Volume 94, Issue 2
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Land use changes, such as deforestation and urbanization, can influence interactions between vectors, hosts, and pathogens. The consequences may result in the appearance and rise of mosquito-borne diseases, especially in remote tropical regions. Tropical regions can be the hotspots for the emergence of diseases due to high biological diversity and complex species interactions. Furthermore, frontier areas are often haphazardly surveyed as a result of inadequate or expensive sampling techniques, which limit early detection and medical intervention. We trialed a novel sampling technique of nonpowered traps and a carbon dioxide attractant derived from yeast and sugar to explore how land use influences mosquito communities on four remote, tropical islands in the Australian Torres Strait. Using this technique, we collected > 11,000 mosquitoes from urban and sylvan habitats. We found that human land use significantly affected mosquito communities. Mosquito abundances and diversity were higher in sylvan habitats compared with urban areas, resulting in significantly different community compositions between the two habitats. An important outcome of our study was determining that there were greater numbers of disease-vectoring species associated with human habitations. On the basis of these findings, we believe that our novel sampling technique is a realistic tool for assessing mosquito communities in remote regions.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. Patz J, Graczyk T, Geller N, Vittor A, , 2000. Effects of environmental change on emerging parasitic diseases. Int J Parasitol 30: 13951405.[Crossref] [Google Scholar]
  2. Williams CR, , 2012. The Asian tiger mosquito (Aedes albopictus) invasion into Australia: a review of likely geographic range and changes to vector-borne disease risk. Trans R Soc S Aust 136: 128136. [Google Scholar]
  3. Walsh J, Molyneux D, Birley M, , 1993. Deforestation: effects on vector-borne disease. Parasitol 106: S55.[Crossref] [Google Scholar]
  4. Morse S, , 1995. Factors in the emergence of infectious diseases. Emerg Infect Dis 1: 715.[Crossref] [Google Scholar]
  5. Vasconcelos PF, Travassos da Rosa A, Rodrigues SG, Travassos da Rosa ES, Dégallier N, Travassos da Rosa JF, , 2001. Inadequate management of natural ecosystem in the Brazilian Amazon region results in the emergence and reemergence of arboviruses. Cad Saude Publica 17: S155S164.[Crossref] [Google Scholar]
  6. Reisen WK, , 2010. Landscape epidemiology of vector-borne diseases. Annu Rev Entomol 55: 461483.[Crossref] [Google Scholar]
  7. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, , 2013. The global distribution and burden of dengue. Nature 496: 504507.[Crossref] [Google Scholar]
  8. van Riper CI, van Riper SG, Goff ML, Laird M, , 1986. The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr 56: 327344.[Crossref] [Google Scholar]
  9. Bird BH, Ksiazek TG, Nichol ST, MacLachlan NJ, , 2009. Rift Valley fever virus. J Am Vet Med Assoc 234: 883893.[Crossref] [Google Scholar]
  10. Gubler DJ, , 2002. The global emergence/resurgence of arboviral diseases as public health problems. Arch Med Res 33: 330342.[Crossref] [Google Scholar]
  11. Wolfe ND, Dunavan CP, Diamond J, , 2007. Origins of major human infectious diseases. Nature 447: 279283.[Crossref] [Google Scholar]
  12. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P, , 2008. Global trends in emerging infectious diseases. Nature 451: 990993.[Crossref] [Google Scholar]
  13. Ritchie SA, Cortis G, Paton C, Townsend M, Shroyer D, Zborowski P, Hall-Mendelin S, van den Hurk AF, , 2013. A simple non-powered passive trap for the collection of mosquitoes for arbovirus surveillance. J Med Entomol 50: 185194.[Crossref] [Google Scholar]
  14. van den Hurk AF, Hall-Mendelin S, Townsend M, Kurucz N, Edwards J, Ehlers G, Rodwell C, Moore FA, McMahon JL, Northill JA, , 2014. Applications of a sugar-based surveillance system to track arboviruses in wild mosquito populations. Vector Borne Zoonotic Dis 14: 6673.[Crossref] [Google Scholar]
  15. Saitoh Y, Hattori J, Chinone S, Nihei N, Tsuda Y, Kurahashi H, Kobayashi M, , 2004. Yeast-generated CO2 as a convenient source of carbon dioxide for adult mosquito sampling. J Am Mosq Control Assoc 20: 261264. [Google Scholar]
  16. Oli K, Jeffery J, Vythilingam I, , 2005. Research note: a comparative study of adult mosquito trapping using dry ice and yeast generated carbon dioxide. Trop Biomed 22: 249251. [Google Scholar]
  17. Smallegange RC, Schmied WH, van Roey KJ, Verhulst NO, Spitzen J, Mukabana WR, Takken W, , 2010. Sugar-fermenting yeast as an organic source of carbon dioxide to attract the malaria mosquito Anopheles gambiae . Malar J 9: 292.[Crossref] [Google Scholar]
  18. Meyer Steiger D, Ritchie S, Laurance S, , 2014. Overcoming the challenges of mosquito (Diptera: Culicidae) sampling in remote localities: a comparison of CO2 attractants on mosquito communities in three tropical forest habitats. J Med Entomol 51: 3945.[Crossref] [Google Scholar]
  19. Stanton D, Fell D, Gooding D, , 2009. Vegetation Communities and Regional Ecosystems of the Torres Strait Islands, Queensland, Australia. Greenslopes, Australia: 3D Environmental Consultants. [Google Scholar]
  20. Bureau of Meteorology, 2014. Climate Statistics for Australian Locations. Available at: http://www.bom.gov.au/climate/averages/tables/cw_027058.shtml. Accessed November 18, 2014. [Google Scholar]
  21. Haddon A, Haddon AC, , 1912. Hunting and fishing. , ed. Reports of the Cambridge Anthropological Expedition to the Torres Straits, Volume 4: Arts and Crafts. Cambridge, UK: Cambridge University Press, 152171. [Google Scholar]
  22. Harris DR, Allen J, Golsen J, Jones R, , 1977. Subsistence strategies across Torres Strait. , eds. Sunda and Sahul: Prehistoric Studies in Southeast Asia, Melanesia and Australia. London, UK: Academic Press, 421463. [Google Scholar]
  23. Shnukal A, , 2004. The post-contact created environment in the Torres Strait Central Islands. Memoirs of the Queensland Museum Cultural Heritage Series 3, 317346. [Google Scholar]
  24. Browne SM, Bennett GF, , 1981. Response of mosquitoes (Diptera: Culicidae) to visual stimuli. J Med Entomol 18: 505521.[Crossref] [Google Scholar]
  25. Hoel DF, Obenauer PJ, Clark M, Smith R, Hughes TH, Larson RT, Diclaro JW, Allan SA, , 2011. Efficacy of ovitrap colors and patterns for attracting Aedes albopictus at suburban field sites in north-central Florida. J Am Mosq Control Assoc 27: 245251.[Crossref] [Google Scholar]
  26. Lee DJ, Hicks M, Griffiths M, Russell R, Marks E, , 1980–1989. The Culicidae of the Australasian Region, Vol. 1–12. Canberra, Australia: Australian Government Publishing Service Press. [Google Scholar]
  27. Chapman H, Kay B, Ritchie S, van den Hurk A, Hughes J, , 2000. Definition of species in the Culex sitiens subgroup (Diptera: Culicidae) from Papua New Guinea and Australia. J Med Entomol 37: 736742.[Crossref] [Google Scholar]
  28. Chandler RC, , 1995. Practical considerations in the use of simultaneous inference for multiple tests. Anim Behav 49: 524527.[Crossref] [Google Scholar]
  29. Anderson MJ, , 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 3246. [Google Scholar]
  30. R Development Core Team, 2009. An Introduction to R, Notes on R: A Programming Environment for Data Analysis and Graphics Version 2.10. 1. Bristol, UK: R Development Core Team. [Google Scholar]
  31. Pinheiro J, Bates D, , 2000. Linear Mixed-Effects Models: Basic Concepts and Examples. Mixed-Effects Models in S and S-PLUS. New York, NY: Springer, 356. [Google Scholar]
  32. Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM, , 2009. Mixed Effects Models and Extensions in Ecology with R. New York, NY: Springer Science and Business Media New York.[Crossref] [Google Scholar]
  33. McCune B, Mefford M, , 2011. PC-ORD. Multivariate Analysis of Ecological Data. Version 6.0. Gleneden Beach, OR: MjM Software. [Google Scholar]
  34. IBM, 2013. SPSS Statistics for Windows Version 22.0. Armonk, NY: IBM Corporation. [Google Scholar]
  35. Beebe NW, Foley DH, Ellis JT, , 2000. Populations of the southwest Pacific malaria vector Anopheles farauti ss revealed by ribosomal DNA transcribed spacer polymorphisms. Heredity 84: 244253.[Crossref] [Google Scholar]
  36. Ritchie SA, Moore P, Carruthers M, Williams C, Montgomery B, Foley P, Ahboo S, van den Hurk AF, Lindsay MD, Cooper B, , 2006. Discovery of a widespread infestation of Aedes albopictus in the Torres Strait, Australia. J Am Mosq Control Assoc 22: 358365.[Crossref] [Google Scholar]
  37. Thongsripong P, Green A, Kittayapong P, Kapan D, Wilcox B, Bennett S, , 2013. Mosquito vector diversity across habitats in central Thailand endemic for dengue and other arthropod-borne diseases. PLoS Negl Trop Dis 7: e2507.[Crossref] [Google Scholar]
  38. Jansen CC, Beebe NW, , 2010. The dengue vector Aedes aegypti: what comes next? Microbes Infect 12: 272279.[Crossref] [Google Scholar]
  39. Standfast H, Barrow G, , 1969. Mosquito collections in a high-rainfall area of north Queensland. J Med Entomol 6: 3943.[Crossref] [Google Scholar]
  40. Hanna JN, Ritchie SA, Merritt AD, van den Hurk A, Phillips DA, Serafin IL, Norton RE, McBride W, Gleeson FV, Poidinger M, , 1998. Two contiguous outbreaks of dengue type 2 in north Queensland. Med J Aust 168: 221225. [Google Scholar]
  41. Garcia-Rejon J, Lorono-Pino M, Farfan-Ale J, Flores-Flores L, Rosado-Paredes E, Rivero-Cardenas N, Najera-Vazquez R, Gomez-Carro S, Lira-Zumbardo V, Gonzalez-Martinez P, , 2008. Dengue virus-infected Aedes aegypti in the home environment. Am J Trop Med Hyg 79: 940950. [Google Scholar]
  42. Jardine A, Lindsay M, Heyworth J, Weinstein P, , 2004. Dry-season mosquito breeding associated with irrigation in the northeast Kimberley region of western Australia: potential impact on mosquito-borne disease transmission. EcoHealth 1: 387398.[Crossref] [Google Scholar]
  43. Keating J, Macintyre K, Mbogo C, Githure J, Beier J, , 2004. Characterization of potential larval habitats for Anopheles mosquitoes in relation to urban land-use in Malindi, Kenya. Int J Health Geogr 3: 113.[Crossref] [Google Scholar]
  44. Kay BH, Boyd AM, Ryan PA, Hall RA, , 2007. Mosquito feeding patterns and natural infection of vertebrates with Ross River and Barmah Forest viruses in Brisbane, Australia. Am J Trop Med Hyg 76: 417423. [Google Scholar]
  45. Jansen CC, Prow NA, Webb CE, Hall RA, Pyke AT, Harrower BJ, Pritchard IL, Zborowski P, Ritchie SA, Russell RC, , 2009. Arboviruses isolated from mosquitoes collected from urban and peri-urban areas of eastern Australia. J Am Mosq Control Assoc 25: 272278.[Crossref] [Google Scholar]
  46. Cooper R, Frances S, Waterson D, Piper R, Sweeney A, , 1996. Distribution of anopheline mosquitoes in northern Australia. J Am Mosq Control Assoc 12: 656663. [Google Scholar]
  47. Russell RC, , 1999. Constructed wetlands and mosquitoes: health hazards and management options—an Australian perspective. Ecol Eng 12: 107124.[Crossref] [Google Scholar]
  48. Ponlawat A, Harrington LC, , 2005. Blood feeding patterns of Aedes aegypti and Aedes albopictus in Thailand. J Med Entomol 42: 844849.[Crossref] [Google Scholar]
  49. Takken W, Verhulst NO, , 2013. Host preferences of blood-feeding mosquitoes. Annu Rev Entomol 58: 433453.[Crossref] [Google Scholar]
  50. Schmidt-Nielsen K, , 1997. Animal Physiology: Adaptation and Environment. Cambridge, UK: Cambridge University Press. [Google Scholar]
  51. Willy Weather Australia. Available at: http://www.willyweather.com.au/qld/far-north/horn-island-airport.html. Accessed November 18, 2014.
  52. Kay BH, Standfast HA, Harris KF, , 1987. Ecology of arboviruses and their vectors in Australia. , ed. Current Topics in Vector Research. New York, NY: Springer Publishing Company, 136.[Crossref] [Google Scholar]
  53. Ritchie SA, Phillips D, Broom A, Mackenzie J, Poidinger M, van Den Hurk A, , 1997. Isolation of Japanese encephalitis virus from Culex annulirostris in Australia. Am J Trop Med Hyg 56: 8084. [Google Scholar]
  54. van den Hurk A, Nisbet D, Hall R, Kay B, Mackenzie J, Ritchie S, , 2003. Vector competence of Australian mosquitoes (Diptera: Culicidae) for Japanese encephalitis virus. J Med Entomol 40: 8290.[Crossref] [Google Scholar]
  55. Hanna JN, Ritchie SA, Phillips DA, Shield J, Bailey MC, Mackenzie JS, Poidinger M, McCall BJ, Mills PJ, , 1996. An outbreak of Japanese encephalitis in the Torres Strait, Australia, 1995. Med J Aust 165: 256261. [Google Scholar]
  56. Hanna J, Ritchie S, Phillips D, Lee J, Hills S, van den Hurk A, Pyke A, Johansen C, Mackenzie J, , 1999. Japanese encephalitis in north Queensland, Australia, 1998. Med J Aust 170: 533. [Google Scholar]
  57. Meyer Steiger DB, Johnson P, Hilbert DW, Ritchie S, Jones D, Laurance SGW, , 2012. Effects of landscape disturbance on mosquito community composition in tropical Australia. J Vector Ecol 37: 6976.[Crossref] [Google Scholar]
  58. Harley D, Ritchie S, Phillips D, van den Hurk A, , 2000. Mosquito isolates of Ross River virus from Cairns, Queensland, Australia. Am J Trop Med Hyg 62: 561. [Google Scholar]
  59. Braks M, Meijerink J, Takken W, , 2001. The response of the malaria mosquito, Anopheles gambiae, to two components of human sweat, ammonia and L-lactic acid, in an olfactometer. Physiol Entomol 26: 142148.[Crossref] [Google Scholar]
  60. Dekker T, Steib B, Carde R, Geier M, , 2002. L-lactic acid: a human-signifying host cue for the anthropophilic mosquito Anopheles gambiae . Med Vet Entomol 16: 9198.[Crossref] [Google Scholar]

Data & Media loading...

  • Received : 25 Feb 2015
  • Accepted : 08 Nov 2015
  • Published online : 03 Feb 2016

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error