Global economic costs of alien birds

Thomas Evans; Elena Angulo; Corey J A Bradshaw; Anna Turbelin; Franck Courchamp

doi:10.1371/journal.pone.0292854

. 2023 Oct 18;18(10):e0292854. doi: 10.1371/journal.pone.0292854

Global economic costs of alien birds

Thomas Evans ^1,^*, Elena Angulo ^1,², Corey J A Bradshaw ^3,⁴, Anna Turbelin ¹, Franck Courchamp ¹

Editor: Mirko Di Febbraro⁵

PMCID: PMC10584179 PMID: 37851652

Abstract

The adverse impacts of alien birds are widespread and diverse, and associated with costs due to the damage caused and actions required to manage them. We synthesised global cost data to identify variation across regions, types of impact, and alien bird species. Costs amount to US$3.6 billion, but this is likely a vast underestimate. Costs are low compared to other taxonomic groups assessed using the same methods; despite underreporting, alien birds are likely to be less damaging and easier to manage than many other alien taxa. Research to understand why this is the case could inform measures to reduce costs associated with biological invasions. Costs are biassed towards high-income regions and damaging environmental impacts, particularly on islands. Most costs on islands result from actions to protect biodiversity and tend to be low and one-off (temporary). Most costs at mainland locations result from damage by a few, widespread species. Some of these costs are high and ongoing (permanent). Actions to restrict alien bird invasions at mainland locations might prevent high, ongoing costs. Reports increased sharply after 2010, but many are for local actions to manage expanding alien bird populations. However, the successful eradication of these increasingly widespread species will require a coordinated, international response.

Introduction

Species that have been introduced through human endeavour to regions that they would not normally inhabit are known inter alia as ‘alien’ species. Some of those species have damaging impacts on wildlife and people–they are further defined as ‘invasive alien’ species [1]. There are more than 400 alien bird species with self-sustaining populations worldwide [2], and some are considered invasive [3]. In recent years, research has improved our understanding of their impacts. Some studies have focussed on specific alien bird species (e.g., predation of native seabirds by the barn owl Tyto alba in Hawai’i [4]; hybridisation between the Chinese hwamei Garrulax canorus and the native Taiwan hwamei Garrulax taewanus in Taiwan [5]; and competition for nest-cavities between the rose-ringed parakeet Alexandrinus krameri and the native Eurasian nuthatch Sitta europaea in Belgium [6]). Other studies have reviewed or assessed the impacts of all alien bird species from an entire order of birds, such as alien Psittaciformes (parrots) in the USA and UK [7], Europe [8], and worldwide [9]. Another study has identified the negative impacts of alien birds caused by a specific type of impact (predation) on small islands [10]. Other studies have focussed on alien birds as an entire taxonomic class, including global reviews of their impacts [11–13], and assessments that have quantified and categorised their environmental and socio-economic impacts by their severity and type [14, 15], and that have identified factors that make native species vulnerable to these impacts [16].

This body of research shows that the impacts of alien birds are widespread and diverse, affecting biodiversity and people across the globe in many different ways. These impacts are often associated with economic costs, either directly due to the damage they cause, or indirectly due to expenditures associated with their management. For example, the Egyptian goose Alopochen aegyptiaca causes damage by grazing crops in the Netherlands [17], while management costs have been incurred when eradicating the common myna Acridotheres tristis from the Seychelles to mitigate its negative impacts on native wildlife [18].

Although cost estimates have been produced for some alien bird species, a global review of their reported economic costs has yet to be completed. Yet such a review could improve understanding of how and where alien birds generate economic costs, and how these costs vary in scale across regions, types of impacts, and species. This information could inform management interventions to reduce the financial burden placed on human societies by alien birds.

InvaCost is a living, publicly available database listing the reported costs of alien species worldwide [19]. It incorporates a methodology to standardise historical cost data in different currencies to current values in a single currency (US$ at the 2017 exchange rate). This enables meaningful comparisons of past and current costs incurred among different regions, and associated with different types of alien species and different types of impact. InvaCost has been used to assess the economic costs associated with several groups of alien species, including ants [20], bivalves [21], crustaceans [22], herpetofauna [23], terrestrial invertebrates [24], fish [25], and mammals [26]. These studies demonstrate that costs associated with alien species can be enormous (e.g., since 1930, the costs associated with the impacts of 12 alien ant species worldwide are > US$10 billion [20]; since the 1960s, costs associated with the impacts of alien mammals worldwide are > US$450 billion [26]) and that they also tend to be underreported [27, 28]. However, data contained within the InvaCost database have yet to be used to assess the costs of alien birds.

In this study, we synthesise data on the reported costs of alien birds across different regions of the world. Based on the results of previous studies, we pose several hypotheses. Because the costs of alien birds have been linked to both their environmental and socio-economic impacts, and these impacts have been reported from many regions of the world [13, 15], we hypothesise that data on costs will be widespread (hypothesis 1). Nevertheless, the costs of alien species tend to be underreported, particularly in low-income regions [29, 30], so costs will be unavailable for many regions (hypothesis 2). The environmental impacts of alien birds are sometimes managed (e.g., recent eradication of house sparrows Passer domesticus on Robinson Crusoe Island, Chile [31]), and some costs will therefore be associated with biodiversity conservation. However, alien-species research tends to focus on damaging environmental impacts [30], so more cost data will be available for damaging alien bird species because they are more likely to be managed (hypothesis 3). Nevertheless, the environmental impacts of some alien bird species are difficult to value economically, such as predation of a native bird species by an alien raptor (bird of prey), and some of these impacts have yet to be managed [10]. Therefore, data on costs will be unavailable for some regions where severe environmental impacts are reported (hypothesis 4). The reported management costs associated with the only other group of terrestrial vertebrate species assessed using InvaCost (mammals) tend to be much lower than their damage costs [26], and the same pattern is likely to be true for birds, particularly because many of their impacts are not managed (hypothesis 5). Many alien bird species are likely to have minor environmental [32, 33] and socio-economic impacts [15], and therefore their economic costs (which are associated with these impacts) will be low compared to many other taxonomic groups of alien species assessed using InvaCost (hypothesis 6).

Materials and methods

Data

We extracted data on the economic costs of alien birds from the InvaCost database [34], which contains > 13,000 records of economic costs associated with alien species that have been gathered through literature searches (see Diagne et al. 2020 [19] for a full description of the InvaCost database and associated methods). We reviewed the 389 entries relating to alien birds, removing 44 records considered unreliable due to a lack of information or discrepancies, and adding six new cost records identified since the publication of the latest version of the database. Thus, our review is based on 351 cost records. We used the expandYearlyCosts function of the invacost R package [35] to distribute cost records annually over their reported timeframe (e.g., a $60,000 cost incurred between 1999 and 2001 would be transformed to $20,000 for each of the three years during which costs were incurred).

InvaCost incorporates a set of descriptors that enable detailed analysis of costs associated with specific attributes of alien species. Using these descriptors, we collected data on: (i) the number of cost records/year, (ii) the reliability of cost records (‘low’ or ‘high’); (iii) the permanence of costs (one-off [temporary] or ongoing [permanent]); and (iv) whether costs were observed (realised) or potential (predicted). We then calculated costs for the following categories by summing costs associated with all records: (v) alien bird order, (vi) alien bird species, (vii) country of reported costs, (viii) type of incurred costs–‘management’ or ‘damage’ (two damage categories: agricultural damage or damage to other assets, including facilities/infrastructure/buildings) or ‘mixed’ if the data did not distinguish between management or damage costs, and (ix) year during which an impact caused costs (summing one-off costs for each year with ongoing costs from previous years).

Analysis

Most records in the InvaCost database described costs associated with a single alien bird species. However, a few cost records (< 3%) were associated with two or three species. In these cases when calculating costs for an alien bird species, we assigned each species the total cost for the record. This is because there was not enough information to assign proportionate costs accurately to each species. For example, these records included costs associated with the management of mixed flocks of Egyptian geese and Canada geese Branta canadensis. In other cases, several alien bird species were associated with a cost record, and they were not clearly named, being described as ‘exotic birds’ or ‘introduced birds’, for example. These costs were not assigned to specific species, but to a category titled ‘diverse/unspecified’.

Over half of all costs were caused by street pigeons Columba livia forma urbana. The impacts of this species are diverse and widespread, and associated costs are difficult to calculate accurately. We therefore assigned them a ‘low’ reliability and categorised them as ‘mixed’ costs (i.e., both damage and management costs), because accurate information on their nature was not available. Given their low reliability, we analysed cost data with and without costs for street pigeons.

Results

The total reported costs associated with the impacts of alien birds amounted to approximately US$3.6 billion (US$1.6 billion with costs for street pigeons excluded). Approximately 97% were observed costs, and 3% were potential costs (with street pigeon costs removed, 94% were observed and 6% potential). With costs for the street pigeon excluded (which had a ‘low’ reliability), most cost records were categorised as ‘high’ reliability (95%; n = 333).

Spatial distribution

Costs tended to be reported in high-income regions of the world, such as Australasia, Western Europe, and USA (Fig 1) (see S1 Fig for costs with street pigeons excluded). No cost data were available for many lower-income regions occupied by alien birds (e.g., India, and most of Africa, Southeast Asia, and South America). However, many reports were for costs incurred on islands, including those within low-income regions such as Socotra (Yemen).

Total costs incurred on islands were much lower than those incurred at mainland locations (even when excluding high costs for street pigeons at mainland locations) (Fig 2). Damage to facilities/infrastructure/buildings was reported at mainland locations, but not on islands; damage to agriculture was reported at both mainland and island locations (Fig 2). Management costs were also reported at both mainland and island locations. However, a higher proportion of total costs on islands (i.e., damage and management costs) were associated with management (53%) when compared with mainland locations (6.3% with costs for street pigeons excluded) (Fig 2). All management costs on islands were for schemes to control or eradicate alien birds, with the costs incurred by stakeholders and government agencies responsible for the protection of the environment.

Fig 2 — (a) total observed costs associated with alien birds incurred at mainland or island locations; (b) proportion of different types of observed costs incurred at mainland or island locations. Costs at mainland locations are shown with and without costs for street pigeons *Columba livia forma urbana*. ‘Mixed’ = combined ‘damage’ and ‘management’ costs (where information was insufficient to separate them). All costs for street pigeons were categorised as ‘mixed’. ‘Damage mixed’ = combined ‘damage to agriculture’, and ‘damage other’ costs (where information was insufficient to separate them).

Almost all potential costs were at mainland locations (Australia, Western Europe, and USA), with only one island potentially incurring costs (New Caledonia). These costs included agricultural damage by Canada geese and Egyptian geese in Europe, common starlings Sturnus vulgaris in Australia, and red-vented bulbuls Pycnonotus cafer in New Caledonia.

Taxonomic distribution

Reported costs were associated with 22 alien bird species from seven orders (approximately 5% of established alien bird species worldwide) (Fig 3). Columbiformes (pigeons and doves) were associated with approximately 55% of all costs; all were caused by street pigeons. Passeriformes (perching birds) were also associated with high costs, with most caused by common starlings (approximately 4% of all costs; 9% when street pigeon costs are excluded). Over one-third (38%) of observed costs were allocated to the ‘diverse/unspecified’ category; with costs for street pigeons removed this figure increased to 86%.

Temporal distribution

Although some cost records were from the last century, most (86%) were from 2000 to the present, with a sharp increase in records after 2010 (63% of reports were from 2010–2019) (Fig 4). However, total cumulative costs year^-1 have remained approximately stable over this period (approximately US$2.5 billion with costs for street pigeons; US$500 million without), and average cumulative costs year^-1 tend to be declining (Fig 4).

Fig 4 — (a) number of observed cost records year^-1 associated with alien birds; (b) total cumulative observed economic costs year^-1 (log_e) associated with alien birds (calculated by summing all one-off (temporary) costs for a year along with all ongoing (permanent) costs for that year and ongoing (permanent) costs for all previous years); (c) average cumulative observed economic costs year^-1 (log_e) associated with alien birds. Costs are shown (i) with and (ii) without costs for street pigeons.

Excluding costs for street pigeons (all of which are ongoing), approximately 64% of observed costs were one-off (temporary) costs. The remainder (36%) were ongoing (permanent) costs associated with damage and the management of alien birds where their complete removal is unlikely (Fig 5). With costs for the street pigeon included, ongoing (permanent) costs amounted to 70% of all costs (the remaining 30% being one-off (temporary) costs).

Fig 5 — ‘Mixed’ = combined ‘damage’ and ‘management’ costs (where information was insufficient to separate them). All costs for street pigeons were categorised as ‘mixed’.

Discussion

The distribution of data on the costs of alien birds is widespread and broadly congruent with the distribution of data describing their environmental and socio-economic impacts [15, 29] (hypothesis 1). More cost data are available in high-income regions of the world such as Australia, Western Europe, and USA (hypothesis 2), most likely because more research on the impacts of alien species tends to occur in these regions [29, 30, 36]. Cost data are unavailable for many low-income regions of the world, as is the case for other groups of alien species such as alien crayfish in Africa [22], alien fish in South America and Africa [25], and alien ants in Eastern Europe, Africa and Southeast Asia [20]. Yet, it is these regions where the impacts of alien bird species might be most problematic because they are more likely to reduce food security [37].

Most alien bird species do not have data describing their costs, and for some this might therefore be because they only occur as aliens in low-income countries, where their costs have not been reported (hypothesis 2). However, another possible explanation is that the environmental and socio-economic impacts of alien birds are often relatively minor [14, 15, 33], and invasion biology research tends to focus on the most damaging alien species [30]. For example, dunnocks Prunella modularis were introduced to New Zealand over 150 years ago, and this species is now common and widespread in southern regions [38]. However, it has been categorised as Data Deficient (DD) under the Environmental Impact Classification for Alien Taxa (EICAT) framework, because there are no data on its impacts from which to complete an EICAT assessment [14]. This suggests that the impacts of the dunnock in New Zealand are likely negligible. Therefore, alien bird species with no cost data could be those with minor impacts that do not warrant priority research to estimate their costs, which are probably low (hypothesis 6). This association between minor impacts and data deficiency for alien bird species has been inferred for their environmental impacts [32], socio-economic impacts [15], and monetary costs (using InvaCost) [39]. Thus, it is possible that a small proportion of established alien bird species have high economic costs. However, it is also possible that high costs are not reported, even in high-income regions. For example, in Europe, data on the costs associated with alien species are not always accessible [40]. Therefore, some alien bird species with no cost data could in fact have high costs.

Furthermore, the total economic costs of alien birds (US$3.6 billion), over half of which are caused by street pigeons alone, are low relative to costs associated with most other taxonomic groups assessed using InvaCost (hypothesis 6). They include terrestrial invertebrates (US$712 billion) [24] (including ants, which alone have costs of US$10.95 billion) [20], mammals (US$462 billion) [26], bivalves (US$63.7 billion) [21], fish (US$37.08 billion) [25], and herpetofauna (US$16.98 billion) [23]. This could be because certain ecological characteristics of birds make them easier to manage and their impacts less damaging. For example, birds are more conspicuous compared to some other taxonomic groups such as terrestrial invertebrates, and might therefore be easier to identify for management–multiple alien populations of African black sugar ants Lepisiota incisa are thought to have gone undetected in Australia for up to five years before their discovery in 2020, and extensive survey work has been necessary to establish their extent [41]. Furthermore, birds tend to occupy habitats above the ground or water level, unlike ants and crayfish, and they do not physically attach themselves to structures, unlike bivalves. Indeed, damage to drinking water, plant water intake infrastructure, and irrigation systems in North America due to fouling by alien bivalve species has cost at least $10 billion since 1980 [21]. Compared to other groups of alien species, birds might therefore be easier to contain, physically remove, and eradicate, despite being highly mobile. Birds also tend not to alter the structure of the environment profoundly, and therefore their impacts do not often require costly remediation, unlike ants [20] and bivalves [21]. Research to improve our understanding of why alien birds tend to have lower costs than many other alien taxa could inform measures to prevent high costs associated with future biological invasions.

Nevertheless, alien bird species can have severe environmental impacts that are difficult to monetise. Indeed, 58% of all alien bird species assessed as ‘harmful’ to biodiversity under the EICAT framework have no reported costs (hypothesis 4). They cause negative impacts through a range of mechanisms including competition, predation, hybridisation, brood parasitism, overgrazing of vegetation, and disease transmission (see S1 Table for details). An example of an alien bird species with severe biodiversity impacts and no cost data is the great horned owl Bubo virginianus. Through predation, this raptor has caused the decline of several native bird species and the extirpation of the Marquesas kingfisher Todiramphus godeffroyi [42] on Hiva Oa (French Polynesia). There are likely to be many intangible, non-monetisable environmental impacts associated with alien birds that adversely affect nature’s contribution to people [43].

Cost data are also congruent with environmental impact data because these costs and impacts are often linked. In these cases, costs are incurred when managing the environmental impacts of alien birds (mainly through their control or eradication). Indeed, approximately 60% of the alien bird species with costs also have environmental impacts defined as being ‘harmful’ under the EICAT framework [44] (Fig 3). The severity of these impacts is the trigger for their management, and hence costs (hypothesis 3). Because the environmental impacts of alien bird species tend to be more severe on islands [10, 45], many of these management costs are incurred on islands.

Nevertheless, management costs on islands are low relative to management costs at mainland locations. Even excluding the high costs associated with the street pigeon at mainland locations, average management costs/records at mainland locations are four times higher than those on islands (US$363,000 versus US$90,000, respectively). This might be because small populations of alien bird species have been eradicated on islands for a low cost (e.g., weka Gallirallus australis eradications on New Zealand’s offshore islands) [46] compared to costs for the ongoing management of large, widespread alien bird populations at mainland locations (e.g., house crows Corvus splendens in East Africa) [47].

Damage costs on islands are also lower than damage costs at mainland locations, perhaps because there are fewer opportunities for alien birds to cause specific types of damage. Indeed, there were no reports of costs associated with damage to facilities/infrastructure/buildings on islands, and a greater proportion of overall costs on islands were associated with management rather than damage when compared to mainland locations. However, although reported damage costs are relatively low on islands, they might be high relative to the income of local communities on those islands, particularly in low-income regions [48]. In these cases, agricultural damage could adversely affect human well-being by compromising food security [37].

The low costs incurred when eradicating populations of alien birds on islands are likely to be one-off costs (temporary), albeit with ongoing costs associated with any post-invasion monitoring. The high costs associated with damage at mainland locations are more likely to be ongoing, where some widespread species (e.g., common starlings) are difficult to remove completely. Indeed, the Western Australian Government has developed a long-term surveillance program to prevent the establishment of common starlings in the region [49], presumably recognising that the eradication of this species in Australia is unlikely. Because management costs to eradicate alien birds are typically lower than their damage costs (hypothesis 5), there could be economic benefits associated with early interventions to prevent the establishment of alien birds, particularly at mainland locations [50].

Alien birds are present on many islands around the world [10], where they can have damaging environmental impacts [45]. Costs associated with their management are likely to be incurred in the future, such as those required for the planned eradication of the Australian masked owl Tyto novaehollandiae from Lord Howe Island (Australia) [51]. Furthermore, although eradication costs tend to be one-off (temporary), they often require sustained effort, imposing a financial burden over several years. For example, the eradication of common mynas on Denis Island (Seychelles) took place in three phases over five years [52]. The eradication of house crows on Zanzibar has so far failed, in part due to a lack of funding for the length of time needed to eradicate this species [47].

A few cost reports are historical, such as damage to agriculture by the Eurasian blackbird Turdus merula in Tasmania during the first half of the last century [53], but most are from 2000 to present. The sharp increase in reports since 2010 might arise because some alien bird species (particularly monk parakeets Myiopsitta monachus and ring-necked parakeets Psittacula krameri) are rapidly becoming more widespread [54], and are being managed with local-scale actions. For example, between 2015 and 2018 there were 75 different cost reports for the management of monk parakeets at 34 different sites in Catalonia, Spain. These local-scale actions tend to have low costs (although they are annual, ongoing costs in Spain) perhaps explaining why total yearly costs for birds as an entire taxonomic group have not increased much over the same period, and why average costs are falling. While these local-scale actions might be effective in addressing local-scale impacts, the successful eradication of alien parrots in Europe will require a coordinated, international response [55, 56]. Another reason why total costs are not rising is that some costly management actions to eradicate widespread species perceived to have the most damaging impacts have now been completed, such as the eradication of African sacred ibises Threskiornis aethiopicus in Europe [57].

Over half of all costs were for street pigeons. They damage buildings with corrosive droppings [58], cause flooding by blocking gutters with droppings and feathers [59], and cover structures with droppings. Maintenance to manage their impacts can be costly; the removal of 350 tonnes of droppings from a bridge in Canada cost US$640,000 [60]. Street pigeons also consume and spoil agricultural produce with droppings [61], and their presence at airports, where they are a risk to airline safety, requires costly exclusion and monitoring activities [62]. This human-commensal species thrives in many cities, and accurately calculating its global costs is challenging because many of its impacts are not reported, such as damage to residential dwellings. In addition, these reported costs are likely to be underestimated given that they have been calculated for only three countries (Canada, UK, and USA).

The higher costs caused by perching birds (Passeriformes) tend to result from agricultural damage. On Zanzibar Island (Tanzania), house crows consume crops, hinder aquaculture operations by stealing bait and pulling bungs out of boats, and attack and kill poultry and young livestock [63]. They also aggressively compete with, and prey on native bird species [64]. Unsuccessful attempts to eradicate the large population of house crows on Zanzibar (> 1 million individuals) [47] have so far cost > US$1.5 million [65]. However, a population of around 50,000 individuals was successfully eradicated in Singapore, costing US$765,000 [66], and a smaller population of 30 individuals was successfully eradicated from the island of Socotra (Yemen), costing US$20,500 [67].

Four waterfowl species (Anseriformes) have reported costs. However, most costs are associated with the control of ruddy ducks Oxyura jamaicensis in Western Europe to prevent hybridisation with native white-headed ducks Oxyura leucocephala [68]. The alien population of ruddy ducks was large and distributed across several countries; the ongoing control program has taken several years, and so far cost > US$28 million. Expensive control of large house crow and ruddy duck populations demonstrates that timely interventions to control alien bird populations at early stages of invasions (when they are relatively small) can prevent spiralling management costs [39, 69].

Two parrot species (Psittaciformes) with the largest alien ranges of all parrot species have reported costs: monk parakeets and rose-ringed parakeets. Introduced to many regions of the world [70, 71], their broad alien distribution provides these species with greater opportunity to cause negative impacts when compared to alien parrot species with smaller ranges [33, 39]. Monk parakeets nest on electrical structures causing power outages [72]. They are an agricultural pest in their native range and are predicted to become a serious pest to agriculture in the Mediterranean if their population continues to grow [73]. They are also a nest-site facilitator, hosting other species of birds (both native and alien) [74, 75]. Rose-ringed parakeets damage agriculture, including almond orchards in Rome [76] (they are also an agricultural pest in their native range) [77], and they compete with native species for nest sites, which has caused declines in populations of Eurasian nuthatches in Belgium [6] and a threatened bat (greater noctule Nyctalus lasiopterus) in Spain [78]. In the UK, the rose-ringed parakeet population is increasing in abundance and range [71, 79], as are populations of this species and monk parakeets in Spain [54]. It is likely that costs associated with damage caused by these species and any future actions to manage their impacts are also increasing [69].

Costs have been reported for two landfowl species (Galliformes)—agricultural damage by common pheasants Phasianus colchicus in Germany [80] and management costs on Santa Cruz Island (USA) incurred to eradicate wild turkeys Meleagris gallopavo due to their negative impacts on biodiversity [81]. Such impacts have also been the catalyst for the eradication of African sacred ibises (Pelecaniformes) in mainland France [57] and weka (Gruiformes) on many of New Zealand’s offshore islands [46].

Many costs assigned to the ‘diverse/unspecified’ category have been incurred in Australia and are associated with agricultural damage, particularly by frugivorous perching birds that consume soft fruit [82], including common starlings, Eurasian blackbirds, common mynas, and house sparrows [83]. Costs assigned to these species are likely to be higher than reported [84]. Other alien bird species with reported environmental and socio-economic impacts [14, 15] do not have reported costs (e.g., rooks Corvus frugilegus in New Zealand), which also suggests that costs associated with alien birds are underreported. Furthermore, costs incurred to control and eradicate alien birds are often not published, including costs for the eradication of house sparrows in Mauritius [85] and street pigeons in the Galapagos [86].

Conclusions

Our review reveals that the economic costs of alien birds are widespread, but also underreported. Just 5% of established alien bird species have data describing their economic costs, and there are regions of the world occupied by many alien bird species where no costs were identified. However, it is likely that many species with no cost data have low, or no, economic costs. Indeed, the characteristics of alien birds and the nature of their impacts is most likely why their costs are lower than other taxonomic groups so far assessed using InvaCost. Nevertheless, some damaging impacts caused by alien birds, such as native species extirpations on islands, are difficult to monetise. Furthermore, some increasingly widespread alien bird species do have high costs (and damaging biodiversity impacts). Their eradication will require a coordinated, international response, but they are being managed with local-scale actions. Further research to understand why the impacts of alien birds tend to be less costly than those caused by other taxonomic groups of alien species could inform measures to reduce the costs associated with biological invasions. Indeed, our study demonstrates that we have much to learn about the economic costs of alien birds. Avenues for future research could include identifying characteristics of alien bird species that cause them to have high economic costs, and factors that cause variation in the distribution of costs across different regions. This research could help to predict the types of species that have the most damaging economic impacts, which could inform biosecurity measures to prevent their introduction as aliens.

Supporting information

S1 Fig. The spatial distribution of the observed economic costs associated with alien birds, with costs for street pigeons excluded (US$, 2017 exchange rate).

k = thousand; m = million; bn = billion. D_ag = costs associated with damage to agriculture; D_fa = costs associated with damage to facilities/infrastructure/buildings; M = cost associated with management. This map was made with Natural Earth. Free vector and raster map data @ naturalearthdata.com.

(DOCX)

Click here for additional data file.^{(785.4KB, docx)}

S1 Table. Alien bird species with no data on economic costs that have been assessed as having ‘harmful’ environmental impacts under the Environmental Impact Classification for Alien Taxa (EICAT) framework (Blackburn et al. 2014).

(DOCX)

Click here for additional data file.^{(22KB, docx)}

Data Availability

All relevant data are within the paper and its Supporting Information files, or freely available from DOI: https://doi.org/10.6084/m9.figshare.12668570.v5.

Funding Statement

Our work was supported by the French National Research Agency [ANR-18-EBI4-0004-07, 2018]; the BNP-Paribas Foundation Climate Initiative [2014-00000004292, 2014]; the AXA Research Fund Chair of Invasion Biology [2019]; and the AlienScenario project funded by BiodivERsA and Belmont-Forum call 2018 on biodiversity scenarios [I 4011-B32, 2018]. Our funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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PLoS One. doi: 10.1371/journal.pone.0292854.r001

Decision Letter 0

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26 Jun 2023

PONE-D-23-06753Global economic costs of alien birdsPLOS ONE

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Reviewer #1: In general, the introduction shows too much very specific (often local) examples and too few general assumptions in my opinion. Please increase literature search, avoid describing specific examples and increase the number of cited works (for instance, take a look at alien parakeets in Europe).

Still I am confused: does InvaCOst include also data on alien birds or, as you said at lines 75-76, alien birds are still excluded? If so, I do not understand the novelty of this work. If not, I do not understand how did you get your data. This is an important issue to be clarified, before I can provide reliable comments on the rest of the MS.

Furthermore, I would like to suggest authors to discuss more about Figure 1, as in Europe several countries are not controlling alien birds, but they are spending for their damages, and these costs are not quantified.

Lines 17-18. Do you refer to worldwide costs? Please clarify.

Keywords. You never mentioned Columba livia as an invasive species in the abstract. Please clarify or try to find different keywords.

Lines 42-43. This is a very specific example. It could be ok, but you have to look at different examples also, as being in the introductive part.

Line 46. Please, change “demonstrates” with “shows”. You have no experiment in your manuscript.

Figure 2. Please, scientific names should be in italics.

Reviewer #2: The paper examines the distribution of economic costs from alien birds over space, time and species. This may help understand the reason for the cost and may help to reduce economics costs of biological invasions.

The data size is however limited with only 351 cost records (333 costs with high reliability) spanning from 1940 -2020. Data for costs from are unavailable for some species and regions. There are also not statistical tests of the hypotheses (some due to lack of data). The data analysis of the cost distribution and underlying mechanism is mainly descriptive. Here are some suggestions to improve the paper:

1 In the regions with reported data, it will be helpful to run a set of regression analysis to see how regions, species, taxonomic groups, impact type (environmental impact data from Reference 20 ), or year fixed effect can explain the variation of the economic costs. This provides stronger tests of the 6 hypotheses.

2 Find some proxy of the economic cost especially in the unreported regions. The paper states that economics costs are likely to be underreported because.:

1) Due to budget constraints, there is no monitoring/research in some regions, particularly low-income regions.

2) Within the reported regions, only costs associated with the most damaging species are reported. The other species may lead to relatively low costs.

It may be possible to use the data from the reported region to infer information about economic costs in the unreported regions. For example, if we know the reason for the invasive species and if one species appears in both reported region(s) and unreported region, can we assume the economics costs in the unreported region is proportional to the economics costs in the reported regions? The proportion can be a function of regional GDP, year, etc.

3The paper also states that some impacts are hard to monetize. So, no cost data even when the environmental impact is reported high.

It can also be helpful to construct a model to predict economic cost based on environmental and social impacts and regional characteristics. It would be interesting to explain the gap between the predicted economic cost and reported cost.

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

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Reviewer #1: Yes: Emiliano Mori

Reviewer #2: No

**********

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PLoS One. 2023 Oct 18;18(10):e0292854. doi: 10.1371/journal.pone.0292854.r002

Author response to Decision Letter 0

12 Jul 2023

We thank both reviewers for their helpful comments, to which we have responded in the attached 'response to comments' document. Our responses are highlighted in blue text. We have highlighted changes to the revised manuscript in yellow, and provided line number references in our responses.

We hope that our manuscript is now suitable for publication.

Best regards

Thomas Evans

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PLoS One. doi: 10.1371/journal.pone.0292854.r003

Decision Letter 1

Mirko Di Febbraro

31 Jul 2023

PONE-D-23-06753R1Global economic costs of alien birdsPLOS ONE

Dear Dr. Evans,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. One of the two reviewers still requires important amendments to reach the manuscript full potential. Specifically, a more robust support to some of the study hypotheses is requested.

Please submit your revised manuscript by Sep 14 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

We look forward to receiving your revised manuscript.

Kind regards,

Mirko Di Febbraro

Academic Editor

PLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #1: Yes

Reviewer #2: Partly

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: No

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Reviewer #1: Authors addressed all of my previous comments. Therefore, the MS can be accepted for publication.

All the best.

Reviewer #2: The paper investigates the distribution of economic costs arising from alien birds, focusing on spatial, temporal, and species variations. The primary approach involves a descriptive analysis of the cost distribution and underlying mechanisms. While the research provides valuable insights, there are some aspects that require clarification and additional support to strengthen the overall findings.

1 Support for Hypothesis 3 (more cost data are available for damaging alien bird species because they are more likely to be managed.)

While the paper mentions that 60% of alien bird species with costs have harmful environmental impacts, it would be more informative to provide a summary of the percentage of each environmental impact category under the Environmental Impact Classification for Alien Taxa (EICAT) framework) to understand the severity of their effects accurately.

2 Support for Hypothesis 4 (data on costs will be unavailable for some regions where severe environmental impacts are reported as environmental impacts are hard to monetize.)

The evidence supporting Hypothesis 4, which suggests that data on costs may be unavailable in regions with severe environmental impacts, lacks substantial support from the data. Calculating the percentage of alien bird species with damaging costs among those with "harmful" or higher impacts would offer more compelling evidence for this hypothesis.

3 Conflicting Evidence for Hypothesis 5

The paper introduces Hypothesis 5, stating that management costs for eradicating alien birds are typically low compared to their damage costs. However, there is conflicting evidence presented in the figures (Figure S4 and Figure S2). In Figure S4, damage cost dominates management costs (with and without street pigeons). But in Figure S2, you have higher percentage of management costs than damage costs when street pigeons are included. Moreover, it would be helpful if you refer to the figure that support your hypothesis.

4 Statement in the abstract and Support for Hypothesis 6.

In the Abstract (Line 24), the paper states that "Research to understand why (alien birds tend to have lower costs than many other alien taxa (Hypothesis 6)) may inform measures to reduce costs associated with biological invasions".

With limited and potentially underreported data, it is hard to justify hypothesis 6. Moreover, the paper discusses the two following reasons of why alien birds have lower costs than the other taxa, but there is no concrete evidence to support these mechanisms:

a). Lower costs for alien birds may come from underestimation:

The paper acknowledges that costs for alien birds may be underestimated due to underreported environmental costs that are challenging to monetize. Additionally, minor environmental and socio-economic impacts of alien birds have led to limited research. These points provide valuable insights into potential reasons for the lower perceived costs of alien birds. However, it would be beneficial to include specific examples or case studies to illustrate the extent of underestimation and its impact on cost assessments.

b). Mechanisms for Lower Costs in Alien Birds than other taxa:

The paper suggests possible mechanisms that could explain why alien birds tend to have lower costs compared to other taxa, such as their habitat preference (above ground or water level). Nevertheless, the paper lacks concrete evidence to support these mechanisms. For example, there is no information provided to demonstrate whether the environmental impacts of alien birds are indeed smaller than those of ants and crayfish. Low environmental costs of alien birds might lead to low costs. However, together with costs underestimation, high environmental impacts of alien birds may end up with lower costs reflected by data. Including empirical data or relevant studies to validate these hypotheses would strengthen the paper's argument.

5 Is Inva cost the only dataset that provides global information about cost of alien birds? Is there any other dataset available even locally? Other relevant data will be able to support the arguments.

Overall, the paper provides valuable insights into the distribution of economic costs associated with alien birds, considering spatial, temporal, and species-related variations. However, the descriptive nature of the data analysis limits the paper's ability to draw robust conclusions. By incorporating specific examples, empirical data, and further support for the hypothesis and proposed mechanisms, the authors can enhance the paper's impact and provide more practical implications for managing biological invasions linked to alien bird species.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Emiliano Mori

Reviewer #2: No

**********

PLoS One. 2023 Oct 18;18(10):e0292854. doi: 10.1371/journal.pone.0292854.r004

Author response to Decision Letter 1

24 Aug 2023

Thank you very much for the additional comments on our manuscript. We have prepared a 'response to comments' document, providing a detailed response to each of these comments. We hope that our manuscript is now acceptable for publication.

Attachment

Submitted filename: ResponseToComments240823.docx

Click here for additional data file.^{(23.1KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0292854.r005

Decision Letter 2

Mirko Di Febbraro

15 Sep 2023

PONE-D-23-06753R2Global economic costs of alien birdsPLOS ONE

Dear Dr. Evans,

Some minor amendments are still required by the referee before accepting the manuscript for publication.

Please submit your revised manuscript by Oct 30 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

We look forward to receiving your revised manuscript.

Kind regards,

Mirko Di Febbraro

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #2: (No Response)

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: (No Response)

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #2: Yes

**********

6. Review Comments to the Author

Reviewer #2: Thank you for addressing my comments. I only have 1 question now.

1 Reliability of Street Pigeon Cost Data:

1) Dataset Information (lines 136-137):

The dataset offers descriptions of the reliability for cost records, categorizing them as 'low' or 'high'.

2) Reference from lines 172-173:

A significant portion (95%) of the cost records (n=333) are marked as 'high' reliability. It's unclear if this percentage includes the costs associated with street pigeons.

3) Reference from lines 163-164:

The costs related to street pigeons have been designated a 'low' reliability and are categorized under 'mixed' costs.

Concerns:

There is ambiguity about the reliability classification for street pigeon costs in the dataset, especially since they constitute over half of all costs (US $2 billion out of US $3.6 billion from reference line 169-171).

If the dataset classifies street pigeon costs as 'high reliability' but they are later marked as 'low', this discrepancy could affect the reliability of the overall cost data (US$3.6 billion). This is particularly important considering:

a) Street pigeons contribute to 50% of the total costs (US $2 billion).

b) The validity of the 'high' reliability label for other birds might be brought into question.

Recommendations:

Kindly provide clarity on the reliability rating assigned to street pigeon costs in the dataset.

It would also be beneficial to include an explanatory note for the "mixed" category (representing both management and damage) in relevant figures or tables.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #2: No

**********

PLoS One. 2023 Oct 18;18(10):e0292854. doi: 10.1371/journal.pone.0292854.r006

Author response to Decision Letter 2

21 Sep 2023

Thank you for raising this additional point, which we have addressed in the attached 'response to comments' document. We appreciate your input, and we hope our manuscript is now suitable for publication.

Best regards

Thomas Evans

Attachment

Submitted filename: Response_to_comments200923.docx

Click here for additional data file.^{(18.4KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0292854.r007

Decision Letter 3

Mirko Di Febbraro

2 Oct 2023

Global economic costs of alien birds

PONE-D-23-06753R3

Dear Dr. Evans,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Mirko Di Febbraro

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

PLoS One. doi: 10.1371/journal.pone.0292854.r008

Acceptance letter

Mirko Di Febbraro

9 Oct 2023

PONE-D-23-06753R3

Global economic costs of alien birds

Dear Dr. Evans:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Mirko Di Febbraro

Academic Editor

PLOS ONE

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Fig. The spatial distribution of the observed economic costs associated with alien birds, with costs for street pigeons excluded (US$, 2017 exchange rate).

(DOCX)

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(DOCX)

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Submitted filename: ResponseToComments240823.docx

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Data Availability Statement

All relevant data are within the paper and its Supporting Information files, or freely available from DOI: https://doi.org/10.6084/m9.figshare.12668570.v5.

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PERMALINK

Global economic costs of alien birds

Thomas Evans

Elena Angulo

Corey J A Bradshaw

Anna Turbelin

Franck Courchamp

Roles

Abstract

Introduction

Materials and methods

Data

Analysis

Results

Spatial distribution

Fig 1. The spatial distribution of the observed economic costs associated with alien birds (US$, 2017 exchange rate).

Fig 2.

Taxonomic distribution

Fig 3. The observed economic costs (loge) associated with 7 bird orders, 22 alien bird species and *diverse/unspecified species.

Temporal distribution

Fig 4.

Fig 5. The proportion of observed costs associated with alien birds that are one-off (temporary) or ongoing (permanent) (with and without costs for street pigeons Columba livia forma urbana).

Discussion

Conclusions

Supporting information

Data Availability

Funding Statement

References

Decision Letter 0

Mirko Di Febbraro

Roles

Author response to Decision Letter 0

Decision Letter 1

Mirko Di Febbraro

Roles

Author response to Decision Letter 1

Decision Letter 2

Mirko Di Febbraro

Roles

Author response to Decision Letter 2

Decision Letter 3

Mirko Di Febbraro

Roles

Acceptance letter

Mirko Di Febbraro

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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Cited by other articles

Links to NCBI Databases

Fig 3. The observed economic costs (log_e) associated with 7 bird orders, 22 alien bird species and *diverse/unspecified species.