SEARCH

SEARCH BY CITATION

Keywords:

  • Mosquito control;
  • arbovirus;
  • vector;
  • statistical modelling;
  • pest management

ABSTRACT:

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Mosquitoes are problematic as vectors and pests in many tropical cities, including Darwin, the principal city in the Northern Territory of Australia. To monitor peaks in mosquito populations, the Medical Entomology unit of the Health Department sets overnight CO2-baited traps weekly. Trap setting and retrieving, followed by mosquito counting and identification, are labor intensive. Aiming to reduce this workload, we tested the hypothesis that fortnightly trapping is as effective as weekly trapping across seasons and ecologically distinct systems in Darwin. We applied cross-sectional negative binomial mixed effects models, which adjusted for rain and calendar month, to existing historical data. Culex annulirostris peaks were effectively identified using fortnightly trapping across all three ecological systems, during wet/dry and build-up seasonal patterns. For Aedes vigilax, fortnightly trapping was adequate in identifying peaks during wet and dry season months, but inadequate during build-up months across all three ecological systems. Therefore, weekly trapping should continue during build-up months, but trapping could be reduced to fortnightly for wet and dry season months for all ecological systems. Trapping for Cx. annulirostris monitoring could be reduced to fortnightly in all areas and seasons. Evaluation of programs can maximize staff efficiency and improve service delivery by reducing the need for unnecessary tasks.


INTRODUCTION

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Darwin, the principal city in the tropical north of the Northern Territory of Australia, has historically been associated with a high burden of endemic mosquito-borne diseases (Russell and Whelan 1986). Furthermore, residential development in Darwin since the 1970s has been concentrated in close proximity to major creeks, swamps, and wetland areas known to support mosquito breeding (Figure 1) (Russell and Whelan 1986). Creek systems and wetlands experience seasonal tidal inundation and wet season pooling of rainwater. This creates a flooding-desiccation cycle providing suitable seasonal larval habitats for the common banded mosquito Culex annulirostris (Skuse) and the northern salt-marsh mosquito Aedes vigilax (Skuse). Culex annulirostris is the most significant pest species in the Northern Territory. It is also a vector for Murray Valley encephalitis virus. The disease from this virus, previously called “Australian encephalitis,” is potentially fatal (Doherty 1972). Aedes vigilax is also recognized as a major human pest species (Mackerras 1926, Marks 1967, Gislason and Russell 1997, Webb and Russell 1999) (Whelan 1989). Both mosquito species are established vectors for Ross River and Barmah Forest virus (Whelan et al. 1997, Russell 1998, Jacups et al. 2008), which constitute the majority of arbovirus infections in Australia (Russell 1994, Russell 1995).

image

Figure 1. Adult mosquito monitoring program-locations routine weekly adult mosquito CO2-baited light trap sites in study analysis.

Download figure to PowerPoint

Larval mosquito ecology varies across Darwin. Different wetland systems produce distinct peak periods of mosquito abundance in response to vegetation characteristics coupled with local weather conditions (Whelan 2007). Although habitats are in relatively close proximity to each other; their vast ecological differences result in locally specific vector prevalence and vector control requirements, and these require individual assessment (Whelan 2007). This is exemplified by the diversity of counts and species reported from adult mosquito traps located around the different wetlands, as populations respond to localized breeding conditions.

The Department of Health's Medical Entomology unit conducts overnight trapping of adult mosquitoes weekly at multiple sites in Darwin urban area using CO2-baited EVS light traps (Whelan 2007). Traps are positioned between wetland breeding sites and urban areas to target mosquito densities in close proximity to residential areas (Figure 1). Trapping adult mosquitoes identifies peaks in mosquito populations and functions as a feedback mechanism for larvicidal controls conducted after rainfall or high tide events. Weekly trapping is labor intensive involving the employment of one staff member. Each week one staff member drives to trap sites, sets traps, and retrieves them the following day. Staff then count and identify mosquito samples and enter counts into a custom-designed database. These tasks are rotated among staff but occupy 40–50 h each week. The wet season months are especially busy, as mosquitoes are abundant in most habitats, resulting in greater time and personnel constraints as mosquito reduction control operations are required.

Using existing data, we sought to test the hypothesis that an alternate, work-reduced mosquito trapping protocol (fortnightly) is as adequate at detecting peaks of Ae. vigilax and Cx. annulirostris as the current (weekly) trapping protocol across three ecologically distinct habitats in Darwin. If fortnightly trapping is as effective as weekly trapping in detecting the magnitude of vector mosquito peaks, then this laborious task could be reduced and staff re-allocated to other mosquito control tasks, thus maximizing the efficiency of the unit and enabling the staffing of mosquito control programs for Darwin's newly developed and expanding residential suburbs.

MATERIALS AND METHODS

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Darwin is situated in the tropical zone of Australia (12° 28′ S, 130° 51′ E) and experiences a monsoon climate, with a high average annual rainfall of 1,708 mm. Most rainfall occurs during the wet season, from November to April. We defined the Darwin “wet season” as December to April inclusive, which differs from the Bureau of Meteorology (BOM) definition, which includes the hot and humid “build-up” months that rarely receive rain in its wet-season definition (Australian Bureau of Meteorology 2009). The build-up to the wet season is defined here as September to November inclusive, with the “dry season” defined as May to August inclusive. Daily rainfall data (Darwin airport rain gauge) was provided by the BOM for the study period (Australian Bureau of Meteorology 2010). Total rainfall by calendar month was used in the analysis.

There are three major larval mosquito sites in the Darwin urban area (Figure 1). These are the tidal creek areas represented by the trap sites at Casuarina, Totem Road, and Coconut Grove (Red traps); the seasonally saline reed swamps around Leanyer and Holmes Jungle (White traps); and the non-tidal freshwater wetland at Marrara (Blue traps) (Figure 1). These three ecologically distinct systems provide suitable breeding habitats for Cx. annulirostris and Ae. vigilax.

Counts of Ae. vigilax and Cx. annulirostris females were collected from overnight EVS traps (manufactured by the Medical Entomology Department) set weekly in 11 locations, as indicated in Figure 1. Mosquito identifications were performed by the Medical Entomology Department in Darwin, with sub-samples of 300 mosquitoes identified to species level, after which the total was estimated by weight (Kurucz et al. 2005). Mosquito species were limited to include only the major vectors of endemic diseases in the region. Monthly averages, calculated from weekly mosquito counts between 1991 and 2005 (180 months), were compared with averages calculated using every second-week mosquito counts (fortnightly).

We compared weekly mosquito trapping protocol with fortnightly trapping using cross-sectional negative binomial models. Multiple models were required to clarify associations across ecological systems. All models included time (month) and rainfall as independent variables and some models included season (wet, dry, build-up). Models included mosquito species together (Ae. vigilax and Cx. annulirostris, Model 1); Cx. annulirostris only- by season (Model 2); and Ae. vigilax only modelled for each ecological system, by season (Model 3).

The best models were determined by Akaike's information criterion and maximum log-likelihood methods (Rabe-Hesketh and Skrondal 2005). As the data were counts, their means follow a gamma distribution. Poisson models or negative binomial models are traditionally used with negative binomial chosen in preference in cases of high over-dispersion, as the mean may not equal the variance. Cross-sectional models allow comparison of data across time periods that are not always equal in length (Beck 2004). Output coefficients indicate the strength and direction of variable association with the regressor. To control for time and seasonal (rainfall) variation, we applied a cross-sectional negative binomial mixed effects model to our count data. The model was in the form of:

  • image

where yit is the dependent variable observed for individual i at time t, Xit is the time-variant regressor, and Zi is the time-invariant regressor. In the random-effects model, the dispersion varies randomly from group to group, such that the inverse of the dispersion has a Beta (r s) distribution. All analyses were performed using STATA version 11.0 (Stata Corp., College Station, TX, U.S.A.).

RESULTS

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Modelling results of both species combined, controlling for rain and month, indicated no difference between weekly vs fortnightly trapping (p= 0.059, Table 1). When the results were separated by mosquito species and season, a trend was observed between weekly vs fortnightly for Cx. annulirostris mosquito peaks during the wet, dry, and build-up seasons (p= 0.098, p= 0.959, p= 0.233, Table 2) respectively, across all three ecosystems combined. When modelling Ae. vigilax only, results indicate statistical differences between weekly vs fortnightly protocols for all three ecosystems during build-up months only. For tidal creeks at Casuarina and Coconut Grove (Red traps) (p= 0.001, Table 3, Model 3A), there were similar results for freshwater systems (Blue traps) (p= 0.001, Table 3, Model 3B), and mangrove/reed systems (White traps), (p= 0.010, Table 3, Model 3C).

Table 1.  Cross-sectional negative binomial mixed effects model. Weekly vs fortnightly adult mosquito trap sampling for Ae. vigilax and Cx. annulirostris.
Model 1Coefficientp95% CI
Total rainfall0.0000.14500.001
Weekly vs fortnightly0.0510.059–0.0020.103
Calendar month–0.0770.000–0.111–0.044
Table 2.  Cross-sectional negative binomial mixed effects modelling results. Weekly vs fortnightly adult mosquito trap sampling for Cx. annulirostris females only.
Model 2 Coefficientp95% CI
Wet season monthsTotal rainfall0.0000.2990.0000.001
Weekly vs fortnightly0.0630.098–0.0120.137
Calendar month–0.1320.000–0.172–0.092
Dry season monthsTotal rainfall–0.0090.092–0.0190.001
Weekly vs fortnightly–0.0020.959–0.0630.060
Calendar month–0.1540.062–0.3150.008
Build-up monthsTotal rainfall0.0030.320–0.0030.008
Weekly vs fortnightly0.0520.233–0.0330.137
Calendar month–0.8310.000–1.276–0.385
Table 3.  Cross-sectional negative binomial mixed effects models. Weekly verses fortnightly adult mosquito trap sampling for Ae. vigilax females only.
  Coefficientp95% CI
Model 3A Tidal Creeks Red traps      
Wet season monthsTotal rainfall0.0030.0000.0010.004
Weekly vs fortnightly0.0040.939–0.0910.098
Calendar month0.1280.0010.0530.203
Dry season monthsTotal rainfall–0.0060.455–0.0210.009
Weekly vs fortnightly0.1140.173–0.0500.278
Calendar month–0.1140.411–0.3860.158
Build-up monthsTotal rainfall0.0030.445–0.0040.009
Weekly vs fortnightly0.3930.0010.1670.618
Calendar month0.2530.378–0.3090.816
Model 3B Freshwater wetland Blue traps      
Wet season monthsTotal rainfall0.0020.0530.0000.003
Weekly vs fortnightly0.0680.420–0.0980.234
Calendar month0.0920.0210.0140.169
Dry season monthsTotal rainfall0.0070.589–0.0180.032
Weekly vs fortnightly–0.0330.801–0.2870.222
Calendar month0.0900.604–0.2500.429
Build-up monthsTotal rainfall0.0070.112–0.0020.015
Weekly vs fortnightly0.4270.0010.1750.679
Calendar month0.0850.811–0.6140.785
Model 3C Mangrove/reed wetland White traps      
Wet season monthsTotal rainfall0.0020.0140.0000.003
Weekly vs fortnightly0.0540.363–0.0630.172
Calendar month0.0690.088–0.0100.148
Dry season monthsTotal rainfall–0.0030.690–0.0200.013
Weekly vs fortnightly0.1140.110–0.0260.253
Calendar month–0.0540.730–0.3590.252
Build-up monthsTotal rainfall0.0090.041<0.0010.018
Weekly vs fortnightly0.2800.0100.0680.492
Calendar month–0.1990.569–0.8820.485

DISCUSSION

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

The results indicate that fortnightly trapping, when conducted at the 11 sites adjoining Darwin's northern suburbs, is as effective for monitoring Cx. annulirostris species as weekly trapping. Additionally, fortnightly trapping was adequate for detecting peaks of Ae. vigilax at all three ecosystem locations during wet and dry season months. However, fortnightly trapping failed to detect the magnitude and timing of Ae. vigilax peaks during build-up months for all three ecological systems. Therefore, routine trapping could be reduced from weekly to fortnightly without a significant loss of information across ecological systems for most of the year.

As a rule, Cx. annulirostris breeds seasonally in temporary ground pools after rain. Eggs are laid in rafts on the water surface and each habitat may support a range of larval instars, which leads to relatively stable numbers of emerging mosquitoes. As rain-filled depressions exist throughout the wet season, and stormwater and waste water discharge can continue well into the dry season, Cx. annulirostris breeding is often continuous throughout the wet season and well into the dry season without obvious sharp population peaks. Nevertheless, breeding in seasonally extended wetlands during the late wet and early dry season generally produces some high population peaks. As Cx. annulirostris population peaks are usually greater than one week's duration, there was no significant difference between weekly and fortnightly trapping regimes; therefore the findings from this study are consistent with the mosquito species ecology.

In contrast to freshwater breeders, Ae. vigilax has a highly fluctuating cycle of population peaks that follow inundation by tides or rain (Kay et al. 1981). Wet season-flooded areas progressively recede until most of the area is dry. From the mid-dry season (July), spring tides inundate Ae. vigilax breeding habitat, increasing productivity. Tidal and /or rain inundation leads to high-density mosquito breeding until late in the wet season when the area becomes flooded, reducing oviposition sites and allowing predation by fish (Ritchie 1984, Jacups et al. 2009). This finding is congruent with other findings from this study site, documenting Ae. vigilax larval densities as highest between October and December each year (Jacups et al. 2009, Kurucz et al. 2009).

Maintaining rigid mosquito control for mosquito borne-disease reduction mandates adult trapping regimes that can provide timely feedback information on Ae. vigilax populations. This enables responses by the medical entomology unit to modify surveillance strategies or larvicide control to reduce mosquito population levels. This is essential for safeguarding against mosquito-borne disease transmission and public distress associated with biting at pest levels. To maximize the efficiency of adult mosquito control operations in Darwin, control should be concentrated on the build-up months between September and December each year. During these months, the medical entomology unit should trap weekly, but during the other months of the year a fortnightly adult trapping program for the northern suburbs would offer a cost effective alternative, freeing up a staff member to assist with other mosquito control programs, and thus maximizing service delivery without the loss of valuable information.

This work bridges the fields of public health and ecology, and tests a management strategy to lower the workload within current programs aimed at pest and mosquito vector reduction. Evaluations such as this assist pest and disease management using existing and simulated data, without the need of additional field experiments. The methodologies developed here could be easily applied to many other areas of service delivery and best practice to ensure that only valuable data is collected and staff are utilized in areas of maximum need.

Acknowledgments

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

We thank the staff at Medical Entomology for on-going surveillance and monitoring of mosquito populations. We thank Raelene Whitters for the creation of Figure 1. We thank the two anonymous reviewers who greatly improved the manuscript. This work was supported by NHMRC and Sidney Myer Foundation postgraduate scholarships.

REFERENCES CITED

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED
  • Australian Bureau of Meteorology. 2009. Australian Bureau of Meteorology Website. Australian Bureau of Meteorology, Darwin . 18/09/2009. http://www.bom.gov.au/announcements/media_releases/nt/20040505.shtml.
  • Australian Bureau of Meteorology. 2010. Australian Bureau of Meteorology Website. 6/11/2008. http://www.bom.gov.au.
  • Beck N. 2001 Time-series-cross-section-data: What have we learned in the past few years? Annu. Rev. Political Sci. 4: 271293.
  • Doherty R.L. 1972. Arboviruses in Australia. Aust. Vet. J. 48: 172179.
  • Gislason, G.M. and R.C. Russell 1997. Oviposition sites of the saltmarsh mosquito, Aedes vigilax (Skuse) (Diptera: Culicidae), at Homebush Bay, Sydney, NSW- a preliminary investigation. Aust. J. Entomol. 36: 97100.
  • Jacups, S.P., P.I. Whelan, and B.J. Currie. 2008. Ross River virus and Barmah Forest virus infections: a review of history, ecology, and predictive models, with implications for tropical northern Australia. Vector Borne Zoonot. Dis. 8: 283298.
  • Jacups, S.P., N. Kurucz, P.I. Whelan, and J.M. Carter. 2009. A comparison of Aedes vigilax larval population densities and associated vegetation categories in a coastal wetland, Northern Territory, Australia. J. Vector Ecol. 34: 311316.
  • Kay, B.H., P. Sinclair, and E.N. Marks. 1981. Mosquitoes: their interrelationships with man, In: R. L. Kitching and R. E. Jones (eds.), The Ecology of Pests. CSIRO publishing, Melbourne . pp. 15774.
  • Kurucz, N., P.I. Whelan, J. Carter, and S.P. Jacups 2009. Vegetation parameters as indicators for salt marsh mosquito larval control in coastal swamps in northern Australia. Arbov. Res. Aust. 10: 8490.
  • Kurucz, N., P. Whelan, S. Jacups, A. Broom, and L. Melville. 2005. Rainfall, mosquito vector numbers and seroconversions in sentinal chickens to Murray Valley encephalitis virus in the Northern Territory. Arbov. Res. Aust. 9: 188192.
  • Mackerras, I.M. 1926. The mosquitoes of the Sydney district. Aust. Nat. 6: 3342.
  • Marks, E.N. (ed.) 1973. An Atlas of Common Queensland Mosquitoes. Univ. Qd. Bksp, St Lucia . 102 pp.
  • Rabe-Hesketh, S. and A. Skrondal. 2005. Multilevel and Longitudinal Modeling Using STATA . Stata Press, Texas .
  • Ritchie, S. 1984. Record winter rains and the minimal populations of Aedes taeniorhynchus (Wiedemann): Cause and effect? J. Fla. Anti-Mosq. Assoc. 55: 1421.
  • Russell, R.C. 1994. Ross River virus: disease trends and vector ecology in Australia. Bull. Soc. Vector Ecol. 19: 7381.
  • Russell, R.C. 1995. Arboviruses and their vectors in Australia: an update on the ecology and epidemiology of some mosquito-borne arboviruses. Rev. Med. Vet. Entomol. 83: 141158.
  • Russell, R.C. 1998. Mosquito-borne arboviruses in Australia: the current scene and implications of climate change for human health. Intl. J. Parasitol. 28: 955969.
  • Russell, R.C. and P.I. Whelan. 1986. Seasonal prevalence of adult mosquitoes at Casuarina and Leanyer, Darwin. Aust. J. Ecol. 11: 99105.
  • Webb, C.E. and R.C. Russell. 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. Mosq. Contr. Assoc. 15: 242249.
  • Whelan, P.I. 1989. Integrated mosquito control in Darwin. Arbo. Res. Aust. 5: 178185.
  • Whelan, P.I. 2007. Mosquito vector control in the Northern Territory. NT Disease Contr. Bull. 14: 1218.
  • Whelan, P.I., A. Merianos, and G. Hayes. 1997. Ross River virus transmission in Darwin Northern Territory, Australia. Arbov. Res. Aust. 7: 337345.