Behavioural flexibility, innovation

Non-human animals face challenges posed daily by our anthropogenically modified world.

Apart from the direct impacts of the “super predator” (Darimont et al. 2015), humans impose a striking array of effects on wildlife. Urbanization triggered habitat change, one of the largest scale anthropogenic alteration of the environment, has several effects on non-human animal (henceforth ‘animal’) populations and communities, for example by rapidly and extensively altering the structure of habitats and food availability (for non-avian animals reviewed by McKinney 2008; for birds by Seress and Liker 2015). Hundreds of millions of birds die each year due to collisions with man-made structures, it arguably is one of the main sources of anthropogenic mortality of birds in the United States of America (Smallwood 2013; Loss et al.

2014), and linear establishments such as roads with their traffic cause a tremendous negative effect on animal abundance (Fahrig and Rytwinski 2009). Altered food availability in urban habitats influences diet composition, which in turn affects not only individual condition, but also breeding performance (Harrison et al. 2010; Plummer et al. 2013). Moreover, direct anthropogenic effects go far beyond city limits; fisheries threat non-target marine species through incidental capture in a variety of fishing gear, causing human induced decline in some populations of these species, many of which are threatened (see e.g. the review for USA fisheries by Moore et al. 2009). Another risk for marine animals is to ingest or to entangle with debris of mainly land originated plastic waste (e.g. for marine turtles, see Schuyler et al. 2014).

Furthermore, one of the most important phenomena of human influence on the Earth’s ecosystem, the facilitation of the spreading of species outside their original range, has a detrimental effect on the native species in the way of their expansion, and requires adaptation from the invaders and the invaded alike (Clavero and García-Berthou 2005). These rapid processes that leave their marks even at the most remote corners of the biosphere have led to the introduction of a new era in the history of Earth, the so called “Anthropocene”.

The profound changes in the environment caused by human activity are either distinct from the challenges animals met in their evolutionary past (e.g. habitat fragmentation caused by linear establishments), or come at a rate much faster than usual on an evolutionary time scale (e.g. large-scale habitat change caused by the combined effect of urbanization and climate

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change). Finding a way to cope with daily life in a swiftly changing world probably has never been more pressing for the individual animals. For humans, to mitigate the negative effects we have on wildlife it is imperative to understand the mechanisms by which animals may react to the alterations (Greggor et al. 2019). Three basic mechanisms may be implemented by organisms in order to counteract these effects and keep on surviving and reproducing:

dispersion to habitats that are more favourable, genetic adaptation, and phenotypic plasticity.

Dispersion is often inhibited by natural or anthropogenic barriers, and although evolutionary changes are always under way, the speed of genetic alterations may at times be unable to keep the pace with environmental changes, especially for species with relatively long generation time. However, the expression of a genotype can vary through phenotypic plasticity, allowing alternative phenotypes of a certain genotype to occur (West-Eberhard 1989), in order to adapt to environmental conditions. This type of adaptation may precede and complement micro-evolutionary processes (Miranda 2017), and can come in various forms. It may include, mutually non-exclusively and possibly non-independently, morphological variance (Repka and Pihlajamaa 1996), physiological changes (McKechnie et al. 2006), or behavioural responses.

Note that behavioural responses are particularly labile; therefore, it might be especially appropriate for giving prompt responses to environmental challenges. Behaviour itself is partially genetically determined, the extent of which varies with species and trait (Yong-Kyu 2009). Heritability of behaviour normally ensures that species cope well with the dominant abiotic and biotic interactions that naturally occur in their native habitat. However, if these conditions change, existing behavioural patterns might prove inappropriate, indeed they may induce negative effects on individual fitness. Behavioural flexibility, which is the ability of an individual to change its existing behavioural patterns (West-Eberhard 1989), can enhance the adjustment of behaviour to the new conditions. For example, bird species with more flexible behaviour are more successful invaders, and in temperate Palearctic birds higher behavioural flexibility, larger brain size, and higher propensity for novel behaviours help resident species to cope with seasonal changes (Sol et al. 2002, 2005). This is furthered by the advantage that behavioural flexibility also allows for reversibility when fluctuation of stimuli necessitate it (Van Buskirk 2012); for example abandoning hiding behaviour after predators became absent results in more effective foraging (Orizaola et al. 2012). Still, in case of some anthropogenic changes behavioural plasticity might prove maladaptive, and therefore can further the negative impacts on a population contributing to the operation of ecological traps (López-Sepulcre and Kokko 2012); for example failed breeding of caddis fly Hydropsyche pellucidula on glass

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buildings (Kriska et al. 2008), or attempted breeding of common terns (Sterna hirundo) on rod fishing platforms that failed due to unpredictable human activity (personal observation).

For humans, innovations are key features in the history of the success of the species, and form the ultimate base of our culture. Similarly, innovation is prominent in the animal kingdom (Reader and Laland 2003) affecting ecological and evolutionary processes. Research on human innovation has an extensive literature, with the somewhat shorter history of works on animal innovation that roots back to the landmark paper of Fisher and Hinde (1949). Despite this prevalence of the topic, the definition of innovation remains controversial (Ramsey et al.

2007; Reader et al. 2016), although a demand for clarification of the term aroused decades ago (Kummer and Goodall 1985). Some authors regard innovation as a product, whereas others as a process (reviewed in Chapter I. of Reader and Laland 2003). Nevertheless, innovations are regarded as new behaviour patterns or modifications of existing behaviours in an unusual context to help an individual to utilize its environment in a novel way (Reader and Laland 2003;

Griffin and Guez 2014, 2016; Tebbich et al. 2016). Innovation and flexibility of behaviour are traditionally regarded as related, where innovativeness is a component of behavioural flexibility and it is also a promising candidate as a proxy for it (Reader and Laland 2003; Reader et al.

2016). Behavioural flexibility and innovation however are not interchangeable concepts, as former is used for a broader domain of plasticity in behaviour (Audet and Lefebvre 2017), moreover recent studies suggest that the relationship between flexibility and innovative behaviour may vary; they may be positively or negatively associated or the link between them may be indirect (Reader and Laland 2003; Griffin et al. 2013a; Chow et al. 2016). Furthermore, Reader and Laland (2003) argue that innovations have the distinct property of being novel behaviours that are new not only for the individual itself, but also for the whole population, whereas flexibility may arise from the reaction norm of the species. The significance of innovative behaviour is conspicuous, as a tendency to innovate appeared independently in different taxa, meanwhile convergent evolutionary processes linked to innovation are described even in phylogenetically less related taxa (e.g. selection towards larger brain size, see Lefebvre et al. 2004; Overington et al. 2009b; Reader et al. 2011).

Innovative behaviours have become a central topic in the past decade, given their vast potential to facilitate adaptation to novel or changing environments (Griffin and Guez 2014;

Reader et al. 2016). Innovation on one hand can bring benefits, and believed to be adaptive by enabling animals to better exploit their environment; e.g. find novel food resources (Fisher and Hinde 1949), use novel materials to repel parasites (Suárez-Rodríguez et al. 2013), attain more attractive sexual displays (Elias et al. 2006; Madden 2007), or deceive social companions in

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order to acquire resources (Byrne 2003). On the other hand, innovative behaviour is expected to have costs; besides the time and energy invested in such behaviour it is assumed for example to increase predation risk (Overington et al. 2011b), and it may incur risk of injury or poisoning (Bostic and Banks 1966), or elevated parasite load (Garamszegi et al. 2007; Vas et al. 2011).

The trade-off between these fitness costs and benefits should determine the occurrence of innovation, yet studies investigating them are still scarce.