Biodiversity and Conservation

, Volume 23, Issue 9, pp 2289–2303 | Cite as

Shifts from native to invasive small mammals across gradients from tropical forest to urban habitat in Borneo

  • Konstans Wells
  • Maklarin B. Lakim
  • Robert B. O’Hara
Original Paper


Urbanization has paved the way for the spread of commensal rodents at global scale. However, it is largely unknown how these species use tropical anthropogenic landscapes originally covered with forests and inhabited by diverse small mammal assemblages. We surveyed non-flying small mammals in various urban and suburban habitat types and adjacent forest in the tropical town of Kota Kinabalu in Borneo. We used occupancy and polynomial regression models to determine variation in species occurrences along gradients of land-use intensity. Müller’s sundamys (Sundamys muelleri) was the only native small mammal species found in urban and suburban landscapes with a continuous decrease in occurrence probability from forests to urban habitats. The invasive Asian black rat (Rattus rattus species complex) and the invasive Asian house shrew (Suncus murinus) had the highest occurrence probabilities in habitats of intermediate land-use intensity, but Asian black rats are also likely to occasionally invade forested habitats and occupied urban habitats in sympatry with the Norway rat (Rattus norvegicus). In urban and suburban habitats, fallow land possibly favoured the occurrence of S. muelleri and S. murinus. Other native small mammal species (Muridae, Sciuridae, Tupaiidae) were found only in forested areas. Our study shows that native small mammals found in forest are largely replaced by invasive species in urban and suburban habitats. Due to their occurrence in habitats of various land use intensities, S. muelleri and R. rattus comprise central links between forest wildlife and urban species, an association that is important to consider in studies of parasite and disease transmission dynamics.


Co-occurrence Anthropogenic landscape Species invasion Occupancy model Polynomial regression Urbanization 



We are grateful to the Sabah Biodiversity Council (Majlis Biodiversity Sabah) for research permits JKM-MBS.1000-2/2(35), JKM-MBS.1000-2/2(63). We extend our gratitude to all citizens in Sabah who provided access to their properties or were in other ways helpful during field work. We thank Jorimia Molubi, Brigitte Fiala and K. Eduard Linsenmair for logistic support. We also thank Eva Gerstner and Fred Tuh Y. Yuh and the Sabah Parks research department team for technical and logistic support. Kristina Cockle, Christoph F. J. Meyer and anonymous reviewers provided helpful comments on the manuscript. The Centre of Scientific Computing (CSC) of the Goethe University in Frankfurt provided computation facilities, R.B.O. was supported by the „Landesoffensive zur Entwicklung wissenschaftlich-ökonomischer Exzellenz“ programme (Hesse, Germany).

Supplementary material

10531_2014_723_MOESM1_ESM.kml (435 kb)
Supplementary material 1 (KML 435 kb)
10531_2014_723_MOESM2_ESM.doc (37 kb)
Supplementary material 2 (DOC 37 kb)


  1. Achard F et al (2002) Determination of deforestation rates of the world’s humid tropical forests. Science 297:999–1002CrossRefPubMedGoogle Scholar
  2. Aplin KP, Brown PR, Jacob J, Krebs CJ, Singleton GR (2003) Field methods for rodent studies in Asia and the Indo-Pacific. ACIAR Monogr 100:223Google Scholar
  3. Aplin KP et al (2011) Multiple geographic origins of commensalism and complex dispersal history of black rats. PLoS One 6:e26357PubMedCentralCrossRefPubMedGoogle Scholar
  4. Araújo MB, Luoto M (2007) The importance of biotic interactions for modelling species distributions under climate change. Glob Ecol Biogeogr 16:743–753CrossRefGoogle Scholar
  5. Banerjee S, Carlin BP, Gelfand AE (2004) Hierarchical modeling and analysis for spatial data. Chapman & Hall/CRC, Boca RatonGoogle Scholar
  6. Bernard H, Fjeldså J, Mohamed M (2009) A case study on the effects of disturbance and conversion of tropical lowland rain forest on the non-volant small mammals in North Borneo: management implications. Mammal Study 34:85–96CrossRefGoogle Scholar
  7. Bradley CA, Altizer S (2007) Urbanization and the ecology of wildlife diseases. Trend Ecol Evol 22:95–102CrossRefGoogle Scholar
  8. Brook BW, Sodhi NS, Ng PKL (2003) Catastrophic extinctions follow deforestation in Singapore. Nature 424:420–423CrossRefPubMedGoogle Scholar
  9. Bryan JE, Shearman PL, Asner GP, Knapp DE, Aoro G, Lokes B (2013) Extreme differences in forest degradation in Borneo: comparing practices in Sarawak, Sabah, and Brunei. PLoS One 8:e69679PubMedCentralCrossRefPubMedGoogle Scholar
  10. Carlin B, Chib S (1995) Bayesian model choice via Markov chain Monte Carlo methods. J R Stat Soc B 57:473–484Google Scholar
  11. Chung KPS, Corlett RT (2006) Rodent diversity in a highly degraded tropical landscape: Hong Kong, South China. Biodivers Conserv 15:4521–4532CrossRefGoogle Scholar
  12. Corlett RT (1992) The ecological transformation of Singapore, 1819–1990. J Biogeogr 19:411–420CrossRefGoogle Scholar
  13. Cushman SA, McGarigal K (2002) Hierarchical, multi-scale decomposition of species-environment relationships. Landsc Ecol 17:637–646CrossRefGoogle Scholar
  14. Dellaportas P, Forster J, Ntzoufras I (2002) On Bayesian model and variable selection using MCMC. Stat Comput 12:27–36CrossRefGoogle Scholar
  15. Dobson A, Foufopoulos J (2001) Emerging infectious pathogens of wildlife. Philos Trans R Soc B 356:1001–1012CrossRefGoogle Scholar
  16. Eccard JA, Ylonen H (2003) Interspecific competition in small rodents: from populations to individuals. Evol Ecol 17:423–440CrossRefGoogle Scholar
  17. JRC FAO (2012) Global forest land-use change 1990–2005. In: Lindquist EJ et al (eds) FAO Forestry Paper No. 169. Food and Agriculture Organization of the United Nations and European Commission Joint Research Centre. Rome, FAO Google Scholar
  18. Gelman A, Carlin JB, Stern HS, Rubin DB (2005) Bayesian data analysis, 2nd edn. Chapman & Hall/CRC, Boca RatonGoogle Scholar
  19. Gibson L et al (2013) Near-complete extinction of native small mammal fauna 25 years after forest fragmentation. Science 341:1508–1510CrossRefPubMedGoogle Scholar
  20. Gorog AJ, Sinaga MH, Engstrom MD (2004) Vicariance or dispersal? Historical biogeography of three Sunda shelf murine rodents (Maxomys surifer, Leopoldamys sabanus and Maxomys whiteheadi). Biol J Linn Soc 81:91–109CrossRefGoogle Scholar
  21. Gregory SD, MacDonald DW (2009) Prickly coexistence or blunt competition? Opuntia refugia in an invaded rodent community. Oecologia 159:225–236CrossRefPubMedGoogle Scholar
  22. Harris DB (2009) Review of negative effects of introduced rodents on small mammals on islands. Biol Invasions 11:1611–1630CrossRefGoogle Scholar
  23. Harris DB, MacDonald DW (2007) Interference competition between introduced black rats and endemic Galapagos rice rats. Ecology 88:2330–2344CrossRefPubMedGoogle Scholar
  24. Heikkinen RK, Luoto M, Virkkala R, Pearson RG, Körber JH (2007) Biotic interactions improve prediction of boreal bird distributions at macro-scales. Glob Ecol Biogeogr 16:754–763CrossRefGoogle Scholar
  25. Herbreteau V, Bordes F, Jittapalapong S, Supputamongkol Y, Morand S (2012) Rodent-borne diseases in Thailand: targeting rodent carriers and risky habitats. Infect Ecol Epidemiol 2:18637Google Scholar
  26. Jenkins CN, Pimm SL, Joppa LN (2013) Global patterns of terrestrial vertebrate diversity and conservation. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1302251110 Google Scholar
  27. Jones KE et al (2008) Global trends in emerging infectious diseases. Nature 451:990–994CrossRefPubMedGoogle Scholar
  28. Liu J, Daily GC, Ehrlich PR, Luck GW (2003) Effects of household dynamics on resource consumption and biodiversity. Nature 421:530–533CrossRefPubMedGoogle Scholar
  29. Lunn D, Spiegelhalter D, Thomas A, Best N (2009) The BUGS project: evolution, critique and future directions. Stat Med 28:3049–3067CrossRefPubMedGoogle Scholar
  30. MacKenzie DI, Nichols JD, Royle JA, Pollock KH, Bailey LL, Hines JE (2006) Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. Elsevier, AmsterdamGoogle Scholar
  31. Maitz WE, Dickman CR (2001) Competition and habitat use in native Australian Rattus: is competition intense, or important? Oecologia 128:526–538CrossRefGoogle Scholar
  32. Mazerolle MJ, Villard MA (1999) Patch characteristics and landscape context as predictors of species presence and abundance: a review. Ecoscience 6:117–124Google Scholar
  33. McKinney ML (2002) Urbanization, biodiversity, and conservation. Bioscience 52:883–890CrossRefGoogle Scholar
  34. Musser G, Carleton M (2005) Superfamily Muroidea. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference, vol 2, 3rd edn. Johns Hopkins University, Baltimore, pp 894–1531Google Scholar
  35. O’Brien SM, Dunson DB (2004) Bayesian multivariate logistic regression. Biometrics 60:739–746CrossRefPubMedGoogle Scholar
  36. Ovaskainen O, Hottola J, Siitonen J (2010) Modeling species co-occurrence by multivariate logistic regression generates new hypotheses on fungal interactions. Ecology 91:2514–2521CrossRefPubMedGoogle Scholar
  37. Pagès M et al (2013) Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex). Mol Ecol 22:1019–1034CrossRefPubMedGoogle Scholar
  38. Paine CET, Beck H (2007) Seed predation by neotropical rain forest mammals increases diversity in seedling recruitment. Ecology 88:3076–3087CrossRefPubMedGoogle Scholar
  39. Prevedello JA, Dickman CR, Vieira MV, Vieira EM (2013) Population responses of small mammals to food supply and predators: a global meta-analysis. J Anim Ecol 82:927–936CrossRefPubMedGoogle Scholar
  40. Rickart EA, Balete DS, Rowe RJ, Heaney LR (2011) Mammals of the northern Philippines: tolerance for habitat disturbance and resistance to invasive species in an endemic insular fauna. Divers Distrib 17:530–541CrossRefGoogle Scholar
  41. Saito M, Koike F (2013) Distribution of wild mammal assemblages along an urban–rural–forest landscape gradient in warm-temperate East Asia. PLoS One 8:e65464PubMedCentralCrossRefPubMedGoogle Scholar
  42. Schipper J et al (2008) The status of the world’s land and marine mammals: diversity, threat, and knowledge. Science 322:225–230CrossRefPubMedGoogle Scholar
  43. Shearman P, Bryan J, Laurance WF (2012) Are we approaching ‘peak timber’ in the tropics? Biol Conserv 151:17–21CrossRefGoogle Scholar
  44. Singleton GR, Belmain S, Brown PR, Aplin K, Htwe NM (2010) Impacts of rodent outbreaks on food security in Asia. Wildl Res 37:355–359CrossRefGoogle Scholar
  45. Sodhi NS, Koh LP, Brook BW, Ng PKL (2004) Southeast Asian biodiversity: an impending disaster. Trends Ecol Evol 19:654–660CrossRefPubMedGoogle Scholar
  46. Stenseth N et al (2003) Mice, rats, and people: the bio-economics of agricultural rodent pests. Front Ecol Environ 1:367–375CrossRefGoogle Scholar
  47. Stokes VL, Banks PB, Pech RP, Spratt DM (2009) Competition in an invaded rodent community reveals black rats as a threat to native bush rats in littoral rainforest of south-eastern Australia. J Appl Ecol 46:1239–1247CrossRefGoogle Scholar
  48. Stuebing RB, Gasis J (1989) A survey of small mammals within a Sabah tree plantation in Malaysia. J Trop Ecol 5:203–214CrossRefGoogle Scholar
  49. Terborgh J et al (2001) Ecological meltdown in predator-free forest fragments. Science 294:1923–1926CrossRefPubMedGoogle Scholar
  50. Tyre AJ, Tenhumberg B, Field SA, Niejalke D, Parris K, Possingham HP (2003) Improving precision and reducing bias in biological surveys: estimating false-negative error rates. Ecol Appl 13:1790–1801CrossRefGoogle Scholar
  51. Umetsu F, Metzger JP, Pardini R (2008) Importance of estimating matrix quality for modeling species distribution in complex tropical landscapes: a test with Atlantic forest small mammals. Ecography 31:359–370CrossRefGoogle Scholar
  52. Wells K, Kock D, Lakim MB, Pfeiffer M (2006) Is Rattus rattus invading the primary rainforest on Borneo? Malay Nat J 59:73–79Google Scholar
  53. Wells K, Kalko EKV, Lakim MB, Pfeiffer M (2007) Effects of rain forest logging on species richness and assemblage composition of small mammals in Southeast Asia. J Biogeogr 34:1087–1099CrossRefGoogle Scholar
  54. Wells K, Corlett RT, Lakim MB, Kalko EKV, Pfeiffer M (2009) Seed consumption by small mammals from Borneo. J Trop Ecol 25:555–558CrossRefGoogle Scholar
  55. Wisz MS et al (2013) The role of biotic interactions in shaping distributions and realised assemblages of species: implications for species distribution modelling. Biol Rev 88:15–30PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Konstans Wells
    • 1
    • 2
  • Maklarin B. Lakim
    • 3
  • Robert B. O’Hara
    • 4
  1. 1.The Environment Institute, School of Earth and Environmental SciencesThe University of AdelaideAdelaideAustralia
  2. 2.Institute of Experimental EcologyUniversity of UlmUlmGermany
  3. 3.Sabah ParksKota KinabaluMalaysia
  4. 4.Biodiversity and Climate Research Centre (BiK-F)Frankfurt am MainGermany

Personalised recommendations