Abstract
Prey incorporate information about risk, safety, and the reliability of both of these cues when assessing risk of predation. Here, we report results of an experiment testing avoidance of chemical alarm cues derived from skin extract of blacknose shiners, Notropis heterolepis (BNS), attraction toward a visible shoal of five BNS, and the combination of both, on fishes in Deming Lake where BNS occur. We then repeated the experiment in nearby Budd Lake where BNS do not occur. BNS avoided traps with conspecific alarm cues but did not respond to the presence of BNS shoals. We recorded responses by similar-sized heterospecifics that share predators with BNS to see if they respond to BNS as indicators of risk and safety. Fathead minnows, Pimephales promelas (FHM) avoided traps chemically labeled with BNS alarm cue when a shoal was absent and avoided BNS shoals when traps were labeled with water (control). When both BNS alarm cue and BNS shoal were combined, FHM antipredator response to BNS alarm cue invoked a shoaling response with the BNS shoal in the trap. The more distantly related redbelly dace, Chrosomus eos (RBD), responded weakly to BNS cues in Deming Lake and ignored them in Budd Lake. Non-cyprinid species (brook stickleback Culaea inconstans and pumpkinseed sunfish, Lepomis gibbosus) did not respond to either olfactory or visual cues of BNS in Deming Lake. In Budd Lake, neither avoidance of BNS alarm cue or attraction to BNS shoals surpassed the threshold of statistical significance, indicating a role of ecological familiarity and learned recognition of risk and safety in cross-species reactions to olfactory and visual cues of heterospecifics.
Significance statement
Small fish, such as minnows, avoid areas marked by injury-released chemical cues because these cues are released only in the context of predation and are attracted to groups of fish because shoals offer safety from predation. In this study fathead minnows Pimephales promelas (FHM) avoided alarm cue of blacknose shiners Notropis heterolepis (BNS) in Deming Lake where both species occur but not in Budd Lake where BNS do not occur. FHM were not attracted to BNS shoals in either lake. However, when a shoal of BNS was combined with BNS alarm cue a synergism occurred where antipredator responses to BNS alarm cue induced FHM to seek safety by shoaling with BNS shoals. The synergism occurred in Deming Lake where BNS alarm cue and shoals are ecologically familiar but not in Budd Lake where BNS do not occur. These data show that behavioral responses by prey to olfactory and visual cues are tempered by sympatry (ecological familiarity) and confidence in the reliability of those cues.
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https://datadryad.org/stash/share/9gUG3yDqxV0Cd46kMmi5TqwF_zeN7JQGDk9T0PzLL6k.
Key to variables in dataset: Deming1Budd2 = source lake of catch data, SpongeAlarm1Water2 = chemical content of sponge, JarShoalYes1No2 = whether the jar contained a shoal or not, Set = replicate set within each lake. FHM = number of fathead minnows per trap, FHMrank = rank of fathead minnow catch per trap within lake, RBD = number of northern redbelly dace per trap, rbdrank = rank of redbelly dace catch per trap within lake, BNS = number of blacknose shiners per trap, bnsrank = rank of blacknose shiner catch per trap in Deming Lake, PKS = number of pumpkinseed sunfish per trap, pksrank = rank of pumpkinseed sunfish per trap in Deming Lake, Stickleback = number of brook stickleback per trap, sbrank = rank of stickleback per trap in Deming Lake.
References
Anderson KA, Mathis A (2016) Friends in low places: Responses of a benthic stream fish to intra-prey-guild alarm cues. Ethology 122:954–962. https://doi.org/10.1111/eth.12563
Brown GE, Adrian JC, Smyth E, Leet H, Brennan S (2000) Ostariophysan alarm pheromones: laboratory and field tests of the functional significance of nitrogen oxides. J Chem Ecol 26:139–154. https://doi.org/10.1023/A:1005445629144
Brown GE, Adrian JC, Shih ML (2001) Behavioural responses of fathead minnows to hypoxanthine-3-N-oxide at varying concentrations. J Fish Biol 58:1465–1470. https://doi.org/10.1111/j.1095-8649.2001.tb02301.x
Brunner E, Konietschke F, Pauly M, Puri ML (2017) Rank-based procedures in factorial designs: hypotheses about non-parametric treatment effects. J Roy Stat Soc B 79:1463–1485. https://www.jstor.org/stable/44682537. Accessed 27 June 2023
Carreau-Green ND, Mirza RS, Martinez ML, Pyle GG (2008) The ontogeny of chemically mediated antipredator responses of fathead minnows Pimephales promelas. J Fish Biol 73:2390–2401. https://doi.org/10.1111/j.1095-8649.2008.02092.x
Chia JSM, Wall ES, Wee CL, Rowland TA, Cheng RK, Cheow K, Guillemini K, Jesuthasan S (2019) Bacteria evoke alarm behaviour in zebrafish. Nat Commun 10:3831. https://doi.org/10.1038/s41467-019-11608-9
Chivers DP, Mirza RS (2003) Fathead minnows learn to recognize heterospecific alarm cues they detect in the diet of a known predator. Behaviour 140:1359–1369. https://doi.org/10.1163/156853903771980620
Chivers DP, Wisenden BD, Hindman CJ et al (2007) Epidermal ‘alarm substance’cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation. Proc R Soc Lond B 274:2611–2619. https://doi.org/10.1098/rspb.2007.0709
Crane AL, Demers EE, Feyten LE, Ramnarine IW, Brown GE (2022) Exploratory decisions of Trinidadian guppies when uncertain about predation risk. Anim Cogn 25:581–587. https://doi.org/10.1007/s10071-021-01575-4
Dall SR (2010) Managing risk: the perils of uncertainty. Evol Behav Ecol 12:194–206
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
Farnsley S, Kuhajda B, George A, Klug H (2016) Fundulus catenatus (northern studfish) response to the potential alarm cue chondroitin sulfate. Southeast Nat 15:523–533. https://doi.org/10.1656/058.015.0315
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, Brown GE, Chivers DP (2018) Understanding the effect of uncertainty on the development of neophobic antipredator phenotypes. Anim Behav 136:101–106. https://doi.org/10.1016/j.anbehav.2017.11.024
Ferrari MCO, Crane AL, Chivers DP (2016) Certainty and the cognitive ecology of generalization of predator recognition. Anim Behav 111:207–211. https://doi.org/10.1016/j.anbehav.2015.10.026
Ferrari MCO, Gonzalo A, Messier F, Chivers DP (2007) Generalization of learned predator recognition: an experimental test and framework for future studies. Proc R Soc Lond B 274:1853–1859. https://doi.org/10.1098/rspb.2007.0297
Ferrari MCO, 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 LE, 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
Feyten LE, Demers EE, Ramnarine IW, Brown GE (2019) Predation risk assessment based on uncertain information: interacting effects of known and unknown cues. Curr Zool 65:75–76. https://doi.org/10.1093/cz/zoy083
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
Gaynor KM, Brown JS, Middleton AD, Power ME, Brashares JS (2019) Landscapes of fear: spatial patterns of risk perception and response. Trends Ecol Evol 34:355–368. https://doi.org/10.1016/j.tree.2019.01.004
Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311. https://doi.org/10.1016/0022-5193(71)90189-5
Henkanaththegedara SM, Stockwell CA (2014) Intraguild predation may facilitate coexistence of native and non-native fish. J Appl Ecol 51:1057–1065. https://doi.org/10.1111/1365-2664.12285
Hume JB, Wagner M (2018) A death in the family: sea lamprey (Petromyzon marinus) avoidance of confamilial alarm cues diminishes with phylogenetic distance. Ecol Evol 8:3751–3762. https://doi.org/10.1002/ece3.3930
Johnson DD, Blumstein DT, Fowler JH, Haselton MG (2013) The evolution of error: Error management, cognitive constraints, and adaptive decision-making biases. Trends Ecol Evol 28:474–481. https://doi.org/10.1016/j.tree.2013.05.014
Johnson MI, Hanson KA, Simon JM, Shastri A, Wisenden BD (2023) Ring a bell? Variable recognition of a multicomponent auditory stimulus associated with predation risk by zebrafish responding to full and partial matches. Behaviour 160:409–426. https://doi.org/10.1163/1568539X-bja10210
Kasumyan AO, Lebedeva NY (1979) New data on the nature of the alarm pheromone in cyprinids. J Ichthyol 19:109–114
Keenleyside MHA (1955) Some aspects of the schooling behaviour of fish. Behaviour 8:183–248. https://www.jstor.org/stable/4532829. Accessed 29 Mar 2023
Krause J, Godin J-GJ (1994) Shoal choice in the banded killifish (Fundulus diaphanus, Teleostei, Cyprinodontidae): effects of predation risk, fish size, species composition and size of shoals. Ethology 98:128–136. https://doi.org/10.1111/j.1439-0310.1994.tb01063.x
Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford
Krause J, Godin JGJ, Brown D (1996) Phenotypic variability within and between fish shoals. Ecology 77(5):1586–1591. https://doi.org/10.2307/2265553
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(4):636–648. https://doi.org/10.5061/dryad.m60f221
Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, Basutkar P, Tivey AR, Potter SC, Finn RD, Lopez R (2019) The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res 47:W636–W641. https://doi.org/10.1093/nar/gkz268
Manassa RP, Dixson DL, McCormick MI, Chivers DP (2013) Coral reef fish incorporate multiple sources of visual and chemical information to mediate predation risk. Anim Behav 86:717–722. https://doi.org/10.1016/j.anbehav.2013.07.003
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
Mathuru AS, Kibat C, Cheong WF, Shui G, Wenk MR, Friedrich RW, Jesuthasan S (2012) Chondroitin fragments are odorants that trigger fear behavior in fish. Curr Biol 22:538–544. https://doi.org/10.1016/j.cub.2012.01.061
Mirza RS, Chivers DP (2001a) Are chemical alarm cues conserved within salmonid fishes? J Chem Ecol 27:1641–1655. https://doi.org/10.1023/A:1010414426082
Mirza RS, Chivers DP (2001b) Learned recognition of heterospecific alarm signals: the importance of a mixed predator diet. Ethology 107:1007–1018. https://doi.org/10.1046/j.1439-0310.2001.00728.x
Paijmans KC, Booth DJ, Wong MY (2019) Towards an ultimate explanation for mixed-species shoaling. Fish Fish 20:921–933. https://doi.org/10.1111/faf.12384
Pandey S, Stockwell CA, Snider MR, Wisenden BD (2021) Epidermal club cells in fishes: a case for ecoimmunological analysis? Int J Mol Sci 22:1440. https://doi.org/10.3390/ijms22031440
Parra KV, Adrian JC Jr, Gerlai R (2009) The synthetic substance hypoxanthine 3-N-oxide elicits alarm reactions in zebrafish (Danio rerio). Behav Brain Res 205:336–341. https://doi.org/10.1016/j.bbr.2009.06.037
Pfeiffer W (1977) The distribution of fright reaction and alarm substance cells in fishes. Copeia 1977:653–665. https://doi.org/10.2307/1443164
Pfeiffer W, Riegelbauer G, Meier G, Scheibler B (1985) Effect of hypoxanthine-3(N)-oxide and hypoxanthine-1(N)-oxide on central nervous excitation of the black tetra Gymnocorymbus ternetzi (Characidae, Ostariophysi, Pisces) indicated by dorsal light response. J Chem Ecol 11:507–523. https://doi.org/10.1007/BF00989562
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
Pollock MS, Pollock RJ, Chivers DP (2006) Social context influences the antipredator behaviour of fathead minnows to chemical alarm cues. Ethology 112:801–806. https://doi.org/10.1111/j.1439-0310.2006.01222.x
Schaerf TM, Dillingham PW, Ward AJ (2017) The effects of external cues on individual and collective behavior of shoaling fish. Sci Adv 3:e1603201. https://doi.org/10.1126/sciadv.1603201
Schutz F (1956) Vergleichende Untersuchungen über die Schreckreaktion bei Fischen und deren Verbreitung. Z Vergl Physiol 38:84–135. https://doi.org/10.1007/BF00338623
Steinke D, Salzburger W, Meyer A (2006) Novel relationships among ten fish model species revealed based on a phylogenomic analysis using ESTs. J Mol Evol 62:772–784. https://doi.org/10.1007/s00239-005-0170-8
Stout CC (2017) Minnows and molecules: resolving the broad and fine-scale evolutionary patterns of Cypriniformes. PhD thesis, Auburn University
Tang ZH, Wu H, Huang Q, Kuang L, Fu SJ (2017) The shoaling behavior of two cyprinid species in conspecific and heterospecific groups. PeerJ 5:e3397. https://doi.org/10.7717/peerj.3397
Tonn WM, Magnuson JJ (1982) Patterns in the species composition and richness of fish assemblages in northern Wisconsin lakes. Ecology 63:1149–1166. https://doi.org/10.2307/1937251
Ward AJW, Axford S, Krause J (2003) Cross–species familiarity in shoaling fishes. Proc R Soc Lond B 270:1157–1161. https://doi.org/10.1098/rspb.2003.2337
Wisenden BD (2008) Active space of chemical alarm cue in natural fish populations. Behaviour 145:391–407. https://doi.org/10.1163/156853908783402920
Wisenden BD (2015) Chemical cues that indicate risk of predation. In: Sorensen PW, Wisenden BD (eds) Fish Pheromones and Related Cues. Wiley-Blackwell Press, Hoboken
Wisenden BD, Barbour KA (2005) Antipredator responses to skin extract of redbelly dace by free-ranging populations of redbelly dace and fathead minnows. Environ Biol Fish 72:227–233. https://doi.org/10.1007/s10641-004-8753-6
Wisenden BD, Chivers DP, Brown GE, Smith RJF (1995) 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 (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, 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, Rugg ML, Korpi NL, Fuselier LC (2009) Estimates of active time of chemical alarm cues in a cyprinid fish and an amphipod crustacean. Behaviour 146:1423–1442. https://doi.org/10.1163/156853909X440998
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
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We are grateful to two anonymous reviewers for constructive suggestions that improved the clarity and impact of this manuscript.
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Funding for supplies was provided by the Itasca Biological Field Station, College of Biological Sciences, University of Minnesota. CMA, BJS and MAS were supported by the Environmental & Conservation Sciences Graduate program.
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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.
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Wisenden, B.D., Andebrhan, A.A., Anderson, C.M. et al. Olfactory cues of risk and visual cues of safety interact with sympatry and phylogeny in sha** behavioral responses by littoral fishes. Behav Ecol Sociobiol 77, 91 (2023). https://doi.org/10.1007/s00265-023-03367-x
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DOI: https://doi.org/10.1007/s00265-023-03367-x