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Volume 50, No. 2

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Digging in! Burrowing penguins and surface predators


Authors

LAURA X.L. TAN1*, KASUN B. EKANAYAKE2, WOUTER F.D. VAN DONGEN1, PETER DANN3, DUNCAN R. SUTHERLAND3 & MICHAEL A. WESTON1
1Marine Animal Ecology Group, Wageningen University, Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands (hannah.madden@wur.nl)
2Caribbean Netherlands Science Institute, PO Box 65, St. Eustatius, Caribbean Netherlands, NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University, PO Box 59, 1790 AB Den Burg, Texel, The Netherlands
3Department of Forestry and Environmental Conservation, Clemson University, Clemson, South Carolina, USA
4US Geological Survey - South Carolina Cooperative Fish and Wildlife Research Unit and Department of Forestry and Environmental Conservation, Clemson University, Clemson, South Carolina, USA

Citation

TAN, L.X.L., EKANAYAKE, K.B., VAN DONGEN, W.F.D., DANN, P., SUTHERLAND, D.R. & WESTON, M.A. 2022. Digging in! Burrowing penguins and surface predators. Marine Ornithology 50: 177 - 187

Received 23 January 2022, accepted 01 June 2022

Date Published: 2022/10/15
Date Online: 2022/09/22
Key words: raven, penguin, burrow, predator risk, prey response, adaptation

Abstract

A native Australian corvid, Little Raven Corvus mellori, has emerged as a dominant and problematic predator of an ecologically and economically important seabird, the Little Penguin Eudyptula minor. In 2013, ravens successfully preyed upon clutches/broods of the burrow-nesting penguin, especially those in shallower, more accessible burrows. Individual raven size might mediate which ravens attack penguins; smaller ravens may be able to enter burrows more easily; alternatively, larger ravens may be more capable of overcoming penguin parental defence. Here, we consider the predator-prey interactions to assess whether associations with burrow characteristics persisted and examine whether raven size mediated propensity to prey upon penguin eggs. We compared data from the 2013 and 2015 penguin breeding seasons at Phillip Island (Victoria, Australia) for differences in clutch survival and burrow characteristics. We also examined raven morphometrics to determine if any physical differences existed between known burrow-predators (“culprits”) and other birds. During the 2013 breeding season, penguins suffered clutch losses of 61.1% compared with 33.9% in 2015. Burrow characteristics changed between seasons—most noticeably, burrows were deeper in 2015 and ravens no longer discriminated between burrow characteristics. Culprits were heavier and larger. While we could not eliminate inter-annual variability as a possible contributing factor, our results were consistent with rapid adaptation of prey and predator to intense emergent depredation. Penguins may now construct deeper burrows, and ravens evidently no longer select more vulnerable burrows. Larger ravens may be more capable of approaching and attacking penguin burrows.

References


ANDERSON, M.J., GORLEY, R.N. & CLARKE, K.R. 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. Plymouth, UK: PRIMER-E Ltd.

ANDERSON, M.J. & WILLIS, T.J. 2003. Canonical analysis of principal coordinates: A useful method of constrained ordination for ecology. Ecology 84: 511-525. doi:10.1890/0012-9658(2003)084[0511:CAOPCA]2.0.CO;2

AVERY, M.L., PAVELKA, M.A., BERGMAN, D.L., DECKER, D.G., KNITTLE, C.E. & LINZ, G.M. 1995. Aversive conditioning to reduce raven predation on California Least Tern eggs. Colonial Waterbirds 18: 131-138. doi:10.2307/1521474

BIRD, C.D. & EMERY, N.J. 2009. Rooks use stones to raise the water level to reach a floating worm. Current Biology 19: 1410-1414. doi:10.1016/j.cub.2009.07.033

BLIGHT, L.K., RYDER, J.L. & BERTRAM, D.F. 1999. Predation on Rhinoceros Auklet eggs by a native population of Peromyscus. The Condor 101: 871-876. doi:10.2307/1370079

BROOK, B.W., SODHI, N.S., SOH, M.C.K. & LIM, H.C. 2003. Abundance and projected control of invasive House Crows in Singapore. The Journal of Wildlife Management 67: 808-817. doi:10.2307/3802688

BROWN, M.J. & JONES, D.N. 2016. Cautious crows: Neophobia in Torresian Crows (Corvus orru) compared with three other corvoids in suburban Australia. Ethology 122: 726-733. doi:10.1111/eth.12517

BULL, L.S. 2000. Factors influencing Little Penguin Eudyptula minor egg success on Matiu-Somes Island, New Zealand. Emu - Austral Ornithology 100: 199-204. doi:10.1071/MU9924

CERCHIARA, J.A. 2018. Penguins. In: SWANSON, P. & SKINNER, M.K. (Eds.) Encyclopedia of Reproduction, 2nd Edition. Volume 6. Sydney, Australia: Elsevier. doi:10.1016/B978-0-12-809633-8.20610-9

CHEN, J.-N., LIU, N.-F., YAN, C. & AN, B. 2011. Plasticity in nest site selection of Black Redstart (Phoenicurus ochruros): a response to human disturbance. Journal of Ornithology 152: 603-608. doi:10.1007/s10336-010-0622-9

CHIARADIA, A., FORERO, M.G., HOBSON, K.A. & CULLEN, J.M. 2010. Changes in diet and trophic position of a top predator 10 years after a mass mortality of a key prey. ICES Journal of Marine Science 67: 1710-1720. doi:10.1093/icesjms/fsq067

CHIARADIA, A.F. & KERRY, K.R. 1999. Daily nest attendance and breeding performance in the Little Penguin Eudyptula minor at Phillip Island, Australia. Marine Ornithology 27: 13-20.

CLARK, T.J., BONNET-LEBRUN, A.-S., CAMPIONI, L., CATRY, P. & WAKEFIELD, E. 2019. The depth of Sooty Shearwater Ardenna grisea burrows varies with habitat and increases with competition for space. Ibis 161: 192-197. doi:10.1111/ibi.12631

COATES, P.S., O'NEIL, S.T., BRUSSEE, B.E. ET AL. 2020. Broad-scale impacts of an invasive native predator on a sensitive native prey species within the shifting avian community of the North American Great Basin. Biological Conservation 243: 108409. doi:10.1016/j.biocon.2020.108409

COLOMBELLI-NÉGREL, D. 2019. Benefits, costs and trade-offs of nesting habitat selection in Little Penguins. Journal of Ornithology 160: 515-527. doi:10.1007/s10336-019-01636-z

CONNER, W.E. & CORCORAN, A.J. 2012. Sound strategies: The 65-million-year-old battle between bats and insects. Annual Review of Entomology 57: 21-39. doi:10.1146/annurev-ento-121510-133537

COOK, T.R., LESCROËL, A., CHEREL, Y., KATO, A. & BOST, C.-A. 2013. Can foraging ecology drive the evolution of body size in a diving endotherm? PLoS One 8: e56297. doi:10.1371/journal.pone.0056297

DANN, P. 1991. Distribution, population trends and factors influencing the population size of Little Penguins Eudyptula minor on Phillip Island, Victoria. Emu - Austral Ornithology 91: 263-272. doi:10.1071/MU9910263

DANN, P. & CHAMBERS, L. 2013. Ecological effects of climate change on Little Penguins Eudyptula minor and the potential economic impact on tourism. Climate Research 58: 67-79. doi:10.3354/cr01187

DANN, P., NORMAN, F.I., CULLEN, J.M., NEIRA, F.J. & CHIARADIA, A. 2000. Mortality and breeding failure of Little Penguins, Eudyptula minor, in Victoria, 1995-96, following a widespread mortality of Pilchard, Sardinops sagax. Marine and Freshwater Research 51: 355-362. doi:10.1071/MF99114

DAWKINS, R. & KREBS, J.R. 1979. Arms races between and within species. Proceedings of the Royal Society B 205: 489-511. doi:10.1098/rspb.1979.0081

DOHERTY, T.S., GLEN, A.S., NIMMO, D.G., RITCHIE, E.G. & DICKMAN, C.R. 2016. Invasive predators and global biodiversity loss. Proceedings of the National Academy of Sciences 113: 11261-11265. doi:10.1073/pnas.1602480113

DUFFY, D.C. & CAPECE, P.I. 2014. Depredation of endangered burrowing seabirds in Hawai'i: Management priorities. Marine Ornithology 42: 149-152.

DURELL, S.E.A.L.V.D., GOSS-CUSTARD, J.D. & CALDOW, R.W.G. 1993. Sex-related differences in diet and feeding method in the Oystercatcher Haematopus ostralegus. Journal of Animal Ecology 62: 205-215. doi:10.2307/5495

EGGERS, S., GRIESSER, M., NYSTRAND, M. & EKMAN, J. 2006. Predation risk induces changes in nest-site selection and clutch size in the Siberian Jay. Proceedings of the Royal Society B 273: 701-706. doi:10.1098/rspb.2005.3373

EKANAYAKE, K.B., SUTHERLAND, D.R., DANN, P. & WESTON, M.A. 2015a. Out of sight but not out of mind: Corvids prey extensively on eggs of burrow-nesting penguins. Wildlife Research 42: 509-517. doi:10.1071/WR15108

EKANAYAKE, K.B., WESTON, M.A., DANN, P. & SUTHERLAND, D.R. 2016. Corvids congregate to breeding colonies of a burrow-nesting seabird. Austral Ecology 41: 291-301. doi:10.1111/aec.12311

EKANAYAKE, K.B., WESTON, M.A., NIMMO, D.G., MAGUIRE, G.S., ENDLER, J.A. & KÜPPER, C. 2015b. The bright incubate at night: Sexual dichromatism and adaptive incubation division in an open-nesting shorebird. Proceedings of the Royal Society B 282: 20143026. doi:10.1098/rspb.2014.3026

EKANAYAKE, K.B., WHISSON, D.A., TAN, L.X.L. & WESTON, M.A. 2015c. Intense predation of non-colonial, ground-nesting bird eggs by corvid and mammalian predators. Wildlife Research 42: 518-528. doi:10.1071/WR15080

GRIFFITHS, C.L. & RICHARDSON, C.A. 2006. Chemically induced predator avoidance behaviour in the burrowing bivalve Macoma balthica. Journal of Experimental Marine Biology and Ecology 331: 91-98. doi:10.1016/j.jembe.2005.10.002

HAFF, T.M. & MAGRATH, R.D. 2011. Calling at a cost: Elevated nestling calling attracts predators to active nests. Biology Letters 7: 493-495. doi:10.1098/rsbl.2010.1125

HAYWARD, J.L., ATKINS, G.J., REICHERT, A.A. & HENSON, S.M. 2015. Common Ravens (Corvus corax) prey on Rhinoceros Auklet (Cerorhinca monocerata) eggs, chicks, and possibly adults. The Wilson Journal of Ornithology 127: 336-339. doi:10.1676/wils-127-02-336-339.1

HENDERSON, L.A. & TRULIO, L.A. 2019. Can California Ground Squirrels reduce predation risk to Burrowing Owls? Journal of Raptor Research 53: 172-179. doi:10.3356/JRR-17-73

HIGGINS, P.J., PETER, J.M. & COWLING, S.J. (Eds.) 2006. Handbook of Australian, New Zealand and Antarctic Birds. Melbourne, Australia: Oxford University Press.

HUDSON, P.J. 1982. Nest site characteristics and breeding success in the Razorbill Alca torda. Ibis 124: 355-359. doi:10.1111/j.1474-919X.1982.tb03784.x

HUNT, G.R. 2000. Human-like, population-level specialization in the manufacture of pandanus tools by New Caledonian Crows Corvus moneduloides. Proceedings of the Royal Society B 267: 403-413. doi:10.1098/rspb.2000.1015

HUSBY, M. 2019. Nestling begging calls increase predation risk by corvids. Animal Biology 69: 137-155. doi:10.1163/15707563-20181058

IBM CORP. 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, USA: IBM Corp.

JOLLES, J.W., OSTOJIĆ, L. & CLAYTON, N.S. 2013. Dominance, pair bonds and boldness determine social-foraging tactics in Rooks, Corvus frugilegus. Animal Behaviour 85: 1261-1269. doi:10.1016/j.anbehav.2013.03.013

LEIGHTON, P.A., HORROCKS, J.A. & KRAMER, D.L. 2009. How depth alters detection and capture of buried prey: Exploitation of sea turtle eggs by mongooses. Behavioral Ecology 20: 1299-1306. doi:10.1093/beheco/arp139

LIEBEZEIT, J.R. & GEORGE, T.L. 2002. A summary of predation by corvids on Threatened and Endangered species in California and management recommendations to reduce corvid predation. Species Conservation and Recovery Program Report, 2002-02. Sacramento, USA: California Department of Fish and Game.

LIMA, S.L. & DILL, L.M. 1990. Behavioral decisions made under the risk of predation: A review and prospectus. Canadian Journal of Zoology 68: 619-640. doi:10.1139/z90-092

MARCHANT, S. & HIGGINS, P.J. 1990. Handbook of Australian, New Zealand and Antarctic Birds. Melbourne, Australia: Oxford University Press.

MARZLUFF, J.M. 1988. Do Pinyon Jays alter nest placement based on prior experience? Animal Behaviour 36: 1-10. doi:10.1016/S0003-3472(88)80244-6

MARZLUFF, J.M., WALLS, J., CORNELL, H.N., WITHEY, J.C. & CRAIG, D.P. 2010. Lasting recognition of threatening people by wild American Crows. Animal Behaviour 79: 699-707. doi:10.1016/j.anbehav.2009.12.022

MASSARO, M., STARLING-WINDHOF, A., BRISKIE, J.V. & MARTIN, T.E. 2008. Introduced mammalian predators induce behavioural changes in parental care in an endemic New Zealand bird. PLoS One 3: e2331. doi:10.1371/journal.pone.0002331

MATSUI, H., HUNT, G.R., OBERHOFER, K. ET AL. 2016. Adaptive bill morphology for enhanced tool manipulation in New Caledonian Crows. Scientific Reports 6: 22776. doi:10.1038/srep22776

MCIVER, W.R., CARTER, H.R., HARVEY, A.L. ET AL. 2018. Avian and skunk predation of Ashy Storm-petrels at Santa Cruz Island, California. Western North American Naturalist 78: 421-440. doi:10.3398/064.078.0313

MINNAAR, C., BOYLES, J.G., MINNAAR, I.A., SOLE, C.L. & MCKECHNIE, A.E. 2015. Stacking the odds: Light pollution may shift the balance in an ancient predator-prey arms race. Journal of Applied Ecology 52: 522-531. doi:10.1111/1365-2664.12381

MYKYTOWYCZ, R., HESTERMAN, E.R. & PURCHASE, D. 1959. Predation on the wild rabbit by the Australian Raven. Emu - Austral Ornithology 59: 41-43. doi:10.1071/MU959041

NAKAZAWA, A. 2004. The Behaviour of the Little Raven (Corvus mellori) and its Predation of Little Penguin (Eudyptula minor) Eggs on Phillip Island, Victoria. Undergraduate thesis. St. Lucia, Australia: The University of Queensland.

PRINGLE, R.M., KARTZINEL, T.R., PALMER, T.M. ET AL. 2019. Predator-induced collapse of niche structure and species coexistence. Nature 570: 58-64. doi:10.1038/s41586-019-1264-6

PYKE, G.H., PULLIAM, H.R. & CHARNOV, E.L. 1977. Optimal foraging: A selective review of theory and tests. The Quarterly Review of Biology 52: 137-154. doi:10.1086/409852

RANGE, F., BUGNYAR, T., SCHLÖGL, C. & KOTRSCHAL, K. 2006. Individual and sex differences in learning abilities of ravens. Behavioural Processes 73: 100-106. doi:10.1016/j.beproc.2006.04.002

REGEHR, H.M., RODWAY, M.S. & MONTEVECCHI, W.A. 1998. Antipredator benefits of nest-site selection in Black-legged Kittiwakes. Canadian Journal of Zoology 76: 910-915. doi:10.1139/z98-016

REILLY, P.N. & CULLEN, J.M. 1981. The Little Penguin Eudyptula minor in Victoria, II: Breeding. Emu - Austral Ornithology 81: 1-19. doi:10.1071/MU9810001

RICHNER, H. 1989. Phenotypic correlates of dominance in Carrion Crows and their effects on access to food. Animal Behaviour 38: 606-612. doi:10.1016/S0003-3472(89)80005-3

ROCKWELL, C., GABRIEL, P.O. & BLACK, J.M. 2012. Bolder, older, and selective: Factors of individual-specific foraging behaviors in Steller's Jays. Behavioral Ecology 23: 676-683. doi:10.1093/beheco/ars015

ROWLEY, I. 1970. The genus Corvus (Aves: Corvidae) in Australia. CSIRO Wildlife Research 15: 27-71. doi:10.1071/CWR9700027

ROWLEY, I. 1973. The comparative ecology of Australian corvids. IV. Nesting and the rearing of young to independence. CSIRO Wildlife Research 18: 91-129. doi:10.1071/CWR9730091

ROWLEY, I. & VESTJENS, W.J.M. 1973. The comparative ecology of Australian corvids. V. Food. CSIRO Wildlife Research 18: 131-135. doi:10.1071/CWR9730131

SANTISTEBAN, L., SIEVING, K.E. & AVERY, M.L. 2002. Use of sensory cues by Fish Crows Corvus ossifragus preying on artificial bird nests. Journal of Avian Biology 33: 245-252. doi:10.1034/j.1600-048X.2002.330306.x

SAUNDERS, G.R., GENTLE, M.N. & DICKMAN, C.R. 2010. The impacts and management of foxes Vulpes vulpes in Australia. Mammal Review 40: 181-211. doi:10.1111/j.1365-2907.2010.00159.x

SCHOENER, T.W., SPILLER, D.A. & LOSOS, J.B. 2001. Predators increase the risk of catastrophic extinction of prey populations. Nature 412: 183-186. doi:10.1038/35084071

SHANNON, K., WESTON, M.A. & WHISSON, D.A. 2014. Sex bias in captured Little Raven Corvus mellori varies with entry aperture size in a modified Australian crow trap. Corella 38: 22-23.

SHINE, R. 2010. The ecological impact of invasive Cane Toads (Bufo marinus) in Australia. The Quarterly Review of Biology 85: 253-291. doi:10.1086/655116

STOKES, D.L. & BOERSMA, P.D. 1998. Nest-site characteristics and reproductive success in Magellanic Penguins (Spheniscus magellanicus). The Auk 115: 34-49. doi:10.2307/4089109

SUTHERLAND, D.R. & DANN, P. 2014. Population trends in a substantial colony of Little Penguins: Three independent measures over three decades. Biodiversity and Conservation 23: 241-250. doi:10.1007/s10531-013-0597-y

SWINBURNE, N. & JESSOP, R. 2005. Behaviour of the Little Raven Corvus mellori on Phillip Island, Victoria. Australian Field Ornithology 22: 137-145.

TAN, L.X.L., VAN DONGEN, W.F.D., SHERMAN, C.D.H. ET AL. 2021. Transmission of a novel predatory behaviour is not restricted to kin. Biological Invasions 23: 2473-2484. doi:10.1007/s10530-021-02517-4

TROSCIANKO, J., VON BAYERN, A.M.P., CHAPPELL, J., RUTZ, C. & MARTIN, G.R. 2012. Extreme binocular vision and a straight bill facilitate tool use in New Caledonian Crows. Nature Communications 3: 1110. doi:10.1038/ncomms2111

UETA, M. & HIRANO, T. 2006. Population decline of Japanese Lesser Sparrowhawks breeding in Tokyo and Utsunomiya, central Japan. Ornithological Science 5: 165-169. doi:10.2326/1347-0558(2006)5[165:PDOJLS]2.0.CO;2

UETA, M., KUROSAWA, R., HAMAO, S., KAWACHI, H. & HIGUCHI, H. 2003. Population change of Jungle Crows in Tokyo. Global Environmental Research 7: 131-137.

WARHAM, J. 1958. The nesting of the Little Penguin Eudyptula minor. Ibis 100: 605-616. doi:10.1111/j.1474-919X.1958.tb07963.x

WARREN, J.H. 1990. Role of burrows as refuges from subtidal predators of temperate Mangrove Crabs. Marine Ecology Progress Series 67: 295-299. doi:10.3354/meps067295

WIEBE, K.L., KOENIG, W.D. & MARTIN, K. 2007. Costs and benefits of nest reuse versus excavation in cavity-nesting birds. Annales Zoologici Fennici 44: 209-217. [Accessed at http://www.jstor.org/stable/23736733 in May 2021.]

YOUNG, E. 1994. Skua and Penguin: Predator and Prey. Cambridge, UK: Cambridge University Press. doi:10.1017/CBO9780511565311

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