To study problem-solving ability in these birds, three tasks were given in a random order in which birds had to use different techniques to open transparent food containers task 1 and 2 or extract food from within a Styrofoam cup which was transparent on top task 3. Overall, the invasive common myna outperformed the native noisy miner. Common mynas were faster to solve these tasks and showed greater motor diversity and flexibility, which were highly repeatable.
Common mynas also showed repeatability in their persistence when solving the tasks compared to the noisy miners Griffin and Diquelou, These result indicate that mynas show consistent, high levels of persistence, motor diversity, and flexibility, while miners do not. Furthermore, in a later study, task directed motivation making more contact with an apparatus and exploratory behavior moving less within an open space predicted task success in mynas Lermite et al.
Moreover, invasive mynas can learn to remove lids from food wells motor innovation and motivation and neophobia were the best predictors of successful motor innovation Sol et al.
Individuals from highly urbanized habitats were faster problem solvers and were also less neophobic and more exploratory Sol et al. Mynas were also good observational learners. Observing the behavior of an alarmed conspecific when the source of the threat was not visible, however, did not affect the observers behavior Griffin et al. Following Griffin and Diquelou , transparent food containers same as task 1 were presented to seven different Australian bird species: Australian ravens Corvus coronoides , Australian magpies Cracticus tibicen , magpie larks Grallina cyanoleuca , common mynas A.
As with common mynas, European starlings are highly invasive and should perform well in problem-solving tasks if problem solving indeed is a trait enhanced in invasive animals.
Although this was true, Australian ravens were the best problem solvers closely followed by common mynas and European starlings. Except for the Australian magpie another native species like the Australian raven , none of the other species showed much skill in solving the presented task. Motor flexibility range of motor actions predicted problem-solving probability across all species Diquelou et al.
These studies are great examples of how simple tests on wild birds can reveal striking difference in a range of abilities cognitive and non-cognitive and can give some indication of how learning, memory and flexibility are helping invaders colonize novel habitats.
In the UK, they outcompete and replace the native red squirrel Sciurus vulgaris with which they share a number of ecological traits Koprowski, ; Gurnell et al. Wild gray squirrels were better problem solvers compared to wild red squirrels. Animals were given an easy task in which they had to displace lids to gain access to a reward nut , and a hard task in which they had to push or pull a bar to make a nut drop down to the bottom of a box, making it accessible.
In the easy task, more gray squirrels were first-time solvers than red squirrels, and invasive gray squirrels were also faster solvers. In the hard task, more gray squirrels were solvers but both species showed the same performance, were similarly persistent number of attempts , and used similar proportions of effective behaviors; red squirrels were even more efficient sum of the duration of all attempts to solve the task until it was successfully solved; Chow et al.
These results indicate that although both species exhibit similar levels of persistence and motor diversity non-cognitive factors important for successful problem solving other factors such as cognition might explain why more gray squirrels solved the tasks. Invasive wild gray squirrels also had longer lasting spatial memory of caches made by a human experimenter compared to native wild red squirrels MacDonald, However, low sample sizes reduced statistical power and results need to be interpreted with caution.
Furthermore, the difference could have been caused by the fact that gray squirrels rely more on caches MacDonald, and could have a more specialized hippocampus, an essential brain area for spatial memory. The results of these studies indicate that learning and memory could help explain why gray squirrels have been such successful invaders although both species have good problem-solving abilities.
Future studies could investigate if gray squirrels are innately better learners and problem solvers by comparing individuals from the native and introduced range. Moreover, gray squirrels have been introduced to Italy more recently 20th century; Bertolino et al. In summary, comparative research in both invertebrates and vertebrates suggests that cognitive abilities such as learning and memory might help favor invasion success.
However, not all studies have found differences between the tested species Bezzina et al. Furthermore, non-cognitive factors are clearly causing differences between species in task performance Diquelou et al.
It is therefore crucial to take such factors into account to avoid drawing the wrong conclusions about the role of cognition in invasion success. Studies in birds and mammals mainly test problem-solving ability focusing on non-cognitive factors such as motivation and persistence but less on cognitive factors such as inhibition and flexibility.
Studies focusing on species or population comparisons are rare, which underscores how we are only just starting to understand how cognition might aid the invasion process. Moreover, if species innately possess beneficial abilities that help them invade novel habitats or if these abilities emerge as a result of selection is unclear.
The degree to which cognitive abilities are beneficial in the invasion process and if these are general across different invasive species is also unknown. A link between cognitive ability, innovative behavior feeding and problem solving and brain size has emerged in a range of taxa e. Recently, comparative studies have examined the relationship between behavior, cognition, and brain size with a focus on how innovative behavior and cognition might benefit invasive species Sol and Lefebvre, ; Sol et al.
By using data on relative brain size and invasion success after human translocation, Amiel et al. This trend was consistent geographically except for Australasia. Here, the opposite trend was observed, species with smaller brains were more successful Amiel et al. In birds, there is a strong link between relative size of the hyperstriatum ventral which serves a similar function to the mammalian neocortex and cognitive flexibility Timmermans et al.
A large-scale analysis of relative brain size, fecundity, parental investment and invasion success in fishes revealed no correlation between brain size and establishment success in a novel environment Drake, Empirical work on fishes has demonstrated a positive link between brain size and cognition numerical associative learning; Kotrschal et al.
In these studies, however, fishes were artificially bred for larger brain size; if selection acts in a similar manner in natural populations is unclear, and if so, a correlation between brain size and cognitive ability might be much weaker and harder to detect.
It revealed, that species with larger relative brain size were more likely to successfully invade New Zealand and that successful invaders also showed a higher number of foraging innovations.
Other traits were also associated with invasiveness: the number of individuals introduced introduction effort , migration migratory, partially migratory, or sedentary and developmental mode nidicolous vs. Following this study, the inclusion of a much wider range of bird species revealed a similar trend. Again, species that were successful invaders had larger relative brain size and showed more foraging innovations. Anthropogenic environments differ greatly from natural environments and are subject to greater change and disturbance Lowry et al.
It is not surprising to find species that establish themselves in a human dominated environment to also have larger relative brains possibly to deal with these challenging environmental conditions.
Sol et al. They found that birds with larger relative brains were more successful at establishing a population in novel environments and this invasion propensity was also associated with innovativeness; invasive species had more feeding innovations. Additional analyses showed the success of invasive species in coping with novel environments was due to an increase in their cognitive ability and no other mechanisms Sol et al.
The brain size-environmental change hypothesis was also confirmed in mammals. Establishment success was higher in mammals with relatively larger brains and was also associated with introduction effort and habitat generalism Sol et al. Contrary to birds, however, no proxy for cognitive ability e. Nevertheless, a link between relative brain size and cognitive ability has already been established in some mammalian groups e.
Across taxa, the analysis of large multi-species datasets has been useful for investigating the generality of different hypotheses about how cognition could help species become successful invaders. While a link between larger relative brain size and enhanced cognition has been established for some taxa, more effort is still needed to test for the existence of a similar relationship in other taxa.
Importantly, studies using brain size as a proxy for cognitive ability run into a number of constraints and results should be interpreted with caution. Evidence suggests that brains are heterogeneous across taxa and the degree of enlargement and neuron densities of specific brain areas can differ greatly e.
Furthermore, selection may change specific brain areas without an increase in brain size see Does Selection Act on Brain Size? Moreover, analyses are hampered because the relationship between brain size and body size is not linear in all taxa [e. Results of such comparative studies using brain size are, therefore, better used as a starting point for more detailed investigations looking at how individual differences in cognitive ability translate to brain anatomy within species e.
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.
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. Although we can assume that a cognitive ability might not carry the same advantage when facing novel or changing conditions across species, behavioral flexibility, the ability to adapt flexibly to changes in the environment Brown and Tait, , is a trait likely to be advantageous to most, if not all, invaders.
Behavioral flexibility is often described together with innovation and problem solving such that species or individuals that are innovators or problem solvers are behaviourally flexible Lea et al. A key component of behavioral flexibility is that it can be adaptive in a given situation Brown and Tait, Inventing new behaviors or techniques to solve problems such as being confronted with novel foods or having to extract edible foods from within inedible casings e.
Furthermore, being behaviourally flexible in the traditional sense, by flexibly adjusting behavior in situations when old behavior becomes unsuccessful, also carries fitness advantages. Therefore, our definition of behavioral flexibility encompasses any change in behavior that helps individuals to adapt to changing conditions and can be measured using innovation rates, different techniques to solve puzzle box tasks i.
Wright et al. For example, wild North American racoons Procyon lotor caught in their native range, possessed flexible problem-solving skills. They were tested on a multi-access box which could be opened in three different ways.
Across nights, access points were blocked to force animals to abandon old solutions and find new ways to access the reward. Seven of the 20 racoons tested solved the box using all three ways showing high levels of problem-solving ability and flexibility in their use of behaviors to open the box when an old solution became ineffective.
Exploratory behavior and persistence were robust predictors of solving success. Inhibitory control was also assessed by looking at the time spent interacting with a newly locked access point but it did not predict differences in solving success between night two and three. This shows that this species possess an innate ability to solve problems which might be the reason why it is such a successful invader Daniels et al.
Not all successful invaders, however, are great problem solvers. Great-tailed grackles Quiscalus mexicanus showed behavioral flexibility during reversal learning and varying degrees of problem-solving ability. Birds learnt to reverse their preference for finding food in a golden tube to choosing the previously unrewarded silver tube during a reversal stage. Fast learners were, however, not more flexible Logan, a. Problem solving was tested using the Aesop's fable paradigm dropping stones into water to raise the water level and bring a reward closer; Logan, a , a stick tool-use task to extract a piece of bred from between two transparent walls and a horizontal and vertical string pulling task in which a string has to be pulled to bring a reward close enough to reach it; Logan, b.
Although grackles were unable to spontaneously drop stones, use sticks or pull strings to access a reward, birds could learn to drop stones to reach a reward Logan, a , b. However, they could not learn to use stick tools Logan, b. They were also flexible in learning which strategy to use during the Aesop's fable paradigm. Initially birds preferred heavier stones but when these became ineffective, they switched strategy to use lighter stones in higher numbers Logan, a.
Individuals tested in these tasks were wild caught from within their introduced range. If great-tailed grackles are innately good problem solvers has still to be investigated. So far, no direct link between cognition, its fitness value, and invasion success has been demonstrated. Nonetheless, increasing numbers of studies show how behavioral flexibility is enhanced in successful invaders as compared to species that did not establish a viable population in a novel environment e.
Conflating these areas of research will further our understanding of if and how behavioral flexibility aids biological invaders. Learning enables an individual to acquire new information and compensate for shortcomings that might arise from entering a new environment to which it is not adapted, or even maladapted. Theoretical models predict that, if the initial founder population is small, adaptation through genetic change alone is not fast enough to result in a sustainable population; however, learning can help a population persist even if it is initially maladapted to the novel environment Sutter and Kawecki, Importantly, the benefit of learning to buffer differences in fitness between habitats and to increase mean fitness in the novel habitat is higher when the difference between the native and novel habitat is large Sutter and Kawecki, This means that learning could be more beneficial for introduced species than it is during a gradual range expansion.
Learning about the characteristics of a novel habitat has the potential to increase the probability that even a small founder population can persist in a new environment. Fast learning is present in invasive species, as compared to native competitors see earlier discussion of green crabs, common mynahs and gray squirrels.
In addition, invasive American bullfrogs Lithobates catesbeianus , which experienced threat scent of the novel largemouth bass, Micropterus salmoides , combined with conspecific alarm cues as embryos within the egg, hid more inside a refuge when experiencing the threat later in life as larvae after hatching. No effect could be detected in untrained control larvae Garcia et al. These studies give some indication that enhanced learning ability may facilitate invasion success; however, we do not know if these learning abilities have actual fitness consequences increased survival and reproductive success or if these species are innately better learners.
When entering a novel habitat that is dissimilar to the environment in which an individual developed and has adapted to, collecting information about predators, what to eat and where to hide, can be crucial for survival.
Trial-and-error learning can be associated with high costs when sampling noxious foods or encountering dangerous predators, possibly leading to death after first contact. It can therefore be beneficial to rely on the knowledge that other individuals have already accumulated.
Social learning is considered a shortcut to accessing important information that has already been vetted and is beneficial Galef and Laland, During the early stages of the invasion process, the only individuals with relevant information might be congeneric native individuals. Some invasive species are known to use the behavior and alarm signals of native species to quickly learn about food e. For example, lab-reared female guppies that watched the behavior of either a small group of conspecifics or heterospecifics butterfly splitfins, Ameca splendens , when food scent was introduced, changed their behavior accordingly.
Observer fish showed similar behavior to demonstrators by spending more time in the upper layer of their aquarium. When no demonstrators were present or water was added instead of the food odor, observers did not change their behavior showing that their behavior was guided by that of the demonstrators irrespective of whether demonstrators were conspecifics or heterospecifics Camacho-Cervantes et al. Furthermore, a recent study showed that invasive Italian wall lizards, Podarcis sicula , readily learn stimuli associated with a food reward in an artificial foraging task using differently colored food wells from both conspecifics and heterospecifics and made fewer errors when learning socially as opposed to individually Damas-Moreira et al.
Social learning has, however, limitations. It is only really beneficial if the environment is largely stable and information stays relevant for extended periods of time and if animals are selective about what information they learn Galef and Laland, Nonetheless, it might be a powerful tool to spread important information rapidly through an invasive founder population and increase the likelihood that a large enough number of individuals survive and can reproduce.
In some species, smart individuals are preferred as mates e. There is evidence that cognitive ability e. Mate choice for individuals with enhanced cognitive ability has received little attention for a review see Boogert et al. It has also been shown that a number of species have to learn about intraspecific sexual traits to successfully mate and reproduce Ryan et al. During the invasion process, animals might come in contact with congeners that are not dissimilar to themselves.
On the one hand, if courting and mating with congeneric species are costly, enhanced learning for intraspecific traits that help distinguish between species could help avoid such costs and help an establishing population to grow to a sustainable size. On the other hand, hybridization can enhance cognition and adaptability to novel environments through backcrossing of favorable genes acquired from the native species into the parent lineage or through the development of extreme phenotypes that increase fitness in a novel habitat Rice, 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. 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. We need more baseline data on differences between invasive and non-invasive species pairs i.
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. 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. 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. 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. Their survival and fitness can then be measured for a range of traits and island conditions e. 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. 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. 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. Our work on cognition has been supported by Macquarie University and the Australian Research Council. 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. Aamodt, C. Birdsong as a window into language origins and evolutionary neuroscience. B Biol. Amiel, J. Smart moves: effects of relative brain size on establishment success of invasive amphibians and reptiles.
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Galef, B. In chapter three, I tested whether the presence of an ecologically similar species e. Finally, in chapter four I evaluated the consequences of high abundances of signal crayfish on native prey and the behavior of signal crayfish. Accumulated evidence suggests that signal crayfish possess the behavioral traits e. When native communities do not offer much resistance i. The patterns and results suggest that the communities with high prey availability and infrequent disturbances are most at risk of invasion, but that the aggressive nature of this invader makes most communities vulnerable to invasion.
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