Research Article |
Corresponding author: Rachel L. White ( r.white2@brighton.ac.uk ) Academic editor: Uwe Starfinger
© 2019 Rachel L. White, Diederik Strubbe, Martin Dallimer, Zoe G. Davies, Amy J.S. Davis, Pim Edelaar, Jim Groombridge, Hazel A. Jackson, Mattia Menchetti, Emiliano Mori, Boris P. Nikolov, Liviu G. Pârâu, Živa F. Pečnikar, Tristan J. Pett, Luís Reino, Simon Tollington, Anne Turbé, Assaf Shwartz.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
White RL, Strubbe D, Dallimer M, Davies ZG, Davis AJ.S, Edelaar P, Groombridge J, Jackson HA, Menchetti M, Mori E, Nikolov BP, Pârâu LG, Pečnikar Živa F, Pett TJ, Reino L, Tollington S, Turbé A, Shwartz A (2019) Assessing the ecological and societal impacts of alien parrots in Europe using a transparent and inclusive evidence-mapping scheme. NeoBiota 48: 45-69. https://doi.org/10.3897/neobiota.48.34222
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Globally, the number of invasive alien species (IAS) continues to increase and management and policy responses typically need to be adopted before conclusive empirical evidence on their environmental and socioeconomic impacts are available. Consequently, numerous protocols exist for assessing IAS impacts and differ considerably in which evidence they include. However, inclusive strategies for building a transparent evidence base underlying IAS impact assessments are lacking, potentially affecting our ability to reliably identify priority IAS. Using alien parrots in Europe as a case study, here we apply an evidence-mapping scheme to classify impact evidence and evaluate the consequences of accepting different subsets of available evidence on impact assessment outcomes. We collected environmental and socioeconomic impact data in multiple languages using a “wiki-review” process, comprising a systematic evidence search and an online editing and consultation phase. Evidence was classified by parrot species, impact category (e.g. infrastructure), geographical area (e.g. native range), source type (e.g. peer-review), study design (e.g. experimental) and impact direction (deleterious, beneficial and no impact). Our comprehensive database comprised 386 impact entries from 233 sources. Most evidence was anecdotal (50%). A total of 42% of entries reported damage to agriculture (mainly in native ranges), while within Europe most entries concerned interspecific competition (39%). We demonstrate that the types of evidence included in assessments can strongly influence impact severity scores. For example, including evidence from the native range or anecdotal evidence resulted in an overall switch from minimal-moderate to moderate-major overall impact scores. We advise using such an evidence-mapping approach to create an inclusive and updatable database as the foundation for more transparent IAS impact assessments. When openly shared, such evidence-mapping can help better inform IAS research, management and policy.
evidence base, impact assessment, invasive alien species, monk parakeet (Myiopsitta monachus), ring-necked parakeet (Psittacula krameri), Psittaciformes
The number of human-mediated species introductions has been increasing worldwide (
Quantifying the magnitude of IAS impacts remains particularly challenging for various reasons (see
An assessment of the consequences of accepting different types of evidence data on impact assessment outputs has yet to be conducted. However, the current disparity in accepted evidence potentially leads to ambiguous, difficult-to-repeat and even contested impact assessment outcomes (
Impact evidence variables and metadata recorded for each evidence entry in this study. When assignment to a single category is difficult, this can be flagged in the comments column or the entry can be given a dual coding.
Impact evidence variable | Levels | Description |
Species | 11 parrot species | Any one of the 11 parrot species designated “alien” status in Europe by EASIN (see Table |
Impact category | GISS categories (see Suppl. material |
Environmental: (1) competition, (2) transmission of diseases or parasites, (3) herbivory and (4) impacts on ecosystems. Socioeconomic: (5) agricultural production, (6) animal production, (7) forestry production, (8) human health, (9) human well-being, and (10) human infrastructure and administration. |
Geographical area | European | Evidence from Europe (see Suppl. material |
Other non-native range | Evidence from any other non-native range | |
Native range | Evidence from native range | |
Captive | Evidence from captivity (regardless of country) | |
Actual / potential impact | Actual | Evidence from within assessment area (here: Europe). |
Potential | Evidence from native range, other non-native range or captivity. | |
Source type | Peer reviewed | Peer-reviewed publications, academic books and book sections. |
Not peer-reviewed (grey literature) | PhD/Master’s thesis, governmental/NGO reports, conference proceedings, magazine/newspaper article, webpage. | |
Unpublished data | Personal communication, personal observation, unpublished data. | |
Study design | Experimental | Qualitative/quantitative study using a qualitative/quantitative experimental manipulation of the mechanisms by which the invader is presumed to have an effect (allows inference on magnitude and causality of impact). |
Non-experimental | A study that uses a qualitative/quantitative, but non-experimental, scientific sampling design (allows inference on magnitude but not causality of impact). | |
Anecdotal | Casual observation acquired without a sampling design (only allows inferences on presence/absence of impact, not on magnitude or causality). | |
Indirect report | Impact not observed by person reporting it or sources that do not report primary data (impacts cannot be verified). | |
Impact direction | Deleterious | Evidence entry explicitly reports deleterious impact. |
Beneficial | Evidence entry explicitly reports beneficial impact. | |
No impact | Covers cases where no impact is explicitly reported. | |
Metadata | Source identifier; Evidence entry identifier (for entries coming from a source containing multiple pieces of evidence); Year in which evidence was made available; Source language; Geographical region; Country; Detailed location of reported impact (e.g. nearby city or coordinates); Full bibliographic reference of source; Expert assessor name; and a short written description of relevant evidence. |
Parrots are amongst the most prominent pet birds worldwide and the large volume of pet-trade driven exports followed by escape and release has resulted in the establishment of numerous alien populations worldwide (
The European Alien Species Information Network (EASIN) recognises 11 alien parrot species in the EU (Table
Current status of the 11 alien parrot species within Europe (as recognised by EASIN; https://easin.jrc.ec.europa.eu/). Information obtained from GAVIA database (
Species name | Native range | Alien European range (Unknown, Died out) | Europe populations (size) | Other alien range: breeding/established | Impact status (EASIN) |
---|---|---|---|---|---|
Yellow-collared lovebird (Agapornis personatus) | Tanzania | France, Spain | Unknown | Burundi, Kenya | Low/unknown |
Turquoise-fronted amazon (Amazona aestiva) | Argentina, Bolivia, Brazil, Paraguay | Italy, Spain (Germany, Switzerland) | Genoa, Milan, Valencia ( |
USA | Low/unknown |
Yellow-crowned amazon* (Amazona ochrocephala) | Central and South America |
(Germany, Italy: |
Genoa, Milan, Stuttgart (50 since 1984) ( |
Barbados, Cayman Islands, Mexico, Netherlands Antilles, Puerto Rico, Trinidad, USA | Low/unknown |
Blue-crowned parakeet (Aratinga acuticaudata) | South America | Spain, (UK, Italy: |
Barcelona (8 pairs/25 birds) ( |
USA | Low/unknown |
Red-masked parakeet (Aratinga erythrogenys) | Ecuador, Peru | Spain | Barcelona, Seville, Valencia | Cayman Islands, USA, | Low/unknown |
Mitred parakeet (Aratinga mitrata) | Argentina, Bolivia, Peru | Spain | Barcelona (100–150 birds) ( |
Puerto Rico, USA | Low/unknown |
Budgerigar (Melopsittacus undulatus) | Australia | Greece (Germany, Spain, Turkey, Austria, Belgium, Italy ( |
Unknown | Cayman Islands, Dominican Republic, Guadeloupe, Hong Kong, Jamaica, Japan, Mexico, Namibia, Oman, Puerto Rico, Qatar, Spain (Canary Islands), Taiwan, USA, Venezuela | Low/unknown |
Monk parakeet (Myiopsitta monachus) | Argentina, Bolivia, Brazil, Paraguay, Uruguay | Austria, Belgium, Czech Republic, France, Germany, Italy, Netherlands, Portugal, Spain, UK (Denmark, Slovakia) | 30 established populations. More than 22,000 individuals across Europe (Postigo J-L, pers. comm. 2018). | Australia, Canada, Cayman Islands, Chile, Dominican Republic, Guadeloupe, Israel, Japan, Kenya, Mexico, Puerto Rico, USA, Venezuela | High |
Nanday parakeet (Nandayus nenday) | Argentina, Bolivia, Brazil, Paraguay | Spain | Barcelona (5 pairs) ( |
Israel, Puerto Rico, Spain (Canary Islands), USA | Low/unknown |
Alexandrine parakeet (Psittacula eupatria) | Southern Asia | Belgium, Germany, Italy, Turkey (Greece, Netherlands, Spain, UK) ( |
A minimum of 1000 individuals in Europe ( |
Bahrain, Israel, Japan, Jordan, Oman, UAE, Yemen | Low/unknown† |
Ring-necked parakeet (Psittacula krameri) | Southern Asia and sub-Saharan Africa | Austria, Belgium, France, Germany, Greece, Italy, Netherlands, Portugal, Slovenia, Spain, Turkey, UK (Ireland, Switzerland, Ukraine) | 95 populations have established since the 1960s. At least 85,000 birds ( |
Australia, Bahrain, Barbados, Cape Verde, Cayman Islands, China, Cuba, Egypt, Hong Kong, Iran, Iraq, Israel, Japan, Jordan, Kenya, Kuwait, Lebanon, Maldives, Malta, Mauritius, Oman, Philippines, Puerto Rico, Qatar, Reunion, Saudi Arabia, Singapore, South Africa, Thailand, UAE, USA, Venezuela, Yemen | High |
Alien parrot species thus represent an excellent group to explore the added value of the above-mentioned evidence-mapping scheme for conducting impact assessments (Table
We assessed the environmental and socioeconomic impacts of the eleven alien parrot species (Table
We utilised an innovative “wiki-review” process to facilitate comprehensive inclusion of sources and subsequent impact evidence into the evidence-mapping database. The process combined literature searches and preparation of impact review documents and databases by 15 selected experts from the EU collaborative network on alien parrots “ParrotNet” (COST Action ES1304), followed by an online editing and consultation phase conducted by a larger expert panel (open to ParrotNet participants and additional experts).
Each selected expert was first assigned an impact category and conducted a literature review to gather associated evidence on parrot impacts. Although a formal systematic review approach was not used due to the breadth of the study and its inclusive nature, experts conducted systematic keyword searches of the literature (i.e. using search terms pertinent to the respective impact category in combination with the scientific name of each species or either the term “parrot”, “parakeet”, “amazon”, “budgerigar” or “lovebird”). There was no restriction on publication year. Experts classified all evidence found on parrot impacts by geographical area, source type, study design and impact direction (see Table
Upon completion, all impact reviews and associated evidence-mapping databases were placed online and the larger expert panel invited to review, edit and add information. Specifically, they read through one or more impact reviews and added any evidence not yet included, with a focus on evidence from grey literature, unpublished data and evidence in their native language and/or from their country of residence. This subsequent wider-consultation was open between March and December 2016, undertaken by 47 experts in (parrot) invasion biology and covered 17 languages (Bulgarian, Catalan, Dutch, English, Estonian, Finnish, French, German, Hebrew, Italian, Polish, Portuguese, Romanian, Russian, Slovenian, Spanish and Turkish). Several additional relevant sources, published between the end of the consultation period up to May 2017, were added by the lead authors.
Finally, to complement the “wiki-review”, we consulted stakeholders from locations across Europe where parrots have established in order to identify any additional evidence of socioeconomic impact. Stakeholders included representatives of farmer/landowner associations, government officials responsible for agricultural damage or public complaints officers, airport bird collision officials and bird or conservation NGOs. Altogether, 69 stakeholders were contacted between October and December 2015, from nine countries (Belgium, France, Germany, Italy, Netherlands, Portugal, Spain, Turkey and UK) and 41 responded (59% response rate), representing all aforementioned countries except Turkey. All stakeholders who responded to our survey provided anecdotal information on minor damage to crops (notably, by RNP) - information which was already well-captured in our “wiki-review”. Since these insights were not collected by stakeholders in a rigorous way and were mainly based on personal or anecdotal knowledge, these responses were not included in the database, but serve as a form of validation to the findings of the literature search and are summarised separately in Suppl. material
Impact severity was assessed via the GISS impact assessment protocol (
In order to obtain a general overview of the evidence base, we first used descriptive statistics to synthesise and summarise how reported impacts were distributed across species, impact category, geographical area, source type, study design and direction of impact. Secondly, we mapped the spatial distribution of the evidence for deleterious impacts (Europe and worldwide) across impact categories, providing a visual representation of where different reported impacts originated. Finally, we investigated how criteria on evidence inclusion influenced the outcome of IAS impact assessments, for all alien parrots in Europe (combined and per species). Following
A total of 386 independent evidence entries were obtained from 233 sources, spanning from 1895 to 2017 (with a noticeable increase from the late 1990s onwards). Although peer-reviewed publications were the most common evidence source, 42% of entries came from grey literature or unpublished data. Entries spanned sources written in 10 different languages (predominantly English: 71%), from all continents (save Antarctica) and 32 countries (Europe: 39%; other invaded range: 20%; native range: 32%; captive: 9%; Suppl. material
Within Europe (Fig.
Spatial distribution of deleterious impact evidence for the 11 alien parrot species in Europe, by a countries within Europe (n = 122) and b regions across the world (n = 316; Africa, Australia, Europe, Far East, Indian-subcontinent, Latin America, Middle East, North America). Evidence is further split by GISS impact category. Numbers refer to corresponding number of evidence entries, which include those from captivity. Parrot species occurrence data used to derive parrot species richness maps were taken from the Global Biodiversity Information Facility (GBIF, www.gbif.org).
Overall, 29 entries reported evidence of beneficial impact (45%: competition, 41%: herbivory, and 14%: human well-being). Beneficial entries for indirect facilitation of conditions, either by providing resources or by competing with native species’ local competitors, were all anecdotal, with 18% of all competition evidence from Europe being beneficial (referring to nesting cavities made by RNP and Psittacula eupatria, use of MP nests as breeding sites and protection via RNP anti-predatory (‘mobbing’) behaviour). Evidence of beneficial impacts relating to herbivory reported that parrots can disperse seeds of native species or feed on and damage alien plants. Most of this evidence (82%) came from the native ranges of the six respective species and, except for one experimental study, were either anecdotal or non-experimental. Finally, evidence on benefits to human well-being came largely from anecdotal sources, with 75% from Europe (all RNP), one entry from the USA (MP) and none from native ranges.
Almost half (48%) of all evidence entries could not be assigned an impact score. Within the entire database (386 entries), 19 entries scored a “4” for impact severity; these reported potential impact (i.e. outside of Europe) and all but two related to agricultural impact. Only three entries obtained the maximum score of “5”: two reports (one anecdotal and one indirect) of competition between RNP and the endangered Echo parakeet (Psittacula eques) in Mauritius and an indirect report of the RNP being involved in bird-aircraft strikes in the UK. When using all collected evidence recorded in any geographical area, maximum impact across impact categories was highest for both competition and infrastructure (5), whereas mean impact was greatest for agriculture (2.35) and infrastructure (1.93) (see Suppl. material
Impact scores were separated by actual versus potential impact (i.e. recorded within or outside of Europe, respectively), source type and study design (Figs
Impact scores for all 11 alien parrot species combined per impact category, broken down by actual versus potential impact (a mean b maximum) and source type (c mean d maximum). Sample sizes are shown in square brackets and relate to levels as ordered in the legend (x signifies no data with an impact score).
Impact scores for all 11 alien parrot species combined per impact category, broken down by study design (a mean ±SE b maximum). Samples sizes for both plots are shown within the bars of the first plot.
Focusing on the RNP, most scores related to non-experimental evidence of agricultural impact from the native range (Fig.
Mean (red) and maximum (black) impact scores broken down by study design and geographical area for a RNP agricultural impact b RNP competition impact c MP agricultural impact and d MP infrastructure impact. Highest possible impact score = 5.
Agricultural impact by parrots was reported for 16 crops within Europe (mainly maize, plums and tomatoes) and outside Europe for 33 crops (mainly maize and sunflower), although impact severity scores could only be assigned to 11 and 21 crop types, respectively. Although sample sizes were low, the highest actual (European) impact was reported for plums, pumpkin, sunflower, maize and tomato. Potential (non-European) crop impact was greatest for rice, mango, pomegranate, sunflower and maize. Within Europe, most evidence of MP agricultural damage comes from Spain, whereas the damage attributable to the RNP originates mainly from Belgium and the UK.
A range of impact assessment protocols exist to assist necessary prioritisation of IAS management. However, protocols vary in the types of evidence included. Here, we argue that all impact records encountered during any IAS impact assessment should first be summarised into a transparent, openly-accessible, inclusive and standardised evidence base, allowing one to track how variation in accepted evidence influences the severity of final, overall impact scores. We believe doing this will strengthen the existing standards of IAS impact assessments and contribute towards scientifically, socially and politically acceptable IAS management decisions.
Both the evidence-mapping scheme and “wiki-review” used in this study facilitate the creation of such an evidence base. The former enables a more structured and transparent evaluation of impacts for any alien species within any geographical location. It can also allow the interchange or publication of datasets, potentially preventing unnecessary replication of literature review efforts, facilitate rapid updating and enable comparison of outcomes of assessments with respect to different protocols. The “wiki-review” process facilitates the collection of non-peer-reviewed information plus evidence from additional (non-English) languages. Collectively, these two sequential approaches can help address some of the main challenges surrounding the reliability of IAS risk analysis, as highlighted by
The use of the impact evidence-mapping scheme here does not resolve some longstanding important issues, which are part of impact assessments. For instance, the use of anecdotal data, information from the native range, evidence on beneficial impacts, summarising methods for impact severity and setting up clear thresholds to what is considered high or low impact (
A second outstanding issue is how to deal with evidence from the native range and other invaded areas. We argue that impacts from these geographical areas should be mapped but kept separate from evidence obtained from the focal study region, as extrapolation may not be straightforward (
Lastly, evidence-mapping results in a set of recorded impacts, but these need to then be scored and summarised into a single, overall impact score to allow ranking IAS according to the magnitude of the threats they pose. The summarising method has strong implications on the magnitude of impacts assigned to alien species and our results clearly demonstrate that. Both scoring methods (maximum and mean) have strengths and weaknesses and we suggest that summarising impact based on both approaches is of inherent and complementary value for guiding management decisions (see also
The approach followed in this study has resulted in the most comprehensive and transparent assessment of alien parrot impacts within Europe to date. Allowing different levels of the evidence base (Table
Evidence of MP impact in Europe (excluding indirect and anecdotal reports) comes from only two studies reporting agricultural damage in Spain (Barcelona) (
For the remaining nine parrot species, either no or very little information on impacts within Europe were retrieved (mainly indirect reports or anecdotal). These species all have localised and (very) small European populations and negligible actual impact. Even when allowing impact evidence from other invaded ranges or the native range, assessments for these species remain unchanged, except for Amazona aestiva which is an agricultural pest in parts of its native range (e.g.
One of the benefits of the evidence-mapping scheme used here is that it facilitates identification of knowledge gaps and can potentially influence the direction of future IAS research. Roughly half of all entries in our database did not allow assignment of an impact severity score, due to ambiguous evidence; e.g. a given source failing to explicitly associate an impact as coming from a specific parrot species. Although parrots are a relatively well-studied bird group which is at least partly attributable to their being noisy and conspicuous (
One broad reason to explain why little impact data exist for most alien bird species generally, is that some populations may be perceived to cause negligible or no harm (i.e. below the threshold) and, consequently, are not studied (
The outputs from impact assessments alone should not be used to prioritise alien species for management, as impact assessment is only one subcomponent of risk assessment, which in turn is only one subcomponent of risk analysis (Suppl. material
We find limited evidence of widespread (severe) parrot impacts across Europe. Instead, impacts within Europe are predominantly localised and differ across countries/regions. Hence, it is unlikely to be necessary, at present, to put any of the 11 parrot species on the Union List. Most parrots in Europe are currently known from relatively few and disjunct populations and necessary management actions, if any, can be carried out at local or regional levels. RNP and MP are more widespread and populations may span national borders (e.g. across the lowlands of northern France, Belgium, the Netherlands and Germany or across parts of the Mediterranean seaboard;
The rise of “invasive species denialism” (
We acknowledge the support provided by the European Cooperation in Science and Technology (COST Action ES1304: ParrotNet) for the development of this article. The contents of this article are the authors’ responsibility and neither COST nor any person acting on its behalf is responsible for the use that might be made of the information contained in it. We would also like to thank Ingo Kowarik, Matthew Chew and one anonymous reviewer for useful comments on an earlier version of the manuscript. Finally, we would like to thank all ParrotNet members who contributed to the “wiki-review” process, as follows: Tamer Albayrak, Leonardo Ancillotto, Michael Braun, Martina Carrete, Francois Chiron, Philippe Clergeau, Sarah Crowley, Kiraz Erciyas-Yavuz, Gioele Grandi, Dailos Hernández-Brito, Asaf Kaplan, Salit Kark, André van Kleunen, Marine Le Louarn, Alvaro Luna, Yariv Malihi, Riho Marja, Juan Masello, Alexander Mertens, Yoav Motro, Esra Per, Benoit Pisanu, José-Luis Postigo, Stefan Schindler, Juan Carlos Senar, Craig Symes, José L. Tella, Piotr Tryjanowski and Anne Weiserbs. Diederik Strubbe was funded by a Marie Skłodowska‐Curie Action under the Horizon 2020 call (H2020‐MSCA‐IF‐2015; grant number: 706318) and acknowledges the Danish National Research Foundation for support to the Center for Macroecology, Evolution and Climate (grant number: DNRF96).
Supplementary background, methods and results
Data type: background, description, measurement
Explanation note: Appendix A: Supplementary background, Appendix B: Supplementary methods, Appendix C: Supplementary results.
Impact evidence database
Data type: description, measurement
Explanation note: Appendix D: Impact evidence database.