DIVERSITY AND VECTORIAL SYSTEM OF ANOPHELINE MOSQUITOES (DIPTERA: CULICIDAE) IN SELECTED ECO-SETTINGS OF NASARAWA STATE, NIGERIA

ABSTRACT

Mosquitoes are known to constitute nuisance as well as transmit disease-causing organisms (pathogens) to hosts. This study was aimed to determine species distribution, abundance, and diversity of mosquitoes in three selected eco – settings of Nasarawa State, Nigeria. Anopheles mosquitoes were sampled using Pyrethroid Spray Catch (PSC and Centre for Disease control light traps CDC) technique the mosquitoes were identified morphologically using keys. Knockdown resistance (Kdr) was determined following standard protocols. Meal preference was determined using Enzyme Linked Immuno Sorbent Assay (ELISA). Collected mosquitoes were classified based on physiological conditions. Molecular forms of the Anopheline species were determined following standard methods. Six (6) species of Anopheles mosquito vectors were encountered in all the selected eco – settings of Nasarawa State: Anopheles gambiae s.l, An. funestus, An. nili, An. coustani, An. rufipes and An. pharoensis. A total of Fifteen thousand, four hundred and seventeen (15,417) mosquitoes vector were encountered in the study areas between the months of January to December, 2017. Most of the mosquitoes encountered were Anopheline (64.09 %). Analysis revealed significant variations in the relative abundance of mosquito and distribution of the vector across the eco – settings studied. The highest number of mosquitoes was caught in the month of May 2017 (1,273; 12.88 %). An. gambiae s.l were the most dominant species (41.89%) encountered across the eco – settings during the two seasons followed by An. coustani (19.49 %). Indoors An. gambiae s.l. collection accounted for 68.21 %. The indoor resting density was 4.46, 3.99 and 3.65 man/hour/night, for sparse woodland, wooded grassland, and swampy grassland, respectively. Wet season accounted for 57.24 % of the vectors collected. Abdominal conditions analyses revealed 27.40 % were half gravid, 26.08% were gravid and 25.97 % were freshly fed. The highest HBR was recorded in the month of May 2017 (18.30, 22.90, and 23.00 bites/man/hour, for sparse woodland, wooded grassland, and swampy grassland, respectively). Molecular analyses revealed S form An. gambiae s.s constituted 64.47 % of the collection, while 15.47 and 10.93 % were M form An. colluzzi and An. arabiensis. The sporozoite rate was 20.20 % in swampy grassland, 13.20 % in sparse woodland, and 12.80 % in wooded grassland. For the Kdr analyses, 19.02 % of the vectors were (RR) resistant, 31.66% were (RS) heterozygous susceptible and 50.51% were (SS) Susceptible in the study area. Blood meal source analyses revealed 47.47 % was from human, 30.54 % from bovine, and 21.72 % from goats for the study area. Anopheles gambiae s.s had 95.95 % blood meal from human, 45.07 % from bovine and 33.66 % from goats also for single blood meal source 98.56 % was from humans, 44.44% from bovine and 28.32% from goats. Anopheles arabiensis obtained 1.44 % of blood meal source from human, 55.56 % from bovine and 71.67 % from goats mixed blood meal source. Anopheles arabiensis obtained 24.30, 30.43, 33.85, 54.55 % from human/goat, human/bovine, human/bovine/goat and bovine/goats, respectively. This study revealed that Anopheles species were higher in terms of abundance which is very important vectors of malaria in Nigeria. These results indicated that vectors of mosquito-borne diseases are breeding in the study area, most of which are encouraged by human activities.

CHAPTER ONE

1.0        INTRODUCTION

1.1        Background to the study

Malaria is among the world’s most important parasitic diseases, causing approximately 438,000 deaths worldwide in 2015 (WHO, 2015). Controlling this disease is difficult due to many factors, including the emerging resistance to antimalarial drugs by the parasites, increasing resistance among some of the primary vectors, as well as a lack of knowledge about their biology and ecology.  The human vector contact, particularly with An. gambiae s.l., shows a remarkable stability and flexibility, producing extremely high inoculation rate in a range of geographic and seasonal ecological conditions (Adeleke et al., 2010).

Malaria continues to be an ongoing problem in African countries south of the Sahara and although a lot has been achieved in the past 15 years, millions of people still remain at risk of contracting the parasite (Bhatt et al., 2015) Africa provides a stable and ecologically diverse ecosystem and is home to the most efficient malaria vectors in the world (Sinka et al., 2010; Wiebe et al., 2017) and is likely to remain so in the face of global climate change. The major anopheline malaria vectors across sub-Saharan Africa are Anopheles funestus s.s. and three members of the Anopheles gambiae complex: An. gambiae s.s., Anopheles coluzzii and Anopheles arabiensis (Gillies and Coetzee, 1987a; Sinka et al., 2010). However, there are some additional species outside of these that play a role in malaria transmission within their geographic distribution, for example the Anopheles moucheti and Anopheles nili groups (Wiebe et al., 2017). There are host of secondary or incidental vectors (Antonio-Nkondjio et al., 2006; Tabue et al., 2017). Considering that the genus Anopheles contains over 500 species globally, of which only a few are considered important species for malaria transmission (Sinka et al., 2010; Garros and Dujardin, 2013). The morphological identification of species is crucial in order to target scarce resources for controlling the malaria vectors only. Species groups and species complexes are common within the genus Anopheles (Harbach, 2004) and this complicates vector control since not all  species  within  a  complex  have  similar  behaviours  or  similar  roles  in  malaria transmission (Gillies and Coetzee, 1987b; Wiebe et al., 2017). In the An. gambiae complex, for example, species range from the non-vectors Anopheles quadriannulatus and Anopheles amharicus to minor vectors Anopheles melas, Anopheles merus and Anopheles bwambae, to the major vectors An.gambiae, An. coluzzii and An. arabiensis (Gillies and Coetzee, 1987a; Coetzee et al., 2013).

Mosquitoes of the family Culicidae are considered a nuisance and a major public health problem, because their females feeds on human blood and thus transmit extremely harmful diseases,  such  as  malaria,  yellow  fever  and  filariasis.  They  are  estimated  to  transmit diseases to more than 700 million people annually and responsible for the death of about 1 in 17 people (WHO, 2000a).   Effective transmission of mosquito-borne disease requires successful contact between female mosquitoes and their hosts (Xu et al., 2014). Among Anophelinae, the members of the genus Anopheles are best known for their role in transmitting malaria and filariasis worldwide (Service, 1980; WHO, 2013). The malaria caused by Plasmodium parasite is one of the greatest killer diseases in the world (WHO, 2013). World Health Oorganisation (2013) reported an estimated 207 million cases of malaria in 2012 out of which 200 million cases (80.0 %) were in Africa continent. The distribution pattern, transmission and intensity of the disease are dependent on the degree of urbanization and the distance from vector breeding sites (Centre for Disease Control and Prevention, CDC, 2015). The endemicity of malaria in any region is determined by indigenous Anopheles mosquitoes, abundance, feeding, restingbehavior and their Plasmodium infectivity, among other factors (Molta, 2000; WHO, 2003).

Federal Ministry of Health, Abuja reported that at least 50.0 % of Nigerians suffered from one form of malaria or the other making it the most significant health problem in Nigeria (Chukwuocha, 2012). The high transmission rate and prevalence of malaria is as a result of the diverse mosquitoes breeding sites, which include practically receptacle that holds water, such as tins, cans, old tyres, tree holes, cisterns, open pools, drainage, stream and pond (Ingstad et al., 2012). People living in poor rural areas are confronted with a multitude of barriers when assessing malaria prevention especially on the knowledge of the biology and ecology of the vectors, among others (Ingstad et al., 2012).

The mapping of malaria vectors is important in the control of malaria. This is because the species composition and distribution and other biological parameters of the mosquitoes are poorly known in different ecological zones of Nigeria and in most of the malaria endemic areas due to the difficulties in the morphological identification of certain complex species, theknowledge of which is required in the design of vector control programmes and in tackling the prevalence of the disease in endemic areas (Awolola et al., 2002).

Mosquitoes are responsible for the spread and transmission of several harmful diseases such as malaria and lymphatic filariasis. It is known to infect over 700 million people causing 1 million deaths each year especially in developing regions of the world including sub-Saharan Africa (WHO, 2016). Despite years of control efforts, malaria continues to be a major threat to public health in parts of sub-Saharan Africa, Nigeria inclusive. About 97% of Nigeria’s population is at risk of malaria where 60% of hospital outpatient visits and 30% of hospitalization among children under five years and pregnant women occur due to malaria (CDC, 2017). Entomological studies focused on the diversity, density, behavioral patterns and temporal variations of Anopheles species have long been found to be beneficial in the identification and monitoring of malarial vectors (Tadei et al., 1998). A combination of factors that determine the capacity of a vector to transmit malaria include; abundance, anthropophily, zoophily, susceptibility to infection by the malaria parasite, infection rates and female longevity (Aniedu, 1992; Lounibos and Conne, 2000).

Vector-borne diseases remain a major public health issue in the tropical and subtropical regions  of the  world  (WHO,  2016).  Anopheline vector  of malaria consists  of various species with unique behaviour associated with their biting activities and transmission dynamics. Human malarial protozoa are transmitted by mosquitoes of the genus Anopheles. Mosquitoes of the family Culicidae are considered a nuisance and a major public health problem, because their females feeds on human blood and thus transmit extremely harmful diseases, such as malaria, yellow fever and filariasis (WHO, 2015).  Malaria leads to a lot of  social  and  economic  problems,  such  as  school  absenteeism,  lower  agricultural production among others; consequently, more control efforts are required in order to reduce the rates of disease incidences and mortality.

The vectorial capacity of a mosquito population largely determines the intensity of vector- borne disease transmission. The vector competence is also  a crucial parameter for the pathogen to be transmitted. In human malaria, vectorial systems are limited in number.

Only Anopheles females are able to transmit Plasmodium to humans, and, among the more than 450 Anopheles species known, 60 are considered to be actual vectors in the wild (Manguin  et  al.,  2008).  Vectorial  capacity  and  competence  also  present  quantitative features in the sense that some species have a major role in malaria transmission, and others have a minor role. Even at the species level, some populations or individual mosquitoes can have different impacts on transmission (Manguin et al., 2008). Research to understand the genetic determinants of capacity and competence has greatly benefited from the availability of the whole genome sequence for Anopheles gambiae (Holt et al., 2002) with the identification of candidate genes in progress. However, the different aspects of vectorial capacity and competence have not been uniformly studied, and some have been largely overlooked.

There are 465 formally recognized species and more than 50 unnamed members of species complexes. Approximately 70 of these species have the capacity to transmit human malaria parasites and 41 species are considered to be dominant vector species complexes capable of transmitting malaria at a level of major concern to public health (Coetzee et al., 2013; WHO, 2015).

The knowledge of major malaria vectors and their bionomics in Africa remains a problem. Hay et al. (2000) as a focal disease, malaria will therefore differ in its characteristics from place to place, since all malaria vectors do not exhibit identical behavior and ability to transmit parasites. Globally medical reports have shown that mosquito-borne diseases-are responsible for significant effect on human morbidity and mortality throughout the world (WHO, 2013). The global burden is 207 million malaria cases every year resulting into 627,000  deaths  (WHO,  2013),  sub-Saharan  Africa  being  the  most  affected  region. According to the latest WHO malaria report (WHO, 2014), there were in 2014 about 197 million malaria cases worldwide and an estimated 584 000 deaths, mostly among African children.

In  Nigeria, malaria still remains a major health problem with about two-thirds of the population living in malarious areas (WHO, 2015).  Among the malaria vectors in Nigeria Anopheles gambiae complex, An. funestus seems to be the major vectors of malaria transmission in the country though there are other non and minor vectors who are now incriminated to be responsible for the malaria transmission (Awolola et al. 2002).

1.2       Statement of the Research Problem

Vector borne diseases are among the major causes of illness and death, particularly in tropical and subtropical countries; vector control through the use of insecticide plays a key role in the prevention and control of infectious diseases. Anopheles mosquitoes are the major vectors responsible for malaria transmission in the tropical and subtropical regions of the world including Nigeria and Nasarawa state Mosquito control remains an important component of human and animal diseases. Currently, there is little or no empirical data on Anopheles mosquito vector population, dynamics in the eco-settings of Nasarawa State Malaria is characterized by it biological diversity and this diversity is conditioned mostly by the Anopheline mosquitoes that are involved in the transmission through their distribution, behaviour and vectorial capacity. The Anopheline mosquitoes responsible for malaria transmission differs in their distribution and major characteristics from different regions to another and may also differ across the selected eco-setting of Nasarawa state.

In  Nigeria,  mosquitoes  are  regarded  as  public  health  enemies  because of their biting annoyance and noise nuisance, sleeplessness, allergic reaction and disease transmission due to their bites. They transmit human diseases such as malaria, yellow fever, dengue, haemorrhagic fever, filariasis  and  encephalitis.  Mosquito  control  remains  an  important component of human and animal diseases. However, this has been limited by the development and spread of resistance and limited knowledge of mosquito biology. Also significant changes in resistance patterns have been observed over the past 10 years in West Africa.Currently, there is little or no empirical data on Anopheles mosquito vector population, dynamics, species composition, vectorial capacity, malaria prevalence and distribution in Nasarawa State to warrant assessment of the mosquito and malaria situation towards  prompt  and  effective  intervention  strategy.  Malaria  is  characterized  by  its biological diversity. This diversity is conditioned mostly by the vector species that are involved in transmission (including their distribution, behavior and vectorial capacity). It is also conditioned, among others, by seasonality of transmission, pathogenicity of parasites species and by immune response of human hosts.

Malaria is a dreaded disease which differs in its distribution and major characteristics from different countries to another in the tropics and even within the same countries (Phillips, 2001). Nigeria has the largest burden of malaria and lymphatic filariasis in Africa yet very little is known about the distribution of Anopheles mosquitoes that act as vectors for both diseases, how the species interact, overlap or differ across the country Awolola et al., (2002)

1.3       Justification for the Study

Vector control is a major component of the national campaign against malaria in Nigeria. The global strategic plan for Roll Back Malaria recommends that by 2010, 80% of the population at risk need to be protected using effective vector control measures. Anopheles gambiae complex is a group of six morphologically indistinguishable yet genetically and behaviorally distinct mosquito species that vary dramatically in their importance as vectors of malaria in Africa as many as three and possibly four species may be sympatric in some regions, and at least two occur in most malaria-endemic areas. Identification of Anopheles malaria vectors is essential for the identification of areas in Nasarawa State that are at risk of malaria and to also help in the formulation of strategies for effective malaria vector control. Therefore, there is a need for using the Polymerase Chain Reaction assay (PCR) for clear distinct identification of the Anopheline mosquito species as this will help in adopting a specific control measures instead of targeting the assumed vectors.

Identification of Anopheles malaria vector species is essential for recognizing   the eco- settings  in Nasarawa State that are at risk of malaria as this will help in  the formulation of strategies for effective malaria vector control. As not much is known of the species composition,  distribution,  and  abundance  of  Anopheles  and  Plasmodium  species  in Nasarawa State. It is also not known how Anopheles species breed and sustain themselves within the selected eco-settings and also within the wet and dry seasons. The present study attempts to collate information on mosquitoes in terms of species distribution, abundance and the prevalence of malaria in both dry and wet seasons across the three ecological zones of Nasarawa State. It is important to establish the species composition, distribution and abundance, vectorial capacity, ecological and behavioral differences across the selected eco-settings in Nasarawa State.

The understanding of the bionomics of Anopheles species responsible for malaria transmission, including correct and precise identification of the target species and its distribution will aid in deploying appropriate control measures. However, successful application of vector control measures in a given location requires the understanding of the bionomics of Anopheles species responsible for malaria transmission, including correct and precise identification of the target species and its distribution. When planning any vector control intervention, it is essential to assess the behavioural patterns of the local vector populations in order to select a suitable method for the vector control in that locality.The current study will identify Anopheles to species level so that control measures could target the specific malaria vectors instead of targeting the assumed vectors.

Therefore, monitoring of the vectors behaviour should be considered as integral component of any malaria control program. Therefore when planning any vector control intervention, it is essential to assess the behavioural patterns  of the  local vector populations in order to select a suitable method for the vector control in that locality.Because of the heterogeneity in behaviour, mosquitoes have different opportunities to escape from been killed or exit repellent actions of insecticides used in ITNs or IRS. For example many of the mosquitoe species shift to outdoor- or early biting, i.e. shift to zoophily or to exophily activities.Not much is known of the species composition, distribution, and abundance of Anopheles and Plasmodium species in Nasarawa State. It is also not known how Anopheles species breed and sustain themselves within the different ecological zones and also within the wet and dry seasons. Consequently, the present study attempts to collate information on mosquitoes in terms of species distribution, abundance and the prevalence of malaria in both dry and wet seasons across the three ecological zones of Nasarawa State. Consequently, it is important to establish the species composition, distribution and abundance, vectorial capacity, ecological and behavioral differences and also the types of breeding sites utilized by Anopheles species in Nasarawa State.However, successful application of vector control measures in a given location requires the understanding of the bionomics of Anopheles species responsible for malaria transmission, including correct and precise identification of the target species and its distribution.Therefore, when planning any vector control intervention, it is essential to assess the behavioural patterns of the  local vector populations in order to select a suitable method for the vector control in that locality.

In  Nigeria, malaria still remains a major health problem with about two-thirds of the population living in malaria endemic areas (WHO, 2015). As this has continue to thrive due to the complex nature and the vectorial system of the Anopheline vectors which are the principal  vectors  that  transmit  the malaria parasites  to  various  human  host  within  the endemic areas in the world especially in the sub-Saharan African continent more so the complex behaviour of the vectors has contributed in sustaining malaria transmission alongside  their  resistance  behaviour  to  various  classes  of  insecticides  as  there  is  no recorded information on the seasonal abundance of anopheline mosquitoes in  many regions within the, north central Nigeria. Therefore, this study was conducted to investigate the species composition and seasonal population dynamics and their possible association with rainfall and disease transmission prior to any implementation of a National malaria vector control.

1.4       Aim and Objectives of the Study

This  study  was  aimed  at  assessing  the  diversity  and  vectorial  system  of  anopheline mosquitoes (Diptera: Culicidae) in selected eco-settings of Nasarawa State, Nigeria.

The objectives of this study were to determine:

i.      the diversity and abundance of Anopheles mosquitoes in the selected eco – settings of Nasarawa state, Nigeria

ii.      the sibling composition of Anopheles gambiae s.l in the selected eco – settings of Nasarawa State, Nigeria

iii.      the human biting and feeding habits of An. gambiae s.l in the selected eco-settings of Nasarawa State Nigeria

iv.      the infection rate and Kdr resistance of the Anopheles mosquitoes in the selected eco-settings of Nasarawa State Nigeria.

v.         To assess the Entomological Inoculation rates of the Anopheles mosquitoes in the selected eco-settings of Nasarawa State, Nigeria.

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