imports for commercial purposes. Education on the negative consequences of an uncontrolled international wildlife trade should play an important role in our society, in order to prevent the potential consequences of this business on the conservation of biodiversity.
ARM was supported by the Juan de la Cierva Program (FJCI-2014-20653), of the Spanish MECD. Partial funding was obtained by the Spanish Ministry of Agriculture, Food and Environment, Spanish National Park's Network (project 1098/2014). We thank the former director of SOIVRE Málaga, Arturo David Magno-Gómez and the Spanish CITES committee for the invaluable information provided for this article. We also thank Darío Chamorro for advice in the use of vector graphics editors.
L. Souviron-Priego: Main author. She was responsible of writing most of the article, as well as the bibliography search. A. Román Muñoz: Main driver of developing this manuscript. He helped and advised to the main author on the structure of the manuscript. J. Olivero: Adviser. Helped and advised to the main author on the structure of the manuscript, especially in the methods section. J. Mario Vargas: Adviser. He helped in the first stages of the manuscript. J.E. Fa: Main adviser. He was in charge of giving the final assessment, as well as fine-tuning the grammatical structure in English.
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