The temporal multimodal influence of optical and auditory cues on the repellent behaviour of ring-billed gulls (Larus delewarensis)
Caitlin A. Lecker A , Michael H. Parsons A B E , Daniel R. Lecker C , Ronald J. Sarno B and Faith E. Parsons D
+ Author Affiliations
- Author Affiliations
A Department of Biology, State University New York, Empire State College, Hartsdale, NY 10530, USA.
B Department of Biology, Hofstra University, Hempstead, NY 11549, USA.
C Department of Psychology, State University New York, Plattsburgh, Plattsburgh, NY 12901, USA.
D School of Medicine, Columbia University, New York, NY 10032, USA.
E Corresponding author. Email: parsons.hmichael@gmail.com
Wildlife Research 42(3) 232-240 https://doi.org/10.1071/WR15001
Submitted: 7 September 2014 Accepted: 10 May 2015 Published: 17 June 2015
Abstract
Context: A generation of new animal repellents is based on the premise that threat stimuli are best interpreted through multiple sensory pathways. Ring-billed gulls (RBG; Larus delawarensis) offer a unique opportunity to assess the efficacy of multimodal repellents over time. This pest species is repelled by both auditory and optical cues and persists in stable populations, often remaining in the same colony for life. This distinctive attribute makes it possible to assess colonies independently over time and space.
Aims: We assessed the unimodal (single-cue treatment) and multimodal (paired-cue) response by RBG to auditory (conspecific distress call) and optical (green or red laser) cues, along with a double-negative control (flashlight aimed at ground, background noise).
Methods: All stimuli were investigated separately and together within a 3 × 2 factorial design randomised by treatment and site. We predicted that paired stimuli would generate more pronounced (number of gulls fleeing from a roost) and faster (flight initiation time) responses than stimuli presented alone with a control.
Key results: The distress call was more effective than either visual signal and almost nullified our ability to detect a multimodal response. However, the multimodal influence was detected on two levels. Gulls were more likely to flee from either paired treatment (optical + auditory) than from unimodal stimuli (laser light only; P < 0.001) and gulls fled more quickly from multiple cues (P < 0.001). A more subtle, but important, benefit was observed in that – over time – gulls were more likely to flee from either paired treatment (optical or auditory), but not from unimodal treatments (P < 0.005). The latter response may have been due to a fear-conditioned generalisation.
Conclusions: We provide evidence and a causal mechanism to address why multimodal stimuli may be more efficacious as deterrents than single-mode treatments. This species may be more effectively managed, over longer periods of time, through the use of multimodal repellents.
Implications: A better understanding of how multimodal repellents function may help frame novel approaches to animal conservation and to assay better tools and repellents for wildlife management. Even modest multimodal benefits may justify their use, if they delay habituation over time.
Additional keywords: deterrents, distress calls, fear conditioning, habituation, lasersmultisensory, sensitisation.
References
Ahmadinejad, M., Hasani, A., Kharaziyan, F., and Patel, N. B. (2010). The responses of horses to predator stimuli. Iranian Journal of Veterinary Medicine 4, 1–5.Apfelbach, R., Blanchard, C. D., Blanchard, R. J., Hayes, R. A., and McGregor, I. S. (2005). The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurobiology and Biobehavioral Review 29, 1123–1144.
| The effects of predator odors in mammalian prey species: a review of field and laboratory studies.Crossref | GoogleScholarGoogle Scholar |
Baxter, A. T., and Allan, R. A. (2010). Use of lethal control to reduce habituation to blank rounds by scavenging birds. The Journal of Wildlife Management 71, 1653–1657.
Biedenweg, T. A., Parsons, M. H., Fleming, P. A., and Blumstein, D. T. (2011). Sounds scary? Lack of habituation following the presentation of novel sounds. PLoS One 6, e14549.
| Sounds scary? Lack of habituation following the presentation of novel sounds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Ohtb0%3D&md5=2b4fb4e42d95c4eb3d23626fc5efa1c4CAS | 21267451PubMed |
Blackwell, B. F., Bernhardt, G. E., and Dolbeer, R. A. (2002). Lasers as nonlethal avian repellents. The Journal of Wildlife Management 66, 250–258.
| Lasers as nonlethal avian repellents.Crossref | GoogleScholarGoogle Scholar |
Blokpoel, H., and Tessier, G. D. (1984). Overhead wires and monofilament lines exclude ring-billed gulls from public places. Wildlife Society Bulletin 12, 55–58.
Blumstein, D. T., and Daniel, J. C. (2004). Yellow-bellied marmots discriminate between the distress calls of individuals and are more responsive to calls from juveniles. Animal Behaviour 68, 1257–1265.
| Yellow-bellied marmots discriminate between the distress calls of individuals and are more responsive to calls from juveniles.Crossref | GoogleScholarGoogle Scholar |
Blumstein, D. T., Daniel, J. C., Griffin, A. S., and Evans, C. S. (2000). Insular tammar wallabies (Macropus eugenii) respond to visual but not acoustic cues from predators. Behavioral Ecology 11, 528–535.
| Insular tammar wallabies (Macropus eugenii) respond to visual but not acoustic cues from predators.Crossref | GoogleScholarGoogle Scholar |
Bomford, M., and O’Brien, P. H. (1990). Sonic deterrents in animal damage control: a review of device tests and effectiveness. Wildlife Society Bulletin 18, 411–422.
Carrasco, M. F., and Blumstein, D. T. (2012). Mule deer (Odocoileus hemionus) respond to yellow-bellied marmot (Marmota flaviventris) distress calls. Ethology 118, 243–250.
| Mule deer (Odocoileus hemionus) respond to yellow-bellied marmot (Marmota flaviventris) distress calls.Crossref | GoogleScholarGoogle Scholar |
Christensen, J. W., Keeling, L. J., and Nielsen, B. L. (2005). Responses of horses to novel visual, olfactory and auditory stimuli. Applied Animal Behaviour Science 93, 53–65.
| Responses of horses to novel visual, olfactory and auditory stimuli.Crossref | GoogleScholarGoogle Scholar |
Clapperton, B. K., Porter, R. E., Day, T. D., Waas, J. R., and Matthews, L. R. (2012). Designer repellents: combining olfactory, visual or taste cues with a secondary repellent to deter free‐ranging house sparrows from feeding. Pest Management Science 68, 870–877.
| Designer repellents: combining olfactory, visual or taste cues with a secondary repellent to deter free‐ranging house sparrows from feeding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xit1Wmu7Y%3D&md5=82385b0d179c075c92e1fd062c234ebaCAS | 22337510PubMed |
Conover, M. R. (1987). Acquisition of predator information by active and passive mobbers in ring-billed gull colonies. Behaviour 102, 41–57.
| Acquisition of predator information by active and passive mobbers in ring-billed gull colonies.Crossref | GoogleScholarGoogle Scholar |
(a) Cowx, I. G. (2003). ‘Interactions between fisheries and fish-eating birds: optimising the use of shared resources. Interactions between fish and birds: Implications for management’. (John Wiley and Sons: New York.)
Cox, T. E., Murray, P. J., Bengsen, A. J., Hall, G. P., and Li, X. (2014). Do fecal odors from native and non‐native predators cause a habitat shift among macropods? Wildlife Society Bulletin , .
| Do fecal odors from native and non‐native predators cause a habitat shift among macropods?Crossref | GoogleScholarGoogle Scholar |
Cummings, J. L., Knittle, C. E., and Guarino, J. L. (1986). Evaluating a pop-up scarecrow coupled with a propane exploder for reducing blackbird damage to ripening sunflower. In ‘Proceedings of the Twelfth Vertebrate Pest Conference’, (Ed. T. P. Salmon.) pp. 286–291. (University of California: Davis.)
Dall, S. R., and Johnstone, R. A. (2002). Managing uncertainty: information and insurance under the risk of starvation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 357, 1519–1526.
| Managing uncertainty: information and insurance under the risk of starvation.Crossref | GoogleScholarGoogle Scholar | 12495509PubMed |
Emond, M. P., McNeil, R., Cabana, T., Guerra, C. G., and Lachapelle, P. (2006). Comparing the retinal structures and functions in two species of gulls Larus delawarensis and Larus modestus) with significant nocturnal behaviours. Vision Research 46, 2914–2925.
| Comparing the retinal structures and functions in two species of gulls Larus delawarensis and Larus modestus) with significant nocturnal behaviours.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zpslChsQ%3D%3D&md5=77389ff3efd1fda839d99bbd3e0c8679CAS | 16647740PubMed |
Fairbanks, B. F., and Dobson, S. (2007). Mechanisms of the group-size effect on vigilance in Columbian ground squirrels: dilution versus detection. Animal Behaviour 73, 115–123.
| Mechanisms of the group-size effect on vigilance in Columbian ground squirrels: dilution versus detection.Crossref | GoogleScholarGoogle Scholar |
Gallagher, G. R., and Prince, R. H. (2003). Negative operant conditioning fails to deter white-tailed deer foraging activity. Crop Protection 22, 893–895.
| Negative operant conditioning fails to deter white-tailed deer foraging activity.Crossref | GoogleScholarGoogle Scholar |
Gilsdorf, J. M., Hygnstrom, S. E., and VerCauteren, K. C. (2002). Use of frightening devices in wildlife damage management. Integrated Pest Management Reviews 7, 29–45.
| Use of frightening devices in wildlife damage management.Crossref | GoogleScholarGoogle Scholar |
Glaudas, X., and Winne, C. T. (2007). Do warning displays predict striking behavior in a viperid snake, the cottonmouth (Agkistrodon piscivorus)? Canadian Journal of Zoology 85, 574–578.
| Do warning displays predict striking behavior in a viperid snake, the cottonmouth (Agkistrodon piscivorus)?Crossref | GoogleScholarGoogle Scholar |
Gotz, T., and Janik, V. M. (2011). Repeated elicitation of the acoustic startle reflex leads to sensitisation in subsequent avoidance behaviour and induces fear conditioning. BMC Neurobiology 12, 243–250.
Hart, N. S., and Collin, S. P. (2014). Sharks senses and shark repellents. Integrative Zoology , .
| Sharks senses and shark repellents.Crossref | GoogleScholarGoogle Scholar |
Joiris, A., Korati, S., and Van Dyck, H. (2010). Differential bird predator attack rate on seasonal forms of the map butterfly (Araschnia levana L.): does the substrate matter? Ethology 116, 1020–1026.
| Differential bird predator attack rate on seasonal forms of the map butterfly (Araschnia levana L.): does the substrate matter?Crossref | GoogleScholarGoogle Scholar |
Kastelein, R. A., Vaughn, A. D., Schooneman, N. M., Verboom, W. C., and Dehaan, D. (2000). The effect of acoustic distresss on the behavior of harbor porpoises (Phocoena phocoena) in a floating pen. Marine Mammal Science 16, 46–64.
| The effect of acoustic distresss on the behavior of harbor porpoises (Phocoena phocoena) in a floating pen.Crossref | GoogleScholarGoogle Scholar |
Kimball, B. A., Taylor, J., Perry, K. R., and Capelli, C. (2009). Deer responses to repellent stimuli. Journal of Chemical Ecology 35, 1461–1470.
| Deer responses to repellent stimuli.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlehurs%3D&md5=75a0f5710e2f0244adde81208c99f4deCAS | 20013037PubMed |
Kinkel, L. K. (1988). Nest site fidelity in the Ring-billed gull (Larus delawarensis). Ph.D. dissertation. Northern Illinois University, DeKalb, IL.
Kinkel, L. K. (1989). Lasting effects of wing tags on ring-billed gulls. The Auk 106, 619–624.
Little, T. M., and Hill, F. J. (1978). ‘Agricultural Experimentation: Design and Analysis.’ (John Wiley and Sons: New York.)
McKay, H., Russell, I., and Furness, R. (1999). The assessment of the effectiveness of management measures to control damage by fish-eating birds to inland fisheries in England and Wales. Report to the Ministry of Agriculture, Fisheries and Food, Great Britain. Central Science Laboratory; York, England.
McLennan, J. A., Langham, N. P. E., and Porter, R. E. R. (1995). Deterrent effect of eye‐spot balls on birds. New Zealand Journal of Crop and Horticultural Science 23, 139–144.
| Deterrent effect of eye‐spot balls on birds.Crossref | GoogleScholarGoogle Scholar |
McMeniman, C. J., Corfas, R. A., Matthews, B. J., Ritchie, S. A., and Vosshall, L. B. (2014). Multimodal Integration of carbon dioxide and other sensory cues drives mosquito attraction to humans. Cell 156, 1060–1071.
| Multimodal Integration of carbon dioxide and other sensory cues drives mosquito attraction to humans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjsVWgsL8%3D&md5=83dc460d18f3c6c7aad0f27bedec0e6dCAS | 24581501PubMed |
Munoz, N. E., and Blumstein, D. T. (2012). Multisensory perception in uncertain environments. Behavioral Ecology 23, 457–462.
| Multisensory perception in uncertain environments.Crossref | GoogleScholarGoogle Scholar |
Olofsson, M., Vallin, A., Jakobsson, S., and Wiklund, C. (2011). Winter predation on two species of hibernating butterflies: monitoring rodent attacks with infrared cameras. Animal Behaviour 81, 529–534.
| Winter predation on two species of hibernating butterflies: monitoring rodent attacks with infrared cameras.Crossref | GoogleScholarGoogle Scholar |
Parsons, M. H., and Blumstein, D. T. (2010). Familiarity breeds contempt: kangaroos persistently avoid an area with experimentally deployed dingo scents. PLoS One 5, e10403.
| Familiarity breeds contempt: kangaroos persistently avoid an area with experimentally deployed dingo scents.Crossref | GoogleScholarGoogle Scholar | 20463952PubMed |
Partan, S. R., and Marler, P. (1999). Communication goes multimodal. Science 283, 1272–1273.
| Communication goes multimodal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhs1entbY%3D&md5=bd8828475083789726cfa4bbf4ed6a0fCAS |
Piep, M., Radespiel, U., Zimmerman, E., Schmidt, S., and Siemers, B. M. (2008). The sensory basis of prey detection in captive-born grey mouse lemurs, Microcebus murinus. Animal Behaviour 75, 871–878.
| The sensory basis of prey detection in captive-born grey mouse lemurs, Microcebus murinus.Crossref | GoogleScholarGoogle Scholar |
Rankin, C. H., Adams, T., Barry, R. J., Bhatnagar, S., Clayton, D. F., Colombo, J., Coppola, G., Geyer, M. A., Glanzman, D. L., Marsland, S., McSweeney, F. K., Wilson, D. A., Wu, C.-F., and Thompson, R. F. (2009). Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiology of Learning and Memory 92, 135–138.
| Habituation revisited: an updated and revised description of the behavioral characteristics of habituation.Crossref | GoogleScholarGoogle Scholar | 18854219PubMed |
Rojas, J. C., Virgen, A., and Cruz-López, L. (2003). Chemical and tactile cues influencing oviposition of a generalist moth, Spodoptera frugiperda (Lepidoptera: Noctuidae). Environmental Entomology 32, 1386–1392.
| Chemical and tactile cues influencing oviposition of a generalist moth, Spodoptera frugiperda (Lepidoptera: Noctuidae).Crossref | GoogleScholarGoogle Scholar |
Rowe, C. (1999). Receiver psychology and the evolution of multicomponent signals. Animal Behaviour 58, 921–931.
| Receiver psychology and the evolution of multicomponent signals.Crossref | GoogleScholarGoogle Scholar | 10564594PubMed |
Schakner, Z. A., and Blumstein, D. T. (2013). Behavioral biology of marine mammal deterrents: a review and prospectus. Biological Conservation 167, 380–389.
| Behavioral biology of marine mammal deterrents: a review and prospectus.Crossref | GoogleScholarGoogle Scholar |
Smith, C. L., and Evans, C. E. (2008). Multimodal signaling in fowl, Gallus gallus. The Journal of Experimental Biology 211, 2052–2057.
| Multimodal signaling in fowl, Gallus gallus.Crossref | GoogleScholarGoogle Scholar | 18552293PubMed |
Soldatini, C., Albores-Barajas, Y. V., Torricelli, P., and Mainardi, D. (2008). Testing the efficacy of three deterring systems in two gull species. Applied Animal Behaviour Science 110, 330–340.
| Testing the efficacy of three deterring systems in two gull species.Crossref | GoogleScholarGoogle Scholar |
Stankowich, T., and Blumstein, D. T. (2005). Fear in animals: a meta-analysis and review of risk assessment. Proceedings. Biological Sciences 272, 2627–2634.
| Fear in animals: a meta-analysis and review of risk assessment.Crossref | GoogleScholarGoogle Scholar |
Starnberger, I., Preininger, D., and Hödl, W. (2014). From uni- to multimodality: towards an integrative view on anuran communication. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 200, 777–787.
| 24973893PubMed |
Summers, R. W. (1985). The effect of scarers on the presence of starlings (Sturnus vulgaris) in cherry orchards. Crop Protection 4, 520–528.
| The effect of scarers on the presence of starlings (Sturnus vulgaris) in cherry orchards.Crossref | GoogleScholarGoogle Scholar |
Treves, A., Wallace, R. B., and White, S. (2009). Participatory planning of interventions to mitigate human–wildlife conflicts. Conservation Biology 23, 1577–1587.
| Participatory planning of interventions to mitigate human–wildlife conflicts.Crossref | GoogleScholarGoogle Scholar | 19459896PubMed |
Werner, S., and Clark, L. (2006). Effectiveness of a motion-activated laser hazing system for repelling captive Canadian geese. Wildlife Society Bulletin 34, 2–7.
| Effectiveness of a motion-activated laser hazing system for repelling captive Canadian geese.Crossref | GoogleScholarGoogle Scholar |
