Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-10T14:10:34.754Z Has data issue: false hasContentIssue false
  • English
  • Français

The impact of parasites during range expansion of an invasive gecko

Published online by Cambridge University Press:  14 February 2018

Louise K. Barnett Open the ORCID record for Louise K. Barnett [Opens in a new window] ,
Ben L. Phillips ,
Allen C. G. Heath ,
Andrew Coates  and
Conrad J. Hoskin
Louise K. Barnett*
Affiliation:
College of Science and Engineering, James Cook University, Townsville, Queensland 4811, Australia
Ben L. Phillips
Affiliation:
School of Biosciences, University of Melbourne, Parkville, Victoria 3010, Australia
Allen C. G. Heath
Affiliation:
AgResearch Ltd, Hopkirk Research Institute, Palmerston North 4442, New Zealand
Andrew Coates
Affiliation:
School of Biosciences, University of Melbourne, Parkville, Victoria 3010, Australia
Conrad J. Hoskin
Affiliation:
College of Science and Engineering, James Cook University, Townsville, Queensland 4811, Australia
*
Author for correspondence: Louise K. Barnett, E-mail: louisekbarnett@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Host–parasite dynamics can play a fundamental role in both the establishment success of invasive species and their impact on native wildlife. The net impact of parasites depends on their capacity to switch effectively between native and invasive hosts. Here we explore host-switching, spatial patterns and simple fitness measures in a slow-expanding invasion: the invasion of Asian house geckos (Hemidactylus frenatus) from urban areas into bushland in Northeast Australia. In bushland close to urban edges, H. frenatus co-occurs with, and at many sites now greatly out-numbers, native geckos. We measured prevalence and intensity of Geckobia mites (introduced with H. frenatus), and Waddycephalus (a native pentastome). We recorded a new invasive mite species, and several new host associations for native mites and geckos, but we found no evidence of mite transmission between native and invasive geckos. In contrast, native Waddycephalus nymphs were commonly present in H. frenatus, demonstrating this parasite's capacity to utilize H. frenatus as a novel host. Prevalence of mites on H. frenatus decreased with distance from the urban edge, suggesting parasite release towards the invasion front; however, we found no evidence that mites affect H. frenatus body condition or lifespan. Waddycephalus was present at low prevalence in bushland sites and, although its presence did not affect host body condition, our data suggest that it may reduce host survival. The high relative density of H. frenatus at our sites, and their capacity to harbour Waddycephalus, suggests that there may be impacts on native geckos and snakes through parasite spillback.

Keywords

GeckobiaHemidactylus frenatushost–parasite dynamicsinvasive speciesmiteparasite releaseparasite spillbackpentastomeWaddycephalus
Type
Research Article
Information
Parasitology , Volume 145 , Issue 11 , September 2018 , pp. 1400 - 1409
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Present address: Global Ecology, College of Science and Engineering, Flinders University, Adelaide, South Australia 5001, Australia.

References

Ali, JH and Riley, J (1983) Experimental life-cycle studies of Raillietiella gehyrae Bovien, 1927 and Raillietiella frenatus Ali, Riley and Self, 1981: pentastomid parasites of geckos utilizing insects as intermediate hosts. Parasitology 86, 147–160.Google Scholar
Andreou, D, Arkush, KD, Guégan, J-F and Gozlan, RE (2012) Introduced pathogens and native freshwater biodiversity: a case study of Sphaerothecum destruens. PLoS ONE 7, e36998.Google Scholar
Barnett, LK, Phillips, BL and Hoskin, CJ (2017). Going feral: time and propagule pressure determine range expansion of Asian house geckos into natural environments. Austral Ecology (in press) 42, 165–175Google Scholar
Barton, DP (2007) Pentastomid parasites of the introduced Asian house gecko, Hemidactylus frenatus (Gekkonidae), in Australia. Comparative Parasitology 74, 254–259.Google Scholar
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.Google Scholar
Bauer, AM, Russell, AP and Dollahon, NR (1990) Skin folds in the gekkonid lizard genus Rhacodactylus: a natural test of the damage limitation hypothesis of mite pocket function. Canadian Journal of Zoology 68, 1196–1201.Google Scholar
Bolker, BM, Brooks, ME, Clark, CJ, Geange, SW, Poulsen, JR, Stevens, MHH and White, J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24, 127–135.Google Scholar
Bolker, B, Brooks, M, Gardner, B, Lennert, C and Minami, M (2012). Owls example: a zero-inflated, generalized linear mixed model for count data. 1–35. Available at https://groups.nceas.ucsb.edu/non-linear-modeling/projects/owls/WRITEUP/owls.pdfGoogle Scholar
Case, TJ and Taper, ML (2000) Competition, environmental gradients, gene flow and the coevolution of species’ borders. The American Naturalist 155, 583–605.Google Scholar
Coates, A, Barnett, LK, Hoskin, C and Phillips, BL (2017) Living on the edge: parasite prevalence changes dramatically across a range edge in an invasive gecko. The American Naturalist 189, 178–183.Google Scholar
Cole, NC, Jones, CG and Harris, S (2005) The need for enemy-free space: the impact of an invasive gecko on island endemics. Biological Conservation 125, 467–474.Google Scholar
Cox, NJ (2006) Speaking Stata: in praise of trigonometric predictors. Stata Journal 6, 561–579.Google Scholar
Crawley, MJ (2007). The R Book, 1st edn. Imperial College London at Silkwood Park, UK: John Wiley & Sons Ltd.Google Scholar
Dame, EA and Petren, K (2006) Behavioural mechanisms of invasion and displacement in Pacific island geckos (Hemidactylus). Animal Behaviour 71, 1165–1173.Google Scholar
Domrow, R (1992) Acari Astigmata (excluding feather mites) parasitic on Australian vertebrates: an annotated checklist, keys and bibliography. Invertebrate Systematics 6, 1459.Google Scholar
Domrow, R and Lester, LN (1985) Chiggers of Australia (Acari: Trombiculidae): an annotated checklist, keys and bibliograpy. Australian Journal of Zoology 114, 1–111.Google Scholar
Dunn, AM (2009) Parasites and Biological Invasions, 1st edn. London, UK: Elsevier Ltd. doi:10.1016/S0065-308X(08)00607-6.Google Scholar
Dunn, AM and Hatcher, MJ (2015) Parasites and biological invasions: parallels, interactions, and control. Trends in Parasitology 31, 189–199.Google Scholar
Dunn, AM, Torchin, ME, Hatcher, MJ, Kotanen, PM, Blumenthal, DM, Byers, JE, Coon, CAC, Frankel, VM, Holt, RD, Hufbauer, RA, Kanarek, AR, Schierenbeck, KA, Wolfe, LM and Perkins, SE (2012) Indirect effects of parasites in invasions. Functional Ecology 26, 1262–1274.Google Scholar
Floerl, O, Inglis, GJ, Dey, K and Smith, A (2009) The importance of transport hubs in stepping-stone invasions. Journal of Applied Ecology 46, 37–45.Google Scholar
Gendron, AD, Marcogliese, DJ and Thomas, M (2012) Invasive species are less parasitized than native competitors, but for how long? The case of the round goby in the Great Lakes-St. Lawrence Basin. Biological Invasions 14, 367–384.Google Scholar
Goldberg, SR and Bursey, CR (1991) Integumental lesions caused by ectoparasites in a wild population of the side-blotched lizard (Uta stansburiana). Journal of Wildlife Diseases 27, 68–73.Google Scholar
Goldberg, SR and Holshuh, HJ (1992) Ectoparasite-induced lesions in mite pockets of the Yarrow's spiny lizard, Sceloporus jarrovii (Phrynosomatidae). Journal of Wildlife Diseases 28, 537–541.Google Scholar
Hanley, KA, Fisher, RN and Case, TJ (1995) Lower mite infestations in an asexual gecko compared with its sexual ancestors. Evolution 49, 418–426.Google Scholar
Hartigan, A, Fiala, I, Dyková, I, Jirků, M, Okimoto, B, Rose, K, Phalen, DN and Šlapeta, J (2011) A suspected parasite spill-back of two novel Myxidium spp. (Myxosporea) causing disease in Australian endemic frogs found in the invasive Cane toad. PLoS ONE 6, e18871.Google Scholar
Heath, ACG and Whitaker, AH (2015) Mites (Acari: Pterygosomatidae, Macronyssidae) taken from lizards intercepted at the New Zealand border. Systematic and Applied Acarology 20, 739.Google Scholar
Hoskin, CJ, (2011) The invasion and potential impact of the Asian House Gecko (Hemidactylus frenatus) in Australia. Austral Ecology 36, 240–251.Google Scholar
Hudson, P and Greenman, J (1998) Competition mediated by parasites: biological and theoretical progress. Trends in Ecology and Evolution 13, 387–390.Google Scholar
Kelehear, C, Brown, GP and Shine, R (2013). Invasive parasites in multiple invasive hosts: the arrival of a new host revives a stalled prior parasite invasion. Oikos 122, 1317–1324.Google Scholar
Kelehear, C, Spratt, DM, O'Meally, D and Shine, R (2014a) Pentastomids of wild snakes in the Australian tropics. International Journal for Parasitology: Parasites and Wildlife 3, 20–31.Google Scholar
Kelehear, C, Saltonstall, K and Torchin, ME (2014b) An introduced pentastomid parasite (Raillietiella frenata) infects native cane toads (Rhinella marina) in Panama. Parasitology 142, 675–679.Google Scholar
Kelly, DW, Paterson, RA, Townsend, CR, Poulin, R and Tompkins, DM (2009) Parasite spillback: a neglected concept in invasion ecology. Ecology 90, 2047–2056.Google Scholar
Krakau, M, Thieltges, DW and Reise, K (2006) Native parasites adopt introduced bivalves of the North Sea. Biological Invasions 8, 919–925.Google Scholar
Lefèvre, T, Lebarbenchon, C, Gauthier-Clerc, M, Missé, D, Poulin, R and Thomas, F (2009) The ecological significance of manipulative parasites. Trends in Ecology and Evolution 24, 41–48.Google Scholar
Lever, C (2003) Naturalized Reptiles and Amphibians of the World. New York: Oxford University Press.Google Scholar
MacLeod, CJ, Paterson, AM, Tompkins, DM and Duncan, RP (2010) Parasites lost – do invaders miss the boat or drown on arrival? Ecology Letters 13, 516–527.Google Scholar
Menge, BA (1972) Competition for food between two intertidal starfish species and its effect on body size and feeding. Ecology 53, 635–644.Google Scholar
Miller, MA, Kinsella, JM, Snow, RW, Hayes, MM, Falk, BG, Reed, RN, Mazzotti, FJ, Guyer, C and Romagosa, CM (2017) Parasite spillover: indirect effects of invasive Burmese pythons. Ecology and Evolution 8, 830–840.Google Scholar
O'Dowd, DJ, Green, PT and Lake, PS (2003) Invasional “meltdown” on an oceanic island. Ecology Letters 6, 812–817.Google Scholar
Paré, JA (2008) An overview of pentastomiasis in reptiles and other vertebrates. Journal of Exotic Pet Medicine 17, 285–294.Google Scholar
Perkins, TA (2012) Evolutionarily labile species interactions and spatial spread of invasive species. The American Naturalist 179, E37–E54.Google Scholar
Perkins, SE, White, TA, Pascoe, EL and Gillingham, EL (2017) Parasite community dynamics in an invasive vole – from focal introduction to wave front. International Journal for Parasitology: Parasites and Wildlife 6, 412–419.Google Scholar
Phillips, BL, Kelehear, C, Pizzatto, L, Brown, GP, Barton, D and Shine, R (2010) Parasites and pathogens lag behind their host during periods of host range advance. Ecology 91, 872–881.Google Scholar
Prenter, J, Macneil, C, Dick, JTA and Dunn, AM (2004) Roles of parasites in animal invasions. Trends in Ecology and Evolution 19, 385–390.Google Scholar
R Core Team (2017). R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Riley, J, and Self, J, (1981) A redescription of Waddycephalus teretiusculus (Baird, 1862) Sambon, 1922 and a revision of the taxonomy of the genus Waddycephalus (Sambon, 1922), pentastomid parasites of Asian, Australian and Indonesian snakes, with descriptions of eight new species. Systematic Parasitology 3, 243–257.Google Scholar
Riley, J, Spratt, DM, and Presidente, PJA, (1985) Pentastomids (Arthropoda) parasitic in Australian reptiles and mammals. Aust. J. Zool. 33, 39–54.Google Scholar
Rivera, CCM, Negrón, AG and Bertrand, M (2003) Hemidactylus mabouia (Sauria: Gekkonidae), host of Geckobia hemidactyli (Actinedida: Pterygosomatidae), throughout the Caribbean and South America. Caribbean Journal of Science 39, 321–326.Google Scholar
Stolwijk, AM, Straatman, H and Zielhuis, GA (1999) Studying seasonality by using sine and cosine functions in regression analysis. Journal of Epidemiology and Community Health 53, 235–238.Google Scholar
Telfer, S and Bown, K (2012) The effects of invasion on parasite dynamics and communities. Functional Ecology 26, 1288–1299.Google Scholar
Torchin, ME and Mitchell, CE (2004) Parasites, pathogens, and invasions by plants and animals. Frontiers in Ecology and the Environment 2, 183–190.Google Scholar
Torchin, ME, Lafferty, KD, Dobson, AP, McKenzie, VJ and Kuris, AM (2003) Introduced species and their missing parasites. Nature 421, 628–630.Google Scholar
Vanderduys, EP and Kutt, AS (2013) Is the Asian house gecko, Hemidactylus frenatus, really a threat to Australia's biodiversity? Australian Journal of Zoology 60, 361–367.Google Scholar
Walter, DE and Shaw, M (2002) First record of the mite Hirstiella diolii Baker (Prostigmata: Pterygosomatidae) from Australia, with a review of mites found on Australian lizards. Australian Journal of Entomology 41, 30–34.Google Scholar
Wanless, RM, Angel, A, Cuthbert, RJ, Hilton, GM and Ryan, PG (2007) Can predation by invasive mice drive seabird extinctions? Biology Letters 3, 241–244.Google Scholar
Zuur, AF, Leno, EN and Smith, GM (2007) Analyzing Ecological Data in R New York, USA: Springer.Google Scholar
Zuur, AF, Ieno, EN, Walker, N, Saveliev, AA and Smith, GM (2009). Mixed Effects Models and Extensions in Ecology with R. New York, NY: Springer.Google Scholar
Supplementary material: File

Barnett et al. supplementary material

Barnett et al. supplementary material 1

Download Barnett et al. supplementary material(File)
File 156.1 KB