Surrounding land use significantly influences adult mosquito abundance and species richness in urban mangroves

Abstract

Mangroves harbor mosquitoes capable of transmitting human pathogens; consequently, urban mangrove management must strike a balance between conservation and minimizing public health risks. Land use may play a key role in shaping the mosquito community within urban mangroves through either species spillover or altering the abundance of mosquitoes associated with the mangrove. In this study, we explore the impact of land use within 500 m of urban mangroves on the abundance and diversity of adult mosquito populations. Carbon dioxide baited traps were used to sample host-seeking female mosquitoes around nine mangrove forest sites along the Parramatta River, Sydney, Australia. Specimens were identified to species and for each site, mosquito species abundance, species richness and diversity were calculated and were analyzed in linear mixed effects models. We found that the percentage of residential land and bushland in the surrounding area had a negative effect on mosquito abundance and species richness. Conversely, the amount of mangrove had a significant positive effect on mosquito abundance, and the amount of industrial land had a significant positive effect on species richness. These results demonstrate the need for site-specific investigations of mosquito communities associated with specific habitat types and the importance of considering surrounding land use in moderating local mosquito communities. A greater understanding of local land use and its influence on mosquito habitats could add substantially to the predictive power of disease risk models and assist local authorities develop policies for urban development and wetland rehabilitation.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Blitzer EJ, Dormann CF, Holzschuh A, Klein AM, Rand TA, Tscharntke T (2012) Spillover of functionally important organisms between managed and natural habitats. Agr Ecosyst Environ 146:34–43

    Article  Google Scholar 

  2. Brokenshire T, Symonds D, Reynolds R, Doggett S, Geary M, Russell R (2000) A cluster of locally-acquired Ross River virus infection in outer Western Sydney. New South Wales public health bulletin 11:132–134

    Article  PubMed  Google Scholar 

  3. Burgin S, Franklin MJ, Hull L (2016) Wetland loss in the transition to urbanisation: a case study from Western Sydney, Australia. Wetlands 1–10

  4. Claflin SB, Webb CW (2015) Ross River virus: many vectors and unusual hosts make for an unpredictable pathogen. PLoS Pathog. doi:10.1371/journal.ppat.1005070

    PubMed  PubMed Central  Google Scholar 

  5. Crowder DW, Dykstra EA, Brauner JM, Duffy A, Ree C, Martin E, Peterson W, Carrière Y, Dutilleul P, Owen P (2013) West Nile virus prevalence across landscapes is mediated by local effects of agriculture on vector and host communities. PLoS ONE 8:e55006

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Dale PER, Knight JM (2012) Managing mosquitoes without destroying wetlands: an eastern Australian approach. Wetl Ecol Manag 20:233–242

    Article  Google Scholar 

  7. Dale P, Eslami-Andargoli L, Knight J (2013) The impact of encroachment of mangroves into saltmarshes on saltwater mosquito habitats. J Vector Ecol 38:330–338

    Article  PubMed  Google Scholar 

  8. Dale PER, Knight JM, Dwyer PG (2014a) Mangrove rehabilitation: a review focusing on ecological and institutional issues. Wetl Ecol Manag 22:587–604

    Article  Google Scholar 

  9. Dale P, Knight J, Griffin L (2014b) Comparing Aedes vigilax eggshell densities in saltmarsh and mangrove systems with implications for management. Insects 5:984–990

    Article  PubMed  PubMed Central  Google Scholar 

  10. de Little SC, Williamson GJ, Bowman DMJS, Whelan PI, Brook BW, Bradshaw CJA (2011) Experimental comparison of aerial larvicides and habitat modification for controlling disease-carrying Aedes vigilax mosquitoes. Pest Manag Sci 68:709–717

    Article  PubMed  Google Scholar 

  11. Didham RK, Barker GM, Bartlam S, Deakin EL, Denmead LH, Fisk LM, Peters JMR, Tylianakis JM, Wright HR, Schipper LA (2015) Agricultural intensification exacerbates spillover effects on soil biogeochemistry in adjacent forest remnants. PLoS ONE 10:e0116474

    Article  PubMed  PubMed Central  Google Scholar 

  12. Duke NC, Meynecke JO, Dittmann S, Ellison AM, Anger K, Berger U, Cannicci S, Diele K, Ewel KC, Field CD, Koedam N, Lee SY, Marchand C, Nordhaus I, Dohdouh-Guebas F (2007) A world without mangroves? Science 317:41–42

    CAS  Article  PubMed  Google Scholar 

  13. Dwyer PG, Knight JM, Dale PER (2016) Planning development to reduce mosquito hazard in coastal peri-urban areas: case studies in NSW, Australia. In: Balanced urban development: options and strategies for liveable cities, pp. 555–574. Springer, Berlin

  14. Frost CM, Didham RK, Rand TA, Peralta G, Tylianakis JM (2015) Community-level spillover of natural enemies from managed to natural forests. Ecology 96:193–202

    Article  PubMed  Google Scholar 

  15. Gardner AM, Lampman RL, Muturi EJ (2014) Land use patterns and the risk of West Nile virus transmission in central Illinois. Vector-Borne Zoonot 14:339–345

    Article  Google Scholar 

  16. Gislason GM, Russell RC (1997) Oviposition sites of the saltmarsh mosquito, Aedes vigilax (Skuse) (Diptera: Culicidae), at Homebush Bay, Sydney, NSW: A preliminary investigation. Aust J Entomol 36:97–100

    Article  Google Scholar 

  17. Griffin LF, Knight JM (2012) A review of the role of fish as biological control agents of disease vector mosquitoes in mangrove forests: reducing human health risks while reducing environmental risk. Wetl Ecol Manag 20:243–252

    Article  Google Scholar 

  18. Haines PE, Tomlinson RB, Thom BG (2006) Morphometric assessment of intermittently open/closed coastal lagoons in New South Wales, Australia. Estuar Coast Shelf Sci 67:321–332

    Article  Google Scholar 

  19. Hu W, Clements A, Williams G, Tong S (2010) Dengue fever and El Niño/southern oscillation in Queensland, Australia: a time series predictive model. Occup Environ Med 67:307–311

    Article  PubMed  Google Scholar 

  20. Jacups SP, Whelan PI, Markey PG, Cleland SJ, Williamson GJ, Currie BJ (2008) Predictive indicators for Ross River virus infection in the Darwin area of tropical northern Australia, using long-term mosquito trapping data. Trop Med Int Health 13:943–952

    Article  PubMed  Google Scholar 

  21. Jacups SP, Kurucz N, Wheland PI, Carter JM (2009) A comparison of Aedes vigilax larval population densities and associated vegetation categories in a coastal wetland, Northern Territory, Australia. J Vector Ecol 34:311–316

    CAS  Article  PubMed  Google Scholar 

  22. Junglen S, Kurth A, Kuehl H, Quan PL, Ellerbrok H, Pauli G, Nitsche A, Nunn C, Rich SM, Lipkin WI, Briese T, Leendertz FH (2009) Examining landscape factors influencing relative distribution of mosquito genera and frequency of virus infection. EcoHealth 6:239–249

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Kay BH, Jorgensen WK (1986) Eggs of Aedes vigilax (Skuse) and their distribution on plants and soil in a south east Queensland saltmarsh. Aust J Entomol 25:267–272

    Article  Google Scholar 

  24. Knight JM (2011) A model of mosquito-mangrove basin ecosystems with implications for management. Ecosystems 14:1382–1395

    Article  Google Scholar 

  25. Knight J, Griffin L, Dale P, Phinn S (2011) Oviposition and larval habitat preferences of the saltwater mosquito, Aedes vigilax, in a subtropical mangrove forest in Queensland, Australia. J Insect Sci 12:1–11

    Article  Google Scholar 

  26. Lacroix C, Jolles A, Seabloom EW, Power AG, Mitchell CE, Borer ET (2014) Nonrandom biodiversity loss underlies predictable increases in viral disease prevalence. J R Soc Interface 11:20130947

    Article  PubMed  PubMed Central  Google Scholar 

  27. Matson PA, Parton WJ, Power AG, Swift MJ (1997) Agricultural intensification and ecosystem properties. Science 277:504–509

    CAS  Article  PubMed  Google Scholar 

  28. Mayer-Pinto M, Johnston EL, Hutchings PA, Marzinelli EM, Ahyong ST, Birch G, Booth DJ, Creese RG, Doblin MA, Figueira W, Gribben PE, Pritchard T, Roughan M, Steinberg PD, Hedge LH (2015) Sydney Harbour: a review of anthropogenic impacts on the biodiversity and ecosystem function of one of the world’s largest natural harbours. Mar Freshwater Res 66:1088–1105

    Article  Google Scholar 

  29. McLoughlin L (2000) Estuarine wetlands distribution along the Parramatta River, Sydney, 1788–1940: implications for planning and conservation. Cunninghamia 6:579–610

    Google Scholar 

  30. Ng V, Dear K, Harley D, McMichael A (2014) Analysis and prediction of ross river virus transmission in New South Wales, Australia. Vector-Borne Zoonotic Dis 14:422–438

    Article  PubMed  Google Scholar 

  31. O’Meara J, Darcovich K (2015) Twelve years on: ecological restoration and rehabilitation at Sydney Olympic Park. Ecol Manag Restor 16:14–28

    Article  Google Scholar 

  32. Potter A, Johansen CA, Fenwick S, Reid SA, Lindsay MD (2014) The seroprevalence and factors associated with Ross River virus infection in western grey kangaroos (Macropus fuliginosus) in Western Australia. Vector-Borne Zoonotic Dis 14:740–745

    Article  PubMed  Google Scholar 

  33. Ramp D, Ben-Ami D (2006) The effect of road-based fatalities on the viability of a peri-urban swamp wallaby population. J Wildl Manag 70:1615–1624

    Article  Google Scholar 

  34. Ratnayake J, Dale PE, Sipe NG, Daniels P (2006) Impact of biting midges on residential property values in Hervey Bay, Queensland, Australia. J Am Mosq Control Assoc 22:131–134

    Article  PubMed  Google Scholar 

  35. Rogers K, Boon PI, Branigan S, Duke NC, Field CD, Fitzsimons J, Kirkman H, Mackenzie JR, Saintilan N (2016) The state of legislation and policy protecting Australia’s mangrove and salt marsh and their ecosystem services. Mar Policy 72:139–155

    Article  Google Scholar 

  36. Rohe DL, Fall RP (1979) A miniature battery powered CO2 baited light trap for mosquito borne encephalitis surveillance. Bull Soc Vector Ecol 4:24–27

  37. Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–124

    Article  Google Scholar 

  38. Runting RK, Lovelock CE, Beyer HL, Rhodes JR (2016) Costs and opportunities for preserving coastal wetlands under sea level rise. Conserv Lett. doi:10.1111/conl.12239

    Google Scholar 

  39. Russell RC (1998) Mosquito-borne arboviruses in Australia: the current scene and implications of climate change for health. Int J Parasitol 28:955–969

    CAS  Article  PubMed  Google Scholar 

  40. Russell RC (1999) Constructed wetlands and mosquitoes: health hazards and management options—an Australian perspective. Ecol Eng 12:107–124

    Article  Google Scholar 

  41. Russell RC (2009) Mosquito-borne disease and climate change in Australia: time for a reality check. Aust J Entomol 48:1–7

    Article  Google Scholar 

  42. Russell RC, Kay BH (2004) Medical entomology: changes in the spectrum of mosquito-borne disease in Australia and other vector threats and risks, 1972-2004. Aust J Entomol 43:271–282

    Article  Google Scholar 

  43. Schäfer ML, Lundkvist E, Landin J, Persson TZ, Lundström JO (2006) Influence of landscape structure on mosquitoes (Diptera: Culicidae) and dytiscids (Coleoptera: Dytiscidae) at five spatial scales in Swedish wetlands. Wetlands 6:57–68

    Article  Google Scholar 

  44. Srivastava AK, Kharbuli B, Shira DS, Sood A (2013) Effect of land use and land cover modification on distribution of anopheline larval habitats in Meghalaya, India. J Vector Dis 50:121–126

    Google Scholar 

  45. Steiger DM, 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 37:69–76

    Article  PubMed  Google Scholar 

  46. Strid GSM (2008) Mosquitoes (Diptera: Culicidae) of city of Ryde, New South Wales. Gen App Ent 37:37–41

    Google Scholar 

  47. Stryker JJ, Bomblies A (2012) The impacts of land use change on malaria vector abundance in a water-limited, highland region of Ethiopia. EcoHealth 9:455–470

    Article  PubMed  Google Scholar 

  48. Vanwambeke SO, Somboon P, Harbach RE, Isenstadt M, Lambin EF, Walton C, Butlin RK (2007) Landscape and land cover factors influence the presence of Aedes and Anopheles larvae. J Med Entomol 44:133–144

    Article  PubMed  Google Scholar 

  49. Weaver SC, Lecuit M (2015) Chikungunya virus and the global spread of a mosquito-borne disease. NEJM 372:1231–1239

    CAS  Article  PubMed  Google Scholar 

  50. Webb CE (2013) Managing mosquitoes in coastal wetlands. In: Paul S (ed) Workbook for managing urban wetlands in Australia, 1st edn. Sydney Olympic Park Authority, Sydney, pp 321–340

    Google Scholar 

  51. Webb CE, Russell RC (1997) Investigation of the mosquito fauna and larval habitats of the saline wetlands at the Olympic site, Homebush Bay, Sydney. Arbovirus Res Aus 7:308–310

    Google Scholar 

  52. Webb CE, Russell RC (1999) Towards management of mosquitoes at Homebush Bay, Sydney, Australia. I. Seasonal activity and relative abundance of adults of Aedes vigilax, Culex sitiens, and other salt-marsh species, 1993-94 through 1997-98. J Am Mosquito Contr 15:242–249

    CAS  Google Scholar 

  53. Webb CE, Russell RC (2012) Mosquito management plan for Byron Shire Council. Byron Shire Council, Mullumbimby

    Google Scholar 

  54. Webb CE, Doggett SL, Willems KJ, Russell RC, Clancy JC, Geary MJ (2001) Mosquito species recorded from the Sydney Basin Region of NSW. Arbovirus Res Aust 8:391–394

    Google Scholar 

  55. Webb CE, Doggett SL, Russell RC (2016) A guide to the mosquitoes of Australia. CSIRO Publishing, Clayton South

    Google Scholar 

  56. Woodroffe CD, Rogers K, McKee KL, Lovelock CE, Mendelssohn IA, Saintilan N (2016) Mangrove sedimentation and response to relative sea-level rise. Ann Rev Mar Sci 8:243–266

    CAS  Article  PubMed  Google Scholar 

  57. Yang G-J, Bradshaw CJA, Whelan PI, Brook BW (2008) Importance of endogenous feedback controlling the long-term abundance of tropical mosquito species. Popul Ecol 50:293–305

    Article  Google Scholar 

Download references

Acknowledgements

The authors wish to thank the assistance of Mr John Clancy from NSW Health Pathology for assistance with identification of mosquito specimens, Kerry Darcovich and Swapan Paul of Sydney Olympic Park Authority for assistance in selecting sampling sites at Haslams Creek and Powells Creek. Dr. Cameron Webb is employed by NSW Health Pathology but no specific funding, only in kind support, was provided by the organisation for this research. Dr. Suzi Claflin was supported in her travel and stipend while in Australia by a Grant awarded by NSF Graduate Research Fellowship Program in addition to an Orenstein endowment grant. These Grants supported Dr. Claflin during her Post-graduate candidature at Cornell University but were not specifically linked to this individual research project.

Funding

No specific funding was sought or awarded for the research presented in this manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Cameron E. Webb.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 30 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Claflin, S.B., Webb, C.E. Surrounding land use significantly influences adult mosquito abundance and species richness in urban mangroves. Wetlands Ecol Manage 25, 331–344 (2017). https://doi.org/10.1007/s11273-016-9520-0

Download citation

Keywords

  • Mosquitoes
  • Mangroves
  • Urban Ecology
  • Landuse
  • Aedes vigilax
  • Avicennia marina