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Affiliations: 1) Max Planck Institute for Evolutionary Anthropology, Germany; 2) University of California Santa Barbara, USA; 3) Victoria University of Wellington, New Zealand. Corresponding authors: corina_logan@eva.mpg.de, rachael.shaw@vuw.ac.nz, kelseybmccune@gmail.com
Human modifications of environments are increasing, causing global changes that other species must adjust to or suffer from. Behavioral flexibility (hereafter ‘flexibility’) could be key to coping with rapid change. Behavioral research can contribute to conservation by determining which behaviors can predict the ability to adjust to human modified environments and whether these can be manipulated. When research that manipulates behavior in a conservation context occurs, it primarily trains a specific behavior to improve individual success in the wild. However, training a domain general cognitive ability, such as flexibility, has the potential to change a whole suite of behaviors, which could have a larger impact on influencing success in adjusting to human modified environments. This project asks whether flexibility can be increased by experimentally increasing environmental heterogeneity and whether such an increase can help species succeed in human modified environments. We explore whether it is possible to take insights from highly divergent species and apply them to address critical conservation challenges. This pushes the limits in terms of understanding how conserved these abilities may be and to what extent they can be shaped by the environment. We aim to 1) conduct flexibility interventions in flexible species that are successful in human modified environments (great-tailed grackles and California scrub-jays or blue jays) to understand how flexibility relates to success; and 2) implement these interventions in two vulnerable species (toutouwai and Florida scrub-jays) to determine whether flexibility as a generalizable cognitive ability can be trained and whether such training improves success in human-modified environments. This research will significantly advance our understanding of the causes and consequences of flexibility, linking behavior to environmental change, cognition, and success in human modified environments through a comparative and global framework. This registered report launches our reproducible research program, ManyIndividuals (https://github.com/ManyIndividuals/ManyIndividuals), which is a global network of researchers with field sites investigating hypotheses that involve generalizing across many individuals.
Human modified environments are increasing (Goldewijk, 2001; X. Liu et al., 2020; Wu et al., 2011), causing global changes that other species must adjust to or suffer from (Alberti, 2015; Chejanovski et al., 2017; Ciani, 1986; Federspiel et al., 2017). Behavioral flexibility (hereafter ‘flexibility’) could be key for adjusting to such change: individuals interact with their environment through behavior, making it crucial to an ecologically valid understanding of how species adjust to environmental changes (Lee & Thornton, 2021). One of the top priorities for behavioral research to maximize conservation progress is to determine which cognitive abilities and behaviors can predict the ability to adjust to human modified environments and whether these can be manipulated (Moseby et al., 2016). The rare research that manipulates behavior in a conservation context usually focuses on training specific behaviors (for example, predator recognition through predator exposure) to improve individual success in the wild (Jolly et al., 2018; Moseby et al., 2012; Ross et al., 2019; West et al., 2018; see review in Tetzlaff et al., 2019). However, training a general cognitive ability, such as flexibility – the ability to rapidly adapt behavior to changes through learning throughout the lifetime (see the theory behind this definition in Mikhalevich et al., 2017) – has the potential to change a whole suite of behaviors and more broadly influence success in adjusting to human modified environments. Recent evidence supports this hypothesis: as far as we are aware, we were the first to show that flexibility can be manipulated using serial reversal learning of color preferences, and that the manipulated individuals were more flexible in a new context (locus switching on a puzzlebox) as well as being more innovative (solved more loci on a puzzlebox) (C. Logan et al., 2022).
Environments where informational cues about resources vary in a heterogeneous (but non-random) way across space and time are hypothesized to open a pathway for species to functionally detect and react to such cues via flexibility (Mikhalevich et al., 2017). Human modified environments likely provide a different set of informational cues that vary heterogeneously across space and time, and the species that are successful in such environments are likely those who are able to detect and track such cues. Because heterogeneous environments are hypothesized to select for flexibility (Wright et al., 2010), we expect that experimentally manipulating environments to be more heterogeneous will result in an increase in flexibility in individuals, which will then increase their success in such environments (Figure 1). Success can relate to any number of variables regarding the usage of and investment in resources and response to threats, from improved foraging efficiency to increased dispersal and survival within human modified environments, to placing nests in more protective locations. Whether a measure of success is predicted to relate to flexibility depends on what is already known about the particular population and their particular environment.
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Figure 1. The theory behind this research illustrated by a directed acyclic graph (DAG), which is a theoretical model of the causal relationships among the key variables in our investigation. Based on the theoretical background provided by Mikhalevich et al. (2017), we assume that more heterogeneity causes more flexibility, which then causes more success in human modified environments.
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This investigation asks whether flexibility can be increased by experimentally increasing environmental heterogeneity (via serial reversal learning) and whether such an increase can help species succeed in human modified environments. We explore whether it is possible to take insights from highly divergent species and apply them to address critical conservation challenges. Serial reversal learning tasks have been performed with a wide diversity of species (birds: Bond et al., 2007; bumblebees: Strang & Sherry, 2014; stingrays: Daniel & Schluessel, 2020). There is variation across individuals and species in their performance, however almost all previous studies show that individuals improve their flexibility if the reversal intervention is given multiple times in sequence (rats: Mackintosh et al., 1968; guppies: Lucon-Xiccato & Bisazza, 2014; poison frogs: Y. Liu et al., 2016). We aim to conduct a flexibility intervention in flexible species that are successful in human modified environments (great-tailed grackles and California scrub-jays or blue jays) to understand how flexibility relates to success, and implement these interventions in two vulnerable species (toutouwai and Florida scrub-jays) to determine whether flexibility as a generalizable cognitive ability can be trained and whether such training improves success in human modified environments (Figure 2).
While we do not examine the potential spread of the post-manipulation success behaviors from manipulated individuals to individuals that are not involved in our studies, we acknowledge that this is a possibility worthy of future investigation. Manipulating the flexibility of a few individuals could have population-level effects because significant research on social information use in birds (e.g., Valente et al., 2021) demonstrates the potential for the manipulated behavior to disseminate to conspecifics (for example, if manipulated individuals are faster at locating new resources, which could attract the attention of conspecifics, or if unmanipulated individuals copy the manipulated individuals’ nesting or foraging locations). In the event that social learning is not used by a given population to spread the behaviors of manipulated individuals, investing in the training of specific individuals to increase their success in the wild could still have conservation impacts. In some cases, it is possible to train many individuals in a population or a species because there are not many individuals left (Greggor et al., 2021). It is also possible to train all individuals involved in a conservation management event such as a translocation (Greggor et al., 2021). Therefore, there can still be significant population consequences even if each individual needs to be trained to achieve the goal.
This comparative approach will ultimately reveal how conserved these abilities may be and to what extent they can be shaped by the environment. To increase the generalizability of the conclusions from the ManyIndividuals project, we here also provide multiple methodological options that other researchers can use to test these questions in additional species. The results will substantially advance our understanding of the causes and consequences of flexibility, linking behavior to environmental change, cognition, and success in human modified environments through a comparative and global framework.
Prediction 1: Flexibility can be increased in individuals and such an increase improves the likelihood of success in human modified environments. This would indicate that the abilities involved in tracking changing resources in the environment are the same as or related to the abilities involved in succeeding in human modified environments. It would also indicate that flexibility is trainable and that such training could be a useful conservation tool for threatened and endangered species.
Prediction 1 alternative 1: Flexibility can be increased in individuals, but such an increase does not improve the likelihood of success in human modified environments. This would indicate that species associated with human modified environments form this association for reasons other than their flexibility, and that threatened species are likely not very successful in human modified environments for reasons unrelated to their ability to change their behavior with changing circumstances. An alternative could be that the changes induced by the increase in flexibility do not persist for sufficiently long times to make a difference on the subsequent likelihood of success (changes in grackles were still present for four weeks after the manipulation and longer time periods were not attempted so the threshold is unknown C. Logan et al., 2022).
Prediction 1 alternative 2: Flexibility can be increased in some populations, but not others. This would indicate that flexibility manipulations may not work for all populations, and that the effectiveness of such experiments should first be tested in the population of interest before including such an intervention in a conservation plan. If flexibility is not manipulatable in threatened populations, this would indicate that they are likely not very successful in human modified environments because of their inability to change their behavior with changing circumstances, and that flexibility is not trainable. If flexibility is not manipulatable in populations that are successful in human modified environments, this could indicate that they might have used flexibility in the past when originally forming the association, but the need to maintain flexibility in their repertoire is no longer necessary. In populations where flexibility is not manipulatable, this would indicate that the abilities involved in tracking changing resources in the environment are independent of the abilities involved in succeeding in human modified environments.
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