Influence of fire salamander larvae on among-pool distribution of mosquito egg rafts: oviposition habitat selection or egg raft predation?

Many amphibian populations are in decline worldwide. Surprisingly, few studies have examined how such declines may benefit mosquitoes. Amphibian larvae may compete with and prey upon mosquito larvae, and may alter oviposition habitat selection (OHS) of mosquito adults. However, often overlooked, observed among-pool egg distributions attributed to OHS may additionally or alternatively be explained by egg predation. Temporary pools of mountainous areas of the Mediterranean serve as larval habitat for both the mosquito, Culiseta longiareolata, and the salamander, Salamandra infraimmaculata. We found Culiseta larvae and egg rafts to be highly vulnerable to predation by pre-metamorphosing Salamandra larvae, but not to metamorphosing ones. In outdoor mesocosm experiments, oviposition avoidance by Culiseta females in response to caged Salamandra was not demonstrated regardless of salamander developmental stage. Egg raft abundance was significantly reduced in free-roaming, pre-metamorphosing Salamandra but not by metamorphosing ones. Thus, Salamandra larvae may have little deterrence on Culiseta oviposition. Instead, fewer egg rafts are attributed largely to egg predation. This study highlights the importance of egg raft predation in addition to OHS when interpreting the influence of predators on prey egg distributions. It also highlights that a cost of declining amphibian populations is their reduced impacts on mosquito populations.     

Interactive effects of salinity and a predator on mosquito oviposition and larval performance

Oviposition habitat selection (OHS) is increasingly being recognized as playing a large role in explaining mosquito distributions and community assemblages. Most studies have assessed the role of single factors affecting OHS, while in nature, oviposition patterns are most likely explained by multiple, interacting biotic and abiotic factors. Determining how various factors interact to affect OHS is important for understanding metapopulation and metacommunity dynamics. We investigated the individual and interactive effects of three water salinities (0, 15 and 30 p.p.t. NaCl added) and the aquatic predator Anisops debilis Perplexa (Hemiptera: Notonectidae) on OHS and larval performance of the mosquitoes Ochlerotatus caspius Pallas and Culiseta longiareolata Macquart (Diptera: Culicidae) in outdoor-artificial-pool and laboratory experiments. C. longiareolata inhabited only freshwater pools, strongly avoided pools containing A. debilis, and larvae experienced lower survival in the presence of A. debilis. Salinity concentration interacted strongly with the predator in affecting OHS and larval survival of O. caspius; oviposition increased with increasing salinity in the absence of the predator and decreased with increasing salinity in the presence of the predator. O. caspius larval survival in predator-free pools was lowest in freshwater and highest at intermediate salinity. In predator pools, survival was highest at high salinity, where predation rate was shown to be lowest in the laboratory. Our results highlight that assessing the role of single factors in affecting mosquito distributions can be misleading. Instead, multiple factors may interact to affect oviposition patterns and larval performance.     

Multi‐scale oviposition site selection in two mosquito species

1. In organisms characterised by complex life cycles, habitat selection often occurs at multiple spatial scales. For instance, female mosquitoes searching for an appropriate aquatic habitat to oviposit their eggs should also consider the characteristics of the terrestrial landscape in which it is embedded. 2. In this study, a field experiment was conducted to test for multi‐scale oviposition site selection in two mosquito species. Artificial pools were placed in two adjacent landscapes, olive plantations and a citrus orchard, mainly differing in their blooming periods and nectar availability. Pools were organised in three pairs: predatory caged fish were present in both pools, in one pool, or in none. 3. Early during the season, most of the egg rafts were laid by Culiseta longiareolata females in pools located within the blooming citrus orchard. When blooming shifted to the olive plantation, C. longiareolata become opportunistic. Culex pipiens females appeared later on during the season, when egg rafts of C. longiareolata were scarce, and they exhibited a higher selectivity to the olive plantation, although its blooming ended. In addition, the selectivity of C. pipiens to fish‐free pools was stronger than that of C. longiareolata. 4. Culex pipiens was more selective, possibly due to its high dispersal ability, which can lower movement cost and enhance the ability to gather environmental information. A trade‐off among gonotrophic cycles, combined with a shorter breeding season and limited recognition ability of the predatory fish may have reduced C. longiareolata selectivity. These differential oviposition patterns can strongly affect the population and community dynamics of both species.     

Oviposition habitat selection in response to risk of predation in temporary pools: mode of detection and consistency across experimental venue

Natural selection should favor females that avoid ovipositing where risk of predation is high for their progeny. Despite the large consequences of such oviposition behavior for individual fitness, population dynamics, and community structure, relatively few studies have tested for this behavior. Moreover, these studies have rarely assessed the mode of detection of predators, compared responses in prey species that vary in vulnerability to predators, or tested for the behavior in natural habitats. In an outdoor artificial pool experiment, we tested the oviposition responses of two dipteran species, Culiseta longiareolata (mosquito) and Chironomus riparius (midge), to the hemipteran predator, Notonecta maculata. Both dipteran species have similar life history characteristics, but Culiseta longiareolata larvae are highly vulnerable to predation by Notonecta, while Chironomus riparius larvae are not. As their vulnerabilities would suggest, Culiseta longiareolata, but not Chironomus riparius, strongly avoided ovipositing in pools containing Notonecta. An experiment in natural rock pools assessing oviposition by Culiseta longiareolata in response to Notonecta maculata yielded an oviposition pattern highly consistent with that of the artificial pool experiment. We also demonstrated that the cue for oviposition avoidance by Culiseta longiareolata was a predator-released chemical: Notonecta water (without Notonecta replenishment) repelled oviposition for 8 days. Oviposition avoidance and mode of detection of the predator have important implications for how to assess the true impact of predators and for the use of commercially produced kairomones for mosquito control.     

Predation-dependent oviposition habitat selection by the mosquito Culiseta longiareolata: a test of competing hypotheses

We investigated the mechanism underlying oviposition habitat selection (OHS) in the mosquito Culiseta longiareolata. The putative outcome of a trade‐off between the risk of predation and detrimental density dependence, OHS in this species presents an opportunity to test two competing alternatives: (1) a polymorphic scenario, in which a fixed proportion of females constantly avoid ‘predator pools’, while the remainder oviposits at random; and (2) a monomorphic scenario, in which all females oviposit in predator pools with a certain probability. We present a conceptual framework that demonstrates how a simple experimental design – whereby predator incidence in artificial pools is alternated between 0.25 and 0.75 – can distinguish between, or refute, the two scenarios. Given the proportional use, by ovipositing females, of predator‐free pools observed under each treatment, and a bootstrap estimate of the ratio of daily oviposition rates, we find the monomorphic scenario twice as likely as the polymorphic.     

Predator feeding vibrations encourage mosquito larvae to shorten their development and so become smaller adults

1. Water‐borne predator kairomones are known to allow mosquito larvae to detect and identify the presence of a specific predator, so that they can deploy defences tailored to that predator. Kairomones, however, have limitations, and detection of specific water‐borne vibrations produced by a predator would allow fine‐tuning of their anti‐predator defences. 2. Larvae of the mosquito Culiseta longiareolata have previously been shown to recognise the specific vibration pattern of a feeding dragonfly nymph and respond by altering their feeding behaviour from active bottom‐scraping to a more passive surface filter‐feeding, while other water vibrations did not produce this response. Culex perexiguus larvae also responded, but to a much lesser extent. 3. In this study, C. perexiguus larvae responded strongly to dragonfly vibrations by reducing their larval duration from 9.8 to 8.7 days, but this resulted in significantly smaller (and thus probably less successful) adults. However, Culiseta longiareolata larvae did not alter their larval duration in response to dragonfly vibrations.     

Direct and indirect effects of a predatory backswimmer (Notonecta maculata) on community structure of desert temporary pools

Abstract.

• 1 We assessed experimentally the effects of the predatory backswimmer, Notonecta maculata, on naturally colonizing mosquito populations in artificial outdoor pools in the Negev Desert, Israel. A single Notonecta adult per pool (8–15 litres water) had a very large negative impact on populations of Culiseta longiareolata, the most common species found in natural local pools. Notonecta caused large reductions of Culiseta egg rafts and early-instar larvae (instars I and II) and virtually 100% reductions of late-instar Culiseta larvae (instars III and IV) and pupae.
• 2 Notonecta also caused a trophic cascade in the experimental pools; by preying on periphyton-feeding Culiseta larvae, Notonecta indirectly caused significantly higher densities of diatoms, the major component of the periphyton.
• 3 Surveys of nearby natural pools taken between March and May supported the experimental results: a strong negative association between Notonecta and Culiseta among pools occurred as Notonecta increased in numbers and became more widely distributed. Anopheles (occurring only in May) and Culex mosquito immatures were not negatively associated with Notonecta. Culiseta was not associated with surface vegetation whereas both Culex and Anopheles showed strong positive associations with surface vegetation both among and within pools. We attribute the negative association between the predator and Culiseta to local prey extinctions caused by Notonecta in individual pools. Culiseta, being an open water species, is apparently more prone to predation by Notonecta than the vegetation-dwelling Culex and Anopheles.

     

Predation potential of three flatworm species (Platyhelminthes: Turbellaria) on mosquitoes (Diptera: Culicidae)

We conducted a field survey for flatworms to select species as potential biological control agents against Aedes aegypti and Culex pipiens (Diptera, Culicidae) breeding in artificial containers. Laboratory experiments were performed to determine the daily predation rate, differential predation on each mosquito larval instar, selective predation on either A. aegypti or C. pipiens, and predator tolerance to water from artificial containers. Girardia anceps (Tricladida, Paludicola, Dugesiidae), Mesostoma ehrenbergii and Bothromesostoma cf. evelinae (Rhabdocoela, Typhloplanoida, Typhloplanidae) were found in temporary puddles and permanent pools. In the laboratory, they killed between 52% and 100% of immature mosquitoes coexisting in the same habitat. No preference of flatworms for mosquito preys was detected. Predation rate was related to predator size and instar of preys. Girardia anceps and B. evelinae survived after a dry period and when re-flooding occurred, they laid eggs. Tolerance to water from artificial containers was highest in G. anceps and this species could be a suitable predator to reduce mosquito populations from artificial containers using an inoculative approach.     

Are behavioural responses to predation cues linked across life cycle stages?

1. Prey organisms can perceive cues to predation hazard and adopt low‐risk behaviours to increase survival. Animals with complex life cycles, such as insects, can exhibit such anti‐predatory behaviours in multiple life stages. 2. Cues to predation risk may induce ovipositing females to choose habitats with low predation risk. Cues to predation risk may also induce larvae to adopt facultative behaviours that reduce risk of predation. 3. One hypothesis postulates that anti‐predation behaviours across adult and larval stages may be negatively associated because selection for effective anti‐predator behaviour in one stage leads to reduced selection for avoidance of predators in other stages. An alternative hypothesis suggests that selection by predation favours multi‐component defences, with both avoidance of oviposition and facultative adoption of low‐risk behaviours by larvae. 4. Laboratory and field experiments were used to determine whether defensive responses of adult and larval mosquitoes are positively or negatively associated. The study tested effects of waterborne cues from predatory Toxorhynchites theobaldi on oviposition choices and larval behaviours of three of its common prey: Culex mollis, Limatus durhamii and Aedes albopictus. 5. Culex mollis shows strong anti‐predator responses in both life stages, consistent with the hypothesis of a multi‐component behavioural defence. The other two species showed no detectable responses to waterborne predator cues in either adult or larval stages. Larvae of these unresponsive species were significantly more vulnerable to this predator than was C. mollis. 6. For these mosquitoes, species appear either to have been selected for multi‐component defences against predation or to act in ways that could be called predator‐naïve.     

Rapid habituation by mosquito larvae to predator kairomones

Larvae of some species of mosquitoes have been shown to respond to water‐borne kairomones from predators by reducing bottom‐feeding and replacing it with surface filter‐feeding, which uses less movement and is thus less likely to attract a predator. However, if no predator attack takes place, then it would be more efficient to use a risk allocation strategy of habituating their response depending on the predator and the overall risk. The larvae of Culiseta longiareolata Macquart live in temporary rain‐filled pools, where they are exposed to a high level of predation. Within one hour, they responded to kairomones from dragonfly or damselfly nymphs, or to the fish Aphanius, by significantly reducing bottom‐feeding activity. Continued exposure to the predator kairomones resulted in habituation of their response to damselflies, a slower habituation to fish, but no habituation to dragonflies even after 30 h. In contrast, the larvae of Culex quinquefasciatus Say normally live in highly polluted and thus anaerobic water, where the predation risk will be much lower. They also showed a significant reduction in bottom‐feeding after 1 h of exposure to predator kairomones but had completely habituated this response within 6 h of continuous exposure. Some species of mosquito larvae can thus show a very rapid habituation to predator kairomones, while others only habituate slowly depending on the predator and overall predation risk.     

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.     

Predation risk affects egg mortality and carry over effects in the larval stages in damselflies

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Inter- and Intra-Specific Density-Dependent Effects on Life History and Development Strategies of Larval Mosquitoes

We explored how inter- and intra-specific competition among larvae of two temporary-pool mosquito species, Culiseta longiareolata and Ochlerotatus caspius, affect larval developmental strategy and life history traits. Given that their larvae have similar feeding habits, we expected negative reciprocal inter-specific interactions. In a microcosm experiment, we found sex-specific responses of larval survival and development to both intra- and inter-specific larval competition. C. longiareolata was the superior competitor, reducing adult size and modifying larval developmental time of O. caspius. We observed two distinct waves of adult emergence in O. caspius, with clear sex-specific responses to its inter-specific competitor. In males, this pattern was not affected by C. longiareolata, but in females, the timing and average body size of the second wave strongly varied with C. longiareolata density. Specifically, in the absence of C. longiareolata, the second wave immediately followed the first wave. However, as C. longiareolata abundance increased, the second wave was progressively delayed and the resulting females tended to be larger. This study improves our understanding of the way intra- and inter-specific competition combine to influence the life histories of species making up temporary pond communities. It also provides strong evidence that not all individuals of a cohort employ the same strategies in response to competition.     

Effects of Anisops sardea (Hemiptera: Notonectidae) on oviposition habitat selection by mosquitoes and other dipterans and on community structure in artificial pools

We investigated the effects of the predatory backswimmer, Anisops sardea, on oviposition habitat selection of mosquitoes and other dipterans, and on community structure in experimental pools. We predicted that those dipteran species whose larvae were shown to be highly vulnerable to predation by Anisops would avoid Anisops pools when choosing an oviposition site. We established the following treatments in plastic tubs: (1) Control (without Anisops); (2) Free Anisops (ten Anisops within pool but not caged); (3) Caged Anisops (ten Anisops in cage). The pools were open to colonization by insects. We added resting stages of crustaceans and first instar larvae of the mosquitoes Culiseta longiareolata and Culex laticinctus. Among the dipteran species, Culiseta longiareolata, Culex laticinctus, Chironomus riparius (Chironomidae) and Forcipomyia sp. (Ceratopogonidae), only Culisetalarvae were highly vulnerable to predation. As predicted, based on larval vulnerability, Culiseta, but not the other species, avoided Anisops pools when ovipositing. Free Anisops reduced taxon richness. This reduction resulted largely from the elimination of the cladoceran Ceriodaphniasp. and Culiseta in most free Anisops pools. Thus, Anisops sardea structures the community, both by a behavioral response of prey to its presence and by consumption of prey.     

Influence of Predator Presence and Prey Density on Behavior and Growth of Damselfly Larvae (Ischnura elegans) (Odonata: Zygoptera)

Foraging behavior is often determined by the conflicting benefits of energy gain and the risk of mortality from predation or other causes. Theory predicts that animals should have lower activity levels when either the risk of predation or the availability of resources in the environment is high. We investigated the adjustment of the behavior of I. elegans larvae to predator presence (Anax imperator) and prey density (Daphnia sp.) and their interaction in a completely crossed factorial experiment in the lab and the effect of behavior on growth. The foraging activity of the I. elegans larvae was significantly reduced in the presence of a free-swimming predator but not a caged predator. Abdominal movements were significantly reduced at a low prey density. Growth was significantly reduced by the presence of a free swimming predator and low prey densities. These results provide evidence that these damselfly larvae adjust their behavior to the presence of predators to increase their survival at the expense of reduced growth and development.     

A parasite's modification of host behavior reduces predation on its host

Parasite modification of host behavior is common, and the literature is dominated by demonstrations of enhanced predation on parasitized prey resulting in transmission of parasites to their next host. We present a case in which predation on parasitized prey is reduced. Despite theoretical modeling suggesting that this phenomenon should be common, it has been reported in only a few host–parasite–predator systems. Using a system of gregarine endosymbionts in host mosquitoes, we designed experiments to compare the vulnerability of parasitized and unparasitized mosquito larvae to predation by obligate predatory mosquito larvae and then compared behavioral features known to change in the presence of predatory cues. We exposed Aedes triseriatus larvae to the parasite Ascogregarina barretti and the predator Toxohrynchites rutilus and assessed larval mortality rate under each treatment condition. Further, we assessed behavioral differences in larvae due to infection and predation stimuli by recording larvae and scoring behaviors and positions within microcosms. Infection with gregarines reduced cohort mortality in the presence of the predator, but the parasite did not affect mortality alone. Further, infection by parasites altered behavior such that infected hosts thrashed less frequently than uninfected hosts and were found more frequently on or in a refuge within the microcosm. By reducing predation on their host, gregarines may be acting as mutualists in the presence of predation on their hosts. These results illustrate a higher‐order interaction, in which a relationship between a species pair (host–endosymbiont or predator–prey) is altered by the presence of a third species.     

Differential responses to predator cues between two mosquito species breeding in different habitats

1. Natural selection favours females who can correctly assess the predation risk and hence avoid high‐risk oviposition sites and reduce the mortality rate of their offspring. In spite of the potential significance of such behaviour, relatively few studies have assessed the relationship between oviposition behaviour and predation risk. 2. The present study aimed to determine the sublethal effects of predators on oviposition site selection by gravid females, the foraging activity of larvae, and the life history traits of two mosquito species that breed in different habitats, Aedes albopictus Skuse (container breeder) and Culex tritaeniorhynchus Giles (wetland breeder). 3. Female C. tritaeniorhynchus avoided laying eggs at oviposition sites in the presence of a predator cue. In contrast, female A. albopictus laid eggs in both the absence and presence of the predator cue. 4. To examine the effects of predator cues on larval behaviour, experiments were conducted in the absence and presence of a predator cue. Although larval activity was lower in the presence of the predator cue than that in its absence in both species, C. tritaeniorhynchus responded to the predator cue more strongly than A. albopictus. Female A. albopictus that had been reared with caged predators exhibited an extended larval development period, whereas the adult C. tritaeniorhynchus reared in the presence of predators were smaller than those reared in their absence. 5. This finding might explain why C. tritaeniorhynchus avoid laying eggs in predator‐conditioned water, for example to increase the fitness of their offspring, but A. albopictus either cannot detect predator cues or are not sensitive to them.     

Effects of alternative food on cannibalism and herbivore suppression by carabid larvae

1. Predator and alternative food density are important factors influencing herbivore suppression by generalist predators. Herbivore suppression can be reduced if predators forage preferentially on alternative foods. Cannibalism can increase at high predator densities, further reducing herbivore suppression. However, complex interactions are possible, as alternative food can increase predator abundance and survival restoring top‐down effects on herbivores. 2. In two species of carabid larvae (Poecilus chalcites and Anisodactylus ovularis), we studied how alternative foods (fly pupae and grass seeds) and predator density affect predation of black cutworm larvae and how alternative foods affect cannibalism among carabid larvae. 3. Adding alternative food to microcosms generally reduced total predation of cutworms. However, the strength of this effect was dependent on carabid species, larval density, and food type. 4. Increasing larval density from one to three per microcosm reduced per‐capita predation by both species irrespective of alternative food treatment. 5. Alternative food reduced cannibalism in both carabid species and increased survival of carabid larvae in field plots, such that twice as many were captured in plots subsidised with pupae than plots with no alternative food. 6. These results provide new insight into the complex interactions that influence predator survival and herbivore suppression in resource diverse habitats by demonstrating the primacy of intraguild interactions among carabid larvae.     

Density of an intraguild predator mediates feeding group size, intraguild egg predation, and intra- and interspecific competition

Intraguild predation (IGP) is common in most communities, but many aspects of density-dependent interactions of IG predators with IG prey are poorly resolved. Here, we examine how the density of an IG predator can affect feeding group size, IG egg predation, and the growth responses of IG prey. We used laboratory feeding trials and outdoor mesocosm experiments to study interactions between a social intraguild predator (larvae of the wood frog; Rana sylvatica) and its prey (spotted salamander; Ambystoma maculatum). Larvae of R. sylvatica could potentially affect A. maculatum by consuming shared larval food resources or by consuming eggs and hatchlings. However, successful egg predation requires group feeding by schooling tadpoles. We established from five to 1,190 hatchlings of R. sylvatica in mesocosms, then added either 20 A. maculatum hatchlings to study interspecific competition, or a single egg mass to examine IGP. Crowding strongly suppressed the growth of R. sylvatica, and IGP was restricted to the egg stage. In the larval competition experiment, growth of A. maculatum was inversely proportional to R. sylvatica density. In the predation experiment, embryonic mortality of A. maculatum was directly proportional to the initial density of R. sylvatica and the mean number of tadpoles foraging on egg masses. IGP on eggs reduced A. maculatum hatchling density, which accelerated larval growth. Surprisingly, the density of R. sylvatica had no overall effect on A. maculatum growth because release from intraspecific competition via egg predation was balanced by increased interspecific competition. Our results demonstrate that the density of a social IG predator can strongly influence the nature and intensity of interactions with a second guild member by simultaneously altering the intensity of IGP and intra- and interspecific competition.L . A. Burley and A. T. Moyer contributed equally to this work.     

Resource Limitation,Controphic Ostracod Density and Larval Mosquito Development

Aquatic environments can be restricted with the amount of available food resources especially with changes to both abiotic and biotic conditions. Mosquito larvae, in particular, are sensitive to changes in food resources. Resource limitation through inter-, and intra-specific competition among mosquitoes are known to affect both their development and survival. However, much less is understood about the effects of non-culicid controphic competitors (species that share the same trophic level). To address this knowledge gap, we investigated and compared mosquito larval development, survival and adult size in two experiments, one with different densities of non-culicid controphic conditions and the other with altered resource conditions. We used Aedes camptorhynchus, a salt marsh breeding mosquito and a prominent vector for Ross River virus in Australia. Aedes camptorhynchus usually has few competitors due to its halo-tolerance and distribution in salt marshes. However, sympatric ostracod micro-crustaceans often co-occur within these salt marshes and can be found in dense populations, with field evidence suggesting exploitative competition for resources. Our experiments demonstrate resource limiting conditions caused significant increases in mosquito developmental times, decreased adult survival and decreased adult size. Overall, non-culicid exploitation experiments showed little effect on larval development and survival, but similar effects on adult size. We suggest that the alterations of adult traits owing to non-culicid controphic competition has potential to extend to vector-borne disease transmission.