reynaldi s, meiser m. liess m. 2011. effects of the pyrethroid fen vale rate on the alarm response...

8/3/2019 Reynaldi S, Meiser M. Liess M. 2011. Effects of the Pyrethroid Fen Vale Rate on the Alarm Response and on the Vulnerability of the Mosquito Larva Culex Pipi

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Aquatic Toxicology 104 (2011) 5660

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Aquatic Toxicology

j o u rn a l h o mep ag e : www.e l sev i e r. co m/ l o ca t e / aq u a t o x

Effects of the pyrethroid fenvalerate on the alarm response and on thevulnerability of the mosquito larva Culex pipiens molestus to the predatorNotonecta glauca

Sebastin Reynaldi a, b , c, , Maximilian Meiser a , Matthias Liess aa Department System Ecotoxicology, Helmholtz Centre for Environmental Research UFZ, Permoserstrae 15, D-04318 Leipzig, Germanyb Department Bioanalytical Ecotoxicology, Helmholtz Centre for Environmental Research UFZ, Permoserstrae 15, D-04318 Leipzig, Germanyc Department of Agronomical Science, National University of Colombia, Calle 59a 20-63, Medelln, Colombia

a r t i c l e i n f o

Article history:Received 9 February 2011Received in revised form 21 March 2011Accepted 27 March 2011

Keywords:InsecticideMosquito larvae survivalAlarm responseVulnerability to predationShort-term exposure

a b s t r a c t

Previous studies have shown that mosquito larvae retreat from thesurface of water as an alarm responseto sudden changes in light intensity. We investigated the effects of the insecticide fenvalerate on thisalarm response in larvae of the mosquito Culix pipiens molestus and on the related vulnerability of theselarvae to the predator Notonecta glauca . For the alarm response, after 1 h of exposure to fenvalerate, noimmediate effects were observed. However, after a 5-h postexposure period following 1h of exposure,the proportion of larvae that showed the alarm response decreased with increasing fenvalerate concen-tration. The median effective concentration (EC50) was 0.1 g/L. After 6 h of continuous exposure, theEC50 decreased to 0.06 g/L. In addition,vulnerability to thepredator N. glauca increasedafter6 h of con-tinuous exposure. The median time needed for N. glauca to prey 50% of the larvae (PT50) decreased from5h48mininthecontrolto3h8minat0.3 g/Lfenvalerate. No mortalityoccurred after 48h when larvaewere exposed for 6 h in the absence of N. glauca . The median lethal concentration (LC50) was 0.3 g/Lafter 48h of continuous exposure. The decrease in the PT50 was related strongly to the increase in theproportion of larvae that did not exhibit an alarm response. These results show that the alarm response

can be inhibited by low levels of fenvalerate, and this inhibition seems to increase larval mortality dueto predation. 2011 Elsevier B.V. All rights reserved.

1. Introduction

The use of pyrethroid insecticides has increased markedly inrecent years ( Amweg et al., 2005 ). Pyrethroids are a good alter-native to organophosphate insecticides because they are over 10times more effective against pests than organophosphates, whileat the same time less toxic to mammals, including human beings(Amweg et al., 2005 ). In particular, the nonagricultural use of pyrethroids, forexample to control mosquitoes, hasbeenpromoted

by these characteristics.Pyrethroids are hydrophobic compounds that can adsorb

rapidly onto sediments and vegetation in aquatic environments.This characteristic might decrease their bioavailability to aquaticorganisms ( Adelsbach and Tjeerdema, 2003 ). The concentration of fenvaleratein lake enclosures was foundto decrease more than50%

Corresponding author at: Department Bioanalytical Ecotoxicology, HelmholtzCentre for Environmental Research - UFZ, Permoserstrae 15, D-04318 Leipzig,Germany. Tel.: +49 341 235 1515.

E-mail address: [email protected] (S. Reynaldi).

after the rst 24h followinga singlesurface spray ( Dayet al., 1987 ).For this reason, it is expected that, when pyrethroids enter aquaticecosystems, organisms areonly exposed to them for a short period.However, short-term exposure to pyrethroids such as fenvaleratecan cause long-term effects in aquatic organisms ( Liess and Schulz,1996; Schulz and Liess, 2000 ).

Rapid uptakeof fenvalerate can be expected because, in general,pyrethroids are veryhydrophobic: the log ko/w forfenvalerateis 6.4(Adelsbach and Tjeerdema, 2003 ). Exposure for 1 h was sufcient

to cause long-term effects in Limnephilus lunatus : the emergencepattern was affected more by 1 h of exposure to 1 g/L fenvaleratethan by 10h of exposure to 0.1 g/L fenvalerate ( Schulz and Liess,2000 ). This shows that biological responses might vary more withincreasing concentration of fenvalerate than with increasing dura-tion of exposure. However, the median lethal concentration (LC50)of permethrin was 4.67, 1.15 and 0.45 g/L after 1,4 and 24h expo-sure, respectively ( Parsons and Surgeoner, 1991 ). This shows thatlethal effects caused by pyrethroids canalso increase withdurationof exposure in mosquito larvae.

Mosquito larvae breathe atmospheric air through tubes withsiphonal valves that are located at their tails ( Corbet et al., 2000 ).

0166-445X/$ see front matter 2011 Elsevier B.V. All rights reserved.

doi: 10.1016/j.aquatox.2011.03.017
http://dx.doi.org/10.1016/j.aquatox.2011.03.017http://dx.doi.org/10.1016/j.aquatox.2011.03.017http://www.sciencedirect.com/science/journal/0166445Xhttp://www.elsevier.com/locate/aquatoxmailto:[email protected]://dx.doi.org/10.1016/j.aquatox.2011.03.017http://dx.doi.org/10.1016/j.aquatox.2011.03.017mailto:[email protected]://www.elsevier.com/locate/aquatoxhttp://www.sciencedirect.com/science/journal/0166445Xhttp://dx.doi.org/10.1016/j.aquatox.2011.03.017


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S. Reynaldi et al. / Aquatic Toxicology 104 (2011) 5660 57

For this reason, mosquito larvae spend a substantial part of theirtime just under the surface of the water with their head hungdownwards. However, sudden changes in light intensity inducethe larvae to retreat from the surface; they dive towards the bot-tom and return to the surface some minutes later ( Corbet et al.,2000 ). This behavior is considered to be an alarm response becauseit results from theperception of environmental changes ( Mellanby,1958 ). The frequency of this response can depend on tempera-ture ( Mellanby, 1958 ) or availability of food ( Olsson and Klowden,1998 ). Thealarm responsewas shownto berelatedto theavoidanceof predation by larvae of the mosquito Anopheles gambiae becausethe absence of this response increased the vulnerability of theselarvae to the wolf spider Pardosa messingerae (Futami et al., 2008 ).Larvaeof themosquito Culex pipiens showed a specic antipredatorresponse to the backswimmer Notonecta glauca (Sih, 1986 ). Fen-valerate is a neurotoxic pesticide that affects the ion channels of neurons ( Adelsbach and Tjeerdema, 2003 ), which can affect thebehavior of the exposed organisms ( Wendt-Rasch et al., 1998 ).Thus,we hypothesized thatthe pyrethroid fenvalerate would affectthe alarm response and the vulnerability of larvae of the mosquitoCulex pipiens molestus to the predator N. glauca .

2. Materials and methods

2.1. Test organism

Larvae of C. pipiens molestus were bred in glass cylinders, 10cmhigh and 10cm indiameter. These cylinderscontained 100larvae in400 ml of Elendt M4medium( Elendt andBias, 1990 ). The cylinderswere placed in an temperature-controlled room at 20 1 C in alight: dark regime of 16:8 h, with light intensity of approximately15 mmol/m 2 /s. First-stage larvae were fed daily with three dropsof the invertebrate food Liquidzell (Dohse Aquaristik, Grafschaft-Gelsdorf, Germany). From the second stage onwards, larvae werefeddailywith1.5cm 3 ofa 1:1mixtureof driedand powderedleavesof Urtica dioica and ground dog food (Ssniff Spezialitten, Soest,Germany).

2.2. Fenvalerate exposure

To investigate the effects of fenvalerate on the alarm response,fourth-stage larvae were exposed to 0, 0.01, 0.03, 0.06, 0.1, 0.3, and0.6 g/L fenvalerate (CAS: 51630-58-1) in the following schemas:(1) 1h of exposure; (2) 1h of exposure followed by 5h in theabsence of toxicant; (3) 6 h of exposure; and (4) 6 h of exposurefollowed by 18 h in the absence of toxicant. Four groups of 10 lar-vaewere exposedat eachconcentrationas replicates. To investigatethe effects of fenvalerate on vulnerabilityto N. glauca , groupsof 100larvaein thefourth stage were exposed to 0,0.01,0.06, and0.3 g/Lfenvalerate for 6 h.

Fenvalerate (99.9%) was obtained from Riedel-de Han

(Seelze, Germany). A stock solution of 40 mg/L was prepared indimethylsulfoxide (DMSO; 99.8%; Merck , Darmstadt, Germany).The maximum concentration of DMSO in the test mediumwas 0.0003% (v/v). The solutions to which the larvae wereexposed were analyzed by solid-phase extraction of 1-L volumeswith C18 columns (Baker, Phillipsburg, NJ, USA), followed bygas chromatographyelectron-capture detection (CP-3800 Saturn2200, Varian, Walnut Creek, USA). The actual concentration of fen-valerate was 93.1% 16.5 (mean standard error) of the nominalconcentration for the range 0.061 g/L.

2.3. Measurement of effects of fenvalerate on the alarm response

After exposure to fenvalerate, the groups of larvae were placed

in test tubes (3cm in diameter, 6cm high) that contained 40ml of

Elendt M4 medium ( Elendt and Bias, 1990 ). These test tubes wereinitially kept in the dark for approximately 5 min. Subsequently, alight source was placed above the test tubes. The intensity of thelight source was 20 klux ( Olsson and Klowden, 1998 ). After all thelarvae had surfaced and remained motionless, the test tube wascovered for a short period of time. The proportion of larvae thatdived when the illumination was interrupted was recorded andexpressed as a percentage.

2.4. Measurement of effects of fenvalerate on larval survival

The effects of the pesticide on larval survival were tested byexposing groups of 10 larvae continuously to 0 (control), 0.01, 0.06,0.3, and 1 g/Lfenvalerate for6 h or48 h.In both exposureschemas,three groups of 10 larvae were tested per concentration and thesurvival was recorded after 48 h. Exposure for 6 h was tested inorder to ensure the absence of mortality during the vulnerabilityexperiment due to direct effects of the pesticide.

2.5. Measurement of effects of fenvalerate on vulnerability to N. glauca

After exposure to fenvalerate,100larvaeper concentrationwereplaced in plastic containers (30cm long, 20 cm wide and 8 cmdepth) that were lled to a depth of 5 cm with M4 medium. Threeindividuals of N. glauca were added per container. These individu-als were adults (length: 1516mm) and had been starved for twodays before the experiment. The plastic containers were divideddiagonally from the bottom left side to the top right by sheets of plastic (20 cm long, 15 cm high, and 0.5 cm thick) that contained1.5-cm holes. Although both N. glauca and mosquito larvae couldpass through these holes, this setup was intended to mimic natu-ral obstacles such as rocks and vegetation. The density of N. glaucaindividuals was chosen in accordance with Sih (1986) in order toavoid effects of predator density on the predation process. Everyhour for5 h, the number of livinglarvae was recorded and N. glaucaindividuals were exchanged randomly among the containers.

2.6. Statistical analysis

The median concentration of fenvalerate that reduced the num-ber of larvae that exhibited the alarm response to 50% (EC50), themedian time that N. glauca neededto prey 50%of thelarvae (PT50),and the median lethal concentration (LC50) were estimated withthe Hill model (1) .

f ( x) = 100 xnH

xnH + anH 100 (1)

Here, nH is the Hill number and a was the EC50, PT50, or LC50.The PT50 was related to the mean proportion of the larvae (%)

without an alarm response by a linear model. The models wereapplied on the software SigmaPlot (Systat Software, USA).

3. Results

3.1. Effect of fenvalerate on the alarm response

The proportion of larvae that showed an alarm response didnot decrease after 1 h of exposure to fenvalerate at any concentra-tion. However, for 1h of exposure followed by a 5-h postexposureperiod, the proportion of larvae that exhibited the alarm responsebegan to decrease at a concentration of 0.03 g/L and decreasedfurther at higher concentrations ( Fig. 1). In this exposure schema,the median effective concentration (EC50) was 0.1 g/L (Table 1 ).

After 6h of exposure without a postexposure period, the pro-


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Fenvalerate (g/L)

0.001 0.01 0.1 1

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ControlControl

6h exp1h exp

1h exp. & 5h recovery 6h exp. & 18h recovery

1-h exposure 6-h exposure

1-h exposure + 5-h postexposure 6-h exposure + 18-h postexposure

Fig.1. Proportion of mosquitolarvae thatexhibitedthe alarmresponse withincreasing concentrationsof fenvalerate underthe following exposure schemas:1 h of exposure;1 h of exposure followed by 5h in the absence of toxicant; 6 h of exposure; and 6h of exposure followed by 18h in the absence of toxicant.

Table 1The EC50 and the Hill number (H), their probabilities of type I error ( p), and the coefcient of determination ( r 2 ) of the logistic regression, which were estimated by applyingthe Hill equation (1) to the data obtained in the alarm response experiment.

Exposure schemas EC 50 p nH p r 2

1-h exp. 6-h exp. 0.05 0.0001 1.53 0.0001 0.961-h exp. and 5-h post-exp. recovery 0.08 0.0001 1.08 0.0001 0.896-h exp. and 18-h post-exp. recovery 0.33 0.0001 0.62 0.0001 0.87

portion of larvae that showed the alarm response also started to

decrease at a concentration of 0.03 g/L (Fig. 1), but the EC50was 0.06 g/L (Table 1 ). The EC50 increased to 0.37 g/L with6 h of exposure followed by an 18-h postexposure period ( Fig. 1and Table 1 ). No mortality was observed during this experi-ment.

3.2. Effects of fenvalerate on larval survival

No mortality had occurred after 48h when larvae wereexposed to fenvalerate for 6 h in the absence of N. glauca .One dead larva was observed after 48 h of continuous exposureto 0.01 g/L fenvalerate, and the median lethal concentra-tion (LC50) was 0.3 g/L (nH = 1.35, p < 0.0001, and r 2 = 0.93)(Fig. 2).

3.3. Effect of fenvalerate on larval vulnerability to N. glauca

The median time that N. glauca needed to prey 50% of thelarvae (PT50) in the control groups was 5 h 48min. The PT50decreased to 5h 36min and 4h 27min when the larvae wereexposed to 0.01 g/Land 0.06 g/L fenvalerate, respectively. Expo-sure to 0.3 g/L fenvalerate decreased the PT50 to 3h 8 min ( Fig. 3and Table 2 ).

3.4. Relationship between the alarm response and larvalvulnerability

The PT50 was signicantly ( p < 0.01) related to the pro-portion of larvae that failed to exhibit the alarm responseby the following linear model: y = 0.031 x+ 5.96. The PT50

and the proportion of larvae that exhibited the alarm


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Fenvalerate (g/L)

0,001 0,01 0,1 1 10

S u r v i v a

l a f t e r

4 8 h ( % )

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6 h-pulseContinuous

Control

Fig. 2. Number of larvae that avoided predation by N. glauca over time, which wasexpressed as the number of living larvae. The mosquito larvae were exposed to 0,0.01, 0.06, and 0.3 g/L fenvalerate for 6 h. Subsequently, the larvae were placedin fresh medium and N. glauca individuals were introduced. The number of livinglarvae was monitored every hour for 5 h for each concentration.

Time (hours)

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N u m

b e r o

f l i v i n g

l a r v a e

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Control0.01 g/L0.06 g/L0.3 g/L

Fig. 3. Relationshipbetweenthe proportion of larvaethatfailedto exhibit an alarmresponseand themedian timethat N. glauca needed toprey50% ofthe larvae(PT50).The larvae were exposed for 6h to 0.01, 0.06, and 0.3 g/L fenvalerate.

Table 2The PT50 and the Hill number (H), their probabilities of type I error ( p), and thecoefcient of determination ( r 2 ) of the logistic regression, which were estimatedby applying the Hill equation (1) to the data obtained in the larval vulnerabilityexperiment.

Exposure schemas PT 50 p nH p r 2

Control 5 h 48 min 0.0003 3.8 0.0252 0.900.01 g/L 5 h 36 min 0.0004 2.5 0.0122 0.930.06 g/L 4 h 27 min 0.0001 2.2 0.0081 0.950.3 g/L 3 h 8 min 0.0001 1.9 0.0006 0.99

response decreased with increasing fenvalerate concentration(Fig. 4).

4. Discussion

Mosquito larvae retreat from thesurface of thewater upon sud-den changes in light intensity, and this was dened as an alarmresponse ( Mellanby, 1958 ). The results of the present study con-rm the existence of this response, and also show that exposureto fenvalerate can affect it. The proportion of larvae that showedan alarm response decreased with increasing concentration of fen-valerate.However, thisdecreasedepended on theexposureschema

used ( Fig. 1). No effects on the alarm response were observed after

Laevae (%)

0 20 40 60 80 100

P T 5 0 ( h )

0

2

4

6

y=-0.031x+5.96

r 2

=0.96 p< 0.001

Fig. 4. Proportion of larvae that survived at 48h after a continuous and a 6-h-pulseexposure to fenvalerate in the absence of N. glauca individuals. For the continuousexposure, larval survival was signicantly ( p < 0.001)related tothe concentration of fenvalerate by applying theHill equation (1) ; t heestimatedLC50(48 h)was0.3 g/L.

1 h of exposure without a postexposure period. However, after the1-h exposure followed by a 5-h postexposure period, the propor-tion of larvae that failed to exhibit the alarm response increasedwith increasing fenvalerate concentration ( Fig. 1). The results of a previous study showed that 1 h of exposure to 1 g/L fenvaler-ate can be more toxic than 10 h of exposure to a concentration of 0.1 g/L (Schulz and Liess, 2000 ). Fast uptake can be expected forvery hydrophobic pesticides, such as fenvalerate ( Adelsbach andTjeerdema, 2003 ). However, in the present work, the EC50 washigher for 1 h of exposure followed by a 5-h postexposure periodthan for 6h of continuous exposure ( Table 1 ), which suggests thatfenvalerate might be taken up for more than 1 h. Nevertheless, thealarm response can also recover; the EC50 was six times higherwhen the 6-h exposure period was followed by an 18-h postexpo-sure period.

Given that the period when the larvae are more vulnerablemight correspond to the time between the onset of the effects of fenvalerate and the recovery of the alarm response, vulnerabilityto N. glauca was tested for 5 h after the larvae had been exposedto fenvalerate for 6 h. The median time that N. glauca needed toprey 50% of the larvae (PT50) decreased with increasing fenvaler-ateconcentration. ThePT50decreased bymore than1 and 2 h whenthe larvae were exposed to 0.06 and 0.3 g/L fenvalerate, respec-tively ( Table 2 ), which demonstrated a strong increase in the rateof predation of N. glauca on mosquito larvae. Exposure to fenvaler-ate was also shown previously to increase the predation of Baetismayy nymphs by the sh Galaxias zebratus . The activity of themayies increased after exposure to fenvalerate, which probablymade them more visible to the predator ( Schulz and Dabrowski,

2001 ). In the present study, the decrease in PT50 was directlyproportional to the proportion of larvae that failed to exhibit thealarm response ( Fig. 4), which suggests that exposure to fenvaler-ate increases the vulnerability of mosquito larvae to N. glauca byaffecting their avoidance behavior.

Avoidance behavior in response to N. glauca has been observedpreviously in C. pipiens , and it was suggested that this behaviorevolved to reduce the likelihood of capture by N. glauca because C. pipiens and N. glauca co-exist in many aquatic habitats ( Sih, 1986 ).Moreover, this avoidance behavior seems to be genetically deter-mined because larvae of C. pipiens that carried genes for insecticideresistancewere found to be moresusceptible thanwild-type larvaeto predators, including thebackswimmer Plea minutissima (Berticatet al., 2004 ). The avoidance behavior that C. pipiens larvae exhibit

in response to N. glauca consists of an overall reduction of move-


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ment. However, it canalso include a change in habitat use, becausethe larvae were found to cluster close to refuges in the presenceof N. glauca (Sih, 1986 ). This implies that a mosquito larva mightrestrict its movements in response to a particular factor to increaseits survival. Thus, there are two possible explanations for the rela-tionship between vulnerability and the alarm response that wasobserved in the present work. First, the larvae that exhibited noalarm response might have been easier prey for N. glauca . Second,the decrease observed in the alarm response might be a sign of the loss of general environmental perception, whichlarvae need toavoid N. glauca . To elucidate which of these explanations is morerelevant,future experiments should investigate the effects of expo-sure to fenvalerate on other aspects of larval behavior, such asfeeding activity.

Sublethal levels of fenvalerate contamination were used in theexperiments to evaluate the alarm response and larval vulnera-bility. Mortality only occurred after 48 h of continuous exposure(Fig. 4). No mortality occurred during the alarm response exper-iment, or after a period of 48 h following 6 h of exposure in thelarval survival experiment. In the larval vulnerability experiment,the larvae were also exposed to fenvalerate for 6 h, but the post-exposure period was only 6h. A similar 6-h exposure and a seventimes shorter postexposure were applied in the larval vulnerabilityexperiment. This suggests that, in the larval vulnerability experi-ment, theexposure to fenvalerate didnot have anydirect effects onlarvalsurvival, andthe increase in thePT50 was caused exclusivelyby the increase in vulnerability of larvae to N. glauca .

The proportion of larvae that exhibited the alarm response wasshown to be very sensitive to exposure to fenvalerate for as shorta period as 1 h. The results of the present study show that expo-sure to low levels of fenvalerate contamination can increase larvalmortality due to predation. This might allow the volume of insec-ticide sprayed over aquatic habitats to be reduced, which wouldsave money and protect natural diversity while still providingeffective pest control. However, although in the work reportedherein, the effect of exposure to fenvalerate on the predator wasnot investigated, the mobility of N. glauca was previously found tobe extremely sensitive to another pyrethroid, -cyhalothrin, after48 h of continuous exposure in eld and laboratory experiments(Schroer et al., 2004 ). Nevertheless, the results of the present workshowedclear effects of exposure to fenvalerateon thebehavior andvulnerability of the larval prey. The ecological relevance of theseeffects needs to be investigated further.

Acknowledgements

A Postdoctoral scholarship was awarded to S. Reynaldi bythe ALECOL program, academic exchange program betweenthe National University of Colombia and the DAAD (DeutscherAkademischer Austauschdienst/German Academic Exchange).

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