Larval ecology of Anopheles coluzzii in Cape Coast, Ghana: water quality, nature of habitat and implication for larval control

Most African cities are undergoing rapid urbanization. Presently, about 53 % of Ghana’s entire population live in urban areas and this is projected to increase up to 70 % by 2050 [1]. This has rejuvenated interest in the challenges of urban malaria control in the country. Current malaria vector control measures include use of long lasting insecticidal nets and indoor residual spraying. However, these measures alone may be insufficient to achieve malaria elimination in Ghana and in many other endemic countries. A major limitation of the current control measures is the inability to cover the full spectrum of locations where mosquito exposure occurs. The existence of outdoor biting mosquitoes could prevent attainment of malaria elimination, even if it involves a small percentage of malaria vectors [2]. Additional malaria control measures are clearly required. Over the past decade there has been growing interest in larval control intervention to supplement existing malaria control strategies [3‐5]. However, effective implementation requires a good understanding of habitat ecology of Anopheles mosquitoes, which is limited, especially in many urban areas in Ghana.

Comprehensive data on habitat ecology of Anopheles gambiae in urban areas in Ghana dates back more than a century [6]. Since then, there have been few studies on habitat ecology of Anopheles species, which in most cases targets specific ecological or land use settings, such as urban agricultural areas [7, 8]. Indeed, urban agriculture is currently cited as a major breeding site for An. gambiae in many urban areas. In Kumasi (Ghana’s second largest city), for example, urban agriculture is reported to be responsible for the production of over 80 % of malaria mosquitoes in the city [7]. Breeding does take place in some urban areas without any important urban agriculture; however, information on Anopheles larval habitats is woefully inadequate in such urban areas. Clear ecological characteristics of Anopheles larval breeding requirements have not been identified for urban settings. Small, temporary sunny water bodies, relatively clean and mostly without overhanging vegetation have been recognized by several studies as preferred breeding habitats for An. gambiae [9]. Other studies have also reported the breeding of An. gambiae in large permanent and polluted water bodies [10, 11]. However, the term clean or polluted habitat is mostly based on visual examination and is not well defined. Quantifying water quality or pollution in Anopheles breeding habitats may give more insight into Anopheles breeding requirements, particularly in urban settings.

The main objective of the study was to determine Anopheles species composition in the city and characterize their breeding habitats, with particular emphasis on water quality in the breeding habitats. Since Culex larvae are known to colonize polluted habitats, water quality of the Anopheles breeding habitats was compared to that of habitats that were colonized by Culex larvae only. A larval survey was conducted for 15 months in different landscape and land use settings in Cape Coast. Anopheles coluzzii was found to be the dominant Anopheles species, breeding in organic polluted habitats. However, the level of organic pollution appears to be lower in An. coluzzii breeding habitats compared to habitats that were colonized by only Culex larvae. Almost all the habitats were anthropogenic in nature and it seems an improvement of basic hygiene and sanitation with regards to waste management in the city could prevent the formation of many of the Anopheles breeding habitats in Cape Coast.

Understanding the ecological drivers that are responsible for modulating the distribution and habitat segregation of Anopheles species is of paramount importance in malaria control. In the present study, An. coluzzii, An. gambiae and An. melas belonging to An. gambiae complex were found in Cape Coast but their abundance and distribution varied. Anopheles coluzzii dominated in almost all the breeding habitats and was found actively breeding in both rainy and dry seasons in diverse habitats. Habitats that were colonized by An. coluzzii during the rainy season (footprints, tyre tracks, rain pools) are consistent with the known preference of An. gambiae, particularly in rural areas [17]. However, salinity was relatively high in breeding habitats found in this study. In the dry season, An. coluzzii was mostly found cohabiting with Culex species in choke gutters and other organic polluted habitats, which was indicated by high levels of ammonia ions. This is not surprising because from both laboratory experiments [18] and field observations [6, 10, 11, 19], it is becoming clearer that An. coluzzii exhibit some degree of tolerance to high salinity and ammonia ions.

The high prevalence of An. coluzzii in this study is consistent with previous studies in the country. Previous studies in Ghana have shown An. gambiae and An. coluzzii sympatrically co-existing in most locations. However, An. gambiae predominate in the central part of the country whereas An. coluzzii and Anopheles arabiensis predominate in the northern and coastal savannah regions, with An. melas occurring mainly at the coastal areas [20, 21]. The result also conforms to the continental species distribution model that has been described by Tene-Fossog and colleagues [22], which predicted predominance of An. coluzzii along the coastline of west and central Africa. High level of salinity observed in the breeding habitats colonized by An. coluzzii may have contributed to its high prevalence in Cape Coast [22]. The only habitat that An. gambiae dominated was found at the peripheral part of the city, away from the core of the densely urbanized area and away from the coast.

The dominance of An. coluzzii in coastal areas of Ghana has been explained by the wide presence of permanent breeding conditions from irrigation facilities and ponds, resulting from river run-off [20, 21]. Similarly, along its geographical distribution, An. coluzzii is seen to predominate in areas characterized by larger, more temporally stable breeding sites, such as rice paddies and irrigation facilities [23‐25]. On the contrary, this study found An. coluzzii breeding in small ephemeral habitats similar to that described for An. gambiae. Additionally, An. coluzzii and Culex larvae co-existed in marginal habitats such as organic polluted habitats, particularly during the dry season. The absence of An. coluzzii in marginal habitats during the rainy season may suggest that it also has preference for temporary aquatic habitats. However, in the absence of preferred habitat, its ability to tolerate high ions such as ammonia and salinity, perhaps, makes it possible to breed in marginal habitats to maintain its population during unfavourable season.

Considering the diverse nature of APL habitats and different levels of water quality in breeding habitats, further insight could be gained from investigations of chronic exposure of An. coluzzii to organic pollution and its impact on life–history traits. Mireji and colleagues [26] showed that An. gambiae that developed tolerance to some heavy metals occurred at a significant biological cost to the mosquito, adversely affecting its ecological fitness. Similarly, intensive mortality was observed in the early instars of Culex tarsalis that bred in poor water quality habitats [27]. Surprisingly, C. quinquefasciatus, a common mosquito species in organic polluted waters, was absent in this study and it is consistent with a previous study in Cape Coast [28]. The reason for the absence of this cosmopolitan and widely distributed species is not presently clear.

Water quality in the breeding habitats seems to be affected by natural and human influences. On the one hand, the habitats were high in salinity, electrical conductivity and total dissolved solids, which may have been as a result of proximity to the sea, although anthropogenic factors cannot be ruled out. On the another hand, low dissolved oxygen, high ammonia ions and high concentration of thermotolerant bacterial coliforms in some APL habitats may have been caused by organic pollution resulting from high input of solid and liquid waste from households. Presence of faecal bacteria such as Escherichia coli, faecal streptococci and other coliforms also confirmed faecal contamination in the breeding habitats. Nevertheless, a lower level of total ammonia in APL habitats compared to habitats colonized by Culex larvae only and the absence of An. coluzzii in anoxic breeding habitats suggests that its tolerance to organic pollution is probably lower than Culex larvae. This is further supported by the distribution of An. coluzzii in space and time in marginal habitats, which appears to be influenced by some level of water quality, notably temperature and dissolved oxygen (Figs. 3, 4). Interestingly, similar levels of non-ionized ammonia (NH3) were found in APL habitats and habitats colonized only by Culex larvae, which could indicate that the toxic effect of ammonia might be similar in both species since non-ionized ammonia is the principal toxic form of ammonia to organisms.

The rapid urbanization being witnessed in many cities in Africa is associated with pollution and environmental modification. This can create or modify various mosquito larval habitats, which in turn can affect vector composition or distribution. Unlike Cameroon where the impact of urbanization on the prevalence of An. coluzzii has been extensively studied [11], there is no such detailed information available in Ghana and most West African countries. The two highly urbanized areas in the country, Accra (coastal savannah zone) and Kumasi (forest zone) are dominated by An. coluzzii and An. gambiae, respectively. From previous studies, ecological influence rather than urbanization appears to be of greater importance in the distribution of An. gambiae species in Ghana [20, 21, 29]. Ecological factors such as elevation, precipitation and temperature have been shown to be important variables driving the spatial distribution of each of the An. gambiae species [22]. A country-wide assessment of water quality and species distribution may give a clearer picture of the role of urbanization in modulating the distribution of An. gambiae species in Ghana. Presently, there is limited information of water quality levels in Anopheles breeding habitats in the country. For example, data on level of salinity, ammonia ions and other water quality indicators in Anopheles breeding habitats are virtually absent for the central to northern part of Ghana. The few existing data are mostly found for the coastal areas [30‐32].

Most of the APL habitats encountered in this study are consistent with reports from larval surveys conducted piecemeal in other urban areas in Ghana [6, 8, 30, 32] and several urban African countries [10, 11, 33]. Although habitat productivity, which was not assessed in this study, could differ from one habitat to other, it was more evident that the importance of habitats shifted from one habitat type to other with time since no habitat was continuously colonized for an entire season. It seems each type of breeding habitat, regardless of its level of productivity or importance, contributed to the production and maintenance of Anopheles species throughout the year. Most of the breeding habitats found in this study occurred as a result of haphazard and uncontrolled human activities. With the nature of breeding habitats in the study area, larval control intervention could greatly reduce Anopheles population in the city, particularly during the dry season. This may require constant monitoring of larval habitats and improvement of sanitation conditions in the city with regards to waste management. Ironically, there are in existence sanitation and by-laws in Ghana (Ghana Public health Act 851, 2012) that could prevent the formation of many of the Anopheles breeding habitats, however they are rarely enforced. Moreover, from the qualitative study with some of the private property owners, it appears they have inadequate knowledge of the immature stages of mosquitoes and their breeding habitats. Yet, community engagement is one of the most important aspects of mosquito management programmes. Therefore, the following: (1) proper waste management and maintenance of public roads; (2) strict enforcement of hygiene and sanitation by-laws; and, (3) community education on mosquito biology and their breeding places in the local environment could prevent formation of many mosquito breeding habitats, which could make larval control more feasible and cost effective in Cape Coast.

Anopheles coluzzii was found breeding in organic or faecal polluted habitats. Water in most of the breeding habitats either had high level of salinity or ammonia ions, which may be related to the proximity to the coast or urbanization, respectively. Furthermore, high concentration of bacterial fauna including several species of faecal coliforms confirms presence of organic pollution and faecal contamination in An. coluzzii breeding habitats. Organic pollution was lower in An. coluzzii breeding habitats than Culex only habitats. The nature of breeding habitats found in the city demonstrates the opportunistic behaviour of An. coluzzii and how its breeding requirements are so intimately intertwined with the haphazard and uncontrolled human activities in the urban area. Considering the nature of APL habitats, improving basic hygiene and sanitation in the city could make larval control intervention more practical and cost effective.