The introduction of nonnative species can have severe consequences for native species and ecosystems (Carlsson et al. 2009, Vilà et al. 2011). As a result, the Convention on Biodiversity exhorted the contracting parties “to prevent the introduction, control or eradicate those alien species which threaten ecosystems, habitat or species.” Managers of eradication programs must consider, however, that invasive species have far-reaching effects throughout the entire ecosystem, which may cause a control program to result in unintended negative outcomes for native species (Tablado et al. 2010). To address the Convention's aims appropriately and effectively, knowledge of the full effects of introduced species over a wide range of ecosystems and species is required.

The study of biological invasions is rather a new discipline and is growing rapidly on some continents (Pyšek et al. 2008, Speziale et al. 2012). Studies show that nonnative species introductions may produce varying effects on native biotas (Gurevitch and Padilla 2004, Rodriguez 2006, Vilà et al. 2011). However, the analysis of the relationships between introduced species and certain taxa, including raptors, are poorly studied. A review of existing literature to find knowledge gaps may be helpful in guiding future research of the effects of this threat to biodiversity, particularly for raptors.

Raptors can directly promote high biodiversity through resource facilitation (i.e., food resources that are made available by raptors) and through trophic cascades by exerting top-down forces (Estes et al. 2001, Soulé et al. 2005, Sergio et al. 2007, 2008). They may also act as biodiversity indicators by being spatiotemporally associated with biodiversity (Sergio et al. 2008). As top predators and rare species, raptors can be threatened by species population changes at lower trophic levels (Begon et al. 2006, Wilson and Wolkovich 2011). Thus, it is important to monitor the effects of alien species on these top predators. The net effect of introduced species will depend on their capacity to modify the ecosystems and produce cascading effects (Crooks 2002). The goals of our study were (a) to analyze whether the volume of research on the relationship between raptors and exotic species follows the trend of the study of introduced species in general, and (b) to evaluate the effects of nonnative species on raptors by reviewing existing published studies.

Materials and Methods

We used the ISI Web of Knowledge engine to search for articles on biological invasions as related to raptor species. We first performed two separate searches to compare the trend of biological invasions science and raptor science over time. For that we searched title, abstract, and key words for the terms (inva* OR introduced OR alien OR exotic OR nonnative OR nonindigenous) in one search and for (condor OR raptor OR vulture) separately. Then we searched for published articles relating raptors and introduced species by using the following criteria: “(raptor OR vulture OR condor) AND (inva* OR introduced OR alien OR exotic OR nonnative OR nonindigenous).” We refined each search to identify only articles published in journals related to biological or environmental sciences. We performed the search in May 2012 and included articles published up to and including December 2011. We calculated the rate of publication of articles relating raptors and introduced species in respect to total publications in raptor science as a measure of the interest in the effect of nonnative species (hereafter the “exotics in raptor science index”). We conducted an analysis of covariance (ANCOVA) to compare the former rate of publication to the general interest in introduced species over the last 20 yr with the year as a covariate. For that we also calculated the ratio between publications in nonnative species (see criteria above) and the total publication in biological or environmental sciences as a measure of the interest in the study of introduced species in general (by searching the ISI Web of Science the word “species” and refining the search to identify only articles published in journals related to biological or environmental sciences (hereafter the “exotics in general science index”).

We then analyzed each article looking for information on the effects of the introduced species on raptor species to disentangle whether the overall described impact was positive, negative, or neutral. We defined a positive impact when the introduced species possibly favors raptors based on the information provided by the study (e.g., expanded distribution, increased nesting locations, increased food supply, or greater reproductive success). We considered an effect as negative when an introduced species directly or indirectly damages raptors in any way (e.g., via reduced prey availability, direct or indirect poisoning, etc.). We classified effects of introduced species as neutral when we could not classify them as either positive or negative for raptor species, according to the data provided by the study or if this information was ambiguous. We also analyzed trophic relationships affecting raptors, distinguishing between introduced primary producers (as habitat-modifiers), consumers (as prey for raptors and scavengers), top predators, and pathogens.

Results

The volume of both biological invasion research (Fig. 1A) and raptor research has increased greatly in the last 20 yr (Fig. 1B). However, although research analyzing the relationship between introduced species and raptors has increased, this increase was more moderate (Fig. 1C). Part of this trend may be related to the growth of raptor science per se, but it apparently does not reflect the great interest in biological invasions. We found that the interest in studying the effect of introduced species is much higher in general sciences than in raptor science: ANCOVA comparing publications on the effects of introduced species in raptor science (studies on introduced species and raptors over studies on only raptors) with that of general sciences (studies on introduced species within biological or environmental sciences over biological or environmental sciences studies in general) between 1991 and 2011 with the year as a covariate (F_1,39  =  1468.4; P < 0.001; Fig. 2).

Figure 1

Trends of papers yielded by ISI Web of Science searches (see Methods for details) published on: (A) introduced species studies; (B) raptors studies; and (C) raptors in relation to introduced species. Notice the differences in y-axis scale among graphs.

Figure 2

Differences in the interest in publishing the effects of introduced species in raptors science (Exotics in raptors science index) with that of general sciences (Exotics in general science index). Vertical bars denote standard errors. See Methods for more details.

Our systematic search yielded a total of 97 articles that include in the same article one or more raptor species and one or more introduced species. After reviewing each one, we found that only 32% (31 articles) actually analyzed the relationship between raptors and nonnative species. We did not include those articles analyzing the effects of native species extending their distributions and thus considered newly arrived in a raptor ecosystem (e.g., Gutiérrez et al. 2006, Carrete et al. 2010), because in many cases it is not clear if it is a natural or human-mediated expansion. We included a total of 31 articles in our analyses. Of these 31 articles, only about 32% (10) had a clear a priori aim of studying nonnative species. We found studies of raptors and nonnative species on every continent (except for Antarctica; Fig. 3). Although the number of articles found for each continent was low, the effect of the introduced species on raptors appears to be widely distributed (Fig. 3). The analysis of the 31 articles showed that the outcome of nonnative species introductions could either be positive, negative, or neutral. In total, articles on the negative effects outnumbered articles on positive ones (16 to 11, respectively). Considering trophic relationships, based on the articles analyzed, producers modified raptors' habitats, generating indirect effects (Fig. 4). Introduced consumers (prey for raptors) and pathogens directly affect raptors, whereas introduced predators do so indirectly by competing for the same prey (Fig. 4). We found predators and pathogens only exerted negative effects (or neutral in one case), whereas the effect of producers and prey were both negative and positive (Fig. 4; Table 1).

Figure 3

Geographical distribution of the number of papers relating raptors with introduced species in each continent based on a search of articles in the ISI Web of Science (see Methods for details).

Figure 4

Different positive (+) and negative (−) biotic interactions among introduced species and raptors found in a bibliographic search. See Table 1 for further details.

Table 1

Results of the search of peer-reviewed studies in the ISI Web of Knowledge summarizing the aims of the study and effects of introduced species on raptors. The sign or letter within brackets indicates whether the effect is considered as positive (+), negative (−) or neutral (N) (see Methods for definitions).

Table 1

Continued.

Table 1

Continued.

Table 1

Continued.

Introduced primary producers causing habitat-modification effects on raptors were the focus of 39% (12/31) of the selected 31 articles, either by providing nest sites or by allowing the species to extend their distributions. Of these articles, 33% (4 of 12) indicated that raptors species were able to extend their distributions due to the new habitat conditions (e.g., finding new places to nest or perch, to rest or hunt; Table 1). Half of the studies (6 of 12) showed negative impacts of plantations or even-aged monotypic stands of introduced species (Table 1). These studies showed increased nest failures, reduced productivity, or even nest abandonment, arguing that it could be due to reduced prey availability in the new habitats. Two of these articles also reported a neutral impact. We also found two studies showing both positive (expanded distribution and use of human-modified land) and negative (changed roosting behavior and exotic plantations devoid of birds) effects at the same time (Table 1).

Introduced prey as part of raptors' diet was studied in 48% out of the 31 articles analyzed. Articles showing that raptor species feed on nonnative species, which may be considered as a positive outcome for raptors, made up almost half of diet studies (7 of 15; Table 1). The same proportion of studies (7 of 15) showed negative effects. Several of these latter ones (4 of 7) analyzed the effects of poison used to control introduced species, indirectly affecting raptors that fed on this prey. Another two studies evaluated lead poisoning in raptors caused by the consumption of introduced species contaminated or hunted with lead ammunition. Another article indicated the mortal effect of an antiinflammatory drug (diclofenac) used for cattle treatment (Table 1). Neutral effects were considered by three studies (two of which also showed a positive and a negative impact each and were considered above), indicating either that introduced species were minor parts of the raptors' diet or that a change in migration patterns was produced (Table 1).

The remaining articles (13% or 4 articles) of the 31 studies dealt with topics unrelated to introduced prey or to habitat modification. All but one showed negative effects on raptors (Table 1). These included competition with nonnative species (mammalian), and susceptibility to exotic pathogens. Only one of these articles reported a neutral effect.

Discussion

The study of nonnative species has become increasingly popular in recent years (Pyšek et al. 2008, Speziale et al. 2012). Similarly, there has been increased interest in the study of raptors. However, such an increase has not been seen in the study of raptors relative to introduced species and their effects. Any literature search can suffer from biases related to the databases or keywords used. It is likely, however, that any source of bias would only minimally affect the general patterns in publication efforts, and thus our general conclusions on the effects of nonnative species on raptors. Our results suggest that ecologists studying this group of species may not yet be highly concerned with the effect of one of the most important threats to wildlife: the introduction of nonnative species (Sala et al. 2000, Pereira et al. 2010). One fact that may be influencing this result is that raptors themselves do not commonly become invasive species.

We found that raptors are affected by nonnative species within their natural distribution areas, both negatively and positively, and that articles showing negative effects outnumbered articles showing positive ones. Regarding the latter, studies show that raptors can strongly rely on introduced species as a food source or for providing nesting habitat (Sarasola and Negro 2006, Gangoso et al. 2006, Lambertucci et al. 2009, Tablado et al. 2010). As introduced prey become abundant, the probability of a native predator using that prey also increases (Rodriguez 2006). Many native predators adapt to feeding on introduced prey, which can become an important part of their diet and some species can obtain a fitness advantage over species that do not adapt to utilizing the prey (Carlsson et al. 2009). This can lead to a high dependence on introduced species and therefore any change in their availability may have direct or indirect impacts on raptors. This can be a particularly critical factor when native resources decrease due to human intervention (Pavez et al. 2010, Akatani et al. 2011, Lambertucci and Speziale 2011). Some threatened raptor populations are in fact maintained by feeding on exotic resources (Chamberlain et al. 2005, Gangoso et al. 2006, Lambertucci et al. 2009).

Introduced primary producers also exert positive effects. Raptors take advantage of the availability of certain introduced trees, particularly when native vegetation is cut down or new plantations modify the habitat (Sarasola and Negro 2006, Akatani et al. 2011). Most studies that report species using novel habitats created by primary producers (sensu Hobbs et al. 2006; e.g., introduced species plantations) are not exhaustive and have not studied other fitness indicators such as breeding success or nestling survival, as the effects of introduced species were non-expected results (Wilson et al. 2009). Thus, the question remains as to whether the identified positive outcomes were truly positive.

Negative effects exerted by nonnative species ranged from poisoning and pathogen susceptibility to habitat loss and diminished native prey. Particularly important are the consequences of habitat modification by introduced primary producers, which structure the ecosystems in such a way to directly or indirectly provoke an array of negative effects. For example, the new habitat could be considered a sink for the newly arrived raptor species if the shift toward introduced species is detrimental for certain age classes (Cattau et al. 2010). Nonnative species plantations also provoke other negative effects such as nest failure or territory abandonment, and some may not be used by birds at all (Petit et al. 1999, Whitfield et al. 2007, Seaton et al. 2009).

Similarly, introduced prey species can have positive or negative effects on native raptors. Despite the fact that introduced prey increases the available food source for raptors, they can also provoke important negative effects. Fitness indicators for raptors feeding on the introduced apple snail (Pomacea insularum) in the U.S.A. showed that when raptors fed on this introduced prey, juveniles obtained a lower energetic reward than when feeding on native species, thus depressing juvenile survival (Cattau et al. 2010). Other studies have reported that raptors and scavengers can be indirectly affected when feeding in productive systems and that they can be negatively affected by drugs such as diclofenac, used to treat cattle (Naidoo et al. 2009). They can also die through poisoning by feeding on introduced prey, which has either been poisoned to reduce their threat to productive ecosystems, or poisons the raptor through ingestion of lead ammunition used during hunting of the introduced prey species (Eason et al. 2002, Church et al. 2006, Elliott et al. 2008, Lambertucci et al. 2011).

Conclusions

Several studies report some positive effects of nonnative species on raptors, particularly by providing bottom-up benefits (e.g., food). However, introduced species may also exert negative bottom-up effects (e.g., reduced juvenile survival or nesting failure) and we found that it is the negative effects that are more common and varied throughout the analyzed literature. These two contrasting results merit special attention. Control of or eradication actions for introduced species are often advised, particularly when negative effects of their presence have been recorded. However, the role that nonnative species play in the new ecosystem should be identified before programs are outlined. If raptors (or other native species) depend heavily on the introduced species, then target actions should focus first on how to overcome the problem of eradicating the nonnative species without affecting the species that depend on them (Lambertucci et al. 2009, Akatani et al. 2011). For introduced prey species, alternative native prey must be favored before the introduced one is eradiated. Similarly, considering raptors that rely on primary producers mostly for nesting, it is advisable to provide nesting structures or to recover native vegetation when eradicating introduced trees.

Raptors and scavengers perform a variety of keystone ecological services, such as disposing of carcasses, control of rodent populations and other top-down regulations (Sekercioglu et al. 2004, Sekercioglu 2006, Markandya et al. 2008, Newton 2010, Wilson and Wolkovich 2011), which can be affected by introduced species. Primarily it is important to design specific studies to analyze how nonnative species affect the roles raptors perform on ecosystems. It might be valuable to analyze the fitness and the viability of populations that have taken advantage of this novel (introduced) resource to test whether it really favors raptors. It is also important to analyze the role of introduced species in disturbing the native habitat, prey availability or the interactions within ecosystems. Study of the implications of nonnative species for this key group of top predators and scavengers is currently poorly considered and merits special attention and specific design in future studies.