Why conservation biology can benefit from sensory ecology

Abstract

Global expansion of human activities is associated with the introduction of novel stimuli, such as anthropogenic noise, artificial lights and chemical agents. Progress in documenting the ecological effects of sensory pollutants is weakened by sparse knowledge of the mechanisms underlying these effects. This severely limits our capacity to devise mitigation measures. Here, we integrate knowledge of animal sensory ecology, physiology and life history to articulate three perceptual mechanisms—masking, distracting and misleading—that clearly explain how and why anthropogenic sensory pollutants impact organisms. We then link these three mechanisms to ecological consequences and discuss their implications for conservation. We argue that this framework can reveal the presence of ‘sensory danger zones’, hotspots of conservation concern where sensory pollutants overlap in space and time with an organism’s activity, and foster development of strategic interventions to mitigate the impact of sensory pollutants. Future research that applies this framework will provide critical insight to preserve the natural sensory world.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Three different mechanisms underlie ecological effects of sensory pollutants.
Fig. 2: Different sensory mechanisms ask for different solutions.

References

  1. 1.

    Vitousek, P. M., Mooney, H. A., Lubchenco, J. & Melillo, J. M. Human domination of Earth’s ecosystems. Science 277, 494–499 (1997).

  2. 2.

    Seto, K. C., Guneralp, B. & Hutyra, L. R. Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proc. Natl Acad. Sci. USA 109, 16083–16088 (2012).

  3. 3.

    Lomolino, M. V., Channell, R., Perault, D. R. & Smith, G. A. in Biotic Homogenization (eds Lockwood, J. L. & McKinney, M. L.) 223–243 (Springer, 2001).

  4. 4.

    Halfwerk, W. & Slabbekoorn, H. Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance. Biol. Lett. 11, 20141051 (2015).

  5. 5.

    Swaddle, J. P. et al. A framework to assess evolutionary responses to anthropogenic light and sound. Trends Ecol. Evol. 30, 550–560 (2015).

  6. 6.

    Lürling, M. & Scheffer, M. Info-disruption: pollution and the transfer of chemical information between organisms. Trends Ecol. Evol. 22, 374–379 (2007).

  7. 7.

    Kyba, C. C. M. et al. Artificially lit surface of Earth at night increasing in radiance and extent. Sci. Adv. 3, e1701528 (2017).

  8. 8.

    Buxton, R. T. et al. Noise pollution is pervasive in U.S. protected areas. Science 356, 531–533 (2017).

  9. 9.

    Bernhardt, E. S., Rosi, E. J. & Gessner, M. O. Synthetic chemicals as agents of global change. Front. Ecol. Environ. 15, 84–90 (2017).

  10. 10.

    Shannon, G. et al. A synthesis of two decades of research documenting the effects of noise on wildlife. Biol. Rev. 91, 982–1005 (2016).

  11. 11.

    Hallmann, C. A. et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12, e0185809 (2017).

  12. 12.

    van Langevelde, F. et al. Declines in moth populations stress the need for conserving dark nights. Glob. Change Biol. 24, 925–932 (2018).

  13. 13.

    Francis, C. D., Ortega, C. P. & Cruz, A. Noise pollution changes avian communities and species interactions. Curr. Biol. 19, 1415–1419 (2009).

  14. 14.

    Owens, A. C. S. et al. Light pollution is a driver of insect declines. Biol. Conserv. 241, 108259 (2020).

  15. 15.

    Stevens, M. Sensory Ecology, Behaviour, and Evolution (Oxford Univ. Press, 2013).

  16. 16.

    Denzinger, A. & Schnitzler, H. U. Bat guilds, a concept to classify the highly diverse foraging and echolocation behaviors of microchiropteran bats. Front. Physiol. 4, 164 (2013).

  17. 17.

    Kevan, P. G., Chittka, L. & Dyer, A. G. Limits to the salience of ultraviolet: lessons from colour vision in bees and birds. J. Exp. Biol. 204, 2571–2580 (2001).

  18. 18.

    Clarke, D., Whitney, H., Sutton, G. & Robert, D. Detection and learning of floral electric fields by bumblebees. Science 340, 66–69 (2013).

  19. 19.

    Kleist, N. J., Guralnick, R. P., Cruz, A. & Francis, C. D. Sound settlement: noise surpasses land cover in explaining breeding habitat selection of secondary cavity-nesting birds. Ecol. Appl. 27, 260–273 (2017).

  20. 20.

    Morris-Drake, A., Kern, J. M. & Radford, A. N. Cross-modal impacts of anthropogenic noise on information use. Curr. Biol. 26, R911–R912 (2016).

  21. 21.

    McMahon, T. A., Rohr, J. R. & Bernal, X. E. Light and noise pollution interact to disrupt interspecific interactions. Ecology 98, 1290–1299 (2017).

  22. 22.

    Knop, E. et al. Artificial light at night as a new threat to pollination. Nature 548, 206–209 (2017).

  23. 23.

    Van Doren, B. M. et al. High-intensity urban light installation dramatically alters nocturnal bird migration. Proc. Natl Acad. Sci. USA 114, 11175–11180 (2017).

  24. 24.

    Dominoni, D., Borniger, J. & Nelson, R. Light at night, clocks and health: from humans to wild organisms. Biol. Lett. 12, 20160015 (2016).

  25. 25.

    Gaston, K. J., Davies, T. W., Nedelec, S. L. & Holt, L. A. Impacts of artificial light at night on biological timings. Annu. Rev. Ecol. Evol. Syst. 48, 49–68 (2017).

  26. 26.

    Fuller, R. A., Warren, P. H. & Gaston, K. J. Daytime noise predicts nocturnal singing in urban robins. Biol. Lett. 3, 368–370 (2007).

  27. 27.

    Gomes, D. G. E. et al. Bats perceptually weight prey cues across sensory systems when hunting in noise. Science 353, 1277–1280 (2016).

  28. 28.

    Mason, J. T., McClure, C. J. W. & Barber, J. R. Anthropogenic noise impairs owl hunting behavior. Biol. Conserv. 199, 29–32 (2016).

  29. 29.

    Simpson, S. D. et al. Anthropogenic noise increases fish mortality by predation. Nat. Commun. 7, 10544 (2016).

  30. 30.

    Kight, C. R. & Swaddle, J. P. How and why environmental noise impacts animals: an integrative, mechanistic review. Ecol. Lett. 14, 1052–1061 (2011).

  31. 31.

    Francis, C. D. & Barber, J. R. A framework for understanding noise impacts on wildlife: an urgent conservation priority. Front. Ecol. Environ. 11, 305–313 (2013).

  32. 32.

    Fisher, H. S., Wong, B. B. M. & Rosenthal, G. G. Alteration of the chemical environment disrupts communication in a freshwater fish. Proc. R. Soc. B 273, 1187–1193 (2006).

  33. 33.

    Silber, K. The Physiological Basis of Behaviour (Routledge, 2005).

  34. 34.

    Ouyang, J. Q., Davies, S. & Dominoni, D. Hormonally mediated effects of artificial light at night on behavior and fitness: linking endocrine mechanisms with function. J. Exp. Biol. 221, jeb156893 (2018).

  35. 35.

    Dominoni, D., Goymann, W., Helm, B. & Partecke, J. Urban-like night illumination reduces melatonin release in European blackbirds (Turdus merula): implications of city life for biological time-keeping of songbirds. Front. Zool. 10, 60 (2013).

  36. 36.

    Bruening, A., Hölker, F., Franke, S., Kleiner, W. & Kloas, W. Impact of different colours of artificial light at night on melatonin rhythm and gene expression of gonadotropins in European perch. Sci. Total Environ. 543, 214–222 (2016).

  37. 37.

    Kleist, N. J., Guralnick, R. P., Cruz, A., Lowry, C. A. & Francis, C. D. Chronic anthropogenic noise disrupts glucocorticoid signaling and has multiple effects on fitness in an avian community. Proc. Natl Acad. Sci. USA 115, 201709200 (2018).

  38. 38.

    Tennessen, J. B., Parks, S. E. & Langkilde, T. Traffic noise causes physiological stress and impairs breeding migration behaviour in frogs. Conserv. Physiol. 2, cou032 (2014).

  39. 39.

    Zollinger, S. A., Goller, F. & Brumm, H. Metabolic and respiratory costs of increasing song amplitude in zebra finches. PLoS ONE 6, e23198 (2011).

  40. 40.

    Rolland, R. M. et al. Evidence that ship noise increases stress in right whales. Proc. R. Soc. B 279, 2363–2368 (2012).

  41. 41.

    O’Neill, J. S. et al. Metabolic molecular markers of the tidal clock in the marine crustacean Eurydice pulchra. Curr. Biol. 25, R326–R327 (2015).

  42. 42.

    Chan, A. A. Y. H., Giraldo-Perez, P., Smith, S. & Blumstein, D. T. Anthropogenic noise affects risk assessment and attention: the distracted prey hypothesis. Biol. Lett. 6, 458–461 (2010).

  43. 43.

    Brown, J. S. & Kotler, B. P. in Foraging: Behavior and Ecology (eds Stephens, D. W., Brown, J. S. & Ydenberg, R. C.) 437–480 (Univ. Chicago Press, 2007).

  44. 44.

    Miedema, H. & Vos, H. Associations between self-reported sleep disturbance and environmental noise based on reanalyses of pooled data from 24 studies. Behav. Sleep Med. 5, 1–20 (2007).

  45. 45.

    Inger, R., Bennie, J., Davies, T. W. & Gaston, K. J. Potential biological and ecological effects of flickering artificial light. PLoS ONE 9, e98631 (2014).

  46. 46.

    Riffell, J. A. et al. Flower discrimination by pollinators in a dynamic chemical environment. Science 344, 1515–1518 (2014).

  47. 47.

    Rich, C. & Longcore, T. Artificial Night Lighting (Island Press, 2006).

  48. 48.

    Longcore, T. et al. Avian mortality at communication towers in the United States and Canada: which species, how many, and where? Biol. Conserv. 158, 410–419 (2013).

  49. 49.

    Rodríguez, A. et al. Artificial lights and seabirds: is light pollution a threat for the threatened Balearic petrels? J. Ornithol. 156, 893–902 (2015).

  50. 50.

    Singer, M. C. & Parmesan, C. Lethal trap created by adaptive evolutionary response to an exotic resource. Nature 557, 238–241 (2018).

  51. 51.

    Hale, R. & Swearer, S. E. Ecological traps: current evidence and future directions. Proc. R. Soc. B 283, 20152647 (2016).

  52. 52.

    Geipel, I., Amin, B., Page, R. A. & Halfwerk, W. Does bat response to traffic noise support the misleading cue hypothesis? Behav. Ecol. 30, 1775–1781 (2019).

  53. 53.

    Tyack, P. L. et al. Beaked whales respond to simulated and actual navy sonar. PLoS ONE 6, e17009 (2011).

  54. 54.

    Da Silva, A., Samplonius, J., Schlicht, E., Valcu, M. & Kempenaers, B. Artificial night lighting rather than traffic noise affects the daily timing of dawn and dusk singing in common European songbirds. Behav. Ecol. 25, 1037–1047 (2014).

  55. 55.

    Kempenaers, B., Borgström, P., Loës, P., Schlicht, E. & Valcu, M. Artificial night lighting affects dawn song, extra-pair siring success, and lay date in songbirds. Curr. Biol. 20, 1735–1739 (2010).

  56. 56.

    Dwyer, R. G., Bearhop, S., Campbell, H. A. & Bryant, D. M. Shedding light on light: benefits of anthropogenic illumination to a nocturnally foraging shorebird. J. Anim. Ecol. 82, 478–485 (2013).

  57. 57.

    Fleming, P. A. & Bateman, P. W. Novel predation opportunities in anthropogenic landscapes. Anim. Behav. 138, 145–155 (2018).

  58. 58.

    Girling, R. D., Lusebrink, I., Farthing, E., Newman, T. A. & Poppy, G. M. Diesel exhaust rapidly degrades floral odours used by honeybees. Sci. Rep. 3, 2779 (2013).

  59. 59.

    Becker, N., Zgomba, M., Petric, D. & Ludwig, M. Comparison of carbon dioxide, octenol and a host‐odour as mosquito attractants in the Upper Rhine Valley, Germany. Med. Vet. Entomol. 9, 377–380 (1995).

  60. 60.

    Longcore, T. et al. Tuning the white light spectrum of light emitting diode lamps to reduce attraction of nocturnal arthropods. Philos. Trans. R. Soc. B 370, 20140125 (2015).

  61. 61.

    Halfwerk, W., Holleman, L. J. M., Lessells, C. K. M. & Slabbekoorn, H. Negative impact of traffic noise on avian reproductive success. J. Appl. Ecol. 48, 210–219 (2011).

  62. 62.

    Park, D., Hempleman, S. C. & Propper, C. R. Endosulfan exposure disrupts pheromonal systems in the red-spotted newt: a mechanism for subtle effects of environmental chemicals. Environ. Health Perspect. 109, 669–673 (2001).

  63. 63.

    Aulsebrook, A. E., Jones, T. M., Mulder, R. A. & Lesku, J. A. Impacts of artificial light at night on sleep: a review and prospectus. J. Exp. Zool. Part A Ecol. Integr. Physiol. 329, 409–418 (2018).

  64. 64.

    Slabbekoorn, H. Songs of the city: noise-dependent spectral plasticity in the acoustic phenotype of urban birds. Anim. Behav. 85, 1089–1099 (2013).

  65. 65.

    Yuen, S. W. & Bonebrake, T. C. Artificial night light alters nocturnal prey interception outcomes for morphologically variable spiders. PeerJ 5, e4070 (2017).

  66. 66.

    Russ, A., Rüger, A. & Klenke, R. Seize the night: European blackbirds (Turdus merula) extend their foraging activity under artificial illumination. J. Ornithol. 156, 123–131 (2015).

  67. 67.

    Montgomery, J. C., Jeffs, A., Simpson, S. D., Meekan, M. & Tindle, C. Sound as an orientation cue for the pelagic larvae of reef fishes and decapod crustaceans. Adv. Mar. Biol. 51, 143–196 (2006).

  68. 68.

    Stanley, J. A., Radford, C. A. & Jeffs, A. G. Location, location, location: finding a suitable home among the noise. Proc. R. Soc. B 279, 3622–3631 (2012).

  69. 69.

    Hölker, F., Wolter, C., Perkin, E. K. & Tockner, K. Light pollution as a biodiversity threat. Trends Ecol. Evol. 25, 681–682 (2010).

  70. 70.

    Ware, H. E., McClure, C. J. W., Carlisle, J. D. & Barber, J. R. A phantom road experiment reveals traffic noise is an invisible source of habitat degradation. Proc. Natl Acad. Sci. USA 112, 201504710 (2015).

  71. 71.

    San-Jose, L. M. et al. Differential fitness effects of moonlight on plumage colour morphs in barn owls. Nat. Ecol. Evol. 3, 1331–1340 (2019).

  72. 72.

    Kettel, E. F., Gentle, L. K. & Yarnell, R. W. Evidence of an urban peregrine falcon (Falco peregrinus) feeding young at night. J. Raptor Res. 50, 321–323 (2016).

  73. 73.

    Francis, C. D., Kleist, N. J., Ortega, C. P. & Cruz, A. Noise pollution alters ecological services: enhanced pollination and disrupted seed dispersal. Proc. R. Soc. B 279, 2727–2735 (2012).

  74. 74.

    Spoelstra, K. et al. Response of bats to light with different spectra: light-shy and agile bat presence is affected by white and green, but not red light. Proc. R. Soc. B 284, 20170075 (2017).

  75. 75.

    Webb, C. T., Hoeting, J. A., Ames, G. M., Pyne, M. I. & LeRoy Poff, N. A structured and dynamic framework to advance traits-based theory and prediction in ecology. Ecol. Lett. 13, 267–283 (2010).

  76. 76.

    Poot, H. et al. Green light for nocturnally migrating birds. Ecol. Soc. 13, 47 (2008).

  77. 77.

    Dominoni, D. M., Smit, J. A. H., Visser, M. E. & Halfwerk, W. Multisensory pollution: artificial light at night and anthropogenic noise have interactive effects on activity patterns of great tits (Parus major). Environ. Pollut. 256, 113314 (2020).

  78. 78.

    Dominoni, D., Carmona-Wagner, E., Hofmann, M., Kranstauber, B. & Partecke, J. Individual-based measurements of light intensity provide new insights into the effects of artificial light at night on daily rhythms of urban-dwelling songbirds. J. Anim. Ecol. 83, 681–692 (2014).

  79. 79.

    Dorado-Correa, A. M., Rodríguez-Rocha, M. & Brumm, H. Anthropogenic noise, but not artificial light levels predicts song behaviour in an equatorial bird. R. Soc. Open Sci. 3, 160231 (2016).

  80. 80.

    Piggott, J. J., Townsend, C. R. & Matthaei, C. D. Reconceptualizing synergism and antagonism among multiple stressors. Ecol. Evol. 5, 1538–1547 (2015).

  81. 81.

    Francis, C. D. Vocal traits and diet explain avian sensitivities to anthropogenic noise. Glob. Change Biol. 21, 1809–1820 (2015).

  82. 82.

    Thomas, R. J. et al. Eye size in birds and the timing of song at dawn. Proc. R. Soc. B 269, 831–837 (2002).

  83. 83.

    de Jong, M. et al. Dose-dependent responses of avian daily rhythms to artificial light at night. Physiol. Behav. 155, 172–179 (2016).

  84. 84.

    Dominoni, D. M. et al. Dose-response effects of light at night on the reproductive physiology of great tits (Parus major): integrating morphological analyses with candidate gene expression. J. Exp. Zool. Part A Ecol. Integr. Physiol. 329, 473–487 (2018).

  85. 85.

    Bruening, A., Hölker, F., Franke, S., Preuer, T. & Kloas, W. Spotlight on fish: light pollution affects circadian rhythms of European perch but does not cause stress. Sci. Total Environ. 511, 516–522 (2015).

  86. 86.

    Williams, R., Erbe, C., Ashe, E., Beerman, A. & Smith, J. Severity of killer whale behavioral responses to ship noise: a dose-response study. Mar. Pollut. Bull. 79, 254–260 (2014).

  87. 87.

    Kaniewska, P., Alon, S., Karako-Lampert, S., Hoegh-Guldberg, O. & Levy, O. Signaling cascades and the importance of moonlight in coral broadcast mass spawning. eLife 4, e09991 (2015).

  88. 88.

    Evans, J. E., Cuthill, I. C. & Bennett, A. T. D. The effect of flicker from fluorescent lights on mate choice in captive birds. Anim. Behav. 72, 393–400 (2006).

  89. 89.

    Lürling, M. Effects of a surfactant (FFD-6) on Scenedesmus morphology and growth under different nutrient conditions. Chemosphere 62, 1351–1358 (2006).

  90. 90.

    Simpson, S. D. et al. in The Effects of Noise on Aquatic Life II (eds Popper, A. & Hawkins, A.) 1041–1048 (Springer, 2016).

  91. 91.

    Stanley, J. A., Wilkens, S. L. & Jeffs, A. G. Fouling in your own nest: vessel noise increases biofouling. Biofouling 30, 837–844 (2014).

  92. 92.

    Dixson, D. L., Abrego, D. & Hay, M. E. Chemically mediated behavior of recruiting corals and fishes: a tipping point that may limit reef recovery. Science 345, 892–897 (2014).

  93. 93.

    Greif, S. & Siemers, B. M. Innate recognition of water bodies in echolocating bats. Nat. Commun. 1, 107 (2010).

  94. 94.

    Greif, S., Zsebok, S., Schmieder, D. & Siemers, B. M. Acoustic mirrors as sensory traps for bats. Science 357, 1045–1047 (2017).

  95. 95.

    Horváth, G., Kriska, G., Malik, P. & Robertson, B. Polarized light pollution: a new kind of ecological photopollution. Front. Ecol. Environ. 7, 317–325 (2009).

  96. 96.

    Ockendon, N. et al. Mechanisms underpinning climatic impacts on natural populations: altered species interactions are more important than direct effects. Glob. Change Biol. 20, 2221–2229 (2014).

  97. 97.

    Hau, M. et al. Timing as a sexually selected trait: The right mate at the right moment. Philos. Trans. R. Soc. B 372, 20160249 (2017).

  98. 98.

    Dominoni, D. M., Åkesson, S., Klaassen, R., Spoelstra, K. & Bulla, M. Methods in field chronobiology. Philos. Trans. R. Soc. B 372, 20160247 (2017).

  99. 99.

    Gaynor, K. M., Hojnowski, C. E., Carter, N. H. & Brashares, J. S. The influence of human disturbance on wildlife nocturnality. Science 360, 1232–1235 (2018).

  100. 100.

    Stevenson, T. J. et al. Disrupted seasonal biology impacts health, food security and ecosystems. Proc. R. Soc. B 282, 20151453 (2015).

Download references

Acknowledgements

We are grateful to Lory State Park, Colorado, USA, for hosting our workshop in October 2017 that led to this Perspective. We also acknowledge our collaborators at the National Park Service’s Natural Sounds and Night Skies Division. The work was supported by the NASA Ecological Forecasting Grant NNX17AG36G to N.H.C., J.R.B., C.D.F. and D.C.S.

Author information

All authors participated at the workshop in Colorado and actively contributed to round-table discussions. D.M.D., W.H., C.D.F., N.H.C. and J.R.B. laid out the ideas for this manuscript and discussed its content and structure. D.M.D. and W.H. contributed equally to write the initial draft of the paper. C.D.F., N.H.C. and J.R.B. contributed equally to provide feedback and editing on this initial draft. E.B., R.T.B., E.F.-J., K.M.F., M.F.M., D.J.M., E.K.P., B.M.S., D.C.S., J.B.T., C.A.T., L.P.T. and A.W. contributed to this Perspective intellectually and by providing examples and editing. All authors agreed on the final version of the manuscript.

Correspondence to Davide M. Dominoni.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Table

Table with examples of the impacts of sensory pollutants categorized by sensory mechanism.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Dominoni, D.M., Halfwerk, W., Baird, E. et al. Why conservation biology can benefit from sensory ecology. Nat Ecol Evol (2020). https://doi.org/10.1038/s41559-020-1135-4

Download citation