Investigating the impact of black rats (Rattus rattus) on the endemic and threatened avifauna of Christmas Island
Rosalie Willacy
A * , Samantha Flakus B , Eve McDonald-Madden A and Sarah Legge A C
A School of Earth and Environmental Sciences, The University of Queensland, St Lucia, Qld 4072, Australia.
B Parks Australia, Christmas Island, WA 6798, Australia.
C Research Institute of Environment and Livelihoods, Charles Darwin University, Casuarina, NT 0810, Australia.
Abstract
Invasive mammalian predators are a primary cause of extinctions, especially on islands. Baseline data on the impact of invasive mammalian predators are critical for deciding whether their eradication or control should be attempted, and for monitoring ecosystem changes over time if control does occur. Christmas Island is a tropical island with multiple invasive species, including two mammalian predators (black rats, Rattus rattus and feral cats, Felis catus). Black rats are known to prey upon island bird species (including their nests) elsewhere, but the severity of their impacts on Christmas Island birds is unclear. Describing these impacts would help managers decide whether rat control is warranted, especially as a cat eradication program underway on the island could conceivably result in increased rat density.
In this study, we quantify the impacts of rats on Christmas Island bird abundance and nesting success.
The abundance of four endemic forest bird species/subspecies (Christmas Island imperial pigeon, Ducula whartoni, emerald dove, Chalcophaps indica natalis, thrush, Turdus poliocephalus erythropleurus and white-eye, Zosterops natalis) was measured using transect surveys. Nest success was measured using remote sensing camera surveillance for one forest bird species (thrush) and one seabird species (red-tailed tropicbird, Phaethon rubicaudra westralis). We explored whether these measures were related to spatial variation in rat density and activity (measured by trapping and inkcards), the presence of other invasive species, habitat and seasonal variables.
Neither rat density nor activity explained the abundance of any forest bird species. Instead, seasonal and habitat features were more consistent predictors of bird abundance. White-eyes were more abundant near yellow crazy ant (Anoplolepis gracilipes) supercolonies. Nest success for thrushes and red-tailed tropicbirds was either not, or only very weakly, influenced by rats.
Black rats currently have little effect on the population sizes and nesting success of Christmas Island birds.
This study suggests that rat control is not currently a management priority, but ongoing monitoring of rat density, activity, and impacts is needed to ensure management can respond promptly if rat density or impacts change as cat control progresses towards eradication.
Keywords: black rat impact, forest birds, invasive species management, island, island birds, mesopredator release, nest predation, seabirds.
References
Abe T (2007) Predator or disperser? A test of indigenous fruit preference of alien rats (Rattus rattus) on Nishi-jima (Ogasawara Islands). Pacific Conservation Biology 13(3), 213-218.
| Crossref | Google Scholar |
Algar D, Johnston M (2010) Proposed management plan for cats and black rats on Christmas Island. (Western Australian Department of Environment and Conservation) Available at https://library.dbca.wa.gov.au/static/FullTextFiles/025426.pdf
Bal P, Rhodes JR, Carwardine J, Legge S, Tulloch A, Game E, Martin TG, Possingham HP, McDonald-Madden E (2021) How to choose a cost-effective indicator to trigger conservation decisions? Methods in Ecology and Evolution 12(3), 520-529.
| Crossref | Google Scholar |
Barton K (2020) Package “MuMIn” multi-model inference (1.43.17). Available at https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67(1), 1-48.
| Crossref | Google Scholar |
Bergstrom DM, Lucieer A, Kiefer K, Wasley J, Belbin L, Pedersen TK, Chown SL (2009) Indirect effects of invasive species removal devastate World Heritage Island. Journal of Applied Ecology 46(1), 73-81.
| Crossref | Google Scholar |
Bird JP, Martin R, Akçakaya HR, Gilroy J, Burfield IJ, Garnett ST, Symes A, Taylor J, Şekercioğlu ÇH, Butchart SHM (2020) Generation lengths of the world’s birds and their implications for extinction risk. Conservation Biology 34(5), 1252-1261.
| Crossref | Google Scholar |
Bivand R (2021) Tools for handling spatial objects [R package maptools version 1.1-1]. Comprehensive R Archive Network (CRAN). Available at https://CRAN.R-project.org/package=maptools
Blackburn TM, Cassey P, Duncan RP, Evans KL, Gaston KJ (2004) Avian extinction and mammalian introductions on oceanic islands. Science 305(5692), 1955-1958.
| Crossref | Google Scholar |
Boeken M (2016) Breeding success of Red-billed Tropicbirds Phaethon aethereus on the Caribbean Island of Saba. Ardea 104(3), 263-271.
| Crossref | Google Scholar |
Bolam FC, Mair L, Angelico M, Brooks TM, Burgman M, Hermes C, Hoffmann M, Martin RW, McGowan PJK, Rodrigues ASL, Rondinini C, Westrip JRS, Wheatley H, Bedolla-Guzmán Y, Calzada J, Child MF, Cranswick PA, Dickman CR, Fessl B, Fisher DO, Garnett ST, Groombridge JJ, Johnson CN, Kennerley RJ, King SRB, Lamoreux JF, Lees AC, Lens L, Mahood SP, Mallon DP, Meijaard E, Méndez-Sánchez F, Percequillo AR, Regan TJ, Renjifo LM, Rivers MC, Roach NS, Roxburgh L, Safford RJ, Salaman P, Squires T, Vázquez-Domínguez E, Visconti P, Woinarski JCZ, Young RP, Butchart SHM (2021) How many bird and mammal extinctions has recent conservation action prevented? Conservation Letters 14(1), 21.
| Crossref | Google Scholar |
Bonnaud E, Medina FM, Vidal E, Nogales M, Tershy B, Zavaleta E, Donlan CJ, Keitt B, Le Corre M, Horwath SV (2011) The diet of feral cats on islands: a review and a call for more studies. Biological Invasions 13(3), 581-603.
| Crossref | Google Scholar |
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Mächler M, Bolker BM (2017) Modeling zero-inflated count data with glmmTMB. BioRxiv 2017, 132753.
| Crossref | Google Scholar |
Burnham KP, Anderson DR (2002) ‘Model selection and multimodel inference’. (Springer: New York) 10.1007/B97636
Carlsson NOL, Sarnelle O, Strayer DL (2009) Native predators and exotic prey –an acquired taste? Frontiers in Ecology and the Environment 7(10), 525-532.
| Crossref | Google Scholar |
Davis NE, O’Dowd DJ, Green PT, Nally RM (2008) Effects of an alien ant invasion on abundance, behavior, and reproductive success of endemic island birds. Conservation Biology 22(5), 1165-1176.
| Crossref | Google Scholar |
DIISE (2015) The database of island invasive species eradications, developed by Island Conservation, University of California, Santa Cruz, IUCN Species Survival Commission Invasive Species Specialist Group, University of Auckland and Landcare Research New Zealand. Available at http://diise.islandconservation.org
Doherty TS, Glen AS, Nimmo DG, Ritchie EG, Dickman CR (2016) Invasive predators and global biodiversity loss. Proceedings of the National Academy of Sciences of the United States of America 113(40), 11261-11265.
| Crossref | Google Scholar |
Dowding JE, Murphy EC, Springer K, Peacock AJ, Krebs CJ (2009) Cats, rabbits, Myxoma virus, and vegetation on Macquarie Island: a comment on Bergstrom et al. (2009). Journal of Applied Ecology 46(5), 1129-1132.
| Crossref | Google Scholar |
Dueñas M-A, Hemming DJ, Roberts A, Diaz-Soltero H (2021) The threat of invasive species to IUCN-listed critically endangered species: a systematic review. Global Ecology and Conservation 26, e01476.
| Crossref | Google Scholar |
Efford M (2017) Secr 3.1 – spatially explicit capture–recapture in R. Available at https://mran.microsoft.com/snapshot/2017-10-27/web/packages/secr/vignettes/secr-overview.pdf.
Efford M (2021) Habitat masks in the package secr. Available at https://www.otago.ac.nz/density/pdfs/secr-habitatmasks.pdf
Fleet RR (1972) Nesting success of the red-tailed tropicbird on Kure Atoll. The Auk 89(3), 651-659.
| Crossref | Google Scholar |
Fleet RR (1974) The red-tailed tropicbird on Kure Atoll. Ornithological Monographs 16, iii-64.
| Crossref | Google Scholar |
Flores M, Lazo P, Campbell G, Simeone A (2017) Breeding status of the red-tailed tropicbird (Phaethon rubricauda) and threats to its conservation on Easter Island (Rapa Nui). Pacific Science 71(2), 149-160.
| Crossref | Google Scholar |
Geoscience Australia (2013) Christmas Island GIS 2013 datasets. Available at https://data.gov.au/dataset/ds-ga-24c5ba9d-03ed-e3b2-e053-10a3070a0ee1/details?q=
Gillies CA, Williams D (2013) DOC tracking tunnel guide v2.5.2: using tracking tunnels to monitor rodents and mustelids. (Department of Conservation, Science & Capability Group) Available at www.doc.govt.nz
Glen AS, Atkinson R, Campbell KJ, Hagen E, Holmes ND, Keitt BS, Parkes JP, Saunders A, Sawyer J, Torres H (2013) Eradicating multiple invasive species on inhabited islands: the next big step in island restoration? Biological Invasions 15(12), 2589-2603.
| Crossref | Google Scholar |
Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. Journal of Evolutionary Biology 24(4), 699-711.
| Crossref | Google Scholar |
Halpin L, Terrington D, Jones H, Mott R, Wong WW, Dow D, Carlile N, Clarke R (2021) Arthropod predation of vertebrates structures trophic dynamics in island ecosystems. Dryad Dataset. Available at https://datadryad.org/stash/dataset/doi:10.5061/dryad.9kd51c5g2
Harper GA, Bunbury N (2015) Invasive rats on tropical islands: their population biology and impacts on native species. Global Ecology and Conservation 3, 607-627.
| Crossref | Google Scholar |
IUCN (2017) The IUCN red list of threatened species, version 2017-2. Available at http://www.iucnredlist.org
James DJ, McAllen IAW (2014) The birds of Christmas Island, Indian Ocean: a review. Australian Field Ornithology 31(Supplement), S1-S175.
| Google Scholar |
James DJ, Green PT, Humphreys WF, Woinarski JCZ (2019) Endemic species of Christmas Island, Indian Ocean. Records of the Western Australian Museum 34(2), 55-114.
| Crossref | Google Scholar |
Jones HP, Tershy BR, Zavaleta ES, Croll DA, Keitt BS, Finkelstein ME, Howald GR (2008) Severity of the effects of invasive rats on seabirds: a global review. Conservation Biology 22(1), 16-26.
| Crossref | Google Scholar |
Jones HP, Holmes ND, Butchart SHM, Tershy BR, Kappes PJ, Corkery I, Aguirre-Muñoz A, Armstrong DP, Bonnaud E, Burbidge AA, Campbell K, Courchamp F, Cowan PE, Cuthbert RJ, Ebbert S, Genovesi P, Howald GR, Keitt BS, Kress SW, Miskelly CM, Oppel S, Poncet S, Rauzon MJ, Rocamora G, Russell JC, Samaniego-Herrera A, Seddon PJ, Spatz DR, Towns DR, Croll DA (2016) Invasive mammal eradication on islands results in substantial conservation gains. Proceedings of the National Academy of Sciences 113(15), 4033-4038.
| Crossref | Google Scholar |
Legge S, Murphy BP, McGregor H, Woinarski JCZ, Augusteyn J, Ballard G, Baseler M, Buckmaster T, Dickman CR, Doherty T, Edwards G, Eyre T, Fancourt BA, Ferguson D, Forsyth DM, Geary WL, Gentle M, Gillespie G, Greenwood L, Hohnen R, Hume S, Johnson CN, Maxwell M, McDonald PJ, Morris K, Moseby K, Newsome T, Nimmo D, Paltridge R, Ramsey D, Read J, Rendall A, Rich M, Ritchie E, Rowland J, Short J, Stokeld D, Sutherland DR, Wayne AF, Woodford L, Zewe F (2017) Enumerating a continental-scale threat: how many feral cats are in Australia? Biological Conservation 206, 293-303.
| Crossref | Google Scholar |
Luna N, Varela AI, Brokordt K, Luna-Jorquera G (2018) Assessing potential predation risk by introduced predators on unattended eggs in the red-tailed tropicbird, Phaethon rubricauda, on Rapa Nui (Easter Island). Tropical Conservation Science 11,.
| Crossref | Google Scholar |
Medina FM, Bonnaud E, Vidal E, Tershy BR, Zavaleta ES, Josh Donlan C, Keitt BS, Le Corre M, Horwath SV, Nogales M (2011) A global review of the impacts of invasive cats on island endangered vertebrates. Global Change Biology 17(11), 3503-3510.
| Crossref | Google Scholar |
Oksanen J (2020) Package “vegan” (2.5-7). CRAN. Available at https://cran.r-project.org/web/packages/vegan/index.html
Oppel S, Burns F, Vickery J, George K, Ellick G, Leo D, Hillman JC (2014) Habitat-specific effectiveness of feral cat control for the conservation of an endemic ground-nesting bird species. Journal of Applied Ecology 51(5), 1246-1254.
| Crossref | Google Scholar |
Ortega S, Rodríguez C, Mendoza-Hernández B, Drummond H (2021) How removal of cats and rats from an island allowed a native predator to threaten a native bird. Biological Invasions 23, 2749-2761.
| Crossref | Google Scholar |
O’Rourke RL, Anson JR, Saul AM, Banks PB (2020) Limits to alien black rats (Rattus rattus) acting as equivalent pollinators to extinct native small mammals: the influence of stem width on mammal activity at native Banksia ericifolia inflorescences. Biological Invasions 22(2), 329-338.
| Crossref | Google Scholar |
Pattemore DE, Wilcove DS (2012) Invasive rats and recent colonist birds partially compensate for the loss of endemic New Zealand pollinators. Proceedings of the Royal Society B: Biological Sciences 279(1733), 1597-1605.
| Crossref | Google Scholar |
Pianka ER (2008) Optimal reproductive tactics. In ‘Encyclopedia of ecology, five-volume set.’ pp. 2567–2572. (Academic Press) 10.1016/B978-008045405-4.00841-7
Ratcliffe N, Bell M, Pelembe T, Boyle D, Benjamin R, White R, Godley B, Stevenson J, Sanders S (2010) The eradication of feral cats from Ascension Island and its subsequent recolonization by seabirds. Oryx 44(1), 20-29.
| Crossref | Google Scholar |
Rayner MJ, Hauber ME, Imber MJ, Stamp RK, Clout MN (2007) Spatial heterogeneity of mesopredator release within an oceanic island system. Proceedings of the National Academy of Sciences 104(52), 20862-20865.
| Crossref | Google Scholar |
Rendall AR, Sutherland DR, Cooke R, White J (2014) Camera trapping: a contemporary approach to monitoring invasive rodents in high conservation priority ecosystems. PLoS ONE 9(3), e86592.
| Crossref | Google Scholar |
Ricklefs RE (1997) Comparative demography of new world populations of thrushes (Turdus Spp.). Ecological Monographs 67(1), 23-43.
| Crossref | Google Scholar |
Ringler D, Russell JC, le Corre M (2015) Trophic roles of black rats and seabird impacts on tropical islands: mesopredator release or hyperpredation? Biological Conservation 185, 75-84.
| Crossref | Google Scholar |
Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecology Letters 12(9), 982-998.
| Crossref | Google Scholar |
Roper JJ, Sullivan KA, Ricklefs RE (2010) Avoid nest predation when predation rates are low, and other lessons: testing the tropical-temperate nest predation paradigm. Oikos 119(4), 719-729.
| Crossref | Google Scholar |
RStudio Team (2021) RStudio: integrated development for R. RStudio, PBC. Available at http://www.rstudio.com/
Russell JC, Kaiser-Bunbury CN (2019) Consequences of multispecies introductions on island ecosystems. Annual Review of Ecology, Evolution, and Systematics 50(1), 169-190.
| Crossref | Google Scholar |
Sandvik H, Einar Erikstad K (2008) Seabird life histories and climatic fluctuations: a phylogenetic-comparative time series analysis of North Atlantic Seabirds. Ecography 31(1), 73-83 Available at http://www.jstor.org/stable/30244552.
| Crossref | Google Scholar |
Saunier M, Amy M, Barbraud C, Pinet P, Ringler D, Russell JC, Le Corre M (2022) Seabird predation effects and population viability analysis indicate the urgent need for rat eradication from Europa Island, western Indian Ocean. Avian Conservation & Ecology 17(1), 32.
| Crossref | Google Scholar |
Schloerke B (2020) GGally: extension to “ggplot2”. CRAN. Available at https://cran.r-project.org/web/packages/GGally/index.html
Simberloff D, Keitt B, Will D, Holmes N, Pickett E, Genovesi P (2018) Yes we can! Exciting progress and prospects for controlling invasives on islands and beyond. Western North American Naturalist 78(4), 942-958 Available at https://scholarsarchive.byu.edu/wnan/vol78/iss4/50.
| Crossref | Google Scholar |
Szabo JK, Khwaja N, Garnett ST, Butchart SHM (2012) Global patterns and drivers of avian extinctions at the species and subspecies level. PLoS ONE 7(10), e47080.
| Crossref | Google Scholar |
Towns DR, Atkinson IAE, Daugherty CH (2006) Have the harmful effects of introduced rats on islands been exaggerated? Biological Invasions 8(4), 863-891.
| Crossref | Google Scholar |
Travers T, Lea M-A, Alderman R, Terauds A, Shaw J (2021) Bottom-up effect of eradications: the unintended consequences for top-order predators when eradicating invasive prey. Journal of Applied Ecology 58(4), 801-811.
| Crossref | Google Scholar |
Vanderwerf EA, Young LC (2014) Breeding biology of red-tailed tropicbirds Phaethon rubricauda and response to predator control on O’ahu, Hawai’i. Marine Ornithology 42, 73-76 Available at http://www.marineornithology.org/content/get.cgi?ident=42_1_73-76.
| Google Scholar |
VanderWerf EA, Crampton LH, Diegmann JS, Atkinson CT, Leonard DL (2014) Survival estimates of wild and captive-bred released Puaiohi, an endangered Hawaiian thrush. The Condor 116(4), 609-618.
| Crossref | Google Scholar |
Varela AI, Luna N, Luna-Jorquera G (2018) Assessing potential Argentine Ant recruitment to pipping eggs in the red-tailed tropicbird on Rapa Nui (Easter Island). Emu – Austral Ornithology 118(4), 381-385.
| Crossref | Google Scholar |
Vernes K, McGrath K (2009) Are introduced black rats (Rattus rattus) a functional replacement for mycophagous native rodents in fragmented forests? Fungal Ecology 2(3), 145-148.
| Crossref | Google Scholar |
Walker K, Porritt K, Sexton M (2014) Christmas Island vegetation and clearing dataset. Available at https://researchdata.edu.au/christmas-island-vegetation-clearing-dataset/1288111
Willacy RJ, Flakus S, Macgregor NA, Bell E, Tiernen B, James DJ, McAllen IAW, Woinarski JCK, Clarke RH, Brown SM, Baker GB, Garnett ST (2021) Indian Ocean red-tailed tropicbird Phaethon rubricauda westralis. In ‘The action plan for Australian birds’. (Eds ST Garnett, GB Baker) pp. 33–36. (CSIRO Publishing)
Wirtz WO (1972) Population ecology of the Polynesian Rat, Rattus exulans, on Kure Atoll, Hawaii. (University of Hawaii Press) Available at http://scholarspace.manoa.hawaii.edu/handle/10125/449
Woodward PW (2017) The natural history of Kure Atoll, northwestern Hawaiian islands. Atoll Research Bulletin 164, 1-318.
| Google Scholar |
Wyatt KB, Campos PF, Gilbert MTP, Kolokotronis S-O, Hynes WH, DeSalle R, Daszak P, MacPhee RDE, Greenwood AD (2008) Historical mammal extinction on Christmas Island (Indian Ocean) correlates with introduced infectious disease. PLoS ONE 3(11), e3602.
| Crossref | Google Scholar |
Zarzoso-Lacoste D, Ruffino L, Vidal E (2011) Limited predatory capacity of introduced black rats on bird eggs: an experimental approach. Journal of Zoology 285(3), 188-193.
| Crossref | Google Scholar |
Zavaleta ES, Hobbs RJ, Mooney HA (2001) Viewing invasive species removal in a whole-ecosystem context. Trends in Ecology & Evolution 16(8), 454-459.
| Crossref | Google Scholar |
