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Effects of early-life experience on innovation and problem-solving in captive coyotes

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Abstract

Early-life experience often shapes behaviors like innovation and exploration. These behaviors are important to animals encountering novel food resources in diverse habitats, such as mesocarnivores in urban areas. To understand if early-life experiences impact later-life behavior, we examined how coyotes (Canis latrans) responded to a multi-access puzzle box at two life stages: pup (~ 7 weeks) and dispersal (~ 10 months). We first exposed pups, still living with their parents and littermates, to a baited puzzle box. At dispersal age, we again tested both these pups and an age-matched control group that was not exposed to the puzzle box as pups, both as individuals and with their pair-mate. We quantified problem-solving capability, latency to approach, and time spent in proximity to the puzzle box. Most pup litters solved two of the three access points, but no dispersal-age coyotes solved any access point. The amount of time dispersal-age coyotes spent near the box during pair-testing increased with (1) more time spent near the box during single-testing, (2) more time their pair-mate spent near the box during pair-testing, and (3) if their pair-mate came from a litter that previously solved the box. These results suggest that early-life experience and social interactions influence exploratory behavior at dispersal age, but coyotes exhibit increased avoidance behavior at this life stage, which corresponds with the life stage that overall survivorship decreases. Our study provides insight into how early-life experiences shape adult behavior in mesocarnivores.

Significance statement

Exploratory behaviors, including risk-taking and problem-solving, are likely important characteristics for urban-dwelling species, such as coyotes, but how development and sociality influence these traits is poorly understood. Therefore, we presented coyotes with a puzzle box as pups with their littermates and again at dispersal age, both individually and with their pair-mate. Three of four litters solved the puzzle box when housed with their littermates, but no coyotes solved at dispersal age when housed alone or with their pair-mate. Notably, there was a general decrease in exploratory behavior and innovation from pup to dispersal age. However, we found that previous experiences during puzzle-box trials positively influenced the amount of time coyote pairs spent near the puzzle box at dispersal age. Our results suggest that pursuing food resources in novel situations may be constrained by developmental processes, possibly in response to prioritizing future opportunities to reproduce.

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References

  • Audet JN, Ducatez S, Lefebvre L (2016) The town bird and the country bird: problem solving and immunocompetence vary with urbanization. Behav Ecol 27:637–644

    Article  Google Scholar 

  • Auersperg AMI, von Bayern AMP, Gajdon GK, Huber L, Kacelnik A (2011) Flexibility in problem solving and tool use of kea and New Caledonian crows in a multi access box paradigm. PLoS ONE 6:e20231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bateman PW, Fleming PA (2012) Big city life: carnivores in urban environments. J Zool 287(1):1–23

    Article  Google Scholar 

  • Baxter-Gilbert J, Riley JL, Whiting MJ (2019) Bold new world: urbanization promotes an innate behavioral trait in a lizard. Behav Ecol Sociobiol 73:105

    Article  Google Scholar 

  • Behr DM, McNutt JW, Ozgul A, Cozzi G (2020) When to stay and when to leave? Proximate causes of dispersal in an endangered social carnivore. J Anim Ecol 89(10):2356–2366

    Article  PubMed  Google Scholar 

  • Bonnet X, Naulleau G, Shine R (1999) The dangers of leaving home: dispersal and mortality in snakes. Biol Conserv 89:39–50

    Article  Google Scholar 

  • Boves TJ, Belthoff JR (2012) Roadway mortality of barn owls in Idaho, USA. J Wildl Manag 76(7):1381–1392

    Article  Google Scholar 

  • Breck SW, Poessel SA, Mahoney P, Young JK (2019) The intrepid urban coyote: a comparison of bold and exploratory behavior in coyotes from urban and rural environments. Sci Rep 9:2104

    Article  PubMed  PubMed Central  Google Scholar 

  • Bremner-Harrison S, Prodohl PA, Elwood RW (2004) Behavioural trait assessment as a release criterion: Boldness predicts early death in a reintroduction programme of captive-bred swift fox (Vulpesvelox). Anim Conserv 7:313–320

    Article  Google Scholar 

  • Brooks J, Kays R, Hare B (2020) Coyotes living near cities are bolder: implications for dog evolution and human-wildlife conflict. Behaviour 157:289–313

    Article  Google Scholar 

  • Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Maechler M, Bolker BM (2017) GlmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400

    Article  Google Scholar 

  • Brubaker L, Dasgupta S, Bhattacharjee D, Bhadra A, Udell MAR (2017) Differences in problem-solving between canid populations: do domestication and lifetime experience affect persistence? Anim Cogn 20:717–723

    Article  PubMed  Google Scholar 

  • Chow PKY, Lea SEG, Hempel de Ibarra N, Robert T (2017) How to stay perfect: the role of memory and behavioural traits in an experienced problem and a similar problem. Anim Cogn 20:941–952

    Article  PubMed  PubMed Central  Google Scholar 

  • Daniels SE, Fanelli RE, Gilbert A, Benson-Amram S (2019) Behavioral flexibility of a generalist carnivore. Anim Cogn 22:387–396

    Article  PubMed  Google Scholar 

  • Davison RP (1980) The effect of exploitation on some parameters of Coyote populations. All Graduate Theses and Dissertations, pp 6990. https://digitalcommons.usu.edu/etd/6990

  • Drea CM, Carter AN (2009) Cooperative problem solving in a social carnivore. Anim Behav 78:967–977

    Article  Google Scholar 

  • Ducatez S, Sol D, Sayol F, Lefebvre L (2020) Behavioural plasticity is associated with reduced extinction risk in birds. Ecol Evol 4:788–793

    Google Scholar 

  • Duguid S, Melis AP (2020) How animals collaborate: underlying proximate mechanisms. Wiley Interdisc Rev Cogn Sci 11:1–18

    Google Scholar 

  • Fidino M, Gallo T, Lehrer EW et al (2020) Landscape-scale differences among cities alter common species’ responses to urbanization. Ecol Appl 31:e02253

    PubMed  Google Scholar 

  • Forss SIF, Koski SE, van Schaik CP (2017) Explaining the paradox of neophobic explorers: the social information hypothesis. Intern J Primat 38:799–822

    Article  Google Scholar 

  • Fox AMW (1972) Socio-ecological implications of individual differences in wolf litters: a developmental and evolutionary perspective. Behaviour 41:298–313

    Article  Google Scholar 

  • Friard O, Gamba M (2016) BORIS: A free versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol 7:1325–1330

    Article  Google Scholar 

  • Gehrt SD (2006) Urban coyote ecology and management. Ohio State University Extension, Bulletin 929, Columbus

  • Gese EM, Ruff RL, Crabtree RL (1996) Social and nutritional factors influencing the dispersal of resident coyotes. Anim Behav 52:1025–1043

    Article  Google Scholar 

  • Greenberg JR, Holekamp KE (2017) Human disturbance affects personality development in a wild carnivore. Anim Behav 132:303–312

    Article  Google Scholar 

  • Hamer AJ, Mcdonnell MJ (2010) The response of herpetofauna to urbanization: Inferring patterns of persistence from wildlife databases. Austral Ecol 35:568–580

    Article  Google Scholar 

  • Harris CE, Knowlton FF (2001) Differential responses of coyotes to novel stimuli in familiar and unfamiliar settings. Can J Zool 79:2005–2013

    Article  Google Scholar 

  • Harrison D (1992) Dispersal characteristics of juvenile coyotes in Maine. J Wildlife Manage 56:128–138

    Article  Google Scholar 

  • Hartig F (2022) DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models, version 0.4.5. https://cran.r-project.org/package=DHARMa. Accessed 8 September 2022

  • Healy K, Ezard THG, Jones OR, Salguero-Gómez R, Buckley YM (2019) Animal life history is shaped by the pace of life and the distribution of age-specific mortality and reproduction. Ecol Evol 3:1217–1224

    Google Scholar 

  • Henke-von der Malsburg J, Kappeler PM, Fichtel C (2020) Linking ecology and cognition: does ecological specialization predict cognitive test performance? Behav Ecol Sociobiol 74:154

    Article  Google Scholar 

  • Hody JW, Kays R (2018) Mapping the expansion of coyotes (Canislatrans) across North and central America. ZooKeys 2018:81–97

    Article  Google Scholar 

  • Holekamp KE (1984) Natal dispersal in Belding’s ground squirrels (Spermophilus beldingi). Behav Ecol Sociobiol 16(1):21–30

    Article  Google Scholar 

  • Holzman S, Conroy J, Davidson R (1992) Diseases, parasites and survival of coyotes in south-central Georgia. J Wildlife Dis 28:572–580

    Article  CAS  Google Scholar 

  • Jacobson SL, Puitiza A, Snyder R, Sheppard A, Plotnik JM (2022) Persistence is key: Investigating innovation and problem solving by Asian elephants using a novel multi-access box. Anim Cogn 25:657–669

    Article  PubMed  Google Scholar 

  • Johnson CA, Fryxell JM, Thompson ID, Baker JA (2009) Mortality risk increases with natal dispersal distance in American martens. Proc R Soc Lond B 276:3361–3367

    Google Scholar 

  • Johnson WE, Balph DF (1990) Resource acquisition in the presence of novelty by coyotes of different rank. J Wildlife Manage 54:582–586

    Article  Google Scholar 

  • Johnson-Ulrich L, Johnson-Ulrich Z, Holekamp K (2018) Proactive behavior, but not inhibitory control, predicts repeated innovation by spotted hyenas tested with a multi-access box. Anim Cogn 21:379–392

    Article  PubMed  Google Scholar 

  • Johnson-Ulrich L, Yirga G, Strong RL, Holekamp KE (2021) The effect of urbanization on innovation in spotted hyenas. Anim Cogn 24:1027–1038

    Article  PubMed  Google Scholar 

  • Klump B, Martin J, Wild S, Horsch J, Major R, Aplin L (2021) Innovation and geographic spread of a complex foraging culture in an urban parrot. Science 373:456–460

    Article  CAS  PubMed  Google Scholar 

  • Kujiper DPJ, Sahlén E, Elmhagen B, Chamaillé-Jammes S, Sand H, Lone K, Cromsigt JPGM (2016) Paws without claws? Ecological effects of large carnivores in anthropogenic landscapes. Proc R Soc B 283:20161625

    Article  Google Scholar 

  • Kurvers RHJM, Nolet BA, Prins HHT, Ydenberg RC, van Oers K (2012) Boldness affects foraging decisions in barnacle geese: an experimental approach. Behav Ecol 23:1155–1161

    Article  Google Scholar 

  • Ladds Z, Hoppitt W, Boogert NJ (2017) Social learning in otters. R Soc Open Sci 4:170489

    Article  PubMed  PubMed Central  Google Scholar 

  • Larson RN, Brown JL, Karels T, Riley SPD (2020) Effects of urbanization on resource use and individual specialization in coyotes (Canislatrans) in southern California. PLoS ONE 15:e0228881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lazzaroni M, Range F, Bernasconi L, Darc L, Holtsch M, Massimei R, Rao A, Marshall-Pescini S (2019) The role of life experience in affecting persistence: a comparative study between free-ranging dogs, pet dogs and captive pack dogs. PLoS ONE 14:e0214806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li LL, Plotnik JM, Xia SW, Meaux E, Quan RC (2021) Cooperating elephants mitigate competition until the stakes get too high. PLoS Biol 19:3001391

    Article  Google Scholar 

  • Massemin S, Maho YL, Handrich Y (1998) Seasonal pattern in age, sex and body condition of Barn Owls Tyto alba killed on motorways. Ibis 140(1):70–75

    Article  Google Scholar 

  • Mazza V, Guenther A (2021) City mice and country mice: innovative problem solving in rural and urban noncommensal rodents. Anim Behav 172:197–210

    Article  Google Scholar 

  • McDonnell MJ, Hahs AK (2015) Adaptation and adaptedness of organisms to urban environments. Annu Rev Ecol Evol S 46:261–280

    Article  Google Scholar 

  • Mettler AE, Shivik JA (2007) Dominance and neophobia in coyote (Canis latrans) breeding pairs. Appl Anim Behav Sci 102:85–94

    Article  Google Scholar 

  • Michelena P, Sibbald AM, Erhard HW, McLeod JE (2009) Effects of group size and personality on social foraging: the distribution of sheep across patches. Behav Ecol 20:145–152

    Article  Google Scholar 

  • O’Connor VL, Thomas P, Chodorow M, Borrego N (2022) Exploring innovative problem-solving in African lions (Pantheraleo) and snow leopards (Pantherauncia). Behav Process 199:104648

    Article  Google Scholar 

  • Ordeñana MA, Crooks KR, Boydston EE et al (2010) Effects of urbanization on carnivore species distribution and richness. J Mammal 91:1322–1331

    Article  Google Scholar 

  • Parsons MA, Garcia A, Young JK (2022) Scavenging vs hunting affects behavioral traits of an opportunistic carnivore. PeerJ 10:e13366

    Article  PubMed  PubMed Central  Google Scholar 

  • Parsons MA, Newsome TM, Young JK (2022) The consequences of predators without prey. Front Ecol Environ 20:31–39

    Article  Google Scholar 

  • Petelle MB, McCoy DE, Alejandro V, Martin JGA, Blumstein DT (2013) Development of boldness and docility in yellow-bellied marmots. Anim Behav 86:1147–1154

    Article  Google Scholar 

  • Preiszner B, Papp S, Pipoly I, Seress G, Vincze E, Liker A, Bókony V (2017) Problem-solving performance and reproductive success of great tits in urban and forest habitats. Anim Cogn 20:53–63

    Article  PubMed  Google Scholar 

  • R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 9 December 2021

  • Reader SM, Laland KN (eds) (2003) Animal Innovation. Oxford University Press, Oxford

    Google Scholar 

  • Reader SM, Morand-Ferron J, Flynn E (2016) Animal and human innovation: novel problems and novel solutions. Phil Trans R Soc B 371:20150182

    Article  PubMed  PubMed Central  Google Scholar 

  • Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318

    Article  PubMed  Google Scholar 

  • Rowell MK, Pillay N, Rymer TL (2021) Problem solving in animals: proposal for an ontogenetic perspective. Animals 11:866

    Article  PubMed  PubMed Central  Google Scholar 

  • Saliveros AM, Blyth EC, Easter C, Hume GV, McAusland F, Hoppitt W, Boogert NJ (2020) Learning strategies and long-term memory in Asian short-clawed otters (Aonyxcinereus): Learning and memory in otters. R Soc Open Sci 7:201215

    Article  PubMed  PubMed Central  Google Scholar 

  • Schell CJ, Young JK, Lonsdorf EV, Santymire RM, Mateo JM (2018) Parental habituation to human disturbance over time reduces fear of humans in coyote offspring. Ecol Evol 8:12965–12980

    Article  PubMed  PubMed Central  Google Scholar 

  • Schmelz M, Duguid S, Bohn M, Völter CJ (2017) Cooperative problem solving in giant otters (Pteronura brasiliensis) and Asian small-clawed otters (Aonyx cinerea). Anim Cognit 20(6):1107–1114

    Article  Google Scholar 

  • Schuster AC, Carl T, Foerster K (2017) Repeatability and consistency of individual behaviour in juvenile and adult Eurasian harvest mice. Sci Nat 104(3):1–14

    CAS  Google Scholar 

  • Scott JP, Fuller JL (1965) Genetics and the social behavior of the dog. University of Chicago Press, Chicago

    Google Scholar 

  • Seress G, Liker A (2015) Habitat urbanization and its effects on birds. Acta Zool Acad Sci Hungaricae 61:373–408

    Article  Google Scholar 

  • Shivik JA, Palmer GL, Gese EM, Osthaus B (2009) Captive coyotes compared to their counterparts in the wild: does environmental enrichment help? J Appl Anim Welfare Sci 12:223–235

    Article  CAS  Google Scholar 

  • Sol D, Lapiedra O, González-Lagos C (2013) Behavioural adjustments for a life in the city. Anim Behav 85:1101–1112

    Article  Google Scholar 

  • Stanton LA, Bridge ES, Huizinga J, Johnson SR, Young JK, Benson-Amram S (2021) Variation in reversal learning by three generalist mesocarnivores. Anim Cogn 24:555–568

    Article  PubMed  Google Scholar 

  • Stöwe M, Bugnyar T, Heinrich B, Kotrschal K (2006) Effects of group size on approach to novel objects in ravens (Corvuscorax). Ethology 112:1079–1088

    Article  Google Scholar 

  • Therneau TM (2020) Coxme: Mixed effects Cox models. R package version 2.2–16. https://cran.r-project.org/web/packages/coxme/index.html. Accessed 9 December 2021.

  • Tomasello M, Call J (2004) The role of humans in the cognitive development of apes revisited. Anim Cogn 7:213–215

    Article  PubMed  Google Scholar 

  • Torres Ortiz S, Corregidor Castro A, Balsby TJS, Larsen ON (2020) Problem-solving in a cooperative task in peach-fronted conures (Eupsittulaaurea). Anim Cogn 23:265–275

    Article  PubMed  Google Scholar 

  • Turner JW, LaFleur RM, Richardson AT, Holekamp KE (2019) Risk-taking in free-living spotted hyenas is associated with anthropogenic disturbance, predicts survivorship, and is consistent across experimental contexts. Ethology 126:97–110

    Article  Google Scholar 

  • Vrbanec L, Matijević V, Guenther A (2021) Enhanced problem-solving ability as an adaptation to urban environments in house mice. Proc R Soc B 288:20202504

    Article  PubMed  PubMed Central  Google Scholar 

  • Whiten A, van Schaik CP (2007) The evolution of animal ‘cultures’ and social intelligence. Phil Trans R Soc B 362:603–620

    Article  PubMed  PubMed Central  Google Scholar 

  • Windberg L (1996) Coyote responses to visual and olfactory stimuli related to familiarity with an area. Can J Zool 74:2248–2253

    Article  Google Scholar 

  • Windberg L, Anderson HL, Engeman R (1985) Survival of coyotes in southern Texas. J Wildlife Manage 49:301–307

    Article  Google Scholar 

  • Wong BBM, Candolin U (2014) Behavioral responses to changing environments. Behav Ecol 26:665–673

    Article  Google Scholar 

  • Woollard T, Harris S (1990) A behavioural comparison of dispersing and non-dispersing foxes (Vulpes vulpes) and an evaluation of some dispersal hypotheses. J Anim Ecol 1:709–722

    Article  Google Scholar 

  • Wuerz Y, Krüger O (2015) Personality over ontogeny in zebra finches: long-term repeatable traits but unstable behavioural syndromes. Front Zool 12(1):1–4

    Google Scholar 

  • Yoder JM, Marschall EA, Swanson DA (2004) The cost of dispersal: predation as a function of movement and site familiarity in ruffed grouse. Behav Ecol 15:469–476

    Article  Google Scholar 

  • Young JK, Touzot L, Brummer SP (2019) Persistence and conspecific observations improve problem-solving abilities of coyotes. PLoS ONE 14:e0218778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zepeda E, Payne E, Wurth A, Sih A, Gehrt S (2021) Early life experience influences dispersal in coyotes (Canislatrans). Behav Ecol 32:728–737

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank S. Brummer, M. Davis, N. Floyd, S. Keller, A. Merical, C. Gonzalez, and J. Schultz for assisting with animal care and research logistics. K. Palaez, T. Khvtisiashvili, and J. Kruger assisted with coding observation videos. The Young lab and journal reviewers provided feedback that improved the manuscript. This project was funded by the U.S. Department of Agriculture, National Wildlife Research Center. The findings and conclusions in this publication have not been formally disseminated by the U.S. Department of Agriculture and should not be construed to represent any Agency determination or policy. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US government.

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ACG contributed during the investigation and led analysis, writing, reviewing, and editing efforts. MAP contributed during conceptualization, developing methodology, analysis, and reviewing and editing. JKY led funding acquisition and conceptualization and contributed to developing methodology, analysis, reviewing, and editing.

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Correspondence to Julie K. Young.

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Garcia, A.C., Parsons, M.A. & Young, J.K. Effects of early-life experience on innovation and problem-solving in captive coyotes. Behav Ecol Sociobiol 76, 141 (2022). https://doi.org/10.1007/s00265-022-03251-0

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