Seabirds are considered ecosystem engineers, because they facilitate ecosystem functioning (e.g., nutrient cycling), crucial for other marine and terrestrial species, including reptiles. However, studies of seabird-reptile interactions are limited. Here, we assessed the influence of the ‘Critically Endangered’ Whenua Hou Diving Petrel (Pelecanoides whenuahouensis) on the occurrence of two threatened skinks, Stewart Island green skink (Oligosoma aff. chloronoton) and southern grass skink (O. aff. polychroma). We surveyed skinks for 26 consecutive days at 51 sites with and 48 sites without Diving Petrel burrows in the dunes on Codfish Island (Whenua Hou), New Zealand. We used occupancy modelling to assess the influence of burrows on the occurrence of skinks, while accounting for other factors affecting occupancy (Ψ) and detection probabilities (p). Diving Petrel burrows had a contrasting effect on the occurrence of skinks. On average, Ψ̂ of Stewart Island green skinks was 114% higher at sites with burrows compared to sites without, while Ψ̂ of southern grass skinks was only 2% higher. Occurrence of both skinks was negatively influenced by the presence of the other skink species. On average p̂ were low: 0.013 and 0.038 for Stewart Island green and southern grass skinks, respectively. Stewart Island green skinks appear attracted to burrows, which might facilitate thermoregulation (i.e., shelter from temperature extremes). The larger Stewart Island green skinks may subsequently exclude the smaller southern grass skinks at burrows, causing the contrasting relationships. We suggest that these interspecific interactions should be considered when implementing conservation management, e.g., through the order of species reintroductions.
Andersson, D. R. 2008. Model Based Inference in the Life Sciences: A Primer on Evidence. Springer, Berlin.
Andersson, M., A. Krockenberger and L. Schwarzkopf. 2010. Experimental manipulation reveals the importance of refuge habitat temperature selected by lizards. Austral Ecol. 35: 294–299.
Armstrong, D.P. 2016. Using reference sites to account for detection probability in occupancy surveys for freshwater turtles. Herpetol. Conserv. Biol. 11: 505–518.
Bancroft, W.J., D.J. Roberts and M.J. Garkalis. 2005. Burrowing seabirds drive decreased diversity and structural complexity, and increased productivity in insular-vegetation communities. Aust. J. Bot. 53: 231–241.
Berry, O., M.D. Tocher, D.M. Gleeson and S.D. Sarre. 2005. Effect of vegetation matrix on animal dispersal: genetic evidence from a study of endangered skinks. Conserv. Biol. 19: 855–864.
Burnham, K.P. and D.A. Anderson. 2002. Model Selection and Multimodel Inference: A Practical Information-theoretic Approach. Springer, New York.
Buxton, R.T., C.J. Jones, P.O. Lyver, D.R. Towns and S.B. Borelle. 2016. Deciding when to lend a helping hand: a decision-making framework for seabird island restoration. Biodivers. Conserv. 25: 467–484.
Capizzi, D., L. Luiselli and L. Vignoli. 2007. Flight initiation distance in relation to substratum type, sex, reproductive status and tail condition in two lacertids with contrasting habitats. Amphibia-Reptilia 28: 403–407.
Cheke, A. and J.P. Hume. 2008. Lost Land of the Dodo: An Ecological History of Mauritius, Reunion & Rodrigues. Bloomsbury Publishing, London.
Cole, R. 2004. Summary of South Georgian Diving Petrel field observations for 2003/04, Codfish Island/Whenua Hou. Department of Conservation, Invercargill.
Corkery, I., B. Bell and N. Nelson. 2014. Investigating kleptothermy: A Reptile-Seabird association with thermal benefits. Physiol. Biochem. Zool. 87: 216–221.
Corkery, I., B.D. Bell and N.J. Nelson. 2015. Is the breeding behaviour of nesting seabirds influenced by the presence of a predatory reptile—the tuatara?, J. Roy. Soc. New Zeal. 45: 21–30.
de Lange, P.J., J.R. Rolfe, P.D. Champion, S.P. Courtney, P.B. Heenan, J.W. Barkla, E.K. Cameron, D.A. Norton and R.A. Hitchmough. 2013. Conservation status of New Zealand indigenous vascular plants, 2012. Department of Conservation, Wellington
Downes, S. and R. Shine. 1998. Heat, safety or solitude? Using habitat selection experiments to identify a lizard's priorities. Anim. Behav. 55: 1387–1396
Du, W.G., L. Shou and J.Y. Shen. 2006. Habitat selection in two sympatric Chinese skinks, Eumeces elegans and Sphenomorphus indicus: do thermal preferences matter? Can. J. Zool. 84: 1300–1306.
Duncan, R.P. and T.M. Blackburn. 2004. Extinction and endemism in the New Zealand avifauna. Global. Ecol. Biogeogr. 13: 509–517.
Ellis, J.C. 2005. Marine birds on land: a review of plant biomass, species richness, and community composition in seabird colonies. Plant Ecol. 181: 227–241.
Enge, K.M. 2001 The pitfalls of pitfall traps. J. Herptol. 35: 467–478.
Epskamp, S., G. Costantini, J. Haslbeck, A.O.J. Cramer, L.J. Waldorp, V.D. Schmittmann and D Borsboom. 2017. qgraph - Graph plotting methods, psychometric data visualisations and graphical model estimation. R package version 1.4.4. CRAN.
Fischer, J.H., J. Chambon, I. Debski, J.A. Hiscock, R. Cole, G.A. Taylor and H.U. Wittmer. 2018a. Buffering artificial nest boxes for Procellariiformes breeding in exposed habitats: investigating effects on temperature and humidity. Notornis 65: 35–41.
Fischer, J.H., I. Debski, C.M. Miskelly, A.J.D. Tennyson, A. Fromant, J. Tessler, J.A. Hiscock, R. Cole, C.A. Bost, G.A. Taylor and H.U. Wittmer. 2018b. Analyses of phenotypic differentiations between South Georgian Diving Petrel (Pelecanoides georgicus) populations reveal an undescribed and highly-endangered species from New Zealand. PLoS ONE 13 (6): e0197766.
Fischer, J.H., I. Debski, G.A. Taylor and H.U. Wittmer. 2017a. Assessing the suitability of non-invasive methods to monitor interspecific interactions and breeding biology of the South Georgian diving petrel (Pelecanoides georgicus). Notornis 64: 13–20.
Fischer, J.H., I. Debski, G.A. Taylor and H.U. Wittmer. 2018c. Nest site selection of South Georgia diving-petrels, Pelecanoides georgicus on Codfish Island, New Zealand: implications for conservation management. Bird Conserv. Int. 28: 216–227.
Fischer, J.H., F.O. Hjorsvarsdottir, J.A. Hiscock, I. Debski, G.A. Taylor GA and H.U. Wittmer. 2017b. Confirmation of the extinction of South Georgian diving petrels (Pelecanoides georgicus) on Enderby Island. Notornis 64: 48–51.
Fischer, J.H., H. U. Wittmer, E. Setiawan, S. Jaffe and A.J. Marshall. 2017c. Incipient loss of a rainforest mutualism?, J. Threat. Taxa 9: 9734–9737.
Fukami, T., D.A. Wardle, P.J. Bellingham, C.P.H. Mulder, D.R. Towns, G.W. Yeates, K.I Bonner, M.S. Durrett, M.N. Grant-Hoffman and W. M. Williamson. 2006. Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems. Ecol. Lett. 9: 1299–1307.
Graham, N.A.J., S.K. Wilson, P. Carr, A.S. Hoey, S. Jennings and M.A. MacNeil. 2018. Seabirds enhance coral reef productivity and functioning in the absence of invasive rats. Nature 559: 250–253.
Heine, J.C. and T. W. Speir TW. 1989. Ornithogenic soils of the Cape Bird Adelie penguin rookeries, Antarctica. Polar Biol. 10: 89–100.
Herbert, S. and T. Bell. 2012. Survey design options for monitoring lizards at Baring Head, East Harbour Regional Park. EcoGecko Consultants, New Plymouth.
Hines, J.E. 2006. PRESENCE – Software to estimate patch occupancy and related parameters. USGS-PWRC. http://www.mbr-pwrc.usgs.gov/software/presence.html.
Hitchmough, R., B. Barr, M. Lettink, J. Monks, R. Reardon, M. Tocher, D. van Winkel and J. Rolfe. 2016. Conservation status of New Zealand reptiles, 2015. Department of Conservation, Wellington.
Holdaway, R.N., M.D. Jones and N.R.B Athfield. 2003. Establishment and extinction of a population of South Georgian diving petrel (Pelecanoides georgicus) at Mason Bay, Steward Island, New Zealand, during the late Holocene. J. Roy. Soc. New Zeal. 33: 601–622.
Jewell, T. 2017. Skinks of Southern New Zealand (2nd Ed.). Online publication [accessed on 13 February 2018].
Lameris, T.K., J.R. Bennett, L.K. Blight, M. Giessen, M.H. Janssen, J.J.H.J. Schaminee and P. Arcese. 2016. A century of ecosystem change: human and seabird impacts on plant species extirpation and invasion on islands. PeerJ 4: e2208.
Lorrain, A., F. Houlbreque, F. Benzoni, L. Barjon, L. Tremblay-Boyer, C. Menkes, D.P. Gillikin, C. Payri, H. Jourdan, G. Boussarie, A. Verheyden and E. Vidal. 2017. Seabirds supply nitrogen to reef-building corals on remote Pacific islets. Sci. Rep. 7: 3721.
MacKenzie, D. I., L.L. Bailey and J.D. Nichols. 2004. Investigating species co-occurrence patterns when species are detected imperfectly. J. Anim. Ecol. 73: 546–555.
MacKenzie, D.I., J.D. Nichols, J.E. Hines, M.G. Knutson and A.B. Franklin. 2003. Estimating site occupancy, colonization, and local extinction probabilities when a species is detected imperfectly. Ecology 84: 2200–2207.
MacKenzie, D.I., J.D. Nichols, G.B. Lachman, S. Droege, J.A. Royle and C.A. Langtimm. 2002. Estimating site occupancy rates when detection probabilities are less than one. Ecology 83: 2248–2255.
MacKenzie, D.I., J.D. Nichols, J.A. Royle, K.H. Pollock, L.L. Bailey and J.E. Hines. 2018. Occupancy estimation and modelling – Inferring patterns and dynamics of species occurrence. 2nd edition. Elsevier, London.
Markwell, T.J. and C.H. Daugherty. 2002. Invertebrate and lizard abundance is greater on seabird-inhabited islands than on seabird-free islands in the Marlborough Sounds, New Zealand. Ecoscience 9: 293–299.
McClelland, P.J. 2002. Eradication of Pacific rats from Whenua Hou Nature Reserve (Codfish Island), Putauhinu and Rarotoka Isl ands, New Zealand. Turning the tide: eradication of invasive species 27: 173–181.
Melzer, S., T. Bell and G.B. Patterson. 2017. Hidden conservation vulnerability within a cryptic species complex: taxonomic revision of the spotted skink (Oligosoma lineoocellatum; Reptilia: Scincidae) from New Zealand. Zootaxa 4300: 355–379.
Middleton, A. 2007. Two hundred years on Codfish Island (Whenuahou). Department of Conservation, Invercargill.
Milne, T., C.M. Bull and M.N. Hutchinson. 2003. Use of burrows by the endangered pygmy blue-tongue lizard, Tiliqua adelaidensis (Scincidae). Wildlife Res. 30: 523–528.
Miskelly, C.M. and G.A. Taylor. 2004. Establishment of a colony of Common Diving Petrels (Pelecanoides urinatrix) by chick transfers and acoustic attraction. Emu 104: 205–211.
Miskelly, C.M., G.A. Taylor, H. Gummer and R. Williams. 2009. Translocations of eight species of burrow-nesting seabirds (genera, Pterodroma, Pelecanoides, Pachyptila and Puffinus: Family Procellaridae). Biol. Conserv. 142: 1965–1980.
Mulder, C.P. and S.N. Keall. 2001. Burrowing seabirds and reptiles: impact on seeds, seedlings and soils in an isl and forest in New Zealand. Oecologia 127: 350–360.
Orwin, K.H., D.A. Wardle, D.R. Towns, M.G. John, P.J. Bellingham, C. Jones, B.M. Fitzgerald, R.G. Parrish and P.O. Lyver. 2016. Burrowing seabird effects on invertebrate communities in soil and litter are dominated by ecosystem engineering rather than nutrient addition. Oecologia 180: 217–230.
Otero, X.L., S. de la Peña-Lastra, A. Pérez-Alberti, T.O. Ferreira and M.A. Huerta-Diaz. 2018. Seabird colonies as important drivers in the nitrogen and phosphorus cycles. Nat. Commun. 9: 246.
Petren, K. and T.J. Case. 1998. Habitat structure determines competition intensity and invasion success in gecko lizards. P. Natl. Acad. Sci. U.S.A. 95: 11739–11744.
Phillpot, P. 2000 The skinks of Northern Brother Island: Abundance, habitat use, and species interactions. MSc Thesis, Victoria Univ. of Wellington, Wellington.
R Development Core Team . 2016. R: A language and environment for statistical computing. Version 3.3.1. R Foundation for Statistical Computing, Vienna.
Richmont, O.M.W., J.E. Hines and S.R. Beissinger. 2010. Two-species occupancy models: a new parameterization applied to co-occurrence of secretive rails. Ecol. Appl. 20: 2036–2046.
Robertson, H.A., K. Baird, J.E. Dowding, G.P. Elliott, R.A. Hitchmough, C.M. Miskelly, N. McArthur, C.F.J. O'Donnell, P.M. Sagar, R.P. Scofield and G.A. Taylor. 2017. Conservation status of New Zealand birds, 2016. Department of Conservation, Wellington.
Roughton, C.M. 2005. Assessment of Methods to Monitor Otago Skink and Grand Skink Populations, New Zealand. Department of Conservation, Wellington.
Seber, G.A.F. 1982. The Estimation of Animal Abundance and Related Parameters, 2nd Edition. Macmillan, New York.
Seddon, P.J., C.J. Griffiths, P.S. Soorae and D.P. Armstrong. 2014. Reversing defaunation: Restoring species in a changing world. Science 345: 406–412.
Seddon, P.J., C.M. Roughton, J. Reardon and D.I. MacKenzie. 2011. Dynamics of an endangered New Zealand skink: accounting for incomplete detectability in estimating patch occupancy. New Zeal. J. Ecol. 35: 247–253.
Şekercioǧlu, Ç., G.C. Daily and P.R. Ehrlich. 2004. Ecosystem consequences of bird declines. P. Natl. Acad. Sci. U.S.A. 101: 18042–18047.
Çekercioglu, Ç.H. 2006. Increasing awareness of avian ecological function. Trends Ecol. Evol. 21: 464–471.
Souter, N.J., C.M. Bull and M.N. Hutchinson. 2004. Adding burrows to enhance a population of the endangered pygmy blue tongue lizard, Tiliqua adelaidensis. Biol. Conserv. 116: 403–408.
Taylor, G.A. 2000a. Action Plan for Seabird Conservation in New Zealand. Part A: Threatened Seabirds. Department of Conservation, Wellington.
Taylor, G.A. 2000b. Action Plan for Seabird Conservation in New Zealand. Part B: Non-threatened Seabirds. Department of Conservation, Wellington.
Towns, D.R., D.A. Wardle, C.P.H. Mulder, G.W. Yeates, B.M. Fitzgerald, G.R. Parrish, P.J. Bellingham and K.I. Bonner. 2009. Predation of seabirds by invasive rats: multiple indirect consequences for invertebrate communities. Oikos 118: 420–430.
Trainor, S. 2008. Codfish Island South Georgian Diving Petrel: a summary of field observations 2004–2007 and recommendations for future management. Department of Conservation, Invercargill.
Trainor, S. 2009. South Georgian Diving Petrel: a summary of field observations 2007–2009 on Codfish Island. Department of Conservation, Invercargill.
Trewick, S.A. and G.C. Gibb. 2010. Vicars, tramps and assembly of the New Zealand avifauna: a review of molecular phylogenetic evidence. Ibis 152: 256–253.
Tylianakis, J.M., E. Laliberté, A. Nielsen and J. Bascompte. 2010. Conservation of species interaction networks. Biol. Conserv. 143: 2270–2279.
Valiente-Banuet, A., A.M. Aizen, J.M. Alcántara, J. Arroyo, A. Cocucci, M. Galetti, M.B. García, D. García, J.M. Gómez, P. Jordano, R. Medel, L. Navarro, J.R. Obeso, R. Oviedo, N. Ramírez, P.J. Rey, A. Traveset, M. Verdú and R. Zamora. 2015. Beyond species loss: the extinction of ecological interactions in a changing world. Funct. Ecol. 29: 299–307.
Walls, G. 1978. The influence of the tuatara on Fairy Prion breeding on Stephens Island, Cook Strait. New Zeal. J. Ecol. 1: 91–98.
Wardle, D.A., B.J. Bellingham, K.I. Boot and C.P.H. Mulder. 2009. Indirect effects of invasive predators on plant litter quality, decomposition and nutrient resorption on seabird-dominated islands. Ecology 90: 452–464.
Wickes, C. and B. Rance. 2010. Sealers Beach Vegetation Survey. Department of Conservation, Invercargill.
Wickham, H. 2009. ggplot2: Elegant Graphics for Data Analysis. Springer, New York.
Wood, J.R. 2016 Spatial distribution of late Holocene bird bones in the Mason Bay dune system, Stewart Island, New Zealand. J. Roy. Soc. New Zeal. 46: 103–116.
Wood, J.R. and S. Briden. 2008. South Georgian diving petrel (Pelecanoides georgicus) bones from a Maori midden in Otago Peninsula, New Zealand. Notornis 55: 46–47.
Wood, J.R., R.P. Scofield, J. Hamel, C. Lalas and J.M. Wilmshurst. 2017. Bone stable isotopes indicate a high trophic position for New Zealand's extinct South Island adzebill (Aptornis defossor) (Gruiformes: Aptornithidae). New Zeal. J. Ecol. 41: 240–244.