1.1. Malaria in the Southwest Pacific
The malaria transmission zone in the southwest Pacific ranges from Indonesia (Papua Province) through Papua New Guinea (PNG) and the Solomon Islands to Vanuatu. The island of Tanna in Vanuatu marks the southern and eastern limit of the region’s malaria endemic area. The malaria-free island of Aneityum is the most easterly location where anophelines are found (Fig 1). While northern Australia previously experienced regular outbreaks of malaria, the disease was eliminated in 1962  – although it still experiences sporadic outbreaks following reintroductions of the parasites . Malaria remains the most important vector-borne disease in the region with Indonesian Papua, PNG and the Solomon Islands enduring some of the highest attack rates in the world outside Africa .
Malaria is endemic below 1000m, with the degree of endemicity ranging from hypoendemic to holoendemic [4, 5]. Above 1000m malaria tends to be unstable with epidemics of varying degrees of severity [6-8]. Serious control efforts were initiated in the 1950s-1960s as part of the WHO Global Eradication Program, with pilot projects implemented in Papua Province (Indonesia) and PNG (late 1950s) and in the Solomon Islands and Vanuatu (late 1960s). The principal strategy was indoor residual spraying (IRS) with DDT supplemented with mass drug administration of chloroquine .
In 1969, the malaria eradication was abandoned in Papua Province and PNG as it was realized that this goal was not attainable – instead, various control programs were introduced. In PNG, IRS continued until 1984, after which little more was done in the way of malaria vector control until the early 1990s, when insecticide treated bed nets (ITNs) were trialed  prior to widespread distribution. In the Solomon Islands and Vanuatu, full-scale malaria eradication programs (MEP) commenced in the early 1970s but were also abandoned after three years and replaced with control programs . In both countries pyrethroids replaced DDT in IRS in the early 1990s and ITNs became the main method of control . During the 1990s, malaria was successfully eliminated on Aneityum Island, the most southern island of Vanuatu  with mass drug administration as the primary intervention. Recently, renewed efforts at malaria elimination and intensified control were initiated in Tafea Province in Vanuatu and Temotu and Santa Isabel Provinces in the Solomon Islands .
1.2. Geography and climate
This work covers the malarious area of the southwest Pacific as it lies within the Australian faunal region (Fig. 1). This region is made up of numerous islands many of which are mountainous (>4000m) with ranges extending to the coasts and drained by river systems over a narrow coastal plain. In New Guinea, the ranges are fragmented by river valleys, creating extensive lowlands comprising flood plains and swamps. Throughout the region, the climate is dominated by two wind systems and by the influence of mountain barriers and the surrounding oceans. From December to April (the wet season), moist northwesterly winds produce the heaviest and most frequent rains. From May to October (the dry season), southeasterly winds prevail and conditions are drier. However during this period substantial rainfall occurs wherever prominent mountain barriers exist. Thus the climate for most of the region is continuous hot/wet with rainfall >2000mm p.a. with rainless periods rarely exceeding four days. Exceptions occur in southern Western Province and around Port Moresby in PNG where the climate is more monsoonal, the dry season is more pronounced, and the rainfall is less (1600-2000mm p.a.) (Fig. 1) .
Temperature is not a major climatic factor as there is little seasonality and minimal variation throughout each year in a given elevation. However, elevation exerts the main influence on temperature: in coastal and lowland areas (<500m), the mean temperature is 26oC (max 31oC; min 22oC), while in the highland regions (>500m), the mean temperature is 20oC (max 23oC; min 14oC) .
2. Systematics of the malaria vector Groups
The anopheline fauna of the Australian Region is delimited in the west by the Weber Line, which runs through the Moluccas, though there is some incursion east and west of this line by anophelines from the Oriental and Australian Regions (Fig 1 and Table 1). The Australian fauna is highly endemic and most likely of Oriental origin. The malaria vectors in the Australian Region are composed of groups and complexes of closely related, morphologically similar, cryptic or sibling anopheline species. Accurate identification of vector species is essential for interpreting the efficacy of interventions in an area. Since the discovery of cryptic sibling species, the use of morphological characters previously used to identify species has been rendered uncertain. Techniques such as cross-mating, chromosome studies and allozyme analysis were initially deployed to resolve the problems of identifying these sibling species, though none of these can match the speed and simplicity of morphological markers which could be applied in the field. Advances in DNA-based technology with high throughput capability during the past two decades allow large and detailed analyses of vector populations. Although more costly and requiring sophisticated laboratory support, methods such as DNA probe hybridization and PCR are both quick, user-friendly and offer advantages in the study of intraspecific differences between species and for phylogenetic studies. Studies of the
Because of advances in DNA-based technologies, mosquito taxonomists and systematists can now identify, describe, and classify
Anopheles ( Cellia) punctulatus group
The primary vectors of malaria throughout the southwest Pacific region are members of the
Thanks in part to the necessary deployment of Allied defense personnel throughout this region; the taxonomy of this vector group was studied in depth during World War II. Four closely related species were identified –
In 1962, Belkin referred to the group in his taxonomic study of South Pacific mosquitoes . However, this study did not include Irian Jaya, Indonesia (now West Papua/Papua Province) or PNG. Rozeboom and Knight  provide descriptions of the original four members of the
Taxonomic and systematic studies of the group were renewed in the 1970’s when Bryan showed that cross-mating between two
Although proboscis markings are often obvious and easy to detect, proboscis morphology is not a reliable means of distinguishing species in this group. As early as 1945, working in PNG, Woodhill  examined the progeny of wild caught females of the “intermediate form” (now called
The distribution of these species is only beginning to be understood as the group ranges over hundreds of small islands with varying landforms and ecotypes, each island providing opportunities for reproductive isolation and consequent speciation. It is possible that further species may be found when the remote and inaccessible areas of the Moluccas, Indonesian Papua, Papua New Guinea, and the Solomon Islands are more thoroughly surveyed.
2.1.1. Molecular genetic markers
After cross-mating experiments revealed post-mating barriers and the presence of the three species designated
2.1.2. Molecular markers
Allozymes: In the 1990's Foley and colleagues  executed the first population genetic studies into the group using allozyme electrophoresis methods to show that
To facilitate the identification of the large numbers of field-collected material required for malaria studies, Mahon  developed a starch gel allozyme electrophoresis method using two enzymes, lactate dehydrogenase and octanol dehydrogenase. This method was employed to study the distribution of cryptic species of
2.1.3. Species-specific genomic DNA probes
Chromosome banding differences discovered while identifying cryptic species revealed a large variations in the genomic DNA of these species, and suggested possible avenues for producing new technologies for identifying cryptic species. Advances in recombinant DNA technology in the early 1980's enabled the isolation of species-specific repetitive DNA sequences. The use of nucleic acids as characters to identify the members of this group began in 1991 with the development of isotopic DNA probes for the Australian species
2.1.4. PCR-based species diagnostics
126.96.36.199. Ribosomal DNA ITS2
The advent of polymerization chain reaction (PCR) for DNA amplification in the late 1980's facilitated technologies for both cryptic species’ identification and within-species population studies. The most popular marker for species-specific PCR-based diagnosis has been the rDNA gene family. Despite a lack of understanding of the evolution of this non-Mendelian evolving repetitive gene family, its rapidly evolving transcribed spacers allow a simplistic evaluation of genetic discontinuity within and between species. The internal transcribed spacer 2 (ITS2) region proved the most useful for developing two different species diagnostic tools for identifying
Analysis of the ITS2 region reveals substantial insertion and deletion events (indels) between species that are probably due to sequence slippage of common, simple, sequence repeat motifs. Interestingly, no ITS2 PCR-RFLP mixed species hybrids have yet been reported, which would be observed as single mosquitoes sharing RFLP profiles of more than one species. The lack of hybrids at the rDNA locus reinforces the species status for members of this group. Additionally evolutionary information about the
While the ITS1 region has not been examined in as much detail as the ITS2, the ITS1 is an informative marker for intraspecific population studies for some
2.1.5. Evolutionary and phylogenetic studies
Identifying levels of genetic differences among mosquito taxa and the phylogenetic relationships of closely related species allows an understanding of the evolutionary forces acting on mosquito populations. Knowing the evolutionary relationships among vector species can provide insights into understanding the dynamics of disease transmission. Initial attempts to generate a species-level phylogeny of the
The same evolutionary mechanisms that led to the existence of these species have also produced a number of genetically distinct populations within each species that may differ in behaviour and in their potential to transmit malaria parasites. For example, recent investigations have revealed that genotypes of
Anopheles ( Cellia) longirostris complex
Anopheles ( Cellia) lungae complex
Initially described by Belkin , the
Anopheles ( Anopheles) bancroftii group
Two morphological species were initially described in the
3. Species distribution, biology and vectorial status
3.1. Primary vectors
Three species –
In PNG, the Solomon Islands, and Vanuatu, where extensive sampling has occurred and the mosquitoes’ distribution is well understood,
Given that many rural communities throughout the region are connected by unsealed dirt roads, these thoroughfares – along with roads and construction associated with logging and mining activities – have created both extensive larval sites for this species and the corridors along which it can move.
Of the three primary malaria vectors in the southwest Pacific,
It is a moderately long-lived mosquito with parity rates ranging between 0.52 and 0.75 [65, 83]. It has been incriminated as a vector throughout its range [8, 59, 65, 67, 68]. Along with
3.2. Secondary vectors
A number of species have been found infected with human malaria sporozoites throughout the southwest Pacific, but because they have limited distributions or are relatively uncommon, they are considered secondary vectors.
Several genetically structured populations were found within
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Little is known about this vector’s behaviour with regards to malaria transmission although in northern PNG it appears that human feeding activity peaks early in the evening and then declines through the rest of the night .
3.3. Possible vectors
There are several
The members of the
Several species that occur in the region have limited distributions and are too uncommon to play any significant role in malaria transmission. These species include
3.5. Oriental species
Five anopheline species –
4. Vector control
The strategy behind the use of indoor residual spraying (IRS) and insecticidal treated bed nets (ITNs) is to deliver insecticide to vectors which have entered the house to obtain a blood meal. Given that a female mosquito feeds every second or third night, it will seek a blood meal at least 3 to 5 times during the duration of the extrinsic incubation period, allowing 3 to 5 opportunities to contact the insecticide associated with IRS and ITNs before it develops sporozoites in the salivary glands. Ideally, for IRS and ITNs to successfully control malaria, the vector should exhibit the following behaviours: a) be highly anthropophilic, b) feed indoors late at night when the humans are indoors, and c) rest on the insecticide treated surfaces of ITNs or IRS either before or after feeding.
The primary vectors in the southwest Pacific initially were reported to exhibit this type of behaviour to varying degrees.
With the implementation of the eradication program and subsequent control programs using DDT with IRS, populations of
Slooff  studied the house-visiting behaviour of
Studies into the failure of IRS to adequately control populations of
This shift in biting time to early in the night appears fixed in some populations: when spraying was withdrawn, the early night-feeding pattern was maintained. In Temotu and Santa Isabel in the Solomon Islands, where DDT IRS was intensively applied during the eradication program of the early 1970s but only intermittently during the subsequent 35 years,
On Buka Island, in 1961 prior to spraying with DDT,
There were only a limited number of vector control strategies evaluated in the southwest Pacific in the decades following the cessation of the IRS-based elimination campaigns. While the DDT campaigns did not succeed in eliminating malaria, the campaigns were credited with the elimination of filariasis from the Solomon Islands where that disease was transmitted by the members of the
The first study of permethrin treated nets in PNG reported significant reductions in the sporozoite rates in the
In the Solomon Islands, ITNs had significantly greater impacts than IRS on vector infectivity and inoculation rates of
In Vanuatu, malaria was successfully eliminated from the island of Aneityum using a strategy of mass drug administration with pyrimethamine/sulfadoxine (Fansidar), and primaquine, ITNs and larvivorous fish. Falciparum malaria disappeared soon after the start of mass drug administrations . The successful elimination was a function, most likely, of a small island population and the seasonality of transmission together with a high participation of the community in the mass drug administration. The impact of larvivorous fish was believed to be “probably marginal” due to the failure to find all breeding sites and the “incompleteness of predation”.
Interpretation of the impact of these interventions must consider the period when the studies were conducted as reports of changes in behaviours of the vectors (discussed earlier) are known to have occurred; the effectiveness of an intervention is not static but is also dependent on the vectors’ behaviours (e.g., shifts toward early feeding and outdoor biting may reduce the effectiveness of ITNs and IRS, as was demonstrated by Slooff , Taylor  and Sweeney ). Resistance to pyrethroids (and the existence of knockdown resistance genes) has not yet been found in the few studies thus far conducted in the southwest Pacific ; however, 30% of
There is now a renewed interest in malaria control with IRS and ITNs in the Solomon Islands and Vanuatu with elimination programs in some areas and intensified control in all other areas. At the most fundamental level, the intervention measures of IRS and ITNS both rely on the vector feeding late at night when people are indoors. As such, these tools have the potential to provide effective control of late night biting
In 2007, the Bill and Melinda Gates Foundation challenged the malaria community to once again attempt to achieve malaria eradication. The failure of the previous campaigns was due, in part, to attempting to control many vector species with a single intervention that targeted vectors inside houses. Enhancing our chances of eliminating malaria in the southwest Pacific will require the implementation of novel interventions that target vectors based on our knowledge of their behaviours. However, basic knowledge about the biology and behaviours of some vectors and potential vector species in this region is limited. This knowledge gap must be filled before control strategies can be optimized to exploit the vectors’ biological vulnerabilities to control measures. The basic parameters essential to understanding transmission such as feeding habits, host preference, longevity, frequency of feeding and seasonal abundance – which are essential for the selection of effective control strategies –, await discovery for many species. Additionally, we remain uncertain of the complete distribution of species, or the importance of the various genotypes that have been recognized to date in a number of taxon.
Significant advances in DNA technologies have enhanced our ability to both discover and identify cryptic species in the southwest Pacific. These technologies, coupled with immunological and molecular assays to detect malaria parasites in mosquitoes, have led to the resurgence in investigations to incriminate vectors and to characterize their behaviors. We now know that there are 13 species in the
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