Abstract
Navigating risk of predation is a major driver of behavioral decision-making in small fishes. Fish use personal information from olfactory and visual indicators of risk, and also rely upon social cues to inform behavioral trade-offs between risk avoidance and fitness-positive activities such as foraging. Here, fathead minnows (Pimephales promelas), were captured, clipped and released at 48 field sites chemically labeled with either fathead minnow alarm cue (high risk) or water (low risk). We removed the chemical label after 2 h, then monitored area use by clipped and non-clipped fish. In addition, a shoal was placed in traps in half of the risky and half of the safe locations as a visual social cue of safety. We caught 2919 fish in the first sample, of which 594 were fathead minnows. These were clipped and released. The second sample caught 1500 fish, of which 164 were fathead minnows including 11 bearing marks from the first sample. Non-clipped fathead minnows and northern redbelly dace in the general community, which lacked personal information about risk status associated with trap sites, avoided areas previously labeled with alarm cues for at least 2 h after the source of alarm cue was removed, unless an experimental shoal was present at the risky site, in which case they joined the shoal in the trap. Clipped fathead minnows with direct personal knowledge of risk showed a significant shift away from areas labeled with conspecific alarm cue and a significant attraction toward sites seeded with a shoal. Moreover, unlike non-clipped fish in the general community, clipped fathead minnows were not influenced by experimental shoals at sites previously labeled as risky. These data indicate that the influence of social cues of safety depend on whether individual minnows have access to recent personal information about risk.
Significance statement
Animals use information for making decisions about when and where it is safe. Information comes from direct personal experience and/or from observing the behavior of others (social cues). In this study minnows with different levels of personal knowledge about risk responded differently to social cues about safety. Naïve minnows relied on social cues while minnows with personal knowledge of risk associated with an area ignored social cues. This study, conducted on free-living fish in a natural population, show how fish use information about risk and safety when the risk of predation is highly variable in space and time.
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Amlacher J, Dugatkin LA (2005) Preference for older over younger models during mate-choice copying in young guppies. Ethol Ecol Evol 17:161–169. https://doi.org/10.1080/08927014.2005.9522605
Barkhymer AJ, Garrett SG, Wisenden BD (2018) Olfactorily-mediated cortisol response to chemical alarm cues in zebrafish Danio rerio. J Fish Biol 95:287–292. https://doi.org/10.1111/jfb.13860
Barrera JP, Chong L, Judy KN, Blumstein DT (2011) Reliability of public information: predators provide more information about risk than conspecifics. Anim Behav 81:779–787. https://doi.org/10.1016/j.anbehav.2011.01.010
Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525. https://doi.org/10.1093/icb/42.3.517
Brosnan S, Earley RL, Dugatkin LA (2003) Observational learning and predator inspection in guppies (Poecilia reticulata). Ethology 109:823e833. https://doi.org/10.1046/j.0179-1613.2003.00928.x
Brown GE, Godin J-GJ (1999) Who dares, learns: chemical inspection behaviour and acquired predator recognition in a characin fish. Anim Behav 57:475–481. https://doi.org/10.1006/anbe.1998.1017
Brown GE, Elvidge CK, Ramnarine I, Chivers DP, Ferrari MC (2014) Personality and the response to predation risk: effects of information quantity and quality. Anim Cogn 17:1063–1069. https://doi.org/10.1007/s10071-014-0738-z
Carneiro VCL, Delicio HC, Barreto RE (2022) Effects of stress-associated odor on ventilation rate and feeding performance in Nile tilapia. J Appl Anim Welf Sci 25:1–11. https://doi.org/10.1080/10888705.2022.2149268
Chivers DP, Dixson DL, White JR, McCormick MI, Ferrari MC (2013) Degradation of chemical alarm cues and assessment of risk throughout the day. Ecol Evol 3:3925–3934. https://doi.org/10.1002/ece3.760
Coolen I, Bergen YV, Day RL, Laland KN (2003) Species difference in adaptive use of public information in sticklebacks. Proc R Soc Lond B 270:2413–2419. https://doi.org/10.1098/rspb.2003.2525
Coolen I, Ward AJ, Hart PJ, Laland KN (2005) Foraging nine-spined sticklebacks prefer to rely on public information over simpler social cues. Behav Ecol 16:865–870. https://doi.org/10.1093/beheco/ari064
Crane AL, Ferrari MC (2013) Social learning of predation risk: a review and prospectus. In: Clark KB (ed) Social learning theory: phylogenetic considerations across animal, plant, and microbial taxa. Nova Publications, New York, pp 53–82
Crane AL, Ferrari MC (2015) Minnows trust conspecifics more than themselves when faced with conflicting information about predation risk. Anim Behav 100:184–190. https://doi.org/10.1016/j.anbehav.2014.12.002
Dall SR, Giraldeau LA, Olsson O, McNamara JM, Stephens DW (2005) Information and its use by animals in evolutionary ecology. Trends Ecol Evol 20:187–193. https://doi.org/10.1016/j.tree.2005.01.010
Danchin E, Giraldeau LA, Valone TJ, Wagner RH (2004) Public information: from nosy neighbors to cultural evolution. Science 305:487–491. https://doi.org/10.1126/science.1098254
Dugatkin LA, Godin J-GJ (1992a) Reversal of female mate choice by copying in the guppy (Poecilia reticulata). Proc R Soc Lond B 249:179–184. https://doi.org/10.1098/rspb.1992.0101
Dugatkin LA, Godin J-GJ (1992b) Predator inspection, shoaling and foraging under predation hazard in the Trinidadian guppy, Poecilia reticulata. Environ Biol Fish 34:265–276. https://doi.org/10.1007/BF00004773
Dugatkin LA, Godin J-GJ (1993) Female mate copying in the guppy (Poecilia reticulata): age-dependent effects. Behav Ecol 4:289–292. https://doi.org/10.1093/beheco/4.4.289
Faulkner AE, Holstrom IE, Molitor SA, Hanson ME, Shegrud WR, Gillen JC, Willard SJ, Wisenden BD (2017) Field verification of chondroitin sulfate as a putative component of chemical alarm cue in wild populations of fathead minnows (Pimephales promelas). Chemoecology 27:233–238. https://doi.org/10.1007/s00049-017-0247-z
Ferrari MCO, Messier F, Chivers DP (2007) Degradation of chemical alarm cues under natural conditions: risk assessment by larval woodfrogs. Chemoecology 17:263–266. https://doi.org/10.1007/s00049-007-0381-0
Ferrari MC, Wisenden BD, Chivers DP (2010) Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88:698–724. https://doi.org/10.1139/Z10-029
Feyten LEA, Crane AL, Ramnarine IW, Brown GE (2021) Predation risk shapes the use of conflicting personal risk and social safety information in guppies. Behav Ecol 32:1296–1305. https://doi.org/10.1093/beheco/arab096
Frechette JL, Sieving KE, Boinski S (2014) Social and personal information use by squirrel monkeys in assessing predation risk. Am J Primatol 76:956–966. https://doi.org/10.1002/ajp.22283
Friesen RG, Chivers DP (2006) Underwater video reveals strong avoidance of chemical alarm cues by prey fishes. Ethology 112:339–345. https://doi.org/10.1111/j.1439-0310.2006.01160.x
Gibson AK, Mathis A (2006) Opercular beat rate for rainbow darters Etheostoma caeruleum exposed to chemical stimuli from conspecific and heterospecific fishes. J Fish Biol 69:224–232. https://doi.org/10.1111/j.1095-8649.2006.01102.x
Hogan KE, Laskowski KL (2013) Indirect information transfer: three-spined sticklebacks use visual alarm cues from frightened conspecifics about an unseen predator. Ethology 119:999–1005. https://doi.org/10.1111/eth.12143
Kelley JL (2008) Assessment of predation risk by prey fishes. In: Magnhagen C, Braithwaite VA, Forsgren E, Kapoor BG (eds) Fish Behaviour. Enfield Science Publications, Boca Raton, pp 269–302
Kendal RL, Coolen I, van Bergen Y, Laland KN (2005) Trade-offs in the adaptive use of social and asocial learning. Adv Stud Behav 35:333–379. https://doi.org/10.1016/S0065-3454(05)35008-X
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640. https://doi.org/10.1139/z90-092
Luttbeg B, Ferrari MC, Blumstein DT, Chivers DP (2020) Safety cues can give prey more valuable information than danger cues. Am Nat 195:636–648. https://doi.org/10.1086/707544
Mathis A, Smith RJF (1992) Avoidance of areas marked with a chemical alarm substance by fathead minnows (Pimephales promelas) in a natural habitat. Can J Zool 70:1473–1476. https://doi.org/10.1139/z92-203
Mathis A, Smith RJF (1993) Chemical alarm signals increase the survival time of fathead minnows (Pimephales promelas) during encounters with northern pike (Esox lucius). Behav Ecol 4:260–265. https://doi.org/10.1093/beheco/4.3.260
Mathis A, Chivers DP, Smith RJF (1996) Cultural transmission of predator recognition in fishes: intraspecific and interspecific learning. Anim Behav 51:185–201. https://doi.org/10.1006/anbe.1996.0016
Mirza RS, Chivers DP (2001) Chemical alarm signals enhance survival of brook charr (Salvelinus fontinalis) during encounters with predatory chain pickerel (Esox niger). Ethology 107:989–1005. https://doi.org/10.1046/j.1439-0310.2001.00729.x
Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268. https://doi.org/10.1023/A:1008924418720
Pan T, Gladen K, Duncan E, Cotner S, Cotner J, Wisenden BD (2016) Bold, sedentary fathead minnows have more parasites. Zebrafish 13:248–255. https://doi.org/10.1089/zeb.2015.1185
Pellegrini AFA, Wisenden BD, Sorensen PW (2010) Bold minnows consistently approach danger in the field and lab in response to either chemical or visual indicators of predation risk. Behav Ecol Sociobiol 64:381–387. https://doi.org/10.1007/s00265-009-0854-y
Pereira RT, Leutz JDACM, Valença-Silva G, Barcellos LJG, Barreto RE (2017) Ventilation responses to predator odors and conspecific chemical alarm cues in the frillfin goby. Physiol Behav 179:319–323. https://doi.org/10.1016/j.physbeh.2017.06.023
Pitcher TJ, Green DA, Magurran AE (1986) Dicing with death: predator inspection behaviour in minnow shoals. J Fish Biol 28:439–448. https://doi.org/10.1111/j.1095-8649.1986.tb05181.x
Pollock MS, Chivers DP, Mirza RS, Wisenden BD (2003) Fathead minnows, Pimephales promelas, learn to recognize chemical alarm cues of introduced brook stickleback, Culaea inconstans. Environ Biol Fish 66:313–319. https://doi.org/10.1023/A:1023905824660
Sanches FHC, Miyai CA, Pinho-Neto CF, Barreto RE (2015) Stress responses to chemical alarm cues in Nile tilapia. Physiol Behav 149:8–13. https://doi.org/10.1016/j.physbeh.2015.05.010
Schmidt KA, Dall SR, Van Gils JA (2010) The ecology of information: an overview on the ecological significance of making informed decisions. Oikos 119:304–316. https://doi.org/10.1111/j.1600-0706.2009.17573.x
Schmitt MH, Stears K, Shrader AM (2016) Zebra reduce predation risk in mixed-species herds by eavesdropping on cues from giraffe. Behav Ecol 27:1073–1077. https://doi.org/10.1093/beheco/arw015
Smith RJF (1992) Alarm signals in fishes. Rev Fish Biol Fish 2:33–63. https://doi.org/10.1007/BF00042916
Sutrisno R, Schotte PM, Schultz SK, Wisenden BD (2014) Fin-flicking behaviour as a means of cryptic olfactory sampling under threat of predation. Ecol Freshw Fish 23:656–658. https://doi.org/10.1111/eff.12115
Swanner ED, Harding C, Akam S et al (2022) Four meromictic lakes in Itasca State Park, Minnesota, U.S.A. EarthArXiv. https://doi.org/10.31223/X5DW84
Templeton JJ, Giraldeau L-A (1996) Vicarious sampling: the use of personal and public information by starlings foraging in a simple patchy environment. Behav Ecol Sociobiol 38:105–114. https://doi.org/10.1007/s002650050223
Valone TJ (2007) From eavesdropping on performance to copying the behavior of others: a review of public information use. Behav Ecol Sociobiol 62:1–14. https://doi.org/10.1007/s00265-007-0439-6
van Bergen Y, Coolen I, Laland KN (2004) Nine-spined sticklebacks exploit the most reliable source when public and private information conflict. Proc R Soc Lond B 271:957–962. https://doi.org/10.1098/rspb.2004.2684
Webster MM, Laland KN (2008) Social learning strategies and predation risk: minnows copy only when using private information would be costly. Proc R Soc Lond B 275:2869–2876. https://doi.org/10.1098/rspb.2008.0817
Wisenden B (2008) Active space of chemical alarm cue in natural fish populations. Behaviour 145:391–407. https://doi.org/10.1163/156853908783402920
Wisenden BD, Barbour K (2005) Antipredator responses to skin extract of redbelly dace, Phoxinus eos, by free-ranging populations of redbelly dace and fathead minnows, Pimephales promelas. Environ Biol Fish 72:227–233. https://doi.org/10.1007/s10641-004-8753-6
Wisenden BD, Chivers DP (2006) The role of public chemical information in antipredator behaviour. In: Ladich F, Collins SP, Moller P, Kapoor BG (eds) Communication in fishes. Science Publishers, Enfield, NH, pp 259–278
Wisenden BD, Chivers DP, Smith RJF (1994) Risk-sensitive habitat use by brook stickleback (Culaea inconstans) in areas associated with minnow alarm pheromone. J Chem Ecol 20:2975–2983. https://doi.org/10.1007/BF02098403
Wisenden BD, Chivers DP, Brown GE, Smith RJF (1995a) The role of experience in risk assessment: avoidance of areas chemically labelled with fathead minnow alarm pheromone by conspecifics and heterospecifics. Écoscience 2:116–122. https://doi.org/10.1080/11956860.1995.11682275
Wisenden BD, Chivers DP, Smith RJF (1995b) Early warning in the predation sequence: a disturbance pheromone in Iowa darters (Etheostoma exile). J Chem Ecol 21:1469–1480. https://doi.org/10.1007/BF02035146
Wisenden BD, Pollock MS, Tremaine RJ, Webb JM, Wismer ME, Chivers DP (2003) Synergistic interactions between chemical alarm cues and the presence of conspecific and heterospecific fish shoals. Behav Ecol Sociobiol 54:485–490. https://doi.org/10.1007/s00265-003-0653-9
Wisenden BD, Vollbrecht KA, Brown JL (2004) Is there a fish alarm cue? Affirming evidence from a wild study. Anim Behav 67:59–67. https://doi.org/10.1016/j.anbehav.2003.02.010
Wisenden BD, Binstock CL, Knoll KE, Linke AJ, Demuth BS (2010) Risk-sensitive information gathering by cyprinids following release of chemical alarm cues. Anim Behav 79:1101–1107. https://doi.org/10.1016/j.anbehav.2010.02.004
Wisenden BD, Andebrhan AA, Anderson CM et al (2023) Olfactory cues of risk and visual cues of safety interact with sympatry and phylogeny in shaping behavioral responses by littoral fishes. Behav Ecol Sociobiol 77:91. https://doi.org/10.1007/s00265-023-03367-x
Wisenden BD (2014) Chemical cues that indicate risk of predation. In: Sorensen PW, Wisenden BD (eds) Fish pheromones and related cues. Wiley-Blackwell Press, Hoboken, NJ, 131–148. https://doi.org/10.1002/9781118794739.ch6
Wisenden BD, Rugg ML, Korpi NL, Fuselier LC (2009) Lab and field estimates of active time of chemical alarm cues of a cyprinid fish and an amphipod crustacean. Behaviour 146:1423–1442. https://doi.org/10.1163/156853909X440998
Acknowledgments
We are grateful to Lindsey Blake, Daniel Brumm, and Jonathan and Emily Gaenzle Schilling for logistical support at the University of Minnesota Itasca Biological Field Station. We thank Kui Hu, Mariappan Sekhar and Michael Warne for constructive comments on early drafts of the manuscript. Comments from two anonymous reviewers further improved clarity and impact of the manuscript.
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Funding for supplies was provided by the Itasca Biological Field Station, College of Biological Sciences, University of Minnesota. BJS and MIMJ were supported by the Environmental & Conservation Sciences Graduate program, North Dakota State University.
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All applicable international, national, and/or institutional guidelines for the use of animals were followed. All protocols used in this study were reviewed and approved by the University of Minnesota Institutional Animal Care and Use Committee, protocol 2103-38900A. Fish collection was conducted State of Minnesota Department of Natural Resources Special Permit Number 35313.
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Wisenden, B.D., Adkins, C.M., Campbell, S.A. et al. When is it safe to go home? Post-predation assessment of risk and safety when personal information conflicts with social cues. Behav Ecol Sociobiol 78, 59 (2024). https://doi.org/10.1007/s00265-024-03475-2
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DOI: https://doi.org/10.1007/s00265-024-03475-2