Evidence for predatory flatworms as organizers of zooplankton and mosquito community structure in rice fields

I present evidence from two field studies and one laboratory experiment that the predatory flatworm, tentatively indentified as Mesostoma nr. lingua, can be important in organizing invertebrate communities in rice fields. In the first field study, I assessed the importance of various predators including two fishes, in explaining among-plot variation in mosquito abundance during a five week interval. Mosquitofish (Gambusia affinis) abundance was not significantly associated with densities of either mosquito, Culex tarsalis or Anopheles freeborni, except for the final week. Associations between green sunfish (Lepomis cyanellus) juveniles and mosquitoes were demonstrated for only A. freeborni — a positive association. Densities of Mesostoma were negatively associated with C. tarsalis and A. freeborni densities. C. tarsalis, protected from flatworms in small-mesh cages, had a much greater survival rate than those that were exposed in large-mesh cages. C. tarsalis survival, when left unprotected in large-mesh cages, was negatively correlated with field densities of flatworms and with the number of flatworms found inside the cages. Survival was also positively correlated with field densities of mosquitoes.In the second field study, Mesostoma densities were negatively correlated with C. tarsalis, A. freeborni, Cladocera and Ostracoda in rice field enclosures early in the season. Cyclopoid copepod densities were not significantly associated with this predator.In a laboratory experiment, predation by Mesostoma on C. tarsalis larvae was reduced when presented with an alternative prey, Moina micrura (a cladoceran).These results suggest that flatworms, via predation, can have large effects on the structure of mosquito and zooplankton communities in rice fields.     

Programmatic review of the mosquito control methods used in the highly industrialized rice agroecosystems of Sacramento and Yolo Counties,California

In the Sacramento Valley (California, USA), rice (Oryza sativa L.) fields are an economically important crop and productive habitats for the mosquito species Culex tarsalis and Anopheles freeborni. Since 2010, approximately 150 km² of conventional and 16 km² of organic rice have been grown in Sacramento and Yolo Counties. These fields are often within mosquito flight-range of both rural towns and urban centers. Culex tarsalis are highly competent vectors of West Nile virus, and An. freeborni are aggressive, mammalophagic, nuisance biters. The Sacramento–Yolo Mosquito and Vector Control District provides mosquito control for the two counties in its jurisdiction. The principles of Integrated Pest Management are used to control mosquitoes in rice growing areas, relying upon a range of surveillance and control interventions. Larvae are controlled by limiting habitats that enable development of immature mosquitoes while balancing agricultural and wildlife needs, applying larvicides, and the use of Gambusia affinis (mosquitofish). Adult mosquitoes are controlled by ultra-low volume pesticide applications. The program was assessed for larval and adult mosquito control efficacy and areas of programmatic improvement identified. Because rice fields are productive habitats for mosquitoes, complete elimination of the habitat is not a feasible goal, thus efforts are aimed at interrupting disease transmission and reducing the number of mosquitoes that traverse into populated areas.

     

Irrigation scheme or mosquito hazard: a case study in Mwea Irrigation Scheme

A survey of the mosquito fauna in the Mwea-Tebere Irrigation Scheme in Kenya was conducted between 1984 and 1985. Two genera, Anopheles and Culex were found indoors in large numbers. The major species were Anopheles gambiae s.l., Anopheles pharoensis, and Culex quinquefasciatus, comprising 66% and 21% of the total catch, respectively. The large numbers of mosquitoes found resting indoors showed seasonal population fluctuations. The seasonal population increases observed were due to the availability of larval breeding conditions over a long period of time and to man-made environmental changes. These changes included irrigation canals and rice paddies. The irrigation canals and rice paddies were flooded from August till December, thus linking the flooding effects of the two rainy seasons. This enabled mosquitoes to breed continuously for up to 9 months per year.     

Mosquitoes and other aquatic insects in fallow field biotopes and rice paddy fields

Fallow field biotopes that develop from abandoned rice fields are man‐made wetlands that provide new habitats for various aquatic animals. Although consideration of such biotopes generally focuses on their positive aspects, this study evaluated the negative aspects of establishing fallow field biotopes with regard to mosquito breeding sites. To determine whether fallow field biotopes become breeding habitats for vector mosquitoes, we evaluated mosquito fauna in fallow field biotopes and adjacent rice fields. We found larvae of Anopheles lesteri, Anopheles sinensis and Culex tritaeniorhynchus (all: Diptera: Culicidae) in the biotopes. Although abundances of mosquito larvae in the biotopes and rice fields were statistically similar, mosquito abundances in rice fields increased dramatically in August when the water level reduced after the rainy season. The abundance and variety of the mosquitoes' natural predators were greater in biotopes than in rice fields because the former are a permanent and stable aquatic environment. A generalized linear mixed model showed a negative effect of predator diversity on mosquito larvae abundance in both habitats. Although fallow field biotopes become breeding habitats for vector mosquitoes, establishing biotopes from fallow fields in order to protect various aquatic animals, including mosquito insect predators, may help to control mosquito breeding.     

Salinity mediates the competitive interactions between invasive mosquitofish and an endangered fish

The interplay of abiotic factors and competition has a long history in ecology, although there are very few studies on the interaction of salinity and competition in fish. Mosquitofish (Gambusia holbrooki) are among the most invasive fish worldwide, with well documented ecological impacts on several taxa such as amphibians and small native fish. It has been previously hypothesized, based on field observations, that salinity limits the invasive success of mosquitofish and provides a competitive refuge for Mediterranean cyprinodonts. We experimentally tested this hypothesis by examining the agonistic behaviour and food competition between mosquitofish and an endangered native cyprinodont (Aphanius fasciatus) at three salinities (0, 15, 25‰). Intraspecific aggressive behaviour for both species was not significantly affected by salinity. As salinity increased, mosquitofish decreased their aggressive behaviour towards cyprinodonts and captured less prey. In contrast, the cyprinodonts did not change their behaviour with different salinity treatments, with the possible exception of increased defensive acts in higher salinities, but captured more prey with increasing salinity because of the reduced efficiency of mosquitofish. Our study confirms previous field observations that salinity limits the invasive success of mosquitofish and provides one of the few experimental demonstrations that it may mediate behavioural and competitive interactions between fish species. Condition-specific competition of mosquitofish might be expected with other species and ecosystems worldwide and illustrates the importance of integrating biotic and abiotic factors in the study of interspecific interactions.     

Behavioral responses of American toad and bullfrog tadpoles to the presence of cues from the invasive fish, Gambusia affinis

The introduction of non-native predators is thought to have important negative effects on native prey populations. The susceptibility of native prey to non-native or introduced predators may depend on their ability to respond appropriately to the presence of these non-native predators. We conducted a laboratory based behavioral experiment to examine the response of American toad (Bufo americanus) and bullfrog (Rana catesbeiana) tadpoles to the presence of cues from the introduced mosquitofish (Gambusia affinis), a potential tadpole predator. Neither the American toad tadpoles nor the bullfrog tadpoles responded behaviorally to the presence of mosquitofish cues. If tadpoles are unable to respond to the presence of mosquitofish cues appropriately, then their ability to avoid predation by mosquitofish may be compromised and this may contribute to the impacts of mosquitofish on some tadpole populations.     

Assessment of Potential Impacts of Exotic Species on Populations of a Threatened Species, White Sands Pupfish, Cyprinodon tularosa

The potential impact of introduced species on rare taxa is of particular concern to conservation biologists. We evaluate the impacts of western mosquitofish (Gambusia affinis) and virile crayfish (Orconectes virilis) on experimental populations of a threatened species, the White Sands pupfish (Cyprinodon tularosa). Forty experimental pupfish populations were exposed to one of four treatments; (a) 1 crayfish, (b) 4 crayfish, (c) 5 adult mosquitofish and (d) control. Pupfish population size and biomass was monitored over the duration of one breeding season. A repeated measure multiple analysis of covariance revealed a significant effect of treatments on response variables (population size and biomass) (P<0.0001). Mosquitofish had a significant effect on population size and biomass (P=0.0330). The effect of one crayfish was not significant (P=0. 0683). However, 4 crayfish had a significant effect (P<0.0001) on population size. We use these data, along with information on environmental tolerances of crayfish and mosquitofish, to evaluate risks for specific pupfish populations. An erratum to this article is available at .     

The influence of aquatic predators on mosquito abundance in animal drinking troughs in New Zealand

The occurrence and abundance of mosquito populations may be associated with the abundance of predators. We examined the relationship between aquatic predators and populations of mosquitoes in animal water troughs in Waikanae, New Zealand. We also investigated the effects of water volume and environmental factors (temperature, rainfall, wind speed, humidity, and pressure) in order to further understand factors influencing mosquito and predator populations. Logistic regression indicated that the presence or absence of mosquitoes was primarily affected by three factors: predator abundance, week of observation, and water volume. Pearson's correlation indicated that the presence of predators had a positive correlation with water volume (r²= 0.176, p< 0.05). Otherwise, the presence of mosquito larvae in water troughs was negatively correlated with water volume (r²=?0.159, p=0.022) and wind speed (r²=0.142, p=0.041). We established a translocation experiment in which predators or mosquitoes were moved between troughs in order to examine the prey survival rate after exposure to Anisops wakefieldi predators. The survival rate of mosquitoes was not significantly different, between 0–0.1%, irrespective of the number of predators translocated (1–9) or the initial mosquito density (20–70 larvae). Our results suggested that A. wakefieldi predators may have the potential to be a promising biological control tool for the control of mosquito populations by altering mosquito population dynamics.     

Direct and indirect effects of predation on mosquitofish behavior and survival

Predation can have strong direct and indirect effects on the behavior of prey. We investigated whether predation by chain pickerel (Esox niger) caused adult eastern mosquitofish (Gambusia holbrooki) to alter their habitat use and whether pickerel predation influenced survival of adult and neonate mosquitofish. The number of adult mosquitofish using the riskier of three habitats was lowest when two predators occupied the risky habitat, intermediate in the treatment with one predator, and highest when no predators occurred there. More mosquitofish neonates survived high predation treatments than treatments lacking pickerel. We conclude that pickerel predation causes adult mosquitofish to shift to refuge habitats. The pattern of neonate survival suggests that adult habitat use may create a refuge from cannibalism for neonate mosquitofish, resulting in higher neonate survival in treatments with more pickerel. Hence, pickerel predation has a direct effect on adult mosquitofish behavior and a strong indirect effect on neonate survival. Both interspecific and intraspecific predation can effect prey populations and can interact to produce important indirect effects.     

Mosquito female response to the presence of larvivorous fish does not match threat to larvae

1. Several species with complex life‐history traits such as amphibians and insects with aquatic immature stages and terrestrial adults avoid ovipositing in pools containing larvivorous fish. This avoidance response was assumed to be a general one for most fish species. 2. The generality of ovipositing Culex to the presence of three, widespread larvivorous fish species was tested in a set of field experiments with artificial oviposition pools using caged fish. 3. Larval performance was further examined under actual predation by these three fish species. 4. Results show that ovipositing females responded strongly to the presence of caged mosquitofish, Gambusia affinis, while showing no significant response to the presence of caged green sunfish, Lepomis cyanellus, or the pirate perch, Aphredoderus sayanus. All three fish species consumed similar amounts of larvae. 5. This is the first example of species‐specific response differences to predators during mosquito oviposition habitat selection. These results point to the existence of predator‐released kairomones affecting mosquito behaviour. These kairomones may either be species‐specific or vary in concentration among fish, and probably have an important role in the understanding of mosquito spatial distribution.     

The ecological role of chemical stimuli for the zooplankton: predator-induced morphology in Daphnia

Summary Numerous adaptive predator-induced responses occurred when eight clones representing seven Daphnia (Crustacea: Cladocera) species were tested against three common predators: fourth instar larval phantom midge Chaoborus americanus, adult backswimmer Notonecta undulata, and small sunfish Lepomis macrochirus. The predators were confined within small mesh bags, suggesting that the signal for induction is chemical. The induced responses included longer tail spines, longer heads, smaller bodies, increased egg clutches, and decreased lipid reserves. Each Daphnia species responded to each of the three predators in a unique manner. Induced responses in the above characters showed no significant association. The induced morphological changes are generally consistent with current theories of what is an adaptive response for the various sizes of Daphnia exposed to tactile and visual predators. The abundance of induced responses in these experiments suggests that predator-induced responses are a widespread and ecologically important phenomenon of the freshwater zooplankton.     

Can adults of the New Zealand mosquito Culex pervigilans (Bergorth) detect the presence of a key predator in larval habitats?

The influence of predators on mosquito populations may be direct through predation or indirect through sub‐lethal responses of adult mosquitoes in life history traits such as oviposition behavior. In New Zealand, the backswimmer, Anisops wakefieldi, is a common predator of mosquito larvae found in temporary and permanent water bodies. We predicted that the New Zealand native mosquito, Culex pervigilans, whose larvae are vulnerable to predation of Anisops, would likely avoid the containers with the presence of Anisops or its kairomone. We established temporary water containers without predators, free‐roaming predators, caged predators (which were unable to eat mosquitoes), or containers from which predators were removed immediately prior to the experiment (these containers would have remnant kairomones from the predators). Each treatment with Anisops had predator densities of one, three, or nine Anisops. Contrary to our predictions, when choosing oviposition habitats, Cx. pervigilans appeared to ignore the presence of free‐roaming Anisops, caged Anisops, and water with Anisops kairomone. We thus observed no significant differences between the numbers of egg rafts laid by Cx. pervigilans in the different predator treatments nor were the number of egg rafts significantly affected by the density of predators. Rather than the presence of predators, environmental factors including temperature, humidity, and pressure were significantly correlated with mosquito oviposition. These mosquitoes appeared to either ignore the presence of the predator, had no ability to detect the presence of predators, or perhaps the cues from Anisops predators were not sufficiently strong enough to alarm these mosquitoes. We argue that the mosquito has not evolved the ability to detect the presence of these predators while ovipositing.     

Modeling mosquitofish (Gambusia holbrooki) responses to Genapol OXD-080, a non-ionic surfactant, in rice fields

An ecotechnological approach to control crayfish (Procambarus clarkii) infestation in rice fields of the Lower Mondego River Valley (Central Portugal) has recently been investigated. The application of the biodegradable non-ionic surfactant Genapol OXD-080, a fatty alcohol polyglycol ether, in rice paddies at a given concentration (50 mg/l) has been considered as a non-harmful chemical method to mitigate damage caused by crayfish digging activities to rice crops. Therefore, an important requirement regarding the ecological viability of this approach is that populations of non-target species are not significantly affected. A simple mosquitofish (Gambusia holbrooki) population model, in which the relationships with its main food prey were considered, was developed to assess the potential risk to a non-target key species of contaminating the irrigation channels following surfactant application. The model is based on data concerning mosquitofish life cycle and population dynamics, as well as mosquitofish diet and interactions with its main prey species. Quantitative information regarding the acute and sublethal effects of Genapol OXD-080 on mosquitofish and other non-target organisms was obtained from laboratory experiments. Three concentrations of Genapol OXD-080 (0.75, 1 and 2.5 mg/l) were used to simulate a small amount of contamination in irrigation channels. If contamination occurred, the mosquitofish population would tend to decline dramatically, even when submitted to a very small concentration of Genapol OXD-080 (e.g. 0.75 mg/l, 66.7 times lower than the concentration planned to be used in rice paddies). Thus, Genapol OXD-080 could potentially cause vast damage to local mosquitofish populations, and therefore should not be used without taking all precautions to avoid contaminating important biological reservoirs, such as the rice field irrigation channels.     

A comparative study of predation of three aquatic heteropteran bugs on Culex quinquefasciatus larvae

The aquatic bugs Anisops bouvieri Kirkaldy 1704 (Heteroptera: Notonectidae), Diplonychus (=Sphaerodema) rusticus Fabricius 1781, and Diplonychus annulatus Fabricius 1781 (Heteroptera: Belostomatidae) are common members of the freshwater insect communities of the East Calcutta Wetlands along the eastern fringe of Kolkata, India. These insects are established predators of dipteran larvae and other organisms. A comparative account of their predatory efficiency was made using larvae of Culex quinquefasciatus Say 1823 in the laboratory. It was revealed that a single adult of A. bouvieri could consume 28–34 fourth-instar mosquito larvae per day, D. rusticus 11–87 fourth-instar mosquito larvae per day, and D. annulatus 33–122 fourth-instar mosquito larvae per day, depending upon the prey and predator densities. The mean predation rate of A. bouvieri and D. annulatus remained stable over a 6-day feeding period but varied for D. rusticus. The predatory impact (PI) values were 14.77–17.31, 46.9–55.73, and 61.74–72.72 larvae/day for A. bouvieri, D. rusticus, and D. annulatus, respectively. Compared to these, the clearance rate (CR) value range was 9.06–13.25 for A. bouvieri, 13.64–15.99 for D. rusticus, and 13.50–16.52 larvae l/day/predator for D. annulatus. The values of mutual interference, “m,” remained 0.06–0.78 for A. bouvieri, 0.003–0.25 for D. rusticus, and 0.09–0.27 for D. annulatus, and did not vary between the days. The difference in predatory efficiency, CR, and PI values varied significantly among the three predators, indicating the possible difference in the function as predators occupying the same guild. It can be assumed that these predators play an important role in larval population regulation of mosquitoes and thereby impart an effect on species composition and interactions in the aquatic insect communities of the wetlands and other similar habitats where they occur.     

Ex situ evaluation of impacts of invasive mosquitofish on the imperiled Barrens topminnow

Central to the protection of native species is an understanding of impacts of actual or potential invasive species and also the mechanisms through which those impacts are mediated. The introduction and spread of western mosquitofish, Gambusia affinis, into spring systems of the Barrens Plateau region of middle Tennessee is a concern for native species such as the Barrens topminnow, Fundulus julisia. We investigated whether mosquitofish might act as predators on early life stages of topminnows as well as affect the physiological well being of adults through aggressive interactions. A short-term, 24-h laboratory study with mosquitofish and topminnows demonstrated the vulnerability of young topminnow life stages to large mosquitofish predation and aggression. Survival of topminnow young, <16 mm total length (TL), was 0% and was attributed to predation by mosquitofish. Survival of juveniles, 20–30 mm TL, was 25%; juveniles mostly succumbed (post 24-h) to injuries inflicted by large mosquitofish. Adult topminnow survival was 100% but adults faced injury risk, primarily during the initial stages of their interaction with large mosquitofish. A long-term, 60-day laboratory study with syntopic and allotopic populations of adult topminnows and mosquitofish failed to detect any negative impacts on topminnows due to coexistence. Survival, growth, and fecundity of adult topminnows syntopic with mosquitofish were not different from the allotopic population, although injury risk in the form of fin damage was greater syntopically. Thus, predation and aggression towards young topminnows may be the primary mechanisms by which western mosquitofish jeopardize the persistence of native Barrens topminnows in the wild. Our results reemphasize the danger to native aquatic biodiversity of unregulated introductions of Gambusia species.     

Behavioral constraints for the spread of the eastern mosquitofish, Gambusia holbrooki (Poeciliidae)

Eastern mosquitofish (Gambusia holbrooki) are native to the southeastern United States but notoriously invasive elsewhere, and are aggressive predators in ecosystems they inhabit. Information on dispersal behavior is needed to better understand mosquitofish spread upon introduction and potential means to mitigate that spread. We experimentally tested the effects of shallow water depths (3–24 mm) and obstacles (leaf litter) on mosquitofish dispersal behavior, plus a range of conditions relevant to field situations. Mosquitofish dispersed significantly faster in deeper water (p < 0.001) but some dispersed in only 3 mm water depth (i.e., one-half average body depth). Wetland and upland leaf litter at natural densities strongly interfered with mosquitofish dispersal behavior. Based on our results, introduced mosquitofish spread rapidly given unimpeded dispersal corridors (e.g., mowed ditches), and may do so at rates >800 m/day. Also, consistent lack of sexual dimorphism in dispersal behavior indicates that mosquitofish spread is not strongly dependent on female poeciliid reproductive biology. Our results support designation of mosquitofish as highly invasive and suggest that barriers to mosquitofish spread must obstruct dispersal pathways as shallow as 3 mm depth.     

Diversity and fine-scale spatial genetic structure of Cyperus papyrus populations in Lake Naivasha (Kenya) using microsatellite markers

Species introduced outside their native range to serve anthropogenic purposes may have unintended consequences on native organisms. Mosquitofish (Gambusia affinis and Gambusia holbrooki) have been introduced throughout the world to control larval mosquito populations in aquatic environments, but they have also been implicated in the decline of native fish, amphibian, and aquatic invertebrate populations. We investigated the roles of introduced western mosquitofish (G. affinis), and two naturally colonizing predators (crayfish and dragonfly naiads) in inflicting tail injuries observed on ranid frog tadpoles in experimental constructed wetlands. We also examined the influence of vegetation in reducing tail injury severity. We found that mosquitofish significantly increased the prevalence and severity of tail injuries, but crayfish and dragonfly naiads contributed much less to increased injury levels. Furthermore, increased vegetation cover did not significantly attenuate tail injuries. However, after chemical removal of Gambusia, injury prevalence and severity was significantly reduced. Although previous investigations have concluded that mosquitofish prey upon the eggs and larvae of some amphibians, our results illustrate that these fish can cause substantial but apparently sub-lethal injuries to large numbers of larval amphibians in a wetland. Further investigations are needed to determine if these injuries impede the fitness of victims and lead to population reductions.     

Consumptive effects of fish reduce wetland crayfish recruitment and drive species turnover

Predators and dry-disturbances have pronounced effects on invertebrate communities and can deterministically affect compositional turnover between discrete aquatic habitats. We examined the effect of sunfish (Lepomis spp.) predators on two native crayfish, Procambarus alleni and P. fallax, that regionally coexist in an expansive connected wetland in order to test the hypotheses that sunfish predation limits crayfish recruitment (both species) and that it disproportionately affects P. alleni, the species inhabiting temporary wetlands. In replicate vegetated wetlands (18.6 m²), we quantified summertime crayfish recruitment and species composition across an experimental gradient of sunfish density. Separately, we quantified effects of sunfish on crayfish growth, conducted a complimentary predation assay in mesocosms, and compared behavior of the two crayfish. Sunfish reduced P. alleni summertime recruitment by >99% over the full sunfish gradient, and most of the effect was caused by low densities of sunfish (0.22–0.43 m⁻²). P. alleni dominated wetlands with few or no sunfish, but the composition shifted towards P. fallax dominance in wetlands with abundant sunfish. P. fallax survived better than P. alleni over 40 h in smaller mesocosms stocked with warmouth. Sunfish reduced P. fallax recruitment 62% in a second wetland experiment, but growth rates of caged crayfish (both species) were unaffected by sunfish presence, suggesting predatory effects were primarily consumptive. Consistent with life histories of relatively fish-sensitive invertebrates, P. alleni engaged in more risky behaviors in the laboratory. Our results indicate that sunfish predators limit recruitment of both species, but disproportionately remove the more active and competitively dominant P. alleni. Spatially and temporally variable dry-disturbances negatively co-varying with sunfish populations allow for regional coexistence of these two crayfish and may release populations of either species from control by predatory fishes.     

Effects of mosquito larvae removal with Bacillus thuringiensis israelensis (Bti) on natural protozoan communities

The protein crystals produced by Bacillus thuringiensis israelensis (Bti) are used against the larvae of pestiferous flood-water mosquitoes in ephemeral wetlands. Although mosquito larvae are considered important predators on protozoans and bacteria, it is not known how a distinct reduction of mosquito larvae density in natural wetlands caused by application of Bti may indirectly affect these microbial communities. Here we show, in a large scale experiment in six natural wetlands, that the densities of heterotrophic protozoans was on an average 4.5 times higher in wetland areas treated with Bti than in control areas. In addition, the taxonomic richness of heterotrophic protozoans increased on an average of 60% in areas with Bti application compared to control areas. The increase in protozoan density and richness was fairly consistent among sites of different wetland habitats. We discuss the potential implications of our results for other parts of the ecosystem. Handling editor: K. Martens