Volume 49, No. 1



Volumes > 38 (2010-->) Volumes 28-37 (2000-09) Volumes 18-27 (1990-99) Volumes 5-17 (1978-89)
a.k.a. Cormorant

Quick Search by author or article title:


Fishy tales: Behaviour of schooling fish escaping from terns


Authors

KEES HULSMAN GURUDEO ANAND TULARAM

Environmental Futures Research Institute, Griffith University, 170 Kessels Road, Nathan, Queensland 4111, Australia (keesjehulsman@yahoo.com.au or a.tularam20@gmail.com)


Received 25 August 2020, accepted 16 November 2020

Date Published: 2021/04/15
Date Online: 2021/04/10


Download PDF

Citation

HULSMAN, K. & TULARAM, G.A. 2021. Fishy tales: Behaviour of schooling fish escaping from terns. Marine Ornithology 49: 159-166.


Key words: foraging behaviour, predatory behaviour, confusion effect, atherinids, silversides, mathematical model


Abstract

The aim of this study is to develop a better understanding of seabird foraging behaviour and the anti-predator behaviour of their prey. Studies of seabirds' foraging and prey-capture behaviour, as it relates to the evasive and escape behaviour of schooling fish, are sparse. Our study was carried out at One Tree Reef on the southern end of the Great Barrier Reef, Australia. A school of hardyheads Pranesus capricornensis sheltered in the shallows over the sand flats in front of the research station for 14 non-consecutive days. In that time, Lesser Crested Terns Thalasseus bengalensis were observed for 10 hours from above the surface in 37 foraging bouts and for 40 minutes from underwater in at least one foraging bout. In each foraging bout, a single tern dived into the school. We found that terns on average dived at a rate of 0.67 ± 0.35 dives/minute from 4-5 m above the surface. The depth range of dives was 43-58 cm. Therefore, fish within 58 cm of the surface were potentially accessible. The total length of the hardyheads was 10-12 cm, which is within the size range useable by terns. Fish used flash expansion to escape diving terns and formed a vacuole around birds as they slowly ascended to the surface. This escape manoeuvre was effective about 80% of the time. The fish that were caught did not respond to the escape movements of the fish above them and, therefore, were isolated. Fish also used the C-startle response to escape terns underwater and in mid-air. The anti-predator manoeuvres of hardyheads are similar to those observed among Clupea spp. (herrings and sardines) and Ammodytes spp. (sand eels) escaping sub-surface predators. Hardyheads and sardines react in the same way to gannets Morus spp. and terns that plunge dive directly to their prey, partially confirming the prediction that results for plunge-diving gannets are generalisable to other gannets and boobies (Sula spp.), terns and gulls (Larus spp.), tropicbirds (Phaethon spp.), pelicans (Pelecanus spp.), and kingfishers (Alcedinidae).


References

AU, D.W.K. & PITMAN, R.L. 1986. Seabird interactions with dolphins and tuna in the eastern tropical Pacific. The Condor 88: 304-317.

AXELSEN, B.E., ANKER-NILSSEN, T., FOSSUM, P., KVAMME, C. & NØTTESTAD, L. 2001. Pretty patterns but a simple strategy: predator-prey interactions between juvenile herring and Atlantic puffins observed with multibeam sonar. Canadian Journal of Zoology 79: 1586-1596.

BBC EARTH 2014. Shark and Dolphin FEEDING FRENZY | Nature's Great Events | BBC Earth. London, UK: British Broadcasting Corporation. [Accessed at https://www.youtube.com/watch?v=DHeZrLnY3Dk on 07 September 2020.]

BURGER, A.E. 2001. Diving depths of shearwaters. The Auk 118: 755-759.

BURGER, A.E. & SIMPSON, M. 1986. Diving depths of Atlantic Puffins and Common Murres. The Auk 103: 828-830.

BURGER, A.E., WILSON, R.P., GARNIER, D. & WILSON, M.-P.T. 1993. Diving depths, diet, and underwater foraging of Rhinoceros Auklets in British Columbia. Canadian Journal of Zoology 71: 2528-2540.

CAMPHUYSEN, C.J. & WEBB, A. 1999. Multi-species feeding associations in North Sea seabirds: jointly exploiting a patchy environment. Ardea 87: 177-198.

CLUA, E. & GROSVALET, F. 2001. Mixed-species feeding aggregation of dolphins, large tunas and seabirds in the Azores. Aquatic Living Resources 14: 11-18.

CROOK, K.A. & DAVOREN, G.K. 2014. Underwater behaviour of Common Murres foraging on capelin: influences of prey density and antipredator behaviour. Marine Ecology Progress Series 501: 279-290.

DOMENICI, P. 2010. Context-dependent variability in the components of fish escape response: integrating locomotor performance and behavior. Journal of Experimental Zoology A 313A: 59-79.

DUFFY, D.C. 1983. The foraging ecology of Peruvian seabirds. The Auk 100: 800-810.

DUNN, E.K. 1973. Changes in fishing ability of terns associated with windspeed and sea surface conditions. Nature 244: 520-521.

ELLIOTT, K.H., DAVOREN, G.K. & GASTON, A.J. 2008. Time allocation by a deep-diving bird reflects prey type and energy gain. Animal Behaviour 75: 1301-1310.

ERWIN, R.M. 1977. Foraging and breeding adaptations to different food regimes in three seabirds: the Common Tern, Sterna hirundo, Royal Tern, Sterna maxima, and Black Skimmer, Rynchops niger. Ecology 58: 389-397.

GÓMEZ-LAICH, A., QUINTANA, F., SHEPARD, E.L.C. & WILSON, R.P. 2012. Intersexual differences in the diving behaviour of Imperial Cormorants. Journal of Ornithology 153: 139-147.

GÓMEZ-LAICH, A., YODA, K. & QUINTANA, F. 2018 Insights into the foraging behavior of Magellanic Penguins (Spheniscus magellanicus). Waterbirds 41: 332-336. doi:10.1675/063.041.0315

GÖTMARK, F., WINKLER, D.W. & ANDERSSON, M. 1986. Flock-feeding on fish schools increases individual success in gulls. Nature 319: 589-591.

HODGES, C.L. & WOEHLER, E.J. 1994. Associations between seabirds and cetaceans in the Australian sector of the southern Indian Ocean. Marine Ornithology 22: 205-212.

HULSMAN, C. 1977. Feeding and Breeding Biology of Six Species of Sympatric Terns at One Tree Island Great Barrier Reef. PhD dissertation. Brisbane, Australia: University of Queensland.

HULSMAN, K. 1979. Reactions of fish to hunting methods of terns: a means of segregation. Proceedings of the Colonial Waterbird Group 2: 105-109.

HULSMAN, K. 1989. The structure of seabird communities: an example from Australian waters. In: BURGER, J. (Ed.) Seabirds and Other Marine Vertebrates: Competition, Predation, and Other Interactions. New York, USA: Columbia University Press.

IOANNOU, C.C., TOSH, C.R., NEVILLE, L. & KRAUSE, J. 2008. The confusion effect - from neural networks to reduced predation. Behavioral Ecology 19: 126-130.

LITVAK, M.K. 1993. Response of shoaling fish to the threat of aerial predation. Environmental Biology of Fishes 36: 183-192.

MACHOVSKY-CAPUSKA, G.E., VAUGHN, R.L., WÜRSIG, B, KATZIR, G. & RAUBENHEIMER, D. 2011. Dive strategies and foraging effort in the Australasian Gannet Morus serrator revealed by underwater videography. Marine Ecology Progress Series 442: 255-261.

MAGURRAN, A.E. & PITCHER, T.J. 1987. Provenance, shoal size and the sociobiology of predator-evasion behaviour in minnow shoals. Proceedings of the Royal Society B 229: 439-465.

MARRAS, S. & DOMENICI, P. 2013. Schooling fish under attack are not all equal: some lead, others follow. PLoS One 8: e65784. doi:10.1371/journal.pone.0065784

MEHLUM, F., WATANUKI, Y & TAKAHASHI, A. 2001. Diving behaviour and foraging habits of Brünnich's Guillemots (Uria lomvia) breeding in the High-Arctic. Journal of Zoology 255: 413-423.

NELSON, J.B. 1978. The Sulidae: Gannets and Boobies. Oxford, UK: Oxford University Press

NØTTESTAD, L. & AXELSEN, B.E. 1999. Herring school manoeuvres in response to killer whale attacks. Canadian Journal of Zoology 77: 1540-1546.

PARTRIDGE, B.L. 1982. Structure and function of fish schools. Scientific American 246: 114-123.

PAVLOV, D.S. & KASUMYAN, A.O. 2000. Patterns and mechanisms of schooling behavior in fish: a review. Journal of Ichthyology 40: S163-S231

PECK, D.R. & CONGDON, B.C. 2006. Sex-specific chick provisioning and diving behaviour in the wedge-tailed shearwater Puffinus pacificus. Journal of Avian Biology 37: 245-251.

PITCHER, T.J. & WYCHE, C.J. 1983. Predator avoidance behaviours of sand-eel schools: why schools seldom split. In: NOAKES, D.L.G., LINDQUIST, B.G., HELFMAN, G.S. & WARD, J.A. (Eds.) Predators and Prey in Fishes. Dordrecht, Netherlands: Springer.

PODILA, S, & ZHU, Y. 2017. Animating multiple escape maneuvers for a school of fish. GI 17: Proceedings of the 43rd Graphics Interface Conference 2017: 140-147. doi:10.20380/GI2017.18

ROPERT-COUDERT, Y., GRÉMILLET, D., RYAN, P., KATO, A., NAITO, Y. & LE MAHO, Y. 2004. Between air and water: the plunge dive of the Cape Gannet Morus capensis. Ibis 146: 281-290.

SAFINA, C., BURGER, J., GOCHFELD, M. & WAGNER, R.H. 1988. Evidence for prey limitation of Common and Roseate Tern reproduction. The Condor 90: 852-859.

SHOJI, A., ELLIOTT, K., FAYET, A., BOYLE, D., PERRINS, C. & GUILFORD, T. 2015. Foraging behaviour of sympatric razorbills and puffins. Marine Ecology Progress Series 520: 257-267.

TREMBLAY, Y. & CHEREL, Y. 2000. Benthic and pelagic dives: a new foraging behaviour in rockhopper penguins. Marine Ecology Progress Series 204: 257-267.

THIEBAULT, A., SEMERIA, M., LETT, C. & TREMBLAY, Y. 2016. How to capture fish in a school? Effect of successive predator attacks on seabird feeding success. Journal of Animal Ecology 85: 157-167.

VABØ, R. & NØTTESTAD, L. 1997. An individual based model of fish school reactions: predicting antipredator behaviour as observed in nature. Fisheries Oceanography 6: 155-171.

VAUGHN, R.L., WÜRSIG, B., SHELTON, D.S., TIMM, L.L. & WATSON, L.A. 2008. Dusky dolphins influence prey accessibility for seabirds in Admiralty Bay, New Zealand. Journal of Mammalogy 89: 1051-1058

VAUGHN, R., WÜRSIG, B. & PACKARD, J. 2010. Dolphin prey herding: Prey ball mobility relative to dolphin group and prey ball sizes, multispecies associates, and feeding duration. Marine Mammal Science 26: 213-225.

WILSON, R.P., CULIK, B.M., PETERS, G. & BANNASCH, R. 1996. Diving behaviour of Gentoo penguins, Pygoscelis papua; factors keeping dive profiles in shape. Marine Biology 126: 153-162.

WILSON, R.P. & WILSON, M.-P.T. 1988. Foraging behaviour in four sympatric cormorants. Journal of Animal Ecology 57: 943-955.


© Marine Ornithology 2022