Abstract
The saltwater mosquito, Aedes vigilax, is prolific in coastal wetlands including mangroves and saltmarshes. Ae. vigilax is a vector for arboviruses such as Ross River and Barmah Forest viruses, with significant consequences for human health and economic productivity. In Australia the dominant form of mosquito control is chemicals. For mangroves, this is because there is a critical lack of knowledge supporting alternative approaches, such as environmental modification or biological control using larvivorous fish. This review examines the potential of fish as biological agents for the control of mosquito larvae in mangroves. We consider two key aspects: how larvivorous fish use mangroves; and can larvivorous fish reduce larval mosquito populations sufficiently to provide effective mosquito control? The link between fish and mangroves is reasonably well established, where mangroves act as refuge habitat for small and juvenile fish. Also, research has established that fish can be significant predators of mosquitoes, and therefore may be effective control agents. However, studies of fish activity within mangroves are limited to study of the fringe of the mangroves and not the internal structure of mangrove basins and as a result, fish populations within these areas remain unstudied. Also, until recently there was little appreciation of the mangrove-mosquito habitat relationship and, as a consequence, the importance of the mangrove basin as the key mosquito habitat has also been overlooked in the literature. Similarly, the predator/prey relationships between fish and mosquitoes within mangrove basin environments also remain unstudied, and therefore the importance of fish for mosquito management in mangrove basins is not known. There are substantial knowledge gaps regarding the potential of fish in controlling larval mosquitoes in mangroves. The gaps include: understanding of how larvivorous fish use mangrove basins; the nature of the fish-mosquito predator/prey relationship in mangrove basins; and whether larvivorous fish are effective as a mosquito control option in mangroves.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Coastal wetlands including mangroves and saltmarshes are habitats of the saltwater mosquito, Aedes vigilax, where it is prolific. Ae. vigilax is a vector for arboviruses such as Ross River Virus (RRV) and Barmah Forest Virus (BFV) (Kay and Jorgensen 1986). RRV and BFV are polyarthritic diseases (Flexman et al. 1998) that have significant health and economic impacts, costing AUD 3-6 million in health care and lost productivity annually (Woodruff et al. 2006).
Reducing the threat of mosquito borne disease involves reducing the potential for contact between mosquitoes and humans. This is especially important in areas where the mosquito’s mangrove habitats lie near human populations. Most Australians live in coastal areas and in Queensland many low lying coastal regions are adjacent to mangroves that harbour significant mosquito breeding sites. As a result, Queensland has rates of RRV and BFV infection that are some of the highest in the country, accounting for between a third and three quarters of all RRV cases (Russell 2002) and around half of all BFV cases (Naish et al. 2011).
In order to reduce the exposure of humans to mosquito borne disease, the disease vector (mosquito) needs to be controlled. There are three broad categories of mosquito control: using chemical agents (chemical control); altering the structure and/or hydrology of mosquito habitat (physical control or source reduction); and increasing the presence of predators, pathogens and competitors of mosquitoes (biological control) (Dale and Hulsman 1990). In Australia, the dominant form of mosquito control is to use chemicals as part of an integrated mosquito control program that considers a range of approaches. An integrated program has been shown to be more effective than programs that rely on a single approach (Tomerini et al. 2011). For example, successful integrated programs for mosquito control in saltmarshes are well established, and include a range of approaches including chemical and physical methods, such as runnelling in saltmarshes (Hulsman et al. 1989; Dale 2008). However, for mangrove systems there remains a critical lack of knowledge limiting the development of integrated approaches. For example, approaches such as environmental modification and biological control using larvivorous fish need to consider the essential ecological role and ecosystem services provided by mangroves (as identified by Badola and Hussain 2005; Mitsch and Gosselink 2000; Nagelkerken et al. 2008). Research into the mosquito-mangrove habitat has received recent attention (Knight 2011; Knight et al. 2012), that has led to new studies looking at environmentally focused minimal impact mosquito control methods where habitat modification involves restoring tidal processes. A complimentary consequence of restoring tidal processes is enhanced access for fish as predators, but for optimal integrated mosquito control (including chemical, physical and biological approaches) in mangroves, much remains to be done.
This paper reviews the literature on mosquito-fish-mangrove relationships and how these relate to mosquito control. Specific aspects include: fish as a control mechanism for mosquitoes; mangroves as a fish habitat; fish as predators of mosquitoes; and how mosquitoes respond to fish predation. The purpose of the review is to identify gaps in knowledge that currently limits the adoption of larvivorous fish as a mosquito control agent.
Fish as a biological control of larval mosquitoes
Fish that are predators of the aquatic larval stage of mosquitoes are referred to as larvivorous fish. Many other organisms are predators of mosquito larvae including tadpoles, insect larvae (Kumar and Hwang 2006), amphibians (Brodman and Dorton 2006) and even other mosquito larvae (Kerridge 1971); however, fish are the most common and widely studied type of predator used for biological control of mosquitoes. Predation of mosquitoes has been recorded in many habitats, from small plastic containers (Connor 1922) to complex natural ecosystems including coastal wetland environments (Harrington and Harrington 1961, 1982; Hess and Tarzwell 1942; Morton et al. 1988). As a biological control agent larvivorous fish have been demonstrated to be very effective at reducing mosquito larval populations in many parts of the world, in a variety of habitats (Chandra et al. 2008; Kumar and Hwang 2006; Van Dam and Walton 2007).
Environmental hazards: use of exotic fish species to control mosquitoes
Despite its potential, biological control using fish can be environmentally damaging, especially in complex, ecologically important, systems like mangroves. Releasing exotic predatory fish into a wetland to control mosquitoes may disrupt natural ecosystems, with the fish outcompeting native predators and feeding on nontarget organisms (Bence 1988; Hoddle 2004). Notable examples were the introduction of the mosquitofish (Gambusia affinis and Gambusia holbrooki), two species native to North America, which have been introduced into waterways worldwide (Angelon and Petranka 2002; Chandra et al. 2008; Kumar and Hwang 2006; Morton et al. 1988). Significant declines in populations of native fish species have been observed worldwide following the introduction of these mosquitofish (Arthington and Marshall 1999; Kumar and Hwang 2006; Laha and Mattingly 2007), resulting in their designation as significant exotic pests and their use as a control agent being banned in Australia.
Environmentally sound biological control using fish
The mosquitofish experience illustrates the risk of introducing exotic species; however, biological control does have potential to be an effective, environmentally sound form of mosquito control, by using fish that are compatible with the environment. These fish may also be just as, or even more effective at controlling mosquitoes than hazardous species like Gambusia affinis and hoolbrooki. Van Dam and Walton (2007), experimenting in ponds in California, found that relatively small, slow breeding populations of Gila orcutti reduced mosquito numbers as effectively as large, fast breeding Gambusia affinis populations, with far less predation of nontarget invertebrates. In laboratory tests Hurst et al. (2004) compared predation of Culex mosquitoes by seven native Australian fish species and Gambusia holbrooki, and found that three of these species, Melanotaenia duboulayi, Ambassis marianus and Hypseleotris compressa, were equally or more effective predators of Culex mosquito larvae than Gambusia holbrooki.
Improving the conditions for native larvivorous fish that already live in the mangrove forest and enhancing their access to mosquito larvae is a far more environmentally sound approach than introducing an exotic predator. This may be accomplished by improving tidal processes within the mangrove basin, allowing fish access to isolated larval pools. In order to do this, several aspects of the fish-mosquito-mangrove interaction need to be understood: Firstly, how fish use the mangrove habitat, and how environmental factors such as structure, water quality and hydrology influence fish populations within mangroves; secondly, the predator/prey relationship between native fish and mosquitoes, in particular whether the endemic fish eat mosquito larvae; and thirdly, whether this predation is substantial enough to be a viable mosquito control option.
Mangroves as fish habitat
Mangroves are no doubt an important habitat for fish (Laegdsgaard and Johnson 1995; Vidy et al. 2004; Wang et al. 2009), for both permanent (Faunce and Serafy 2006; Nagelkerken et al. 2000) and transient species (Sheridan and Hays 2003). The importance of mangroves for fish has been assessed indirectly, by examining the densities and species richness of fish in habitats adjacent to mangroves, such as mangrove-lined estuaries (Aburto-Oropeza et al. 2008; Hajisamae and Chou 2003; Laegdsgaard and Johnson 2001; Nagelkerken et al. 2001) and tidal creeks adjacent to mangrove stands (Bell et al. 1984; Beumer 1978; Robertson and Duke 1987). A common finding has been that the presence of mangroves created stronger, more robust fish populations in adjacent waters than in waters not adjacent to mangroves.
Mangroves as refuge habitat for fish
In order to understand the importance of mangroves for fish, fish populations need to be studied directly, by sampling fish entering or leaving mangroves, and those residing within the mangrove forest itself (Hindell and Jenkins 2004; Laroche et al. 1997; Morton 1990; Nagelkerken et al. 2000; Robertson and Duke 1990). Studies focusing on these fish populations have recognised the key role mangrove forests play as a refuge habitat for small fish and juveniles, providing a predator-free environment. Tree shading, turbid water and structurally complex forest substrates (due to roots and pneumatophores) provide protection from predators (Abrahams and Kattenfeld 1997; Blaber and Blaber 1980; Cyrus and Blaber 1992; Faunce et al. 2004; Johnston et al. 2007; de la Moriniere et al. 2004; Nagelkerken et al. 2008; Nagelkerken and Faunce 2008; Payne and Gillanders 2009; Robertson and Duke 1987; Thollot et al. 1999; Tse et al. 2008). Mangroves also support a base for food webs, providing a surface on which algae can grow (Aikanathan and Sasekumar 1994; Hyde 1990; Nagelkerken and Faunce 2008; Potts 1980; Proches 2004; Proches and Marshall 2002; Proches et al. 2001; Verweij et al. 2006).
Water quality and distribution of fish in mangroves
Water quality is factor critical for the health of the whole ecosystem, in particular fish communities. Factors such as salinity, pH, temperature and dissolved oxygen (DO) can significantly affect fish growth, metabolism and behaviour (Augley et al. 2008; Brandt et al. 2009; Buentello et al. 2000; Frick and Wright 2002; Howells et al. 1983; Leung et al. 1999; Teien et al. 2004), where extremes can lead to fish mortality with potential for rapid changes in the fish community structure and distribution (Dunson and Dunson 1999; Faunce et al. 2004; Lorenz 1999; Sheaves and Johnston 2008; Weatherley 1972). For example, Dunson and Dunson (1999) examined the effects of low DO on Rivulus marmoratus in mangrove pools. Fish held in hypoxic conditions (at the bottom of pools or in isolated pools with low DO) experienced stunted growth rates and higher mortality rates.
Hydrologic factors
Other environmental factors, such as evaporation (Molles 2005), terrestrial runoff (Easton 1989) and tides (Sheaves and Johnston 2008) can cause water levels and water quality to fluctuate over a wide range. Terrestrial runoff and tides can create hydrologic connections within mangroves (Knight et al. 2008) that enable fish to travel within mangroves and between mangroves and associated coastal waters (Ritchie and Montague 1995). Studies investigating hydrologic mechanisms within mangroves have been focussed on physical processes such as interaction of vegetation and water flow physics (Mazda et al. 1997) and the nature of tidal hydrodynamics into and within mangrove swamps (Mazda et al. 2005; Wolanski 1992). The Manual for the Preservation and Utilization of Mangrove Ecosystems by Mazda et al. (2007) brings together a significant number of mangrove physical process related studies. However, only a few studies have looked at the mosquito–mangrove–hydrology relationship. Ritchie (1990) for Florida mangroves, and most recently Knight (2011) for eastern Australian mangroves, detailed the interaction between tidal hydrodynamics and topographic structure required to create the mosquito’s mangrove habitat. Tidal flow and topography in mangrove systems have been identified as critical factors that create a highly variable environment.
In habitats similar to mangroves, fish populations have been shown to be dramatically affected by variations in tidal flushing. For example, Sheaves and Johnston (2008) examined tidal and freshwater flooding in a sub-tropical Queensland estuary floodplain and found that variations in flooding frequency influenced the distribution of fish in isolated pools. More frequently flushed pools had higher connectivity to the estuary, better water quality, more fish immigration and thus a larger fish population.
Limitations in knowledge of fish mangrove habitats
Despite all the evidence presented above, fish populations within mangroves remain poorly understood. Why there are so few studies of fish related processes within mangroves, including fish ecology studies, is unclear, but it may be largely due to lack of attention paid to internal basin areas as fish habitat. Almost all studies of the fish-mangrove ecosystem have focussed either on environments adjacent to mangroves, or on the mangrove fringe. There is significant heterogeneity in connectivity and water flows within mangroves, and hydrologic processes can vary greatly between the fringe and internal basin areas (Knight et al. 2008). Studies cutting trenches into the mangrove and examining movement of fish across the mangrove fringe strongly indicate that significant fish populations do exist within mangroves, but these remain largely unstudied (Huxham et al. 2008; Vance et al. 1996).
The main reason why fish have not been studied in internal areas of mangroves may be the difficulties of sampling in mangrove basins. Morton (1990) and Hindell and Jenkins (2004) argued that mangrove basins, with their mosaic of open pools and dense pneumatophore stands, were impossible to study using conventional netting techniques (such as cast or drag nets), and therefore kept to the mangrove fringe. Whatever the reason, as a result of this, the effects of physical, water quality and tidal factors on fish populations in mangrove basins are not understood.
Fish as predators of mosquitoes
While it is likely that fish populations do exist within mangrove basins where mosquitoes breed, evidence that these fish predate upon mosquitoes is required if these fish are to be considered as potential biological control agents. Predation by fish on mosquitoes has been observed across a variety of habitats, including freshwater and coastal wetland systems, where a number of factors influence predation efficiency. Many coastal wetland species have been observed feeding on larvae, either in wetlands, other habitats or in laboratory studies, including Psuedomugil signifier and Gobidiiae sp (Morton et al. 1988; Hurst et al. 2004, 2006) in Australia and Rivulus marmoratus (Taylor et al. 1992) and Gambusia affinis (Hess and Tarzwell 1942; Harrington and Harrington 1961) in the USA.
Ecological factors
Ecological factors such as habitat structural complexity and prey preference by predators affects predation of mosquitoes. Structural complexity affects the physical access of predators to prey, where larval habitats easily accessible to predatory fish result in higher predation of mosquitoes (Hess and Tarzwell 1942).
The developmental stage of both predator and prey is another important factor influencing the predator–prey relationship. Younger (smaller) individuals of a species eat the earlier instar mosquito larvae, whereas older (larger) individuals feed primarily on older instars and pupae (Harrington and Harrington 1961; Taylor et al. 1992). Harrington and Harrington (1961) examined this occurrence in detail, looking at Aedes taeniorhynchus (Wiedemann) predation by a number of larvivorous fish in salt marshes in Florida. There was a strong correlation between the size of the fish and the stage of development of the larval prey; smaller fish mainly ate 1st–3rd instar larvae and larger fish ate 4th instar larvae. This has also been demonstrated in more recent studies, for example Taylor et al. (1992), found that the developmental stage of larvae of Ae. taeniorhynchus and Culex quinquefasciatus larvae consumed was directly proportional to the size of Rivulus marmoratus individuals.
Behavioural factors
Behavioural factors are also important for determining predation efficiency of mosquitoes—in particular, feeding habits of predators is important. Due to the episodic and seasonal nature of mosquito production, populations are often low (or virtually non-existent) in winter months and periodically very high in summer months. Ergo, fish that predate upon mosquitoes need to be able to shift their diet to other prey items when mosquitoes are scarce (Morton et al. 1988). Therefore, the presence of generalist fish species is important for mosquito control, as generalists are more likely to be opportunistic predators of mosquito larvae (Harrington and Harrington 1961; Laufer et al. 2009; Murdoch 1969; Pen and Potter 1991; Schleuter and Eckmann 2008). Morton et al. (1988), examining the feeding habits of salt marsh fish species, found that species that preyed upon Ae. vigilax mosquito larvae in peak mosquito seasons (G. affinis, P. signifier and Gobiidae sp) were able to radically shift their diet during non-peak seasons, substituting crustacean larvae for mosquito larvae in winter.
The preference of alternate prey, and their abundance, also affects predation on mosquito larvae, where fish seek out larger or less agile prey to consume (Bence 1988; Knight et al. 2004; Manna et al. 2008). Preference for alternative available prey can reduce the effectiveness of fish as a biological control, and can even benefit mosquitoes because of reduced competition by competitors (Blaustein 1992; Chesson 1989; Manna et al. 2008; Walton 2007). For example, Manna et al. (2008) concluded that Poecilia reticulata was an effective predator of Culex quinquefasciatus larvae, however its effectiveness was severely reduced in the presence of alternate prey (worms and chironomid larvae).
While predation has been documented in many habitats, and the above factors are known, the predator/prey relationship between larvivorous fish and mosquitoes has not been directly examined in the context of the fish-mosquito-mangrove ecosystem. While it is clear that larvivorous fish do predate on mosquitoes, there has been no research specifically examining this form of predation within mangroves. In addition, further research is required to determine if larvivorous fish predation on mosquitoes is sufficient to reduce mosquito populations in mangrove systems, and therefore be eligible as a control strategy.
Mosquito responses to predation by fish
The effects of predation may be seen by focusing on the prey species, rather than focusing on the activities of the fish as predators. Mosquitoes respond to predation in two main ways: at a population level and at an individual behavioural level. Understanding the mosquito response is critical for modelling the effects of predation on mosquito populations.
Mosquito population responses
Many studies have examined mosquito populations following the introduction of predatory fish, and have documented significant reductions in the size of the mosquito population when fish are introduced into a system (Bence 1988; Chandra et al. 2008; Kumar and Hwang 2006; Van Dam and Walton 2007; Walton 2007). However, most studies were conducted in smaller and far less complex habitats than mangroves, such as containers and freshwater ponds, and therefore may not be comparable to mangrove fish-mosquito interactions.
Two studies identified fish predation as the driver of changes in mosquito populations in mangroves (Ritchie 1984 and Kokkinn et al. 2009). Ritchie (1984) documented unusually low adult populations of Ae. taeniorhynchus in Florida mangroves, which were attributed to heavy winter rainfall sustaining large larvivorous fish populations within the mangroves. However, rather than observing predation this study relied on changes in the adult mosquito population as evidence of increased predation by fish, which has to be done with caution, considering the wide dispersal of adult mosquitoes (Chapman et al. 1999). Kokkinn et al. (2009) made qualitative observations of larvivorous fish preying on, and effectively controlling, mosquito populations in coastal pools (including in mangroves). Most predation occurred as the pool connected with the flood-tide with some fish retiring with the ebb and others remaining in the isolated pools, potentially perishing.
Behavioural responses: evolved predator avoidance traits
Evidence of the effects of predation by fish can also be observed by examining evolved responses to the presence of fish. Mosquitoes are able to detect chemical cues in the environment (Davis 1976), which may include detecting the presence of fish in adjacent waterbodies, and therefore avoiding laying eggs in areas where hatching larvae would be at risk of predation. This trait was first identified by Petranka and Fakhoury (1991), who observed a decline in Anopheles oviposition in ponds containing caged-off predatory fish and tadpoles. Since then many other studies have found similar results (Chivers and Smith 1998; Kats and Dill 1998; Kumar and Hwang 2006; Pamplona et al. 2009). The evolution of this behaviour suggests that predation is an important ecological process affecting mosquito populations. However, this is not a trait shared by all mosquitoes. The ability to sense predators varies considerably between species (Louca et al. 2009; Van Dam and Walton 2007), ranging from being completely unable to sense predators (Zuharah and Lester 2010) to being so sensitive that they can detect residual chemicals in the water long after predators have left the waterbody (Angelon and Petranka 2002).
Chemo-avoidance has been demonstrated for coastal wetland mosquito species. For example, Ritchie and Laidlaw-Bell (1994) found that there was significantly less oviposition by Ae. taeniorhynchus on the margins of salt marsh pools containing fish compared to those without, providing evidence that the mosquito is able to sense predators. The study was very significant as it demonstrated chemo-avoidance in a species that lays its eggs on soil, rather than on the water’s surface (most other studies focus on Anopheles and Culex species). Despite the promise this study shows, it conducted in salt marshes, not mangroves, and therefore chemo-avoidance in ovipositing on substrate adjacent to mangrove pools remains to be demonstrated.
Modelling mosquito populations in mangroves
Another way to assess the role of fish as a predator of mosquitoes in mangroves is by examining existing mosquito population models. If fish are an important predator of mosquitoes, the role of predation should be identified in both mosquito population models and models of mangrove ecology. This was seen in a model of Ae. taeniorhynchus populations in Florida mangrove forests (Ritchie and Montague 1995). Using knowledge of feeding habits of fish documented in Australian and American studies, Ritchie and Montague estimated that a predatory fish introduced into a mangrove pool would consume approximately 500 mosquito larvae per week. The capacity for such high rates of predation per fish, combined with oviposition deterrence, has potential for very significant control of the mosquito population, even in very small numbers.
Actual patterns of mosquito distribution within mangrove basins appear to reflect this; areas of higher hydrological connectivity (caused by more frequent tidal flow) have larger fish populations (Hess and Tarzwell 1942; Sheaves and Johnston 2008) and smaller mosquito populations than those less tidally connected (Griffin et al. 2010; Knight et al. 2009) suggesting predation by fish reduces mosquito populations. A limitation of this type of approach is that the model can appear conclusive or complete when neither may be the case. There may be more than one cause of an observed population shift. For example, although predation may be modeled as a cause of population decline (as above), the decline may equally be due to changes in the hydrology that disrupt the mosquito life cycle.
Summary and conclusions
This review has examined the literature surrounding fish in mangroves, and the potential for larvivorous fish to control mosquitoes as an effective biological control approach. Mangrove forests are important habitats for fish, providing an important refuge habitat. However, water quality and tidal hydrology influence fish habitat patterns. There is evidence that fish are significant predators of mosquitoes in mangroves, and thus fish are potential biological control agents for mosquito management.
However, several knowledge gaps were identified that limit our understanding of how fish use mangroves and the predator/prey relationship between fish and mosquitoes. Knowledge of how fish are distributed across the mangrove basin is limited. Mangrove forests can be highly variable environments, both structurally and hydrologically, however as almost all studies of fish relating to mangroves are limited to the mangrove fringe rather than mangrove basin, how this variation affects the size and distribution of fish populations is unknown. As a result, while fish are known predators of mosquitoes, the lack of knowledge of endemic fish populations within mangrove basins means the extent to which fish predation affects mosquito populations is not known.
Enhancing larvivorous fish populations in mangroves has potential as an effective and environmentally acceptable mosquito control approach. Integrating biological control using larvivorous fish into a mosquito control program should improve mosquito control effectiveness. There are three main benefits of integrating biological control into a mosquito control program: reduced mosquito production in mangroves, lowered cost of existing control approaches and a reduction in the risk of mosquito borne disease for people living in coastal regions.
References
Abrahams M, Kattenfeld M (1997) The role of turbidity as a constraint on predator–prey interactions in aquatic environments. Behav Ecol Sociobiol 40(3):169–174
Aburto-Oropeza O, Ezcurra E, Danemann G, Valdez V, Murray J, Sala E (2008) Mangroves in the Gulf of California increase fishery yields. Proc Natl Acad Sci USA 105(30):10456–10459
Aikanathan S, Sasekumar A (1994) The community structure of macroalgae in a low shore mangrove forest in Selangor, Malaysia. Hydrobiologia 285(1–3):131–137
Angelon KA, Petranka JW (2002) Chemicals of predatory mosquitofish (Gambusia affinis) influence selection of oviposition site by Culex mosquitoes. J Chem Ecol 28(4):797–806
Arthington AH, Marshall CJ (1999) Diet of the exotic mosquitofish, Gambusia holbrooki, in an Australian lake and potential for competition with indigenous fish species. Asian Fish Sci 12(1):1–16
Augley J, Huxham M, Fernandes TF, Lyndon AR (2008) The effect of salinity on growth and weight loss of juvenile plaice (Pleuronectes platessa, L.): an experimental test. J Sea Res 60(4):250–254
Badola R, Hussain SA (2005) Valuing ecosystem functions: an empirical study on the storm protection function of Bhitarkanika mangrove ecosystem, India. Environ Conserv 32(1):85–92
Bell JD, Pollard DA, Burchmore JJ, Pease BC, Middleton MJ (1984) Structure of a fish community in a temperate tidal mangrove creek in Botany Bay, New-South-Wales. Aust J Mar Freshw Res 35(1):33–46
Bence JR (1988) Indirect effects and biological control of mosquitoes by mosquitofish. J Appl Ecol 25(2):505–521
Beumer JP (1978) Feeding ecology of four fished from a mangrove creek in north Queensland, Australia. J Fish Biol 12(5):475–490
Blaber SJM, Blaber TG (1980) Factors affecting the distribution of juvenile estuarine and inshore fish. J Fish Biol 17(2):143–162
Blaustein L (1992) Larvivorous fishes fail to control mosquitoes in experimental rice plots. Hydrobiologia 232(3):219–232
Brandt SB, Gerken M, Hartman KJ, Demers E (2009) Effects of hypoxia on food consumption and growth of juvenile striped bass (Morone saxatilis). J Exp Mar Biol Ecol 381:S143–S149
Brodman R, Dorton R (2006) The effectiveness of pond-breeding salamanders as agents of larval mosquito control. J Freshw Ecol 21(3):467–474
Buentello JA, Gatlin DM, Neill WH (2000) Effects of water temperature and dissolved oxygen on daily feed consumption, feed utilization and growth of channel catfish (Ictalurus punctatus). Aquaculture 182(3–4):339–352
Chandra G, Bhattacharjee I, Chatterjee SN, Ghosh A (2008) Mosquito control by larvivorous fish. Indian J Med Res 127(1):13–27
Chapman HF, Hughes JM, Jennings C, Kay BH, Ritchie SA (1999) Population structure and dispersal of the saltmarsh mosquito Aedes vigilax in Queensland, Australia. Med Vet Entomol 13(4):423–430
Chesson J (1989) The effect of alternative prey on the functional response of Notonecta hoffmani. Ecology 70(5):1227–1235
Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5(3):338–352
Connor ME (1922) Notes on the use of fresh water fish as consumers of mosquito larvae in containers used in the home. Am J Public Health 12(3):193–194
Cyrus DP, Blaber SJM (1992) Turbidity and salinity in a tropical northern Australian estuary and their influence on fish distribution. Estuar Coast Shelf Sci 35(6):545–563
Dale PER (2008) Assessing impacts of habitat modification on a subtropical salt marsh: 20 years of monitoring. Wetl Ecol Manag 16:77–87
Dale PER, Hulsman K (1990) A critical review of salt marsh management methods for mosquito control. Rev Aquat Sci 3(2–3):281–311
Davis EE (1976) Receptor sensitive to oviposition site attractants on antennae of mosquito, Aedes aegypti. J Insect Physiol 22(10):1371–1376
de la Moriniere EC, Nagelkerken I, van der Meij H, van der Velde G (2004) What attracts juvenile coral reef fish to mangroves: habitat complexity or shade? Mar Biol 144(1):139–145
Dunson WA, Dunson DB (1999) Factors influencing growth and survival of the killifish, Rivulus marmoratus, held inside enclosures in mangrove swamps. Copeia 3:661–668
Easton C (1989) The trouble with the Tweed. Fish World 3:58–59
Faunce CH, Serafy JE (2006) Mangroves as fish habitat: 50 years of field studies. Mar Ecol Prog Ser 318:1–18
Faunce CH, Serafy JE, Lorenz JJ (2004) Density-habitat relationships of mangrove creek fishes within the southeastern saline Everglades (USA), with reference to managed freshwater releases. Wetl Ecol Manag 12:377–394
Flexman JP, Smith DW, Mackenzie JS, Fraser JRE, Bass P, Hueston L, Michael DA (1998) A comparison of the diseases caused by Ross River virus and Barmah Forest virus. Med J Aust 169(3):159–163
Frick NT, Wright PA (2002) Nitrogen metabolism and excretion in the mangrove killifish Rivulus marmoratus—I. The influence of environmental salinity and external ammonia. J Exp Biol 205(1):79–89
Griffin LF, Knight JM, Dale PER (2010) Identifying mosquito habitat microtopography in an Australian mangrove forest using LiDAR derived elevation data. Wetlands 30(5):929–937
Hajisamae S, Chou LM (2003) Do shallow water habitats of an impacted coastal strait serve as nursery grounds for fish? Estuar Coast Shelf Sci 56:281–290
Harrington RW Jr, Harrington ES (1961) Food selection among fishes invading a high subtropical salt marsh: from onset of flooding through the progress of a mosquito brood. Ecology 42(4):646–666
Harrington RW, Harrington ES (1982) Effects on fishes and their forage organisms of impounding a Florida salt marsh to prevent breeding by salt marsh mosquitos. Bull Mar Sci 32(2):523–531
Hess AD, Tarzwell CM (1942) The feeding habits of Gambusia affinis affinis, with special reference to the malaria mosquito, Anopheles quadrimaculatus. Am J Hyg 35(1):142–151
Hindell JS, Jenkins GP (2004) Spatial and temporal variability in the assemblage structure of fishes associated with mangroves (Avicennia marina) and intertidal mudflats in temperate Australian embayments. Mar Biol 144(2):385–395
Hoddle MS (2004) Restoring balance: using exotic species to control invasive exotic species. Conserv Biol 18(1):38–49
Howells GD, Brown DJA, Sadler K (1983) Effects if acidity, calcium and aluminium on fish survival and productivity—a review. J Sci Food Agric 34(6):559–570
Hulsman K, Dale PER, Kay BH (1989) The Runneling method of habitat modification—an environment-focused tool for salt-marsh mosquito management. J Am Mosq Contr Assoc 5:226–234
Hurst TP, Brown MD, Kay BH (2004) Laboratory evaluation of the predation efficacy of native Australian fish on Culex annulirostris (Diptera:Culicidae). J Am Mosq Control Assoc 20(3):286–291
Huxham M, Kimani E, Augley J (2008) The fish community of an East African mangrove: effects of turbidity and distance from the sea. West Indian Ocean J Mar Sci 7(1):57–67
Hyde KD (1990) A study of the vertical zonation of intertidal fungi on Rhizophora apiculata at Kampong Kapok mangrove, Brunei. Aquat Bot 36(3):255–262
Johnston R, Sheaves M, Molony B (2007) Are distributions of fishes in tropical estuaries influenced by turbidity over small spatial scales? J Fish Biol 71(3):657–671
Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5(3):361–394
Kay BH, Jorgensen WK (1986) Eggs of Aedes vigilax (Skuse) and their distribution on plants and soil in South East Queensland salt marsh. J Aust Entomol Soc 25:267–272
Kerridge P (1971) Aspects of the ecology and biology of the salt-marsh mosquito Aedes vigilax (Skuse). Dissertation, University of Queensland
Knight JM (2011) A model of mosquito–mangrove basin ecosystems with implications for management. Ecosystems 14(8):1382–1395
Knight TM, Chase JM, Goss CW, Knight JJ (2004) Effects of interspecific competition, predation, and their interaction on survival and development time of immature Anopheles quadrimaculatus. J Vector Ecol 29(2):277–284
Knight JM, Dale PER, Dunn RJK, Broadbent GJ, Lemckert CJ (2008) Patterns of tidal flooding within a mangrove forest: Coombabah Lake, Southeast Queensland, Australia. Estuar Coast Shelf Sci 76(3):580–593
Knight JM, Dale PER, Spencer J, Griffin L (2009) Exploring LiDAR data for mapping the micro-topography and tidal hydro-dynamics of mangrove systems: an example from southeast Queensland, Australia. Estuar Coast Shelf Sci 85(4):593–600
Knight J, Griffin L, Dale P, Phinn S (2012) Oviposition and larval habitat preferences of the saltwater mosquito, Aedes vigilax, in a subtropical mangrove forest in Queensland, Australia. J Insect Sci 12(6)
Kokkinn MJ, Duval DJ, Williams CR (2009) Modelling the ecology of the coastal mosquitoes Aedes vigilax and Aedes camptorhynchus at Port Pirie, South Australia. Med Vet Entomol 23(1):85–91
Kumar R, Hwang JS (2006) Larvicidal efficiency of aquatic predators: a perspective for mosquito biocontrol. Zool Stud 45(4):447–466
Laegdsgaard P, Johnson CR (1995) Mangrove habitats as nurseries—unique assemblages of juvenile fish in subtropical mangroves in Eastern Australia. Mar Ecol Prog Ser 126(1–3):67–81
Laegdsgaard P, Johnson C (2001) Why do juvenile fish utilise mangrove habitats? J Exp Mar Biol Ecol 257(2):229–253
Laha M, Mattingly HT (2007) Ex situ evaluation of impacts of invasive mosquitofish on the imperiled Barrens topminnow. Environ Biol Fishes 78(1):1–11
Laroche J, Baran E, Rasoanandrasana NB (1997) Temporal patterns in a fish assemblage of a semiarid mangrove zone in Madagascar. J Fish Biol 51(1):3–20
Laufer G, Arim M, Loureiro M, Pineiro-Guerra JM, Clavijo-Baquet S, Fagundez C (2009) Diet of four annual killifishes: an intra and interspecific comparison. Neotrop Ichthyol 7(1):77–86
Leung KMY, Chu JCW, Wu RSS (1999) Effects of body weight, water temperature and ration size on ammonia excretion by the areolated grouper (Epinephelus areolatus) and mangrove snapper (Lutjanus argentimaculatus). Aquaculture 170(3–4):215–227
Lorenz JJ (1999) The response of fishes to physicochemical changes in the mangroves of northeast Florida Bay. Estuaries 22(2B):500–517
Louca V, Lucas MC, Green C, Majambere S, Fillinger U, Lindsay SW (2009) Role of fish as predators of mosquito larvae on the floodplain of the Gambia River. J Med Entomol 46(3):546–556
Manna B, Aditya G, Banerjee S (2008) Vulnerability of the mosquito larvae to the guppies (Poecilia reticulata) in the presence of alternative preys. J Vector Borne Dis 45(3):200–206
Mazda Y, Wolanski E, King B, Sase A, Ohtsuka O, Magi M (1997) Drag force due to vegetation in mangrove swamps. Mangroves Salt Marshes 1:193–199
Mazda Y, Kobashi D, Okada S (2005) Tidal-scale hydrodynamics within mangrove swamps. Wetl Ecol Manag 13(6):647–655
Mazda Y, Wolanski E, Ridd PV (2007) The Role of physical processes in mangrove environments: manual for the preservation and utilization of mangrove ecosystems. Terrapub, Tokyo
Mitsch W, Gosselink J (2000) Wetlands. Wiley, New York
Molles MC (2005) Ecology: concepts and applications, 3rd edn. McGraw-Hill, Boston
Morton RM (1990) Community structure, density and standing crop of fishes in a subtropical Australian mangrove area. Mar Biol 105(3):385–394
Morton RM, Beumer JP, Pollock BR (1988) Fishes of a subtropical Australian saltmarsh and their predation upon mosquitoes. Environ Biol Fishes 21(3):185–194
Murdoch WW (1969) Switching in general predators. Experiments on predator specificity and stability of prey populations. Ecol Monogr 39(4):335–337
Nagelkerken I, Faunce CH (2008) What makes mangroves attractive to fish? Use of artificial units to test the influence of water depth, cross-shelf location, and presence of root structure. Estuar Coast Shelf Sci 79(3):559–565
Nagelkerken I, Dorenbosch M, Verberk W, de la Moriniere EC, van der Velde G (2000) Importance of shallow-water biotopes of a Caribbean bay for juvenile coral reef fishes: patterns in biotope association, community structure and spatial distribution. Mar Ecol Prog Ser 202:175–192
Nagelkerken I, Kleijnen S, Klop T, van den Brand R, de la Moriniere EC, van der Velde G (2001) Dependence of Caribbean reef fishes on mangroves and seagrass beds as nursery habitats: a comparison of fish faunas between bays with and without mangroves/seagrass beds. Mar Ecol Prog Ser 214:225–235
Nagelkerken I, Blaber SJM, Bouillon S, Green P, Haywood M, Kirton LG, Meynecke JO, Pawlik J, Penrose HM, Sasekumar A, Somerfield PJ (2008) The habitat function of mangroves for terrestrial and marine fauna: a review. Aquat Bot 89(2):155–185
Naish S, Hu W, Mengersen K, Tong S (2011) Spatial and temporal clusters of Barmah Forest virus disease in Queensland, Australia. Trop Med Int Health 16(7):884–893
Pamplona LDC, Alencar CH, Lima JWO, Heukelbach J (2009) Reduced oviposition of Aedes aegypti gravid females in domestic containers with predatory fish. Trop Med Int Health 14(11):1347–1350
Payne NL, Gillanders BM (2009) Assemblages of fish along a mangrove-mudflat gradient in temperate Australia. Mar Freshw Res 60(1):1–13
Pen LJ, Potter IC (1991) Reproduction, growth and diet of Gambusia Holbrooki (Girard) in a temperate Australian river. Aquat Conserv 1(2):159–172
Petranka JW, Fakhoury K (1991) Evidence of a chemically-mediated avoidance-response of ovipositing insects to blue-gills and green frog tadpoles. Copeia 1:234–239
Potts M (1980) Blue green algae (Cyanophyta) in marine coastal environments of the Sinai Peninsula—distribution, zonation, stratification and taxonomic diversity. Phycologia 19(1):60–73
Proches S (2004) Ecological associations between organisms of different evolutionary history: mangrove pneumatophore arthropods as a case study. J Mar Biol Assoc UK 84(2):341–344
Proches S, Marshall D (2002) Epiphytic algal cover and sediment deposition as determinants of arthropod distribution and abundance on mangrove pneumatophores. J Mar Biol Assoc UK 82(6):937–942
Proches S, Marshall DJ, Ugrasen K, Ramcharan A (2001) Mangrove pneumatophore arthropod assemblages and temporal patterns. J Mar Biol Assoc UK 81(4):545–552
Ritchie SA (1984) Record winter rains and the minimal populations of Aedes taeniorhynchus (Wiedemann): cause and effect? J Fl Anti-Mosq Assoc 55(1):14–21
Ritchie SA (1990) A simulation model of water depth in mangrove basin forests. J Am Mosq Control Assoc 6:213–222
Ritchie SA, Laidlaw-Bell C (1994) Do fish repel oviposition by Aedes taeniorhynchus. J Am Mosq Control Assoc 10(3):380–384
Ritchie SA, Montague CL (1995) Simulated populations of the black salt marsh mosquito (Aedes taeniorhynchus) in a Florida mangrove forest. Ecol Model 77(2–3):123–141
Robertson AI, Duke NC (1987) Mangroves as nursery sites—comparisons of the abundance of species composition of fish and crustaceans in mangroves and other nearshort habitats of tropical Australia. Mar Biol 96(2):193–205
Robertson A, Duke N (1990) Mangrove fish communities in tropical Queensland, Australia: spatial and temporal patterns in densities, biomass and community structure. Mar Biol 104(3):369–379
Russell RC (2002) Ross River virus: ecology and distribution. Annu Rev Entomol 47(1):1–31
Schleuter D, Eckmann R (2008) Generalist versus specialist: the performances of perch and ruffe in a lake of low productivity. Ecol Freshw Fish 17(1):86–99
Sheaves M, Johnston R (2008) Influence of marine and freshwater connectivity on the dynamics of subtropical estuarine wetland fish metapopulations. Mar Ecol Prog Ser 357:225–243
Sheridan P, Hays C (2003) Are mangroves nursery habitat for transient fishes and decapods? Wetlands 23(2):449–458
Taylor DS, Ritchie SA, Johnson E (1992) The Killifish Rivulus marmoratus—a potential biocontrol agent for Aedes taeniorhynchus and brackish water Culex. J Am Mosq Control Assoc 8:80–83
Teien HC, Standring WJF, Salbu B, Marskar M, Kroglund F, Hindar A (2004) Mobilization of aluminium and deposition on fish gills during sea salt episodes—catchment liming as countermeasure. J Environ Monitor 6(3):191–200
Thollot P, Kulbicki M, Harmelin-Vivien M (1999) Trophic analysis and food webs of mangrove fish assemblages from New Caledonia. Comptes Rendus de l Academie des Sciences. Serie III. Sciences de la Vie 322(7):607–619
Tomerini DM, Dale PE, Sipe N (2011) Does mosquito control have an effect on mosquito-borne disease? The case of Ross River Virus disease and mosquito management in Queensland, Australia. J Am Mosq Contr Assoc 27:39–44
Tse P, Nip THM, Wong CK (2008) Nursery function of mangrove: a comparison with mudflat in terms of fish species composition and fish diet. Estuar Coast Shelf Sci 80(2):235–242
Van Dam AR, Walton WE (2007) Comparison of mosquito control provided by the arroyo chub (Gila orcutti) and the mosquitofish (Gambusia affinis). J Am Mosq Control Assoc 23(4):430–441
Vance DJ, Haywood MDE, Heales DS, Kenyon RA, Loneragan NR, Pendrey RC (1996) How far do prawns and fish move into mangroves? Distribution of juvenile banana prawns Penaeus merguiensis and fish in a tropical mangrove forest in northern Australia. Mar Ecol Prog Ser 131(1–3):115–124
Verweij MC, Nagelkerken I, de Graaff D, Peeters M, Bakker EJ, van der Velde G (2006) Structure, food and shade attract juvenile coral reef fish to mangrove and seagrass habitats: a field experiment. Mar Ecol Prog Ser 306:257–268
Vidy G, Darboe FS, Mbye EM (2004) Juvenile fish assemblages in the creeks of the Gambia Estuary. Aquat Living Resour 17(1):56–64
Walton WE (2007) Larvivorous fish including Gambusia. J Am Mosq Control Assoc 23(2):184–220
Wang M, Huang ZY, Shi FS, Wang WQ (2009) Are vegetated areas of mangroves attractive to juvenile and small fish? The case of Dongzhaigang Bay, Hainan Island, China. Estuar Coast Shelf Sci 85(2):208–216
Weatherley AH (1972) Growth and ecology of fish populations. Academic Press, London
Wolanski E (1992) Hydrodynamics of mangrove swamps and their coastal waters. Hydrobiologia 247:141–161
Woodruff RE, Guest CS, Gainer MG, Becker N, Lindsay M (2006) Early warning of ross River Virus epidemics—combining surveillance data on climate and mosquitoes. Epidemiology 17(5):569–575
Zuharah WF, Lester PJ (2010) Can adults of the New Zealand mosquito Culex pervigilans (Bergorth) detect the presence of a key predator in larval habitats? J Vector Ecol 35(1):100–105
Acknowledgments
This work was supported, in part, by Griffith University and the Australia Government through provision of an Australian Postgraduate Award.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Griffin, L.F., Knight, J.M. 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. Wetlands Ecol Manage 20, 243–252 (2012). https://doi.org/10.1007/s11273-012-9248-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11273-012-9248-4