Naturalized Parrots of the World: Distribution, Ecology, and Impacts of the World's Most Colorful Colonizers

PART I

BACKGROUND

AND ECOLOGY

1

THE WORLD

PARROT TRADE

Laura Cardador, Pedro Abellán, José D. Anadón,

Martina Carrete, and José L. Tella

INTRODUCTION

International trade is recognized as an important and rapidly growing source of introduction of non-native species worldwide (Hulme 2009). Particularly, the trade in wildlife has been directly related to the introduction of non-native, sometimes invasive bird species (Carrete and Tella 2008; Cardador et al. 2019), among which those belonging to the order Psittaciformes play a dominant role (Beissinger 2001; Blackburn and Duncan 2001). The Psittaciformes include parrots, parakeets, lovebirds, cockatoos, macaws, etc., which we collectively refer to as simply parrots. Almost two-thirds of all existing parrot species have been commonly transported outside their native ranges as pets, and several more are traded locally (Cassey et al. 2004). This trade has strongly contributed to the decline of many parrot species in their native ranges (Collar and Juniper 1992; Tella and Hiraldo 2014). Nearly one-third of all parrot species are threatened under criteria set forth by the International Union for Conservation of Nature (IUCN 2016), but parrots are also among the most widespread introduced birds in the world (Cassey et al. 2004; Strubbe and Matthysen 2009a; Cardador et al. 2016). Almost one-quarter of all transported species find their way into exotic environments, and at least 10% of parrot species have established naturalized populations (Cassey et al. 2004; Abellán et al. 2017), sometimes with undesirable effects on native fauna and human socioeconomic activities (Strubbe and Matthysen 2009b; Hernández-Brito et al. 2014; Menchetti and Mori 2014; Peck et al. 2014).

As with other bird species, the human interest in and transport of parrot species date back centuries (Blackburn et al. 2009; Tella 2011). There is consistent evidence, for example, that pre-Columbian cultures in Central America already transported and kept parrot species in captivity, as the birds’ brightly colored feathers were prized for their use in rituals and decoration. The interest in and transport of alien parrots was also present in ancient Old World civilizations. As far back as the year 326 BCE, Alexander the Great’s expedition transported parakeets to Europe from India, and it is well known that Romans too kept parrots in captivity (Blackburn et al. 2009; Tella 2011).

The interest in parrot species has been maintained throughout history. However, for most of the time, parrot keeping has been mostly a luxury, confined to the wealthiest people, thus involving low numbers of individuals and species (Cassey et al. 2015). It was during the 20th century that the activity became especially popular, stimulated by the accelerated economic growth and the development of efficient transport infrastructures. Today, bird keeping is one of the world’s most popular hobbies (Carrete and Tella 2008), and the demand for birds as pets involves millions of individual parrots annually (Cardador et al. 2017; Reino et al. 2017).

Mosaic, c. 500 CE, of Rose-ringed Parakeets (Psittacula krameri). The collars indicate that these birds were kept as pets, likely having been traded from Africa. Israel Museum, Jerusalem. Photo by Salit Kark.

In this chapter we describe how increases in international parrot trade demand have contributed to increased invasion risks worldwide in recent decades, and we describe some of the factors that might contribute to the success of the traded species. We then analyze temporal trends in international parrot trade numbers, the species’ geographic origins, and their destinations in recent decades. To conclude, we discuss potential conservation implications of parrot trade and propose alternative strategies to combat them.

PARROT TRADE AND INVASIONS

The increased demand for parrots has been accompanied by a dramatic increase in the number of new parrot introductions in non-native areas during the 20th century (Fig. 1.1). These introductions have been related mostly to accidental or unplanned releases by pet owners (Blackburn et al. 2009; Abellán et al. 2016). Nearly 80% of all known parrot introductions occurred after 1950 and are directly linked to annual parrot trade numbers (Cardador et al. 2019) (Fig. 1.2). As biological invasions are a dynamic process, introduced species constitute the pool of species from which establishment, and thereafter spread, of self-sustaining populations in new non-native areas can take place (Blackburn et al. 2011). In turn, the likelihood of establishment and spread of species traded at larger numbers is expected to be higher, because a greater number of individuals of such species are likely to escape.

Several studies have suggested that propagule pressure (understood as a composite measure of the number of individuals released into a region in which they are not native) is one of the most important factors explaining invasion success (Colautti et al. 2006; Blackburn et al. 2009, 2015). Increased propagule pressure favors invasions by overcoming environmental and demographic stochasticity, avoiding genetic bottlenecks (decreased genetic diversity), and increasing standing genetic variation on which selection can act (Facon et al. 2006; Simberloff 2009). Greater propagule pressure increases, first, the likelihood that an alien population will establish a self-sustaining population at a location and, second, the likelihood that an alien population subsequently will spread toward other places to become invasive (Blackburn et al. 2015; Abellán et al. 2017).

Figure 1.1. Frequency distribution of year of introduction for (a) 1,491 parrot introduction events since 1600 for which an estimate of introduction date was available, and (b) 1,352 parrot introduction events that occurred after 1900. Data source: Dyer et al. (2017).

Figure 1.2. Relationships between new parrot species introduced in the wild in Spain and Portugal and total number of wild-caught parrots (a) and species (b) imported. Each dot represents a single year in the period 1976–2005. A Michaelis–Menten curve (dashed lines) was fitted to account for the potential saturation of new species introduced at large import values. The goodness of fit between observed data and the fitted curve is indicated by the Pearson’s correlation coefficient (r). Data sources: CITES (2015) and Cardador et al. (2019).

Additionally, other factors beyond trade numbers, such as breeding origin of traded species, can also affect the probability of invasion of traded species. There is indeed evidence that although captive-bred species, such as Budgerigars (Melopsittacus undulatus), often greatly outnumber species caught in the wild and traded on the pet market, the wild-caught birds are more successful invaders (Carrete and Tella 2008). The greater success of wild-caught cage birds compared to captive-bred ones could be related to the loss in captive-bred birds of the ability to cope with new environments. This hypothesis is supported by experiments with parrots showing that exotic wild-caught individuals have longer physiological responses to acute stress than captive-bred ones (Cabezas et al. 2013). This may facilitate wild-caught individuals in both escaping captivity and facing challenges in new environments. Additionally, wild-caught birds, including parrots, maintain their antipredatory behavior and escape responses in captivity (Carrete and Tella 2015). In contrast, captive-bred birds lose these traits and thus have a lower probability of escaping captivity as well as a lower probability of success if they do escape (Carrete and Tella 2015).

Two Yellow-crested Cockatoos (Cacatua sulphurea) for sale at Yuen Po Street bird market in Hong Kong. The orange-crested individual on the left is of the subspecies C. s. citrinocristata. Yellow-crested Cockatoos are critically endangered due to habitat loss and the pet trade but are regularly seen in Hong Kong’s bird markets. January 2018. Photo by Astrid Andersson.

Environmental similarity between the regions of origin and destination of traded species is also a key determinant of the effect of trade on invasion risks. Recent evidence shows that most invasive species within different taxa occupy areas with similar environmental characteristics to those in their native ranges (Petitpierre et al. 2012; Strubbe and Matthysen 2014). A significant effect of environmental suitability (i.e., similarity with native ranges) on invasion success of parrot species has also been found (Cardador et al. 2016, 2017). While some species can establish alien populations in truly novel areas (Abellán et al. 2017), their capacity to spread and become invasive is expected to be strongly influenced by environmental matching (Duncan et al. 2001; Abellán et al. 2017). In this sense, not only global trade numbers but also trade routes can have important effects on global invasion risks.

THE INTERNATIONAL TRADE IN LIVE PARROTS

Almost all parrot species are listed in the appendices of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES 2015), and thus, their international trade requires permits detailing the number, origin, and destination of the individuals involved. According to CITES data, the total number of live parrots legally traded among countries from 1975 (when CITES entered in force) to 2015 was 19,607,897 individuals (annual mean of 490,197) belonging to 336 species. This figure corresponds to around 25% of the total registered legal bird trade. Only seven species—Grey Parrot (Psittacus erithacus), Senegal Parrot (Poicephalus senegalus), Monk Parakeet (Myiopsitta monachus), Rose-ringed Parakeet (Psittacula krameri), Rosy-faced Lovebird (Agapornis roseicollis), Fischer’s Lovebird (A. fischeri), and Yellow-collared Lovebird (A. personatus)—represented half of all of the parrots traded during this period. Importantly, at least 40% of the total parrot trade involved wild-caught individuals, whose invasive potential is significantly higher than that of captive-bred ones (Carrete and Tella 2008; Abellán et al. 2017). Considering individuals with a known wild-caught origin, only four species represented over 60% of total trade in the period 1975–2015: Grey Parrot, Senegal Parrot, Monk Parakeet, and Rose-ringed Parakeet. It is worth mentioning that Monk Parakeets and Rose-ringed Parakeets are considered two of the most widespread naturalized species of the world (Strubbe and Matthysen 2009a; Cardador et al. 2016; Jackson, chap. 10 this vol.; Uehling et al., chap. 12 this vol.).

Grey Parrots (Psittacus erithacus), originally bound for the illegal pet trade, confiscated from a local bird trapper. Maniema Province, Democratic Republic of Congo, May 2016. Photo by Cintia Garai.

ORIGIN AND DESTINATION OF PARROTS IN THE WILDLIFE TRADE

The sources of parrots in the wildlife trade in recent decades (1975–2015) are, not surprisingly, located within the main native areas of parrot species, namely South and Central America, sub-Saharan Africa, the Indian subcontinent, Indochina, and Indonesia (Fig. 1.3). The geographic focus of the parrot trade is also widespread, although it has undergone notable changes throughout time, as economic growth in developing countries has increased (Weber and Li 2008) and the main importing countries have imposed bans on wild bird imports (Cardador et al. 2017; Reino et al. 2017). In the recent past, the United States (US) and European countries dominated international parrot trade imports (Fig. 1.4). However, importations in these areas have been drastically reduced since the application of two bans. First, the US Wild Bird Conservation Act, enacted in 1992, prohibited the importation of wild birds unless they were collected in accordance with predefined management plans for sustainable use of the species. Second, the Wild Bird Declaration prohibited wild-caught bird importations in the European Union (EU). It was adopted in 2005, first as a temporal measure to prevent the spread of avian flu and other diseases and since 2007 as an indefinite measure also focused on conservation and animal welfare.

Figure 1.3. Main exporter countries of parrot species from 1975 to 2015. Total number of individuals traded (a) and total number of individuals traded with a known wild origin (b) are shown. Data source: CITES (2015).

The reduction of the US and EU wild bird markets after the bans reduced invasion risks (Cardador et al. 2019) but also led to important redirections of commercial species. Notable increases in importations occurred in Mexico, South America, countries of the former Soviet Union, and across Southeast Asia after the application of the US ban, whereas Mexico and the Middle East became the main destinations of commercial parrot species after the EU ban (Fig. 1.4). As a result of such redirections, the cumulative world surface exposed to alien parrots actually increased after the successive bans. Additionally, as new destinations include areas environmentally similar to those of the species’ origins, they are susceptible to invasion, which has led to a general increase in global invasion risk (Cardador et al. 2017). In fact, since the redirection of commerce, some new invasions have been described, such as the introduction of Monk Parakeets in Mexico (MacGregor-Fors 2011), and additional invasion events are likely in the near future (Cassey et al. 2015; Cardador et al. 2017).

From a socioeconomic point of view, changes in trade routes observed after the application of the US and EU bans have resulted in a change in the relationship between importations and countries’ socioeconomic development. Thus, considering parrot importation data from the past few decades, it can be seen that while a clear positive relationship between parrot importations and gross domestic product existed at a global scale before 1992, this relationship became weaker after the application of the US ban and almost null after the application of the EU ban in 2005 (Fig. 1.5). Such changes are of considerable concern, since the redirection of trade from developed countries, where knowledge and resources to combat invasive species are available and social awareness is high, to developing countries, which are less well equipped to deal with invasions, may strongly increase invasion risks and impacts in these areas (Nuñez and Pauchard 2010; Early et al. 2016).

Figure 1.4. Trade patterns for parrot species in different geographic areas in three main periods between 1975 and 2015 (CITES 2015). Spatial (a) and temporal (b) patterns are shown. Imports are based on live individuals from the direct international trade to reduce double counting of reexported specimens. Note that in (b), importations represent cumulative values across regions and are expressed in million individuals. In (b), vertical dashed lines represent wild-bird trade bans of the United States in 1992 and the European Union in 2005.

Figure 1.5. Relationships between the number of parrot species imported and gross domestic product (GDP) in the periods (a) 1975–1992, (b) 1993–2005, and (c) 2006–2015. Each dot represents a single year in a given region. Linear regressions (dashed lines) were fitted and the coefficient of determination (R²) is provided. Parrot imports and GDP per region represent cumulative values across countries included in those same regions. Data sources: CITES (2015) and World Bank (2019).

Interestingly, private demand for pet animals in countries subject to wildlife trade bans is now mainly satisfied by domestic trade of captive-bred species (Cassey et al. 2015; Cardador et al. 2019). As mentioned, captive-bred species are less successful than wild-caught species at establishing themselves in novel environments due to behavioral and physiological adaptations to captivity (Carrete and Tella 2008, 2015; Cabezas et al. 2013). This contributes to the invasion risk imbalance between developed and non-developed countries.

FINAL REMARKS

It is increasingly acknowledged that human activities interact with ecological processes in multiple ways. Increasing international trade, in particular, is accelerating the dispersal of alien species across the globe and inherently contributing to the homogenization of species assemblages at a global scale (McKinney and Lockwood 1999; Capinha et al. 2015). While it is widely recognized that wildlife trade is currently the most important and increasing source of alien vertebrates, such as parrot species, trade regulations are usually not instituted because of invasion risks. Additionally, although biological invasions are a global issue, responsibility for protection against invaders lies mostly with national governments. This has led to important differences in legislation among countries, even for those signatories of the Convention on Biological Diversity (CBD), which includes prevention, eradication, and control of invasive species as a commitment (McGeoch et al. 2010). Additionally, when applied, this legislation takes the form mostly of defensive measures (mainly bans and quarantines) to protect particular importer countries or regions against the potentially harmful effects of imported species. While these regulations offer an option to reduce the invasion likelihood in countries or regions of implementation, they do not tackle the problem of invasive species as a global issue, as risky species can still be exported to other countries. To avoid unintended consequences of national or regional regulations, such as unexpected geographic redirections or taxonomic changes, in the international pet trade (Cardador et al. 2017; Reino et al. 2017), more global, intercontinental strategies addressing biological invasions as a global issue are required. Applying the precautionary principle, blanket bans, such as the EU ban, should be seriously considered at a global scale. However, blanket bans are widely debated, as they can be difficult to apply, can be counterproductive—by promoting illegal trade or the development of new markets to support demand—and may produce negative impacts on the livelihoods of local human communities from the exporting countries (Cooney and Jepson 2005; Roe 2006; Rivalan et al. 2007). Alternatively, a trade regulation framework similar to that developed by CITES—the primary international instrument available to monitor and control wildlife trade of threatened species—should be created with the aim of creating binding international standards to regulate, monitor, and control the trade of potentially harmful species in both importer and exporter countries.

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2

THE DISTRIBUTION

OF NATURALIZED

PARROT POPULATIONS

Kay Royle and Wayne B. Donner

INTRODUCTION

Humans have been intentionally introducing birds and other animals outside their native ranges for approximately 5,000 years for a variety of reasons, including for sport, for food, for plumage, as a biological control, for conservation, and even out of curiosity (Lever 2005; Cassey et al. 2015). Sometimes this process has been an intentional introduction and release of species, and at other times it has been accidental. Regardless of the process, however, the outcome has been the same: new species are introduced into new environments and ecosystems. If the introduced species becomes established—that is, has a self-sustaining population in an area outside its native range—it can be classified as being a naturalized species in that area (Blackburn and Duncan 2001a; Dyer et al. 2017). Previously, the term naturalized has been used in as a synonym for invasive or alien, but it is used throughout this review, and this volume generally, to describe a species that is established in a new environment (Colautti and MacIsaac 2004).

Among vertebrates, birds have been transported around the world more than any other group, and the order Psittaciformes (parrots) has been especially successful (Ancillotto et al. 2016). Parrots have experienced higher numbers of introductions across the globe than would be expected by chance alone (Blackburn and Duncan 2001a), driven, for the most part, by the pet trade (Cassey et al. 2015). One of the challenges in tracking the global transport of birds is that changes in taxonomic treatment result in legislative lags, as conservation organizations catch up with taxonomic amendments (Garnett and Christidis 2017). A recent example of this is the African Grey Parrot (Psittacus erithacus), classified as a single species up until 2011. According to the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), this was, and remains, one of the most widely traded of all the parrot species. Since 2011, however, the species’ taxonomy has been amended, and it is now split into the Grey Parrot (Psittacus erithacus) and the Timneh Parrot (P. timneh), both initially classified as vulnerable and now as endangered (BirdLife International 2019). Such splitting and lumping of species is undoubtedly confounding scientific population studies and the simplification of environmental legislation (Garnett and Christidis 2017).

The current number of extant parrot species (excluding subspecies) is 381, according to the International Ornithologists’ Union checklist (Gill and Donsker 2019), up from the previous classification of 356 (Marsden and Royle 2015). This increase reflects a new focus on genetic differences among taxa as well as separation of ecologically distinct taxa. As a result of taxonomic changes in the classification of species, the number and distribution of introduced and naturalized species will also change. Thus, the number of recognized naturalized parrots is constantly changing, varying from study to study. In 2005, Lever suggested that of the 350 parrot species then recognized, 34 had established non-native populations. Two years later, Runde et al. (2007) stated that there were 39 naturalized parrot species. In 2014, Menchetti and Mori stated that 60 parrot species had breeding populations outside their natural range. One of the most recent studies, by Avery and Shiels (2018), states that 54 species have been introduced, and 38 of these have become established. Furthermore, the chapters in this volume suggest that the number of naturalized parrots is much larger than any of these earlier numbers suggest. What is the true number? The uncertainty of the answer highlights the problem with attempting to answer the most basic of questions: How many parrot species have populations outside their natural range?

NATURALIZED PARROTS

In this chapter we use records from one of the most recently established databases on invasive bird species: the Global Avian Invasions Atlas (GAVIA) (Dyer et al. 2017). The GAVIA database contains over 27,000 records of bird species, denoting each species’ invasive status as: established, breeding, unsuccessful, died out, extirpated, or unknown. We extracted studies dating between 1993 and 2012, which resulted in 2,941 records for invasive parrots, revealing a total of 129 species, recorded across 106 countries or territories. The majority of records belong to populations classified as either unknown or established (Table 2.1); however, their status may have changed across studies in the database. GAVIA follows the International Union for Conservation of Nature’s (IUCN) taxonomy; we made the taxonomy consistent with that of the IOC World Bird List (Gill and Donsker 2019) by reclassifying the genus of seven species.

TABLE 2.1

Categories of invasion status of parrots based on the GAVIA database, excluding introductions. The fact that there are more unknown records than any other highlights the lack of historical knowledge for invasive parrots. See Appendix 2.1 for more details.

Of the current extant parrot species, 47 species in 21 genera have at least one naturalized population. According to the IUCN (2019), six of these species are endangered, one of them critically, the Yellow-crested Cockatoo (Cacatua sulphurea). The six endangered species are now present in eight countries or territories. The genus Amazona contains the most endangered species (four) and also the most established species (eight). The Rose-ringed Parakeet (Psittacula krameri), Monk Parakeet (Myiopsitta monachus), and Budgerigar (Melopsittacus undulatus) have the most records of all the species in the GAVIA database. In addition to the 47 naturalized species, 16 other species have had at least one established population recorded outside their native range but within their native country and so are being classed as reintroductions in this review (e.g., Kakapo, Strigops habroptila).

Monk Parakeets (Myiopsitta monachus) being fed in a park in Barcelona, Spain. In the city, up to 40% of the food Monk Parakeets consume may be provided by humans. The birds are marked with numbered collars, as part of Juan Carlos Senar’s research of the parrots’ life history and movements. January 2019. Photo by Alba Ortega-Segalerva.

POPULATION STATUS OF NATURALIZED PARROTS

Alien species are now the second-largest threat to native species after biological resource use (Bellard et al. 2016) and are linked to negative economic impacts and the transportation of diseases (Shirley and Kark 2009; Menchetti and Mori 2014; Evans et al. 2016). Some parrot species are highly invasive and compete with native species for food, while others seem to utilize alternative food sources (Mori et al. 2017). A large number of parrot species are considered pests where they occur naturally (Lever 2005; Russello et al. 2008), but it is difficult to estimate the true extent of damage in introduced ranges because it is rarely quantified (Menchetti and Mori 2014). Some species cause ecological damage (Cassey et al. 2004a), while others come into conflict with humans by causing significant damage to crops, orchards, and even ornamental gardens (Menchetti and Mori 2014). These issues highlight why empirical data on the threat and spread of naturalized species is an important conservation tool, for both the species in question and also the habitats and native species found in their new ranges.

Of the 47 established parrot species listed in GAVIA, nine have populations classified as increasing, a further seven are stable, and the rest have decreasing populations (Table 2.2) (Birdlife International 2019).

The United States (US), including Hawaii, is particularly well studied, with 304 established records, almost a third (28.6%) of the global records in GAVIA for Psittaciformes. Based on the GAVIA database, 19 species have been recorded in the US, four of which account for the majority of records, each with over 40 established populations recorded: Red-crowned Amazon (Amazona viridigenalis), Budgerigar, Monk Parakeet, and Rose-ringed Parakeet. A more complete analysis by Uehling et al. (2019), however, has shown that the numbers of naturalized parrots in the US is actually larger than evidenced from the GAVIA records. Uehling et al. (2019) document that for the contiguous US, there are now 25 different species breeding in 23 states, with Florida, California, and Texas supporting the largest numbers of naturalized parrots.

In the years between 1986 and 1991, a total of 17 invasive parrot species were counted in Florida alone, with nine of these found breeding in more than one location (Pranty and Epps 2002; Butler 2005). By 2003, this number had risen to 22 breeding species and an additional three breeding but not yet established (Pruett-Jones et al. 2005; Uehling et al. 2019). One of the most frequently released species, either accidentally or intentionally, is the Budgerigar (Uehling et al. 2019). It was first reported as breeding in Florida in 1963 and had established a population by 1977. It reached a peak population of between 6,000 and 8,000 individuals in 1978, followed by a sharp decline, from which it apparently never fully recovered (Butler 2005). Dramatic declines of Budgerigars have been reported in both the US and the United Kingdom (UK), with a sudden reduction of bird feeders as the suspected cause for the UK population crash (Butler 2005). Sudden declines in other parrot populations in the US have been reported—e.g., Red-masked Parakeet (Psittacara erythrogenys) and White-winged Parakeet (Brotogeris versicolurus)—but without obvious causes (Aagaard and Lockwood 2016), highlighting the difficulty in determining long-term population dynamics.

Rose-ringed Parakeets and Monk Parakeets both established populations in the US in the 1970s (Strubbe and Matthysen 2009) and have been the subjects of several studies (e.g., South and Pruett-Jones 2000; Pruett-Jones et al. 2012; Avery and Shiels 2018). Population estimates of Rose-ringed Parakeets differ among studies (Butler 2005), but naturalized populations generally appear to be increasing and expanding (Avery and Shiels 2018). While many species of naturalized parrots are rapidly increasing, some of their ranges seem to be restricted, possibly by climate or food sources but also in part because of their natural limited dispersal habits (Butler 2005). Rose-ringed and Monk Parakeets suffer heavy losses in colder weather, so it is likely that their numbers will increase with climate change, as this will reduce the extent of winter cold, which seems to be a limiting factor (Strubbe and Matthysen 2009).

TABLE 2.2

Species of naturalized parrots whose populations are stable, increasing, or decreasing in size. Almost one-sixth of all naturalized parrots have increasing populations, according to Birdlife International, including the three most common species: Rose-ringed Parakeet, Monk Parakeet, and Budgerigar. Species are listed in alphabetical order by common name.

Population changes may be attributable to differences in survey effort, observation methods, or seasonal fluctuations (Simberloff 1995; Garrett 1997; Bibby et al. 2000). Over the years, citizen science increasingly has been used across various disciplines as a source of large data sets (e.g., eBird.org or the British Trust for Ornithology’s Breeding Bird Survey) (Tulloch et al. 2013; Sullivan et al. 2014). Citizen science allows for the collection of data that would otherwise be impossible due to a lack of scientific resources (Tulloch et al. 2013). Parrots are often brightly colored, conspicuous, and vocal, and therefore are easily seen by members of the public (Cassey et al. 2004a). However, data of this nature should be used with caution because projects differ in their yield of usable data (Tulloch et al. 2013). Misidentification may occur when morphologically similar species are found in close proximity, and studies that do not span long time frames may also produce limited results for long-lived birds like parrots. Determining whether there is an established, self-sustaining population, or whether the adults present are nonbreeding individuals that will die out, can be complex (Long 1981; Runde et al. 2007). Many invasive species exhibit time lags between their release and exponential population growth, so their presence may go undetected for many years (Sakai et al. 2001; Crooks 2005; Aagaard and Lockwood 2014). Although this delay is a common feature of alien invasions, the reason for it still remains unclear (Sakai et al. 2001; Crooks 2005). A more sensible approach, therefore, is to investigate individual species and areas over time. This, however, is unfeasible given the amount of time and effort needed for micro-scale studies. However, while data are deficient for the majority of species (Mori et al. 2017), some have more data available than others. A greater quantity of data is available for those birds that are easier to observe; however, its quality is not always suitable for reliable statistical analysis (Lodge 1993).

Definitive conclusions are hard to draw from existing data on introduction, success, or failure rates (Mack et al. 2000). The GAVIA database reveals that ~41% of all species’ records have the status unknown, highlighting the lack of knowledge in studies (Table 2.1). Unsuccessful invasions may often go unnoticed, are harder to detect, and may be underrepresented (Lodge 1993); therefore, data on these species are simply not available (Simberloff 1995; Sol and Lefebvre 2000).

Scarlet-fronted Parakeets (Psittacara wagleri) inspecting drainpipes for potential nest sites. Miami Springs, Florida, US, May 2011. Photo by Roelant Jonker.

Native but urbanized White-winged Parakeets (Brotogeris versicolurus) coming into roost at the Praça Santuário de Nazaré in Belém, Brazil. January 2009. Photo by Roelant Jonker.

SUCCESS OF NATURALIZED SPECIES

One of the key research subjects in avian invasions is determining the factors that drive the success of one species over another in becoming naturalized. It has been suggested that some species, e.g., Rose-ringed Parakeet, seem to be successful wherever they are introduced, while others, e.g., Tepui Parrotlet (Nannopsittaca panychlora), Plain Parakeet (Brotogeris tirica), and Grey-cheeked Parakeet (Brotogeris pyrrhoptera), seem unable to succeed at all (Mori et al. 2013). The reasons for this may be biological, or they may be environmental, as even closely related species seem to differ in their ability to become established once introduced. The closely related naturalized species Yellow-headed (Amazona oratrix) and White-fronted (A. albifrons) Amazons provide one example. Both are native to Central America and Mexico and have been introduced into other areas of Mexico, Puerto Rico, and the US. The more widespread Yellow-headed Amazon is classified as endangered, due to a decreasing global population, whereas the White-fronted Amazon is classified as a species of least concern and is increasing in numbers (Birdlife International 2019).

Discovering whether any common biological traits are shared among naturalized or invasive species could be advantageous in future conservation efforts (Griffith et al. 1989; Strubbe and Matthysen 2009). However, there is a lack of historical data on biological factors affecting success rates of establishment (Sol and Lefebvre 2000). Failed attempts often go unreported, so most data come from successfully established species, which can lead to interpretative bias if not accounted for (Lodge 1993).

Several studies have investigated the biological traits of introduced bird species, including body weight (Green 1997; Cassey et al. 2004a), fecundity (Cassey et al. 2004a), migratory habits (Kolar and Lodge 2001; Cassey et al. 2004a), and forebrain size and adaptability (Sol and Lefebvre 2000). Many regional studies suggest that biology can affect introduction success (e.g., Cassey 2002), but this may be because specific traits are influenced by the nonrandom distribution of birds (Lockwood 1999; Blackburn and Duncan 2001a).

Studies have shown that certain traits appear to affect introduction and establishment differently. Body weight has been suggested as a successful trait for invasive birds, but its effect on introduction and establishment may differ among families. There are large morphological variations within naturalized psittaciforms, which range in length from 15 cm to 95 cm (Juniper and Parr 2010). The largest of these is the Redand-green Macaw (Ara chloropterus), which can weigh up to 1.7 kg (Collar et al. 2020), and among the smallest is the Grey-headed Lovebird (Agapornis canus), which weighs only 25–35.5 g (Collar and Kirwan 2020). Green (1997) found that greater body weight had a positive effect on the introduction success of New Zealand exotics, but these results varied, based on whether statistics were carried out within a family or not. Cassey et al. (2004a) found similar results with parrots but noted that morphology may be indirectly related to the chance of establishment: longer-lived or larger, more colorful birds may be more likely to be traded. Birds that have a longer life span are also more likely to be deliberately released, because of the amount of care needed in captivity (Cassey et al. 2004a).

The chance of a species being introduced increases with higher fecundity (e.g., greater clutch size and fledging success, etc.) (Cassey 2002; Cassey et al. 2004a). However, a slower rate of population growth (e.g., longer generation times, lower fecundity, and longer fledging periods, etc.) appears to be a factor in becoming established for introduced species (Cassey et al. 2004b; Blackburn et al. 2009a). These findings are contradicted somewhat by Blackburn and Duncan (2001b), who found that family-level traits (e.g., body mass, clutch size, and incubation period) had no significant effect on the chances of naturalization success.

Regional studies show that sedentary species are more likely to establish in new areas following release than migratory birds (Kolar and Lodge 2001; Cassey 2002), especially with the same introductory effort (Veltman et al. 1996). However, once a migratory species is established in a new range, it is more likely to spread widely, due to natural dispersal habits (Kolar and Lodge 2001). It is thought that dispersal behaviors reduce the chances of a breeding individual finding a suitable mate during the initial phases of colonization (Veltman et al. 1996).

A broader diet in the native range of an invasive parrot species may also contribute to success among naturalized populations (Cassey et al. 2004a). Indeed, a greater diet breadth is correlated with successful establishment (Lockwood 1999). Species that are habitat or diet specialists are far less likely to colonize than those that are generalists (Brooks 2001). Therefore, species that readily exploit novel food sources are more likely to persist in new environments (Sol and Lefebvre 2000; South and Pruett-Jones 2000; Nicolakakis et al. 2003). Behavioral flexibility can be an advantage in colonizing new areas (Sol and Lefebvre 2000; Nicolakakis et al. 2003). Parrots are sociable birds, and there is some evidence that Rose-ringed and Monk Parakeets have formed mixed flocks, which may be mutually beneficial, at the expense of native species (Ancillotto et al. 2016). With expanding urbanization, species that are able to exploit these areas and new niches are more likely to succeed.

FACTORS AFFECTING SPECIES TRANSPORT

One of the biggest factors influencing the transport of non-native species is the pet trade (Carrete and Tella 2008; Smith et al. 2009), especially since globalization closed the gaps in geography and facilitated international trade (Hulme 2009; Mori et al. 2017). An estimated two-thirds of parrot species have been transported to areas outside their native range (Beissinger 2001; Cassey et al. 2004a; Ancillotto et al. 2016), and these numbers seem to be increasing (Lockwood et al. 2019). Escape from suppliers, breeders, or owners (Carrete and Tella 2008; Hulme 2009; Lockwood et al. 2019) is likely to be one of the reasons parrots have so many populations in urban areas and why their numbers and diversity peak around ports of entry (Runde et al. 2007).

As well as being an indirect contributor of non-native parrots, the pet trade may also be confounding research into the distribution and abundance of established species. Perceived increases in numbers could simply be because of the increase of parrot imports (particularly from the Neotropics to the US) and the subsequent accidental releases (Garrett 1997). It may also be possible to draw incorrect conclusions about specific traits because the phylogenetic associations that are leading to taxonomic patterns in data may be caused by human influences on their distribution (Lockwood 1999; Blackburn and Duncan 2001a).

There seems to be a general trend for naturalized parrots to have strong associations with humans (Avery and Shiels 2018), and the proportion of naturalized species is higher in urban and suburban areas (Runde et al. 2007). Many parrots are tolerant of a wide variety of ecological factors and show a high level of synanthropy (Mori et al. 2013), becoming established in urban areas with greater amounts of exotic flora, which may be a suitable foraging source (Garrett 1997). This may be because of a specific reliance on humans or because urban areas are where the majority of releases and escapes occur (Butler 2005; Menchetti and Mori 2014). Particularly successful species, such as the Rose-ringed Parakeet and the Monk Parakeet, have close associations with humans and inhabit areas with greater human populations (Strubbe et al. 2015; Domènech et al. 2003; Crowley, chap. 3 this vol.). Both parakeets are synanthropic and are often found in close association with humans in their native ranges (Minor et al. 2012; Strubbe et al. 2015). Monk Parakeets have a diverse diet and have adapted to use bird feeders over winter (South and Pruett-Jones 2000; Minor et al. 2012).

MacArthur and Wilson (1967) determined that founder population size was important in the success of island colonizations. This led to a now a widely used theory in the study of both invasive and naturalized bird species. The theory is that one of the primary factors that determine success of naturalized species is related to the numbers of birds released (known as introduction effort) (Green 1997; Lockwood 1999; Sol and Lefebvre 2000; Kolar and Lodge 2001; Cassey et al. 2005; Runde et al. 2007). Introduction effort relates to propagule size and number; propagule size is the total number of individuals in a single release event, and the propagule number is the amount of separate releases (Cassey et al. 2004b). Greater introduction success rates are correlated with larger numbers of a species being released into a site and with the species’ repeated release (Blackburn and Duncan, 2001a). If propagule size is excluded from statistical modeling, then other factors appear to be more important—e.g., habitat generalism, migratory behavior, range size, and the proximity of source and destination latitudes (Cassey et al. 2004b).

Results of studies into influencing factors of colonization are likely to be confounded by the nonrandom nature of the species being introduced and the location of that introduction (Lockwood 1999; Blackburn and Duncan 2001a; Cassey et al. 2004b). This may lead to the conclusion that introduction appears to be correlated with specific traits, whereas in fact, the traits relate more to which species are selected for the pet trade