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Does humic acid alter visually and chemically guided foraging in stickleback fish?

Abstract

Sensory systems function under the influence of multiple, interacting environmental properties. When environments change, so may perception through one or more sensory systems, as alterations in transmission properties may change how organisms obtain and use information. Humic acids, a natural and anthropogenically produced class of chemicals, have attributes that may change chemical and visual environments of aquatic animals, potentially with detrimental consequences on their ability to locate necessary resources. Here, we explore how environmental disturbance affects the way threespine sticklebacks (Gasterosteus aculeatus) use visual and olfactory information during foraging. We compared foraging behavior using visual, olfactory, and bimodal (visual and olfactory) information in the presence and absence of humic acids. We found evidence that humic acids reduced olfactory-based food detection. While visual perception was not substantially impaired by humic acids, the visual sense alone did not compensate for the loss of olfactory perception. These findings suggest that a suite of senses still may not be capable of compensating for the loss of information from individual modalities. Thus, senses may react disparately to rapid environmental change, and thereby push species into altered evolutionary trajectories.

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References

  1. Bannister LH (1965) The fine structure of the olfactory surface of teleostean fishes. J Cell Sci 106:333–342

  2. Berg K, Voigt R, Atema J (1992) Flicking in the lobster Homarus americanus: recordings from electrodes implanted in antennular segments. Biol Bull 183:377–378. https://doi.org/10.1086/BBLv183n2p377

  3. Boughman JW (2001) Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944–948

  4. Chase R, Wells MJ (1986) Chemotactic behaviour in octopus. J Comp Physiol A 158:375–381. https://doi.org/10.1007/BF00603621

  5. Cooper WE (1998) Prey chemical discrimination indicated by tongue-flicking in the eublepharid gecko Coleonyx variegatus. J Exp Zool 281:21–25. https://doi.org/10.1002/(SICI)1097-010X(19980501)281:1%3c21:AID-JEZ4%3e3.0.CO;2-E

  6. Dalton P, Doolittle N, Nagata H, Breslin PAS (2000) The merging of the senses: integration of subthreshold taste and smell. Nat Neurosci 3:431–432. https://doi.org/10.1038/74797

  7. Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153

  8. Engstrom-Ost J, Candolin U (2007) Human-induced water turbidity alters selection on sexual displays in sticklebacks. Behav Ecol 18:393–398. https://doi.org/10.1093/beheco/arl097

  9. Fabian NJ, Albright LB, Gerlach G et al (2007) Humic acid interferes with species recognition in zebrafish (Danio rerio). J Chem Ecol 33:2090–2096. https://doi.org/10.1007/s10886-007-9377-z

  10. Fisher HS, Wong BBM, Rosenthal GG (2006) Alteration of the chemical environment disrupts communication in a freshwater fish. Proc R Soc B Biol Sci 273:1187–1193. https://doi.org/10.1098/rspb.2005.3406

  11. Geyer S, Fischer M, Wolf M, et al (1996) Agriculture and its impacts on the isotope geochemistry and structural composition of dissolved organic carbon. In: Isotopes in water resources management. V. 1. Proceedings of a symposium

  12. Hale R, Treml EA, Swearer SE (2015) Evaluating the metapopulation consequences of ecological traps. Proc R Soc B Biol Sci 282:20142930. https://doi.org/10.1098/rspb.2014.2930

  13. Halfwerk W, Slabbekoorn H (2015) Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance. Biol Lett 11:20141051. https://doi.org/10.1098/rsbl.2014.1051

  14. Hansten C, Heino M, Pynnönen K (1996) Viability of glochidia of Anodonta anatina (Unionidae) exposed to selected metals and chelating agents. Aquat Toxicol 34:1–12

  15. Heuschele J, Candolin U (2007) An increase in pH boosts olfactory communication in sticklebacks. Biol Lett 3:411–413. https://doi.org/10.1098/rsbl.2007.0141

  16. Heuschele J, Mannerla M, Gienapp P, Candolin U (2009) Environment-dependent use of mate choice cues in sticklebacks. Behav Ecol 20:1223–1227. https://doi.org/10.1093/beheco/arp123

  17. Hiermes M, Mehlis M, Rick IP, Bakker TCM (2015) Habitat-dependent olfactory discrimination in three-spined sticklebacks (Gasterosteus aculeatus). Anim Cogn 18:839–846. https://doi.org/10.1007/s10071-015-0850-8

  18. Honkanen T, Ekström P (1992) Comparative study of the olfactory epithelium of the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius). Cell Tissue Res 269:267–273

  19. Hubbard PC, Barata EN, Canario AVM (2002) Possible disruption of pheromonal communication by humic acid in the goldfish, Carassius auratus. Aquat Toxicol 60:169–183

  20. Jaeger RG, Goy JM, Tarver M, Márquez CE (1986) Salamander territoriality: pheromonal markers as advertisement by males. Anim Behav 34:860–864. https://doi.org/10.1016/S0003-3472(86)80071-9

  21. Longcore T, Rich C (2004) Ecological light pollution. Front Ecol Environ 2:191–198

  22. Madliger CL (2012) Toward improved conservation management: a consideration of sensory ecology. Biodivers Conserv 21:3277–3286. https://doi.org/10.1007/s10531-012-0363-6

  23. McKinnon JS, Rundle HD (2002) Speciation in nature: the threespine stickleback model systems. Trends Ecol Evol 17:480–488

  24. McLennan DA (2003) The importance of olfactory signals in the gasterosteid mating system: sticklebacks go multimodal. Biol J Linn Soc 80:555–572

  25. Mesquita RM, Canario AV, Melo E (2003) Partition of fish pheromones between water and aggregates of humic acids. Consequences for sexual signaling. Environ Sci Technol 37:742–746

  26. Mobley RB, Tillotson ML, Boughman JW (2016) Olfactory perception of mates in ecologically divergent stickleback: population parallels and differences. Evol Ecol Res 17:551–564

  27. Morris DP, Zagarese H, Williamson CE et al (1995) The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnol Oceanogr 40:1381–1391. https://doi.org/10.4319/lo.1995.40.8.1381

  28. Muller-Schwarze D (2006) Chemical ecology of vertebrates. Cambridge University Press, Cambridge

  29. Nevitt GA (1991) Do fish sniff? A new mechanism of olfactory sampling in pleuronectid flounders. J Exp Biol 157:1–18

  30. Ormond CI, Rosenfeld JS, Taylor EB (2011) Environmental determinants of threespine stickleback species pair evolution and persistence. Can J Fish Aquat Sci 68:1983–1997. https://doi.org/10.1139/f2011-113

  31. Partan SR (2017) Multimodal shifts in noise: switching channels to communicate through rapid environmental change. Anim Behav 124:325–337. https://doi.org/10.1016/j.anbehav.2016.08.003

  32. Partan SR, Marler P (1999) Communication goes multimodal. Science 283:1272–1273

  33. Pratt JW (1959) Remarks on zeros and ties in the Wilcoxon signed rank procedures. J Am Stat Assoc 54:655–667. https://doi.org/10.1080/01621459.1959.10501526

  34. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  35. Rafferty NE, Boughman JW (2006) Olfactory mate recognition in a sympatric species pair of three-spined sticklebacks. Behav Ecol 17:965–970. https://doi.org/10.1093/beheco/arl030

  36. Rennison DJ, Owens GL, Heckman N et al (2016) Rapid adaptive evolution of colour vision in the threespine stickleback radiation. Proc R Soc B Biol Sci 283:20160242. https://doi.org/10.1098/rspb.2016.0242

  37. Rodd FH, Hughes KA, Grether GF, Baril CT (2002) A possible non-sexual origin of mate preference: are male guppies mimicking fruit? Proc R Soc Lond B Biol Sci 269:475–481. https://doi.org/10.1098/rspb.2001.1891

  38. Rowe C (1999) Receiver psychology and the evolution of multicomponent signals. Anim Behav 58:921–931

  39. Rowe C, Guilford T (1999) The evolution of multimodal warning displays. Evol Ecol 13:655–671

  40. Santonja M, Minguez L, Gessner MO, Sperfeld E (2017) Predator–prey interactions in a changing world: humic stress disrupts predator threat evasion in copepods. Oecologia 183:887–898. https://doi.org/10.1007/s00442-016-3801-4

  41. Scott R (2001) Sensory drive and nuptial colour loss in the three-spined stickleback. J Fish Biol 59:1520–1528. https://doi.org/10.1006/jfbi.2001.1806

  42. Secondi J, Okassa M, Sourice S, Théry M (2014) Habitat-dependent species recognition in hybridizing newts. Evol Biol 41:71–80. https://doi.org/10.1007/s11692-013-9248-1

  43. Secondi J, Rodgers G, Bayle F et al (2015) Mate preference, species recognition and multimodal communication in heterogeneous environments. Evol Ecol 29:217–227. https://doi.org/10.1007/s10682-014-9744-5

  44. Seehausen O, van Alphen Jacques J M, Witte Frans (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808–1811. https://doi.org/10.1126/science.277.5333.1808

  45. Taylor EB, Boughman JW, Groenenboom M et al (2006) Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol Ecol 15:343–355. https://doi.org/10.1111/j.1365-294X.2005.02794.x

  46. Thomas JD (1997) The role of dissolved organic matter, particularly free amino acids and humic substances, in freshwater ecosystems. Freshw Biol 38:1–36

  47. Webster MM, Atton N, Ward AJW, Hart PJB (2007) Turbidity and foraging rate in threespine sticklebacks: the importance of visual and chemical prey cues. Behaviour 144:1347–1360

  48. Zhao Q, Zhu L (2016) Effect of humic acid on prometryn bioaccumulation and the induction of oxidative stress in zebrafish (Danio rerio). RSC Adv 6:16790–16797

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Acknowledgements

We are grateful to Marquita Tillotson and Savannah Foster for their assistance in carrying out behavioral trials and data collection, as well as the members of the Boughman lab who provided animal care. We thank Courtney Larson, Miranda Wade, Scott Warner, Nikki Cavalieri, Murielle Ålund, the BEACON Chemical Communication Group, and two anonymous reviewers for useful comments in preparation of this manuscript. Nicole Jess, Andrew Denhardt and MSU CSTAT provided valuable statistical consultation. This work was supported by grants from the National Science Foundation to JWB.

Funding

This study was funded by a National Science Foundation Career Grant (Career Grant deb-0952659) and a National Science Foundation Dimensions of Biodiversity Grant (deb-1638778), awarded to JWB.

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Correspondence to Robert B. Mobley.

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The authors declare that they have no conflict of interest.

Ethical approval

All the applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All the procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted (Michigan State University Institutional Animal Care and Use Committee permit number 04/13-092-00).

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Mobley, R.B., Weigel, E.G. & Boughman, J.W. Does humic acid alter visually and chemically guided foraging in stickleback fish?. Anim Cogn 23, 101–108 (2020). https://doi.org/10.1007/s10071-019-01319-5

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Keywords

  • Vision
  • Olfaction
  • Humic acid
  • Multimodal shift
  • Habitat change