Abstract
Innovative behavior is considered one of the main factors facilitating the adaptation of animals to urban life. However, the relationship between urbanization and innovativeness is equivocal, perhaps reflecting aspects of urban environments that influence differently the behavioural traits underlying the occurrence of an innovation. In this work, we analysed the variation in innovative problem-solving performance between urban and rural individuals of the Caracara Chimango (Milvago chimango), with the goal of determining which behavioural trait (or combination) most explained such variation. We found that urban raptors outperformed rural ones in their solving speed and solving level (number of solutions) with a multiaccess box. They also showed more persistence, motor flexibility and diversity, as well as higher effectiveness in their solving attempts than rural chimangos. Sex was not an important factor. Urban chimangos showed less neophobia and spent more time exploring the box than rural birds during the initial habituation period, which probably determined the amount of information about the system that each individual had at the beginning of first problem solving trial. This difference in novelty response both directly and indirectly, through its relationship with persistence, motor flexibility and proportion of effective attempts, explained variability in solving performance. All individuals showed a decrease in solving latency, and an increase in solving level with experience, indicating that learning occurred in both raptor groups. This improvement occurred in parallel with changes in the afore-mentioned traits, though the pattern of improvement differed between urban and rural chimangos. We suggest that the characteristics of urban areas modulate the novelty response of chimangos, along with other correlated non-cognitive behavioural traits, which act in combination to increase the chances that novel problems could be quickly solved, and the resulting new behaviours established in city populations of this species.
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References
Aprile G, Bertonatti, C (1996) Manual sobre rehabilitación de fauna. Boletín Técnico FVSA (Fundación Vida Silvestre Argentina), Buenos Aires, Argentina.
Audet JN, Ducatez S, Lefebvre L (2016) The town bird and the country bird: problem solving and immunocompetence vary with urbanization. Behav Ecol 27(2):637–644. https://doi.org/10.1093/beheco/arv201
Benson-Amram S, Holekamp KE (2012) Innovative problem solving by wild spotted hyenas. Proc R Soc B 279(1744):4087–4095. https://doi.org/10.1098/rspb.2012.1450
Benson-Amram S, Weldele ML, Holekamp KE (2013) A comparison of innovative problem-solving abilities between wild and captive spotted hyaenas Crocuta Crocuta. Anim Behav 85(2):349–356. https://doi.org/10.1016/j.anbehav.2012.11.003
Biondi LM, Bó MS, Favero M (2005) Dieta del chimango (Milvago chimango) durante el periodo reproductivo en el sudeste de la provincia de Buenos Aires. Argentina Ornitol Neotrop 16:31–42
Biondi LM, Bó MS, Vassallo AI (2008) Experimental assessment of problem solving by Milvago chimango (Aves: Falconiformes). J Ethol 26:113–118. https://doi.org/10.1007/s10164-007-0035-2
Biondi LM, Bó MS, Vassallo AI (2010) Inter-individual and age differences in exploration, neophobia and problem-solving ability in a Neotropical raptor (Milvago chimango). Anim Cogn. https://doi.org/10.1007/s10071-010-0319-8
Biondi LM, Guido J, Madrid E, Bó MS, Vassallo AI (2013) The effect of age and sex on object exploration and manipulative behavior in a neotropical raptor, the chimango caracara, Milvago chimango. Ethology 119:221–232. https://doi.org/10.1111/eth.12056
Biondi LM, Guido J, Bó MS, Muzio RN, Vassallo AI (2015) The role of stimulus complexity, age and experience in the expression of exploratory behaviour in the Chimango Caracara, Milvago chimango. Anim Cogn 18:139–150. https://doi.org/10.1007/s10071-014-0785-5
Biondi LM, Fuentes GM, Córdoba RS, Bó MS, Cavalli M, Paterlini CA, Castano MV, García GO (2020) Variation in boldness and novelty response between rural and urban predatory birds: The Chimango Caracara, Milvago chimango as study case. Behav Process 173:104064. https://doi.org/10.1016/j.beproc.2020.104064
Cabezas VM, Schlatter RP (1987) Hábitos y comportamiento alimentario de Milvago chimango Vieillot, 1816 (Aves, Falconidae). An Mus Hist Nat Valp 18:131–141
Carrete M, Tella JL, Blanco G, Bertellotti M (2009) Effects of habitat degradation on the abundance, richness and diversity of raptors across Neotropical biomes. Biol Conserv 142(10):2002–2011. https://doi.org/10.1016/j.biocon.2009.02.012
Cauchard L, Boogert NJ, Lefebvre L, Dubois F, Doligez B (2013) Problem solving performance is correlated with reproductive success in a wild bird population. Anim Behav 85:19–26. https://doi.org/10.1016/j.anbehav.2012.10.005
Chow PKY, Lea SEG, Leaver LA (2016) How practice makes perfect: the role of learning, flexibility, and persistence in problem solving efficiency. Anim Behav 112:273–283. https://doi.org/10.1016/j.anbehav.2015.11.014
Christensen RHB (2018) “Ordinal—Regression Models for Ordinal Data.” R package version 2018.8–25. http://www.cran.r-project.org/package=ordinal/.
Cole EF, Morand-Ferron J, Hinks AE, Quinn JL (2012) Cognitive ability influences reproductive life history variation in the wild. Curr Biol 22:808–1812. https://doi.org/10.1016/j.cub.2012.07.051
Cole EF, Quinn JL (2011) Personality and problem-solving performance explain competitive ability in the wild. Proc. R. Soc. B.2791168–1175. http://doi.org/https://doi.org/10.1098/rspb.2011.1539
Daniels SE, Fanelli RE, Gilbert A, Benson-Amram S (2019) Behavioral flexibility of a generalist carnivore. Anim Cogn 22:387–396. https://doi.org/10.1007/s10071-019-01252-7
Diquelou MC, Griffin AS, Sol D (2016) The role of motor diversity in foraging innovations: A cross-species comparison in urban birds. Behav Ecol 27(2):584–591. https://doi.org/10.1093/beheco/arv190
Ducatez S, Audet JN, Lefebvre L (2014) Problem-solving and learning in Carib grackles: individuals show a consistent speed-accuracy trade-off. Anim Cogn 18:485–496. https://doi.org/10.1007/s10071-014-0817-1
Ferguson-Lees J, Christie DA (2001) Raptors of the World. Houghton Mifflin, Harcourt, Boston
Ferrer-Sánchez Y, Rodríguez-Estrella R (2015) Man-made environments relationships with island raptors: endemics do not cope with habitat changes, the case of the island of Cuba. J Biodivers Conserv Bioresour Manag 24:407–425. https://doi.org/10.1007/s10531-014-0819-y
Greenberg R (2003) The role of neophobia and neophilia in the development of innovative behaviour of birds. In: Reader SM, Laland KN (eds) Animal Innovation. Oxford University Press, Oxford, pp 175–196
Griffin AS (2016) Innovativeness as an emergent property: a new alignment of comparative and experimental research on animal innovation. Phil Trans R Soc. https://doi.org/10.1098/rstb.2015.0544
Griffin AS, Diquelou MC (2015) Innovative problem solving in birds: a cross-species comparison of two highly successful passerines. Anim Behav 100:84–94. https://doi.org/10.1016/j.anbehav.2014.11.012
Griffin AS, Guez D (2014) Innovation and problem solving: a review of common mechanisms. Behav Process 109(Pt B):121–134. https://doi.org/10.1016/j.beproc.2014.08.027
Griffin AS, Guez D (2016) Bridging the gap between cross-taxon and within species analyses of behavioral innovations in birds: Making sense of discrepant cognition e innovation relationships and the role of motor diversity. Adv Study Behav 48:1–40. https://doi.org/10.1016/bs.asb.2016.02.001
Griffin AS, Guez D, Lermite F, Patience M (2013) Tracking changing environments: innovators are fast, but not flexible learners. PLoS ONE 8:e84907. https://doi.org/10.1371/journal.pone.0084907
Griffin AS, Diquelou MC, Perea M (2014) Innovative problem solving in birds: a key role of motor diversity. Anim Behav 92:221–227. https://doi.org/10.1016/j.anbehav.2014.04.009
Griffin AS, Netto K, Peneaux C (2017) Neophilia, innovation and learning in an urbanized world: A critical evaluation of mixed findings. Curr Opin Behav Sci 16:15–22. https://doi.org/10.1016/j.cobeha.2017.01.004
Guez D, Griffin AS (2016) Unraveling the key to innovative problem solving: A test of learning versus persistence. Behav Ecol 27(5):1449–1460. https://doi.org/10.1093/beheco/arw055
Guido JM, Biondi LM, Vassallo AI, Muzio RN (2017) Neophobia is negatively related to reversal learning ability in females of a generalist bird of prey, the Chimango Caracara, Milvago chimango. Anim Cogn 20:591–602. https://doi.org/10.1007/s10071-017-1083-9
Kozlovsky DY, Weissgerber EA, Pravosudov VV (2017) What makes specialized food-caching mountain chickadees successful city slickers? Proc r Soc b Biol Sci 284:25–27. https://doi.org/10.1098/rspb.2016.2613
Lefcheck JS (2016) piecewiseSEM: Piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579. https://doi.org/10.1111/2041-210X.12512
Lefebvre L (2011) Taxonomic counts of cognition in the wild. Biol Lett. https://doi.org/10.1098/rsbl.2010.0556
Liker A, Bokony V (2009) Larger groups are more successful in innovative problem-solving in house sparrows. Proc Natl Acad Sci U S A 106(19):7893–7898. https://doi.org/10.1073/pnas.0900042106
Massen JJM, Antonides A, Arnold A-MK, Bionda T, Koski SE (2013) A behavioral view on chimpanzee personality: exploration tendency, persistence, boldness, and tool-orientation measured with group experiments. Am J Primatol 75:947–958. https://doi.org/10.1002/ajp.22159
O’Hara M, Mioduszewska B, von Bayern A, Auesperg A, Bungyar T, Wilkinson A, Huber L, Gajdon GK (2017) The temporal dependence of exploration on neotic style in birds. Sci Rep 7:4742. https://doi.org/10.1038/s41598-017-04751-0
Overington SE, Cauchard L, Cote KA, Lefebvre L (2011) Innovative foraging behaviour in birds: what characterizes an innovator? Behav Process 87(3):274–285. https://doi.org/10.1016/j.beproc.2011.06.002
Papp S, Vincze E, Preiszner B, Liker A, Bókony V (2015) A comparison of problem-solving success between urban and rural house sparrows. Behav Ecol Sociobiol 69:471–480. https://doi.org/10.1007/s00265-014-1859-8
Prasher S, Evans JC, Thompson MJ, Morand-Ferron J (2019) Characterizing innovators: Ecological and individual predictors of problem-solving performance. PLoS ONE 14(6):e0217464. https://doi.org/10.1371/journal.pone.0217464
Ramsey G, Bastian ML, van Schaik C (2007) Animal innovation defined and operationalized. Behav Brain Sci 30:393–407. https://doi.org/10.1017/S0140525X07002373
Reader SM, Laland KN (2003) Animal innovation: an introduction. In: Reader SM, Laland KN (eds) Animal Innovation. Oxford University Press, Oxford, pp 4–35
Reader SM, Morand-Ferron J, Flynn E (2016) Animal and human innovation: novel problems and novel solutions. Phil Trans R Soc. https://doi.org/10.1098/rstb.2015.0182
Shipley B (2002) Cause and correlation in biology: a user’s guide to path analysis, structural equations and causal inference. Cambridge University Press, Cambridge, UK
Shipley B (2009) Confirmatory path analysis in a generalized multilevel context. Ecology 90:363–368. https://doi.org/10.1890/08-1034.1
Sol D, Duncan RP, Blackburn TM, Cassey P, Lefebvre L (2005) Big brains, enhanced cognition, and response of birds to novel environments. Proc Natl Acad Sci U S A 102:5460–5465. https://doi.org/10.1073/pnas.0408145102
Sol D, Griffin AS, Bartomeus I, Boyce H (2011) Exploring or avoiding novel food resources? The novelty conflict in an invasive bird. PLoS ONE 6:e19535. https://doi.org/10.1371/journal.pone.0019535
Sol D, Griffin AS, Bartomeus I (2012) Consumer and motor innovation in the common myna: The role of motivation and emotional responses. Anim Behav 83(1):179–188. https://doi.org/10.1016/j.anbehav.2011.10.024
Sol D, Lapiedra O, González-Lagos C (2013) Behavioural adjustments for a life in the city. Anim Behav 85:1101–1112. https://doi.org/10.1016/j.anbehav.2013.01.023
Sol D, Lapiedra O, Ducatez S (2020) Cognition and Adaptation to Urban Environments. In: Szulkin M, Munshi-South J, Charmantier A (eds) Urban Evolutionary Biology. Oxford University Press, Oxford, pp 253–267
Solaro C, Sarasola JH (2019) Urban living predicts behavioural response in a neotropical raptor. Behav. Process 169:103995. https://doi.org/10.1016/j.beproc.2019.103995
Tebbich S, Griffin AS, Peschl MF, Sterelny K (2016) From mechanisms to function: an integrated framework of animal innovation. Phil Trans R Soc. https://doi.org/10.1098/rstb.2015.0195
Therneau T, Grambsch P, Pankratz VS (2003) Penalized survival models and frailty. J Computational and Graphical Statistics 12:156–175
Therneau T, Grambsch P (2000) Modeling Survival Data: Extending the Cox Model. Springer-Verlag.
Thornton A, Samson J (2012) Innovative problem solving in wild meerkats. Anim Behav 83:1459–1468. https://doi.org/10.1016/j.anbehav.2012.03.018
van Horik JO, Madden JR (2016) A problem with problem solving: Motivational traits, but not cognition, predict success on novel operant foraging tasks. Anim Behav 114:189–198. https://doi.org/10.1016/j.anbehav.2016.02.006
West-Eberhard MJ (2003) Developmental Plasticity and Evolution. Oxford University Press, New York
White CM, Olsen PD, Cliff LF (1994) New world vultures to Guineafowl. In: Del Hoyo J, Sargalat EA (eds) Handbook of the Birds of the World 2. Lynx Editions, Barcelona, pp 216–247
Acknowledgements
We thank Analia Medina and Rodrigo Santiago Córdoba for their assistance during the capturing and managing of raptors. We appreciate the improvements in English usage made by Sanjay Prasher through the Association of Field Ornithologists' program of editorial assistance. This work was conducted with funds provided by the Universidad Nacional de Mar del Plata (EXA 842/17, 15/E795).
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LMB conceived of the project, LMB, GMF and MSB caught birds, LMB and GMF performed the research and the analysis, LMB wrote the first draft of the manuscript and MSB edited it. MSB and LMB provided funding for the research project.
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The capture of raptors adhered to guidelines for the use of animals in research and to the legal requirements of Argentina: Disposition N 45, Exp. N 22500–24126/13, Dirección Contralor y Uso de Recursos Naturales y pesqueros, Ministerio de Asuntos Agrarios de la Provincia de Buenos Aires. The experimental protocol design and the housing and care conditions had the approval of the National University of Mar del Plata Animal Ethics Committee (RD 179/2015), and meets the latest ASAB/ABS ethical guidelines (https://doi.org/10.1016/j.anbehav.2019.11.002). All individuals were released with identifier-coloured bands at their original habitats after complete the experimental tests.
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Appendix
General design of piece-wise structural equation models (psem) proposed to test the direct and indirect effect of several behavioural traits on problem-solving performance. The variable ‘persistence’ was represented by rate of attempts in the model including solving latency as end point, and working time in the case of solving level as model’s endogenous variable
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Biondi, L.M., Fuentes, G. & Susana, M. Behavioural factors underlying innovative problem-solving differences in an avian predator from two contrasting habitats. Anim Cogn 25, 529–543 (2022). https://doi.org/10.1007/s10071-021-01569-2
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DOI: https://doi.org/10.1007/s10071-021-01569-2