Quick learning, quick capture: largemouth bass that rapidly learn an association task are more likely to be captured by recreational anglers
Individuals show consistent differences in their approach to novel tasks (i.e., “cognitive syndromes”), whereby “fast” individuals are bold and solve new problems quickly compared to “slow” individuals. While a “fast” approach can be advantageous in some situations, these individuals are often more likely to make mistakes and subject themselves to greater risk, including from predation. What is unknown is how these tendencies impact survival in environments where humans constitute a predatory risk (such as the case of fish targeted by commercial or recreational fishing). To address this gap, we assessed learning performance in 60 largemouth bass Micropterus salmoides using an active-avoidance task that required fish to learn to associate a conditioned stimulus (overhead light) with an unconditioned aversive stimulus (chasing with a net) to successfully shuttle through a small opening to a safe area of an aquarium. These same fish were also tested for proactivity in a restraint test (frequency of leaping to escape a net out of water) before being subjected to angling trials in a naturalistic pond setting. Performance on the active-avoidance task was positively associated with angling vulnerability, as individuals captured by anglers also successfully shuttled on nearly twice as many trials as uncaptured fish. Proactivity was not associated with angling vulnerability or learning performance. These results indicate that a fast cognitive strategy may be maladaptive for fish populations subjected to angling. In addition, because cognitive performance is heritable, fisheries selection based on cognitive traits could cause an evolutionary shift toward slow learning strategies in exploited populations.
Individual behavioral and cognitive traits can be linked with fitness, especially in human-altered environments. For many freshwater fish, recreational angling by humans poses a major threat, with some individual fish being more vulnerable to capture than others. However, no work has defined whether cognitive traits are linked with an individual’s vulnerability. To address this, we conducted a study examining if learning performance is linked to angling vulnerability in largemouth bass, a popular sportfish species. We found that fish that learned to associate a light with a negative stimulus (chasing with a net) and successfully avoid chasing were more likely to be caught in an angling trial. This means that, for targeted species, a fast learning strategy is disadvantageous, and that heavily exploited populations could experience evolutionary shifts toward slower learning speed due to the selective capture of fast-learning individuals.
KeywordsCognitive syndromes Behavioral syndromes Fisheries-induced evolution Learning performance Coping styles
The authors of this paper acknowledge Justin Rondón, who assembled the arena setup for this study and assisted with data collection during the active-avoidance learning task. The authors also acknowledge Lisa Mitchem, who provided helpful feedback and assistance during the planning of this project. The authors also thank the two anonymous reviewers who provided comments that resulted in substantial improvements to the manuscript.
This study was funded by a grant through the United States Fish and Wildlife Service’s Sport Fish Restoration program; project F-69-R to J.A.S.
Compliance with ethical standards
This work was supported by Federal Aid in Sport Fish Restoration Project via the United States Fish and Wildlife Service, project F-69-R to J.A.S. All experimental procedures were approved by and conducted in accordance with the University of Illinois Institutional Animal Care and Use Committee (IACUC), protocol no. 17065. All aspects of the manuscript were produced by the authors, with no permission needed for any material from other parties.
Conflict of interest
The authors declare that they have no conflict of interest.
- Boulton K, Couto E, Grimmer AJ, Earley RL, Canario AVM, Wilson AJ, Walling CA (2015) How integrated are behavioral and endocrine stress response traits? A repeated measures approach to testing the stress-coping style model. Ecol Evol 5:618–633. https://doi.org/10.1002/ece3.1395 CrossRefPubMedPubMedCentralGoogle Scholar
- Castanheira MF, Herrera M, Costas B, Conceicao LEC, Martins CIM (2013) Linking cortisol responsiveness and aggressive behaviour in gilthead seabream Sparus aurata: indication of divergent coping styles. Appl Anim Behav Sci 143:75–81. https://doi.org/10.1016/j.applanim.2012.11.008 CrossRefGoogle Scholar
- Chivers DP, Smith RJF (1995) Free-living fathead minnows rapidly learn to recognize pike as predators. J Fish Biol 46:949–954. https://doi.org/10.1111/j.1095-8649.1995.tb01399.x CrossRefGoogle Scholar
- Edeline E, Carlson SM, Stige LC, Winfield IJ, Fletcher JM, James JB, Haugen TQ, Vollestad LA, Stenseth NC (2007) Trait changes in a harvested population are driven by a dynamic tug-of-war between natural and harvest selection. P Natl Acad Sci USA 104:15799–15804. https://doi.org/10.1073/pnas.0705908104 CrossRefGoogle Scholar
- Hessenauer JM, Vokoun JC, Suski CD, Davis J, Jacobs R, O'Donnell E (2015) Differences in the metabolic rates of exploited and unexploited fish populations: a signature of recreational fisheries induced evolution? PLoS One 10:e0128336. https://doi.org/10.1371/journal.pone.0128336 CrossRefPubMedPubMedCentralGoogle Scholar
- Jorgensen C, Enberg K, Dunlop ES, Arlinghaus R, Boukal DS, Brander K, Ernande B, Gardmark AG, Johnston F, Matsumura S, Pardoe H, Raab K, Silva A, Vainikka A, Dieckmann U, Heino M, Rijnsdorp AD (2007) Ecology - managing evolving fish stocks. Science 318:1247–1248. https://doi.org/10.1126/science.1148089 CrossRefPubMedGoogle Scholar
- Koeck B, Závorka L, Aldvén D, Naslund J, Arlinghaus R, Thornqvist P, Winberg S, Bjornsson BT, Johnsson JI (2018) Angling selects against active and stress-resilient phenotypes in rainbow trout. Can J Fish Aquat Sci. (published online. https://doi.org/10.1139/cjfas-2018-0085, https://doi.org/10.1139/cjfas-2018-0085)
- Koolhaas JM, Korte SM, de Boer SF, Van der Vegt BG, Van Reenen CG, Hopster H, De Jong IC, Ruis MA, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935. https://doi.org/10.1016/S0149-7634(99)00026-3 CrossRefPubMedGoogle Scholar
- Mota Silva PI, Martins CIM, Engrola S, Marino G, Overli O, Conceicao LEC (2010) Individual differences in cortisol levels and behaviour of Senegalese sole (Solea senegalensis) juveniles: evidence for coping styles. Appl Anim Behav Sci 124:75–81. https://doi.org/10.1016/j.applanim.2010.01.008 CrossRefGoogle Scholar
- Nieman DA, Clady MD, Gebhart GE (1979) Sexual maturity of small yearling largemouth bass in Oklahoma. Proc Okla Acad Sci 59:51–52Google Scholar
- Redpath TD, Cooke SJ, Suski CD, Arlinghaus R, Couture P, Wahl DH, Philipp DP (2010) The metabolic and biochemical basis of vulnerability to recreational angling after three generations of angling-induced selection in a teleost fish. Can J Fish Aquat Sci 67:1983–1992. https://doi.org/10.1139/F10-120 CrossRefGoogle Scholar
- Revelle W (2018) psych: Procedures for Personality and Psychological Research, Northwestern University, Evanston, Illinois, USA. https://CRAN.R-project.org/package=psychVersion=1.8.10