Human society is changing the world at an alarming rate. Overpopulation, globalization, and climate change have led to unprecedented levels of habitat transformation resulting in negative effects on species, populations, and entire ecosystems. Consequently, many species living in altered environments either need to rapidly adapt or potentially face local extirpation (WWF, 2018). Conversely, some organisms may benefit from anthropogenic environments and human activity. For example, some species can take advantage of the existing vast global transport networks and use it to hitchhike and colonize new locations and thereby expand their range (Chapple et al., 2012; Lockwood et al., 2013; Lewis et al., 2016). This invasion process is complex, and encompasses multiple stages. Each stage poses a different set of obstacles that animals need to overcome in order to become invasive (Blackburn et al., 2011). A species that fails at any stage of the process will thus not become invasive (Figure 1). Nevertheless, biological invasions have been steadily increasing in the last century (Essl et al., 2011; Lewis et al., 2016), and therefore, understanding why some species are successful invaders is of great interest.

Whether an organism needs to adapt to changes in their current environment, or whether they are introduced into a completely novel environment, they need to be able to adapt or change their behavior quickly in order to survive (Tuomainen and Candolin, 2011). While selection may favor particular phenotypes and behavioral types, the degree to which an organism can plasticly adjust behavior (behavioral plasticity) may also be crucial in determining the outcome of an invasion (Chapple et al., 2012; Griffin et al., 2016). In addition to behavioral plasticity, cognitive ability can plausibly give some species an advantage in the invasion process because an ability to use resources and to learn and retain the location of resources and threats should be adaptive in novel environments (Shettleworth, 2001, 2010). It is thus not surprising that cognitive ability is increasingly being recognized for the potentially important role it may play in selection affecting fitness (Cole et al., 2012; Thornton et al., 2014; Budaev et al., 2019), which highlights the importance it can have on the success of invaders.

Behavioral flexibility–the ability of an individual to adapt its behavior to changes in the environment (Brown and Tait, 2015) by, e.g., stopping current behavior and initiating new behavior (Brown and Tait, 2015), solving a novel problem (problem-solving) or solving an existing problem in a novel way (innovation) is likely associated with invasion success (Reader and Laland, 2002; Sol et al., 2002; Shettleworth, 2010). This is because being more flexible can help an individual to better cope with novel habitats, predators, or resources (Sol et al., 2002; Wright et al., 2010; Chapple et al., 2012), which can ultimately increase their fitness (Sol et al., 2002). Measuring behavioral flexibility is challenging, but some metrics include the ability and speed with which animals conduct reversal learning (e.g., Brown and Tait, 2015; Lea et al., 2020) and their ability to deal with response inhibition (e.g., Diamond, 2013; Daniels et al., 2019), proficient problem solving across multiple domains (e.g., Logan, 2016a,b; Chow et al., 2018; Daniels et al., 2019; Lea et al., 2020), and the frequency of learning innovations (e.g., Sol and Lefebvre, 2000; Sol et al., 2002; Lea et al., 2020). A link between brain size (as a proxy of behavioral flexibility) and invasion success has been reported for invasive birds (Sol et al., 2002, 2005), mammals (Sol et al., 2008), amphibians and reptiles (Amiel et al., 2011). These reviews and comparative studies are powerful because they give us the big picture of how widely distributed a trait or relationship may be and sets the stage for later hypothesis testing. Another approach is to compare the cognitive ability of closely related species that may compete for the same resources, particularly when one species is native and the other is invasive (e.g., Roudez et al., 2008; Bezzina et al., 2014; Griffin and Diquelou, 2015; Chow et al., 2018). These studies typically address how species compete for ecological resources but differences in their ability to exploit resources may be independent of direct competition and may instead be a consequence of behavior and/or cognitive ability (e.g., Foucaud et al., 2016). Because cognitive abilities are often correlated with other factors such as motivation, personality, feeding ecology, sociality and life history (e.g., Tebbich et al., 2010; Carere and Locurto, 2011; Titulaer et al., 2012; van Horik and Madden, 2016; Dougherty and Guillette, 2018), disentangling the role of cognition in determining invasion success is challenging.

In this review, we have the following aims: (1) to review the evidence that cognition can influence invasion success; (2) characterize the features of cognitive ability that are likely to give individuals an advantage during the invasion process; and (3) propose future directions for studying the link between cognitive ability, fitness, and invasive success. To this end, we first conduct a systematic review of the literature on cognitive abilities that likely relate to invasion success (behavioral flexibility, problem solving, learning and memory) in both invertebrates and vertebrates. We also review the literature on brain size (as a proxy for cognitive ability) as it relates to invasive species. We then examine cognitive traits that could give species an advantage in a competitive, novel environment. Last, we describe an experimental approach to studying the role of cognition in determining invasive success and outline ways in which we can properly link invasive ability and cognition in a fitness framework.

We searched Web of Knowledge, Scopus and ProQuest for publications on biological invasions (using the keywords “invasi^*,” “invad^*,” “establish^*,” and “introdu^*”), cognition (using the keywords “cogni^*,” “learning,” “flexi^*,” and “innovat^*”) and fitness (using the keywords “fitness,” “surviv^*,” and “reprod^*”) focusing on animals (using the keyword “animal^*”). To refine our very broad search, we excluded publications based on the keywords “educat^*,” “child^*,” “physic^*,” and “gluco^*” (Figure 2). To get the largest possible number of hits with these search terms, we made sure that we included all words starting with these terms by applying ^*. Additionally, we used the built in options each database provided to further refine our searches (for more details see electronic Supplementary Material).

We downloaded 4,737 references as RIS files to import into EndNote (version X9.3.2) of which 892 were removed as duplicates. Only 2,000 of the 8,254 entries identified in Scopus could be downloaded (sorted by relevance). Of the remaining 3,845 we selected 61 based on the title. To be included in our sample, the title had to include any mention of cognitive ability such as learning, cognitive or behavioral flexibility, memory, inhibition, etc. To ensure no publications were missed, studies on behavior (which might encompass some cognitive ability) were included as well. Furthermore, the title had to mention either that the behavior or cognitive ability has a fitness or adaptive value (or increases reproductive success) and that it was tested in an invasive species or a species that successfully invaded an urban habitat. This ensured a broad selection of publications. We then conducted a forward search on these 61 entries resulting in an additional 40 entries (selection based on title). After full text download we looked at the abstracts of the 101 articles (61 + 40 = 101) and selected 27 as being relevant for our review. We included articles if the abstract (1) described a cognitive ability (studies solely looking at behavior were excluded at this stage); and (2) focused on invasiveness (an invasive species, comparing performance between invasive and native species or comparing performance between individuals from the source population and invasive population). We then conducted a backwards search (based on title) on the 27 selected articles resulting in an additional 11 publications. A second forward search on these 11 articles resulted in no new entries. Finally, we conducted a second backward search (resulting in one additional entry) and a final forward search (resulting in no new publications). We identified 113 articles based on title and selected 31 of those based on their abstract (Figure 2).

We then proceeded to read the full text of these 31 articles. Based on content, they were then divided into articles comparing species cognitive ability either directly (N = 10) or through a proxy such as brain size (N = 6) and articles looking at cognitive performance of a single invasive species (N = 12). The other three articles were reviews. Although studying the cognition of a single invasive species is interesting, without a comparison, it is unclear if the tested ability is associated with enhanced invasion success, consequently, some were used as examples to help identify possible useful cognitive abilities associated with invasion success (N = 10) but were not part of the main literature review.

Our review, therefore, focuses on those studies that make a comparison. To get a comprehensive picture of the cognitive abilities of the invasive species on which these comparative studies focus, we did an additional search for studies testing further cognitive abilities in these invasive species. We conducted these additional searches in Scopus using the species name (common or scientific) and “cognition” as the search terms (see electronic Supplementary Material for details). Studies were included if they were conducted on wild animals (either in the wild or testing wild caught individuals) and on a task that measured problem solving, innovation, behavioral flexibility, social learning, associative learning of ecologically relevant stimuli (food or threat) or spatial learning. We identified an additional 10 studies to those found in our initial search (N = 12). One of these studies was a species comparison which our initial search had missed and was included in our final sample. Overall, we identified 17 studies comparing performance between species and 21 studies testing cognitive performance on a single species (supporting literature). All searchers were conducted in November and December 2019 (Figure 2).

To investigate if successful invaders possess enhanced cognition, a comparison of their cognitive ability to that of their congeneric non-invasive counterparts can give some indication of how cognition aids biological invasions. Although this seems a straightforward way to tackle the question if cognition benefits invasive species, only a small fraction of research has focused on a direct comparison between native and invasive congeners and even fewer have compared performance of the source population to the invasive population. Luckily, these few studies span a wide range of taxa from invertebrates such as crabs (Roudez et al., 2008; Ramey et al., 2009), crayfish (Hazlett et al., 2002) and flies (Foucaud et al., 2016), to vertebrates including mammals (MacDonald, 1997; Sol et al., 2008; Chow et al., 2018), birds (Sol et al., 2002, 2005; Diquelou et al., 2015; Griffin and Diquelou, 2015), fishes (Drake, 2007), reptiles (Amiel et al., 2011; Bezzina et al., 2014) and amphibians (Amiel et al., 2011) and provide a good first insight into how cognition may enhance invasive species success (Supplementary Table 1) in competing with the resident species assemblage already adapted to the invaded environment.

During invasion into a new habitat, animals will inevitably face environmental conditions which are novel and to which they are not optimally adapted. The faster way to adapt to changing conditions is through behavioral plasticity and flexible behavior. Shifts in behavior most likely follow after experience with a certain situation allowing the individual to learn an appropriate response. Animals might innovate solutions to problems by modifying existing behavior, come up with new behaviors, or learn socially from conspecifics or even native congeneric heterospecifics (Wright et al., 2010; Damas-Moreira et al., 2018). Cognitive ability can play an important role during the different stages of the invasion process, but which abilities increase invasion success within or across stages? Below, we provide some examples of cognitive abilities which are likely to be involved in increasing the likelihood that a species becomes established in a novel environment (based on work presented in the previous section).

The way forward is multi-faceted, but a good starting point is studies that compare invasive and non-invasive species, source and invasive populations, and experimental studies which link or test for links between fitness, cognitive ability, and invasive ability. Ten years ago, no longitudinal studies of invasive populations were available (Wright et al., 2010), a big gap that has not been filled. Additionally, we found only one study comparing learning (female fruit flies choosing between oviposition sites) between individuals from the source and invasive population (Foucaud et al., 2016), an approach also listed by Wright et al. (2010). We need more baseline data on differences between invasive and non-invasive species pairs (i.e., congeneric species) and between invasive and source populations. The challenge will be to conduct direct tests of how cognitive ability affects fitness with links to either survival or reproductive success in the future as manipulation of cognitive ability will likely also change associated abilities (cognitive and non-cognitive; e.g., Cauchard et al., 2017). This will create a clearer picture of what attributes make a species a more successful invader than less invasive species.

Simple cognitive tests that can be used in the wild and on a wide range of species would be especially valuable, although bringing wild caught individuals to the lab and testing an array of cognitive abilities also has merit. Careful consideration should also be given to which cognitive abilities to investigate, based on a species' ecology and sociobiology. We need to think in terms of aspects of cognition that are most likely to be beneficial during an invasion event. At the same time, cognition often correlates with non-cognitive traits including motivation or neophobia (e.g., Sol et al., 2011, 2012b) which should be measured simultaneously. Moreover, correlation between cognitive traits might occur warranting additional controls for such co-variation. We also would like to highlight that, so far, fitness benefits of enhanced cognitive ability have often been implied, but less often directly studied (e.g., Thornton et al., 2014; Dayananda and Webb, 2017; Ashton et al., 2018). Studying the value of cognitive ability during biological invasions is not an easy task but certainly one that has a substantial pay-off.

Future research could look to studies of Anolis lizards (anoles) for insight on how to experimentally study the role of cognition in invasions. Anoles have become the poster child of experimental vertebrate evolution because large numbers of known individuals can be introduced on to small islands and they have sufficiently short generation time to study selection in “ecological” time. Their survival and fitness can then be measured for a range of traits and island conditions (e.g., predator vs. predator-free, different habitats, etc.), thereby creating a picture of how selection acts on traits in novel environments. As it turns out, the brown anole (Anolis sagrei) is now a common invasive species documented in far flung locations from Florida (USA) to Taiwan, including regions such as Hawai'i. Florida is also home to a large number of invasive species including many species of lizards because of its tropical climate and an historically lax control of animal imports. We highlight this because Florida is a potential epicenter for a range of studies on how cognitive ability may link to invasive ability because the spread of these species can be easily monitored. This state also has a large number of artificial islands in their inter-coastal waterways which are used for selection studies (e.g., Fargevieille et al., 2019). We suggest using these same islands for experimental studies involving the release of anoles of known cognitive ability to monitor their survival and replicate it among islands. Likewise, both invasive brown anoles and native green anoles of known cognitive ability could be released on to the same islands. These islands are small and can be easily manipulated. For example, in addition to introducing pairs of native and invasive anoles, the native green anole could first be introduced and established before subsequently releasing brown anoles. This would replicate real-world conditions where invasive and native species come into contact. Likewise, common garden experiments in which native and invasive anoles are first raised under the same conditions before being released onto islands would control for any variance contributed by the developmental environment. We also suggest assaying all individuals for behavior, such as boldness, exploratory behavior, and propensity to disperse (this can be done in large outdoor arenas). Furthermore, traits such as motivation and persistence should be measured during cognitive testing to ensure that these traits are not causing differences between species rather than cognition. It is important to be able to disentangle the effects of cognitive ability and behavior on invasive ability. And with respect to cognitive ability, although time consuming, we suggest multiple tests that focus on spatial learning and give a measure of behavioral flexibility because these traits are likely to be crucial to survival in novel environments.

In summary, there is increasing evidence that cognition influences fitness (e.g., Cole et al., 2012; Cauchard et al., 2013, 2017; Dayananda and Webb, 2017; Ashton et al., 2018; Madden et al., 2018). In the case of biological invasions, when organisms are exposed to new environments, cognitive ability is predicted to improve the probability of successful establishment. In this scenario, individuals with better cognitive ability are therefore more likely to be selected for. This hypothesis requires testing and we have suggested a potential experimental paradigm using Anolis lizards, but there are many others. We also encourage more empirical work comparing pairs of invasive and non-invasive species that are closely related and more studies comparing populations at the invasion source and the invasion front in order to better understand invasions and the role of selection. Understanding invasions in light of a species' cognitive ability and the relative fitness of potential behavioral and cognitive styles is a field with great potential. We hope this review will help stimulate innovative research in this direction.

BS did the integrative review and wrote the bulk of the paper, ID-M wrote the bulk of the introduction and MW wrote the bulk of the future directions section. All authors contributed to writing and revising all sections of the manuscript. All authors conceived the framework for the paper.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.