Skip to main content
SpringerLink
Log in

The threatened Pookila (Pseudomys novaehollandiae) hosts a diverse macrobiome of arthropods at varying risks of co-extinction

  • ORIGINAL PAPER
  • Published:
Journal of Insect Conservation Aims and scope Submit manuscript

Abstract

The Pookila (Pseudomys novaehollandiae) is a threatened Australian mammal emblematic of the global decline of many vertebrate taxa. While conservationists are concerned with the survival of threatened vertebrates, few consider the rich diversity of symbiotic arthropods which often depend on these hosts for survival. Using P. novaehollandiae as a case study, we demonstrate that even opportunistic sampling can rapidly expand knowledge of the species richness of arthropod symbiont communities on poorly studied vertebrate hosts. We also demonstrate how DNA barcoding can be integrated to provide rapid and inexpensive identification capabilities for non-specialists. Finally, we show how various metrics and methods can be used to quantify and qualify extinction risk of poorly known arthropod symbionts to provide the foundations for conservation action.

Implications for insect conservation: This study highlights how opportunistic sampling coupled with DNA barcoding and extinction risk metrics can be used to rapidly and inexpensively characterise the arthropod macrobiomes of rare vertebrates and evaluate the risk of decline of their component taxa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ardura A, Linde AR, Moreira JC, Garcia-Vazquez E (2010) DNA barcoding for conservation and management of amazonian commercial fish. Biol Conserv 143(6):1438–1443

    Article  Google Scholar 

  • Brodie JF, Williams S, Garner B (2021) The decline of mammal functional and evolutionary diversity worldwide. PNAS 118(3):e1921849118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burns PA (2019) Testing the decline of the New Holland mouse (Pseudomys novaehollandiae) in Victoria. Aust Mammal 42(2):185–193

    Article  Google Scholar 

  • Burns PA, Clemann N, White M (2020) Testing the utility of species distribution modelling using Random forests for a species in decline. Austral Ecol 45(6):706–716

    Article  Google Scholar 

  • Burns PA, Rowe K, Parrott M, Roycroft EJ (2023) Population genomics of decline and local extinction in the endangered Australian Pookila. Biol Conserv 284:e110183

    Article  Google Scholar 

  • Cardoso P, Erwin TL, Borges PA, New TR (2011) The seven impediments in invertebrate conservation and how to overcome them. Biol Conserv 144(11):2647–2655

    Article  Google Scholar 

  • Carlson CJ, Hopkins S, Bell KC, Doña J, Godfrey SS, Kwak ML, Lafferty KD, Moir ML, Speer KA, Strona G, Torchin M (2020) A global parasite conservation plan. Biol Conserv 250:e108596

    Article  Google Scholar 

  • Department of Natural Resources and Environment (2015) Threatened Species Protection Act 1995 - Threatened Species List - Vertebrate Animals. https://nre.tas.gov.au/conservation/threatened-species-and-communities/lists-of-threatened-species/threatened-species-vertebrates. accessed 13 June 2023

  • Department of Energy, Environment and Climate Action (2023) Flora and Fauna Guarantee Act 1988 - Threatened List June 2023. Victorian State Government, Victoria. https://www.environment.vic.gov.au/__data/assets/pdf_file/0021/655410/FFG-Threatened-List-June-2023.pdf. accessed 13 June 2023

  • Domrow R (1961) New and little known Laelaptidae, Trombiculidae and Listrophoridae (Acarina) from Australasian mammals. Proc Linn Soc NSW 86:60–95

    Google Scholar 

  • Domrow R (1987) Acari Mesostigmata parasitic on Australian vertebrates: an annotated checklist, keys and bibliography. Invertebr Syst 1(7):817–948

    Article  Google Scholar 

  • Dormann CF, Fründ J, Blüthgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Open J Ecol 2(1):7–24

    Article  Google Scholar 

  • Dormann CF, Fruend J, Gruber B, Dormann MCF (2014) Package ‘bipartite’. Visualizing bipartite networks and calculating some (ecological) indices (Version 2.04). (R Foundation for Statistical Computing.) https://cran.r-project.org/web/packages/bipartite/index.html

  • Dunn RR (2005) Modern insect extinctions, the neglected majority. Conserv Biol 19(4):1030–1036

    Article  Google Scholar 

  • Dunnet GM, Mardon DK (1974) A monograph of Australian fleas (Siphonaptera). Aust J Zool 22(30):1–273

    Google Scholar 

  • Fellin E, Schulte-Hostedde A (2022) Effects of ticks on community assemblages of ectoparasites in deer mice. Ticks Tick Borne Dis 13(1):e101846

    Article  Google Scholar 

  • Geller J, Meyer C, Parker M, Hawk H (2013) Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Mol Ecol Res 13(5):851–861

    Article  CAS  Google Scholar 

  • Grunin K (1973) The first discovery of larvae of the mammoth bot-fly Cobboldia (Mamontia, subgen. n.) russanovi sp. n.(Diptera, Gasterophilidae). Entomologicheskoe Obozrenie 52:228–233 (English translation in Entomological Review

    Google Scholar 

  • Hastriter MW, Whiting MF (2002) Macropsylla novaehollandiae (Siphonaptera: Hystrichopsyllidae), a new species of flea from Tasmania. Proc Entomol Soc 104(3):663–671

    Google Scholar 

  • Herrera JP, Moody J, Nunn CL (2021) Predictions of primate–parasite coextinction. Philos Trans R Soc Lond B Biol Sci 376(1837):e20200355

    Article  Google Scholar 

  • Hopkins S, Kwak M (2023) New IUCN Species Survival Commission Parasite Specialist Group launched in 2023. Oryx 57(3):283–283

    Article  Google Scholar 

  • Horak IG, Camicas JL, Keirans JE (2003) The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida): a world list of valid tick names. In: Ticks and Tick-Borne Pathogens: Proceedings of the 4th International Conference on Ticks and Tick-Borne Pathogens The Banff Centre Banff, Alberta, Canada 21–26 July 2002. Springer Netherlands, pp 27–54

  • IUCN Standards and Petitions Committee (2022) Guidelines for Using the IUCN Red List Categories and Criteria. Version 15.1. Prepared by the Standards and Petitions Committee. Downloadable from https://www.iucnredlist.org/documents/RedListGuidelines.pdf. Accessed on 13th December 2022

  • IUCN redlist (2022b) Smoky Mouse (Pseudomys fumeus). https://www.iucnredlist.org/species/18550/22398566. Accessed on 13th December 2022

  • IUCN redlist (2022a) New Holland Mouse (Pseudomys novaehollandiae). https://www.iucnredlist.org/species/18552/22398752. Accessed on 13th December 2022

  • Jenkins Shaw J (2021) Notes on the genus Myotyphlus Fauvel, 1883 (Coleoptera: Staphylinidae) in Tasmania. Aust Entomol 48(1):33–38

    Google Scholar 

  • Jenkins Shaw J, Kwak ML, Burns PA, Solodovnikov A (2017) New host records of the rove beetle ‘Myotyphlus Newtoni’ Solodovnikov and Jenkins Shaw, 2016 (Coleoptera: Staphylinidae: Staphylininae), with notes on its association with mammals. Aust Entomol 44(4):209–212

    Google Scholar 

  • Jenkins Shaw J, Żyła D, Solodovnikov A (2020) Molecular phylogeny illuminates Amblyopinini (Coleoptera: Staphylinidae) rove beetles as a target for systematic and evolutionary research. Syst Entomol 45(2):430–446

    Article  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evo 35(6):1547–1549

    Article  CAS  Google Scholar 

  • Kwak ML (2018) Australia’s vanishing fleas (Insecta: Siphonaptera): a case study in methods for the assessment and conservation of threatened flea species. J Insect Conserv 22(3):545–550

    Article  Google Scholar 

  • Kwak ML, Hastriter MW (2020) The Australian giant fleas Macropsylla Rothschild, 1905 (Siphonaptera: Macropsyllidae: Macropsyllinae), their identification, evolution, ecology, and conservation biology. Syst Parasitol 97(1):107–118

    Article  PubMed  Google Scholar 

  • Kwak ML, Heath AC, Cardoso P (2020) Methods for the assessment and conservation of threatened animal parasites. Biol Conserv 248:e108696

    Article  Google Scholar 

  • Lazenby BT, Bell P, Driessen MM, Pemberton D, Dickman CR (2018) Evidence for a recent decline in the distribution and abundance of the New Holland mouse (Pseudomys novaehollandiae) in Tasmania, Australia. Aust Mammal 41(2):179–185

    Article  Google Scholar 

  • Leray M, Yang JY, Meyer CP, Mills SC, Agudelo N, Ranwez V, Boehm JT, Machida RJ (2013) A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents. Front Zool 10(1):34

    Article  PubMed  PubMed Central  Google Scholar 

  • MacKenzie K, Pert C (2018) Evidence for the decline and possible extinction of a marine parasite species caused by intensive fishing. Fisher Res 198:63–65

    Article  Google Scholar 

  • Meier R, Shiyang K, Vaidya G, Ng PKL (2006) DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success. Syst Biol 55:715–728

    Article  PubMed  Google Scholar 

  • Mihalca AD, Gherman CM, Cozma V (2011) Coendangered hard-ticks: threatened or threatening? Parasite Vector 4(1):1–7

    Article  Google Scholar 

  • New TR, Van Praagh BD, Yen AL (2012) Invertebrate conservation status and the limits of reliable information: examples from Victoria, Australia. Vic Nat 129(3):68–76

    Google Scholar 

  • Nielsen DH, Robbins RG, Rueda LM (2021) Annotated world checklist of the Trombiculidae and Leeuwenhoekiidae (1758–2021)(Acari: Trombiculoidea), with notes on nomenclature, taxonomy, and distribution. Zootaxa 4967(1):1–243

    Article  Google Scholar 

  • Poulin R, Mouillot D (2003) Parasite specialization from a phylogenetic perspective: a new index of host specificity. Parasitol 126(5):473–480

    Article  CAS  Google Scholar 

  • Price RD, Hellenthal RA, Palma RL (2003) World checklist of chewing lice with host associations and keys to families and genera. The chewing lice: world checklist and biological overview. Illinois Natural History Survey Special Publication, Illinois

    Google Scholar 

  • R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna Austria. https://www.R-project.org/

  • Roberts FHS (1970) Australian ticks. CSIRO Publishing, Melbourne, Australia

    Google Scholar 

  • Rózsa L, Vas Z (2015) Co-extinct and critically co-endangered species of parasitic lice, and conservation-induced extinction: should lice be reintroduced to their hosts? Oryx 49:107–110

    Article  Google Scholar 

  • Schoolmeesters P (2019) World Scarabaeidae database (version Jan 2019) Roskov Y, Ower G, Orrell T, Nicolson D, Bailly N, Kirk PM, (Eds.), Species 2000 & ITIS Catalogue of Life, Naturalis, Leiden (2019) http://www.catalogueoflife.org/col

  • Solodovnikov A, Jenkins Shaw J (2017) The remarkable Australian rove beetle genus Myotyphlus: its cryptic diversity and significance for exploring mutualism among insects and mammals (Coleoptera: Staphylinidae). Austral Entomol 56(3):311–321

    Article  Google Scholar 

  • Srivathsan A, Lee L, Katoh K, Hartop E, Kutty SN, Wong J, Yeo D, Meier R (2021) ONTbarcoder and MinION barcodes aid biodiversity discovery and identification by everyone, for everyone. BMC Biol 19(1):1–21

    Article  Google Scholar 

  • Threatened Species Sect. (2023) Tapeworm (Tasmanian Devil) (Dasyurotaenia robusta): Species Management Profile for Tasmania’s Threatened Species Link. https://www.threatenedspecieslink.tas.gov.au/Pages/Tapeworm-(Tasmanian-Devil).aspx. Department of Natural Resources and Environment Tasmania. Accessed 8th May 2023

  • Truett GE, Heeger P, Mynatt RL, Truett AA, Walker JA, Warman ML (2000) Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechnique 29(1):52–54

    Article  CAS  Google Scholar 

  • Whiting MF, Whiting AS, Hastriter MW, Dittmar K (2008) A molecular phylogeny of fleas (Insecta: Siphonaptera): origins and host associations. Cladistic 24(5):677–707

    Article  Google Scholar 

Download references

Funding

This work was partly supported by JSPS KAKENHI [20KK0151 and 22F22084].

Author information

Authors and Affiliations

  1. Parasitology Laboratory, Department of Disease Control, Faculty of Veterinary Medicine, Hokkaido University, 9 Chome Kita 18 Jonishi, Kita Ward, Sapporo, Hokkaido, 060-0818, Japan

    Mackenzie L. Kwak & Ryo Nakao

  2. IUCN Parasite Specialist Group, Gland, Switzerland

    Mackenzie L. Kwak

  3. Wildlife Conservation & Science, Zoos Victoria, Parkville, VIC, Australia

    Phoebe A. Burns

  4. Monte L. Bean Life Science Museum, Brigham Young University, 290 MLBM, PO Box 20200, Provo, UT, 84602-0200, USA

    Michael W. Hastriter

  5. Natural History Museum of Denmark of the University of Copenhagen, Zoological Museum, Universitetsparken 15, Copenhagen, 2100, Denmark

    Josh Jenkins Shaw

  6. Norwegian Biodiversity Information Centre, Trondheim, Norway

    Josh Jenkins Shaw

Authors
  1. Mackenzie L. Kwak
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Phoebe A. Burns
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael W. Hastriter
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Josh Jenkins Shaw
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ryo Nakao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MLK: Conceptualization; Data collection, Data analysis, Roles/Writing - original draft; Writing - review & editing. PB: Data collection; Writing - review & editing. JJS: Data collection; Writing - review & editing. MWH: Data collection; Writing - review & editing. RN: Writing - review & editing.

Corresponding author

Correspondence to Mackenzie L. Kwak.

Ethics declarations

Competing interests

The authors declare no competing interests.

Disclosure statement

The authors declare that they have no financial or non-financial interest arise from the direct applications of this paper.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kwak, M.L., Burns, P.A., Hastriter, M.W. et al. The threatened Pookila (Pseudomys novaehollandiae) hosts a diverse macrobiome of arthropods at varying risks of co-extinction. J Insect Conserv (2024). https://doi.org/10.1007/s10841-024-00559-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10841-024-00559-2

Keywords

Search

Navigation