Opportunistic foraging by heteropteran mosquito predators

Nabaneeta Saha AElig Gautam Aditya AElig Goutam K Saha AEligStephanie E Hampton

Received 15 April 2008 Accepted 29 April 2009 Published online 22 May 2009

Springer Science+Business Media BV 2009

Abstract Tropical aquatic environments host a

large number of predatory insects including heteropt-

eran water bugs Anisops bouvieri Kirkaldy 1704

(Heteroptera Notonectidae) Diplonychus (=Sph-

aerodema) rusticus Fabricius 1781 (Heteroptera

Belostomatidae) and Diplonychus (=Sphaerodema)

annulatus Fabricius 1781 (Heteroptera Belostomat-

idae) feeding on a range of organisms In tropical and

subtropical wetlands ponds and temporary pools

these predators play a role in regulation of dipteran

populations particularly mosquitoes and chirono-

mids Their relative abilities to control mosquitoes

depend in part on predator preference for mosquitoes

in relation to other natural prey and the predatorsrsquo

propensities to switch to mosquitoes as mosquito

density increases The prey electivity and switching

dynamics of these predatory water bugs were evalu-

ated in the laboratory under various prey densities

using two instars (II and IV) of chironomid and

mosquito larvae as prey Studies of electivity at

relatively high densities (20 prey L-1) in small (5 L)

vessels demonstrated that all predators showed oppor-

tunistic foraging as the mosquitochironomid ratio

changed with some evidence that mosquito larvae

were positively selected over chironomids In partic-

ular Anisops showed strong electivity for mosquitoes

when presented with any ratio of large mosquito and

chironomid prey in the high density experiment

although the preference was not expressed in lower

density (25 prey L-1) treatments executed in 40 L

vessels In these lower density treatments D rusticus

demonstrated higher electivity for mosquitoes when

the mosquitochironomid ratio was high consistent

with non-significant trends observed in the higher

density experiment The positive electivity of D rust-

icus for mosquitoes was reinforced in an experiment

executed over 16 days at varying prey ratios in which

D rusticus mosquito electivity was high and consis-

tent while D annulatus showed slight avoidance of

mosquito larvae and Anisops remained largely oppor-

tunistic in foraging on prey in proportion with

availability Anisops and D rusticus are potentially

good biocontrol agents for mosquito larvae in that

they preferentially consume mosquitoes under many

circumstances but can readily forage on other prey

when mosquito density is low

N Saha G Aditya G K Saha (amp)

Department of Zoology University of Calcutta

35 Ballygunge Circular Road Kolkata 700019 India

e-mail gkszoorediffmailcom

N Saha

e-mail nabaneetasahagmailcom

G Aditya

e-mail gautamaditya2001yahoocom

G Aditya

Department of Zoology The University of Burdwan

Golapbag Burdwan 713104 India

S E Hampton

National Center for Ecological Analysis and Synthesis

University of California Santa Barbara CA 93101 USA

e-mail hamptonnceasucsbedu

123

Aquat Ecol (2010) 44167ndash176

DOI 101007s10452-009-9250-y

Keywords Prey selection Manlyrsquos a-index Mosquito larvae Chironomid larvae Diplonychus sp Anisops sp

Introduction

Generalist predators in aquatic insect communities

can maintain stability by avoiding competition

given their greater plasticity in prey choice (Sy-

mondson et al 2002) and by remaining abundant in

varied resource environments due to their ability to

switch to different prey (Murdoch 1969 Oaten and

Murdoch 1975 Murdoch et al 1985 Symondson

et al 2002) Heteropterans are particularly impor-

tant and widespread generalist predators in fresh-

water systems playing a major role in shaping the

structure and the abundance of prey species popu-

lation (Scott and Murdoch 1983 Blaustein 1998

Gilbert and Burns 1999 Hampton et al 2000)

These qualities favor the use of heteropteran

predators as biocontrol agents particularly because

native predators do not raise the societal concerns

that accompany introduced biocontrol agents (Wa-

age et al 1988) The ready use of alternate prey in

the absence of favored prey maintains high levels of

native predator populations that can take advantage

of prey regarded as nuisance organisms such as

mosquito larvae when the nuisance populations

increase Thus heteropterans such as notonectids

and belostomatids may be regarded as likely

natural agents for long-term biocontrol of mosquito

larvae Where the failure of mosquitofish to control

mosquitoes has been noted the propensity of

mosquitofish to decimate natural invertebrate ene-

mies of mosquitoesmdashspecifically notonectidsmdashhas

been implicated (Blaustein 1992) The usefulness of

native heteropterans as long-term biocontrol agents

depends in part on their preferential consumption of

mosquito larvae and their ability to readily prey on

non-target species in the absence of mosquito

larvae

In tropical aquatic habitats particularly in wet-

lands rice-fields and temporary pools controphic

mosquito and chironomid immatures co-exist sharing

common predators The abundance of these dipteran

species is known to be affected by predation by

notonectids (Blaustein 1998 Eitam et al 2002

Blaustein et al 2004 Hampton 2004) copepods

(Kumar and Rao 1999 2003 Rao and Kumar 2002

Rey et al 2004) coleopterans (Von Kogel 1987

Lundkvist et al 2003 Aditya and Saha 2006 Aditya

et al 2006) and larval odonates (Fincke et al 1997

Stav et al 2005) Such assemblages of multiple prey

and predators in aquatic environments can be

exploited for biological control using a community

ecology approach (Murdoch et al 1985 Symondson

et al 2002 Blaustein and Chase 2007)

In India and other tropical areas (Mogi et al 1995

1999 Victor et al 1991 Victor and Reuben 1999

Gilbert et al 1999 Sunish and Reuben 2002 Das

et al 2006) hemipteran bugs like Anisops bouvieri

Kirkaldy 1704 (Heteroptera Notonectidae) Diplony-

chus (=Sphaerodema) annulatus Fabricius 1781

(Heteroptera Belostomatidae) and D rusticus Fab-

ricius 1781 (Heteroptera Belostomatidae) are preda-

tors of dipteran immatures (Panickar and Rajagopalan

1977 Hati 1988 Saha and Raut 1992 Nishi and

Venkatesan 1997 Aditya et al 2004 2005) and a

wide range of other aquatic organisms like snails of

the genera Lymnaea Gyraulus Indoplanorbis and

Physa (Raut et al 1988 Roy and Raut 1994 Aditya

and Raut 2001 2002a b) These predators regulate

dynamics of the communities in these aquatic hab-

itats and thus can be considered as biological

resources against pest and vector mosquitoes The

ability of these water bugs to utilize alternate prey

(eg chironomid larvae) when target prey (eg

mosquito larvae) are in low availability would

support their usefulness as biocontrol predators

Equally the effect of the availability of alternate

prey on the survival of target prey species in a

community with a common predator species must be

assessed Relative size of the target and non-target

prey generally affects predator preference as exhib-

ited by the copepods Mesocyclops thermocyclopoides

(Kumar and Rao 2003) the dragonfly nymph Anax

imperator (Stav et al 2005) and the dytiscid beetles

Rhantus sikkimensis (Aditya and Saha 2006) and

R consputus (Von Kogel 1987) The water bugs

considered in the present study have differences in

prey size preferences and predatory attributes with

respect to their larval mosquito prey (Saha et al

2007a b) The presence of chironomid larvae as

alternate prey might influence heteropteran prey

choice in terms of size and species

168 Aquat Ecol (2010) 44167ndash176

123

Keywords Prey selection Manlyrsquos a-index Mosquito larvae Chironomid larvae Diplonychus sp Anisops sp

Introduction

Generalist predators in aquatic insect communities

can maintain stability by avoiding competition

given their greater plasticity in prey choice (Sy-

mondson et al 2002) and by remaining abundant in

varied resource environments due to their ability to

switch to different prey (Murdoch 1969 Oaten and

Murdoch 1975 Murdoch et al 1985 Symondson

et al 2002) Heteropterans are particularly impor-

tant and widespread generalist predators in fresh-

water systems playing a major role in shaping the

structure and the abundance of prey species popu-

lation (Scott and Murdoch 1983 Blaustein 1998

Gilbert and Burns 1999 Hampton et al 2000)

These qualities favor the use of heteropteran

predators as biocontrol agents particularly because

native predators do not raise the societal concerns

that accompany introduced biocontrol agents (Wa-

age et al 1988) The ready use of alternate prey in

the absence of favored prey maintains high levels of

native predator populations that can take advantage

of prey regarded as nuisance organisms such as

mosquito larvae when the nuisance populations

increase Thus heteropterans such as notonectids

and belostomatids may be regarded as likely

natural agents for long-term biocontrol of mosquito

larvae Where the failure of mosquitofish to control

mosquitoes has been noted the propensity of

mosquitofish to decimate natural invertebrate ene-

mies of mosquitoesmdashspecifically notonectidsmdashhas

been implicated (Blaustein 1992) The usefulness of

native heteropterans as long-term biocontrol agents

depends in part on their preferential consumption of

mosquito larvae and their ability to readily prey on

non-target species in the absence of mosquito

larvae

In tropical aquatic habitats particularly in wet-

lands rice-fields and temporary pools controphic

mosquito and chironomid immatures co-exist sharing

common predators The abundance of these dipteran

species is known to be affected by predation by

notonectids (Blaustein 1998 Eitam et al 2002

Blaustein et al 2004 Hampton 2004) copepods

(Kumar and Rao 1999 2003 Rao and Kumar 2002

Rey et al 2004) coleopterans (Von Kogel 1987

Lundkvist et al 2003 Aditya and Saha 2006 Aditya

et al 2006) and larval odonates (Fincke et al 1997

Stav et al 2005) Such assemblages of multiple prey

and predators in aquatic environments can be

exploited for biological control using a community

ecology approach (Murdoch et al 1985 Symondson

et al 2002 Blaustein and Chase 2007)

In India and other tropical areas (Mogi et al 1995

1999 Victor et al 1991 Victor and Reuben 1999

Gilbert et al 1999 Sunish and Reuben 2002 Das

et al 2006) hemipteran bugs like Anisops bouvieri

Kirkaldy 1704 (Heteroptera Notonectidae) Diplony-

chus (=Sphaerodema) annulatus Fabricius 1781

(Heteroptera Belostomatidae) and D rusticus Fab-

ricius 1781 (Heteroptera Belostomatidae) are preda-

tors of dipteran immatures (Panickar and Rajagopalan

1977 Hati 1988 Saha and Raut 1992 Nishi and

Venkatesan 1997 Aditya et al 2004 2005) and a

wide range of other aquatic organisms like snails of

the genera Lymnaea Gyraulus Indoplanorbis and

Physa (Raut et al 1988 Roy and Raut 1994 Aditya

and Raut 2001 2002a b) These predators regulate

dynamics of the communities in these aquatic hab-

itats and thus can be considered as biological

resources against pest and vector mosquitoes The

ability of these water bugs to utilize alternate prey

(eg chironomid larvae) when target prey (eg

mosquito larvae) are in low availability would

support their usefulness as biocontrol predators

Equally the effect of the availability of alternate

prey on the survival of target prey species in a

community with a common predator species must be

assessed Relative size of the target and non-target

prey generally affects predator preference as exhib-

ited by the copepods Mesocyclops thermocyclopoides

(Kumar and Rao 2003) the dragonfly nymph Anax

imperator (Stav et al 2005) and the dytiscid beetles

Rhantus sikkimensis (Aditya and Saha 2006) and

R consputus (Von Kogel 1987) The water bugs

considered in the present study have differences in

prey size preferences and predatory attributes with

respect to their larval mosquito prey (Saha et al

2007a b) The presence of chironomid larvae as

alternate prey might influence heteropteran prey

choice in terms of size and species

168 Aquat Ecol (2010) 44167ndash176

123

Methods

Adult water bugs A bouvieri D annulatus and D

rusticus were collected from the wetlands along the

Eastern Metropolitan Bypass Kolkata India with an

insect net and maintained in the laboratory within

plastic buckets containing 20 L of pond water

ad libitum mosquito and chironomid larvae as food

and some specimens of the plant Vallisneria spiralis

serving as resting sites for the water bugs The

rostrum by body length (RB) ratio of A bouvieri

ranged between 006 and 012 (A bouvieri rostrum

length 04ndash08 mm mean 062 plusmn 015 SE body

length 58ndash69 mm mean 622 mm plusmn 038 SE) The

same ratio (RB) ranged between 014 and 018 for D

rusticus and between 016 and 02 for D annulatus

(D rusticus rostrum length 193ndash29 mm mean

242 mm plusmn 038 SE body length 148ndash162 mm

mean 153 mm plusmn 053 SE D annulatus rostrum

length 35ndash45 mm mean 402 mm plusmn 028 SE body

length 212ndash231 mm mean 223 mm plusmn 062 SE)

Mosquito larvae were collected from the sewage

drains of Ballygunge Science College campus Bal-

lygunge Kolkata India In the experiments two sizes

of the prey were considered The IV instar larvae

(51ndash60 mm 23ndash27 mg) of Cx quinquefasciatus

(large prey) were separated from the heterogeneous

population by sieving The smaller instars obtained

after sieving were maintained for growth to IV instar

stage following EntGuide3 (wwwpherecorg) The

small sized prey larvae to be used in the experiments

were obtained by rearing the egg rafts collected from

the drains Ten to fifteen rafts were placed within

enamel trays of 30 9 20 9 10 cm capacity contain-

ing de-chlorinated tap water After hatching the zero-

day-old larvae were provided with yeast granules as

food and water was changed every 24 h The 3- to 4-

day-old larvae (15ndash25 mm 11ndash15 mg) were con-

sidered as the small sized prey and used in the

experiments

Larvae of Chironomus sp (Subfamily Chironom-

inae Tribe Chironomini) were collected from the

sewage drains of the same site on a regular basis

during the course of the experiment The larvae were

segregated according to the sizes (large sized larvae

[20 mm in length 31ndash51 mg corresponding to the

IV instars and small larvae 20 mm in length

19ndash23 mg equivalent to the II instars) using a

pipette and kept separately within enamel trays

(30 9 20 9 10 cm) containing tap water and fine

sediments from the sewage drains These smaller and

larger larvae were used in the experiments

The experimental animals were maintained in the

laboratory under constant conditions of temperature

(25ndash30C) humidity (80ndash85) and photoperiod

(14 h L 10 h D) Prior to the experiments the

predators were fed to satiation and starved for 24 h

Controls without predators were run with a number of

replicates equal to those of treatments The experi-

ments were conducted within plastic trays (36 9

27 9 6 cm) or glass aquaria (38 9 36 9 36 cm)

with 5 or 40 L pond water (pH 95ndash105) In all the

experimental and control setsmdashmesocosms five

sticks of the macrophytes Jussia repens and a few

leaves of Vallisneria spiralis and five to six small

pebbles were added to the water to simulate natural

conditions The macrophytes and the stones provided

refuges and resting places for the predators and the

prey

Experimental design

Experiment I Prey selection at high densities

The first experiment was performed within plastic

trays containing 5 L of pond water with one adult

predator per tray and 100 prey arranged in five

different proportions (1000 7525 5050 2575

0100) of two prey types The four prey combinations

used weremdashsmall and large mosquito larvae small

and large chironomid larvae small mosquito and

chironomid larvae and large mosquito and chirono-

mid larvae The number of prey alive was counted

after 24 h to record the predation rate Nine replicates

were performed per predator and prey combination

and ratio Data obtained were used to calculate prey

electivity as Chessonrsquos a (Chesson 1983)

ai frac14 ln pi=R ln pj

where ai is the electivity for prey type i and p is the

proportion of prey type i or j remaining at the end of

the experimental period for m number of prey types

Electivity is a measure of the extent to which prey are

eaten out of proportion to their availability in the

environment and is affected by multiple factors in

the predation cycle (Gerritsen and Strickler 1977)

such as encounter rates predator preference and

Aquat Ecol (2010) 44167ndash176 169

123

handling ability Electivity is sometimes termed

lsquolsquopreferencersquorsquo (Hassell and Southwood 1978) in spite

of underlying behavioral complexities The value of aranges from 0 to 1 with the value for non-selective

feeding being 05 in presence of two prey types

Values above 05 indicate positive selection while

values below 05 indicate negative selection The

deviations of a from non-selective feeding (05) were

assessed by constructing bootstrapped confidence

intervals (Efron and Tibshirani 1991) for each mean

a using R software (boot bootci lsquolsquobasicrsquorsquo bootstrap-

ping for confidence intervals R = 9999) that allow

one to determine whether the confidence intervals

overlap the non-selective value 05 or each other

Experiment II Prey selection at low densities

Here the three predators were exposed to mosquito

and chironomid larvae in the ratio of 2575 5050 and

7525 within glass aquaria (38 9 36 9 36 cm) con-

taining 40 litres of water The preferred size ranges of

the prey species were as deduced from Experiment 1

ie the notonectids were offered a combination of

small mosquito and chironomid larvae whereas the

large sized prey larvae were used for the belostom-

atids (see lsquolsquoResultsrsquorsquo) The a index and confidence

intervals were calculated as for Experiment I to

determine whether electivity differed under lower

prey densities

Experiment III Prey preference and switching over

time

This experiment was framed following a modified

design of Murdoch et al (1975) where the predators

were divided into two groups In series A a single

predator was offered mosquito and chironomid larvae

in four ratios throughout 16 days each ratio being

continued for 4 days in the following sequence 14

23 32 and 41 In series B the predators were run

through a reverse ratio for the two prey species The

number of each species of prey killed was recorded

every 24 h and prey replenished For each predator

we conducted repeated measures ANOVA in MA-

NOVA context (JMP 70 SAS Institute Zar 1999) to

determine whether electivity (a) changed differen-

tially over time as mosquitochironomid ratio

increased (Series A) or decreased (Series B) over

16 days (Time x Series) For Anisops lower

replication (n = 6) prevented the use of all 16 daysrsquo

data instead we used data from days 3 4 7 8 11 12

15 and 16 In doing so the behavior of Anisops was

evaluated on the last 2 days following a prey ratio

change Replication of the belostomatid treatments

was sufficient (n = 9) to include all 16 daysrsquo data

Mauchlyrsquos criterion suggested that compound sym-

metry must be rejected (P 0001) for all three

species reinforcing the decision to treat the repeated

measures in multivariate context an approach that

reduces power but makes no assumptions about the

form of the covariance matrix (Potvin et al 1990 Zar

1999) A Dunn-Sidak correction was used to adjust afor multiple tests accounting for the non-indepen-

dence of the three repeated measures ANOVAs

Results

The predators and the prey remained active within the

experimental sets While the mosquitoes characteris-

tically remained primarily on the upper surface at the

interface between the water and wall of the containers

or the floating macrophytes the chironomid larvae

remained in the substratum nearer to the stones Both

prey distributions tended to be patchy rather than

uniform in both experimental and control sets The

predators exhibited differential movements while

chasing prey The belostomatids showed varied

movements while chasing compared to the notonect-

ids that showed mostly horizontal movements The

belostomatids could turn and chase the prey even at

the bottom portion of the containers which was not

observed in the notonectids However all the preda-

tors consumed both the prey types mosquito and

chironomid larvae

Experiment I Predation rate and selection at high

densities

In absence of any alternate prey a single adult A

bouvieri could consume 29ndash41 small and 16ndash36 large

chironomid larvae per day Equivalent values for

mosquito prey were 30ndash60 and 7ndash15 respectively

The belostomatid bugs D rusticus preyed upon

38ndash55 large and 47ndash89 small mosquito larvae and

34ndash85 large and 48ndash61 small chironomid larvae per

day In contrast to this D annulatus preyed upon

29ndash51 and 44ndash61 small mosquito and chironomid

170 Aquat Ecol (2010) 44167ndash176

123

respectively For the larger prey the values ranged

from 43 to 61 and 79 to 99 respectively However

when more than one type of prey was available to the

predators they consumed different numbers of each

prey type (Fig 1) from which electivity was

estimated

Anisops disproportionately consumed smaller chir-

onomids and big mosquitoes over big chironomids

but showed no strong preference for small mosqui-

toes or small chironomids when presented together

Some saturation may have occurred with mosquitoes

when mosquitoes became especially abundant

(7525) in these high density treatments (Fig 1)

Where only mosquitoes were available at equality

(5050) Anisops disproportionately consumed the

smaller mosquito but at high densities and low

densities of big mosquitoes Anisops ate mostly the

bigger mosquitoes Big mosquitoes were strongly

favored over big chironomids though some satura-

tion may be evident at high densities of big mosqui-

toes as electivity declined

Diplonychus rusticus showed almost no evidence

for discriminating consumption although some pref-

erence for smaller prey was evident at equality

(Fig 1) D rusticus slightly favored small chirono-

mids over small mosquitoes and more strongly

favored small mosquitoes over big mosquitoes At

unequal densities D rusticus was quite opportunistic

(ie exhibiting no apparent preference)

Diplonychus annulatus favored big chironomids

over small chironomids at all densities with the

apparent preference significantly increasing when big

chironomids were at highest density (Fig 1) No

positive electivity was evident for small mosquitoes

over small chironomids except where densities of

mosquitoes became quite high possibly indicating

some saturation in consumption of the mosquitoes at

high density Small mosquitoes were strongly favored

over big mosquitoes and there was discernible

positive electivity for big chironomids over big

mosquitoes Together we could interpret these results

as generally opportunistic predation when mosqui-

toes and chironomids are presented to D annulatus

though some larger prey may be more difficult to

handle for this predator

Experiment II Prey selection at lower densities

At the lower densities offered in Experiment 2

all predators showed some opportunistic feeding (a 05) especially when prey were in equality (Fig 2)

Among these predators D annulatus demonstrated

the strongest avoidance of mosquitoes when chiron-

omids dominated the prey assemblage (25 mosqui-

toes to 75 chironomids) D rusticus expressed some

positive electivity for mosquitoes as they became

more abundant an apparent preference that was not

evident at the much higher densities presented in

Experiment 1

Fig 1 For experiment 1 Manlyrsquos selectivity index (a) for the

first prey that is listed in X-axis labels For example 2575 Pref

for Big Over Small Chironomid refers to the positive electivity

for big chironomids in treatments with 25 big and 75 small

chironomid prey Prey were offered in varying ratios shown

on the X-axis at densities of 20 prey L-1 in 5 L vessels

Selectivity of 05 indicates no preference or predation at rates

proportional to each preyrsquos abundance in the environment

Confidence intervals were derived through bootstrapping

Aquat Ecol (2010) 44167ndash176 171

123

Experiment III prey preference and switching

over time

All predators increased and decreased consumption of

prey in response to prey dominance shifts to some

degree (Fig 3) but none of the predators showed any

significant electivity changes over time in response to

increases or decreases in the mosquito chironomid

ratio Rather D rusticus maintained a relatively high

average electivity in favor of mosquitoes (mean

a = 067 plusmn 013 SD) D annulatus exhibited a rela-

tively low average electivity for mosquito larvae (mean

a = 026 plusmn 009 SD) and Anisops remained oppor-

tunistic in its foraging (mean a = 052 plusmn 0009 SD)

Discussion

The heteropteran water bugs A bouvieri D annul-

atus and D rusticus belong to the same guild As

predators in aquatic environments they share com-

mon prey but occupy different microhabitats and

employ different modes of predation The belostom-

atids D annulatus and D rusticus are associated

with aquatic macrophytes like Jussiaea repens

Vallisneria spiralis Pistia stratoites and Ipomoea

aquatica in the littoral zone of annual or perennial

aquatic bodies Associated with these macrophytes

are snails of the genus Lymnaea Indoplanorbis

Gyraulus and Physa as well as the chironomid and

mosquito immatures which are common prey items

of D annulatus and D rusticus (Aditya and Raut

2002a b Aditya et al 2004) Densities of dipteran

immatures are far greater at all times than gastropods

in the majority of habitats for the belostomatids

(Sunish and Reuben 2002 Das et al 2006) The

notonectids A bouvieri are adapted to the open water

zone and are associated mostly with open water

macrophytes like Wolffia microscopica and Lemna

major and L gibba Mouthparts of A bouvieri differ

from the belostomatids in that they have a smaller

sized rostrum and forelegs well adapted for smaller

prey The larger bent rostrum is characteristic of the

belostomatids and aids in catching snail prey The

spatial orientations of these water bugs differ as well

While the belostomatids dive into the depths of water

bodies the notonectids demonstrate horizontal move-

ment near the surface Only in some instances do

notonectids show vertical movements when revers-

ing the direction of swimming The notonectids A

bouvieri can also fall prey to belostomatids when

preferred prey items are low (Saha and Raut 1992)

Irrespective of these differences these water bugs

share chironomid and mosquito immatures as prey

together influencing the structure of the insect com-

munities in wetlands ponds and bogs Our experi-

mental results suggest that these predators all can prey

heavily on immature dipterans influencing commu-

nity structure and potentially controlling mosquito

densities In general the predators were extremely

Fig 2 For experiment 2

Manlyrsquos selectivity index

(a) for mosquito larvae over

chironomids Prey were

offered in varying ratios

shown on the X-axis at

densities of 25 prey L-1 in

40 L vessels Selectivity of

05 indicates no preference

or predation at rates

proportional to each preyrsquos

abundance in the

environment Confidence

intervals were derived

through bootstrapping The

actual number of prey

consumed is shown belowfor each treatment

172 Aquat Ecol (2010) 44167ndash176

123

Experiment III prey preference and switching

over time

All predators increased and decreased consumption of

prey in response to prey dominance shifts to some

degree (Fig 3) but none of the predators showed any

significant electivity changes over time in response to

increases or decreases in the mosquito chironomid

ratio Rather D rusticus maintained a relatively high

average electivity in favor of mosquitoes (mean

a = 067 plusmn 013 SD) D annulatus exhibited a rela-

tively low average electivity for mosquito larvae (mean

a = 026 plusmn 009 SD) and Anisops remained oppor-

tunistic in its foraging (mean a = 052 plusmn 0009 SD)

Discussion

The heteropteran water bugs A bouvieri D annul-

atus and D rusticus belong to the same guild As

predators in aquatic environments they share com-

mon prey but occupy different microhabitats and

employ different modes of predation The belostom-

atids D annulatus and D rusticus are associated

with aquatic macrophytes like Jussiaea repens

Vallisneria spiralis Pistia stratoites and Ipomoea

aquatica in the littoral zone of annual or perennial

aquatic bodies Associated with these macrophytes

are snails of the genus Lymnaea Indoplanorbis

Gyraulus and Physa as well as the chironomid and

mosquito immatures which are common prey items

of D annulatus and D rusticus (Aditya and Raut

2002a b Aditya et al 2004) Densities of dipteran

immatures are far greater at all times than gastropods

in the majority of habitats for the belostomatids

(Sunish and Reuben 2002 Das et al 2006) The

notonectids A bouvieri are adapted to the open water

zone and are associated mostly with open water

macrophytes like Wolffia microscopica and Lemna

major and L gibba Mouthparts of A bouvieri differ

from the belostomatids in that they have a smaller

sized rostrum and forelegs well adapted for smaller

prey The larger bent rostrum is characteristic of the

belostomatids and aids in catching snail prey The

spatial orientations of these water bugs differ as well

While the belostomatids dive into the depths of water

bodies the notonectids demonstrate horizontal move-

ment near the surface Only in some instances do

notonectids show vertical movements when revers-

ing the direction of swimming The notonectids A

bouvieri can also fall prey to belostomatids when

preferred prey items are low (Saha and Raut 1992)

Irrespective of these differences these water bugs

share chironomid and mosquito immatures as prey

together influencing the structure of the insect com-

munities in wetlands ponds and bogs Our experi-

mental results suggest that these predators all can prey

heavily on immature dipterans influencing commu-

nity structure and potentially controlling mosquito

densities In general the predators were extremely

Fig 2 For experiment 2

Manlyrsquos selectivity index

(a) for mosquito larvae over

chironomids Prey were

offered in varying ratios

shown on the X-axis at

densities of 25 prey L-1 in

40 L vessels Selectivity of

05 indicates no preference

or predation at rates

proportional to each preyrsquos

abundance in the

environment Confidence

intervals were derived

through bootstrapping The

actual number of prey

consumed is shown belowfor each treatment

172 Aquat Ecol (2010) 44167ndash176

123

opportunistic in their foraging a quality that would

allow them to persist at high densities on non-target

prey when mosquito densities are low Anisops and D

rusticus showed the highest predation rates on mos-

quito larvae overall and D rusticus showed the most

consistent positive electivity for mosquitoes across

changing prey ratios in the 16 day experiment (Fig 3)

Anisops showed strong electivity in favor of mosquito

larvae at times (Figs 1 2 3) consistent with its

pelagic habit that may bring it in more frequent contact

with surface dwelling mosquito larvae versus bottom-

dwelling chironomids

Size of the prey was also a significant factor for

Anisops and D annulatus (Fig 1) For Anisops

smaller sizes were generally preferred within each

prey taxon consistent with its morphology that

improves its agility with small prey In contrast D

annulatus preferred large over small chironomids but

small over large mosquitoes Such an idiosyncracy in

size preference may suggest behavioral traits that

vary among the life stages of the prey and affect the

predatorrsquos effectiveness

The density of the prey species affected the

predation rate and prey electivity of the predators

Fig 3 For experiment 3 number of prey consumed and

Manlyrsquos selectivity index adjusted for prey depletion (a) for

mosquitoes over chironomids throughout a 16 day experiment

Mosquito proportions increased in Series A and decreased in

Series B Prey were offered in varying ratios shown for each 4-

day period Selectivity of 05 indicates no preference or

predation at rates proportional to each preyrsquos abundance in the

environment Standard error bars are shown for mean a

Repeated measures ANOVA revealed no significant

differences in a for Anisops (Time x Treatment

F(73) = 704 P = 021 Treatment F(19) = 006 P = 099

Time F(73) = 060 P = 099) D rusticus (Time x Treatment

F(151) = 14351 P = 021 Treatment F(115) = 589

P = 009 Time F(151) = 38190 P = 012) nor D annulatus(Time x Treatment F(151) = 17038 P = 018 Treatment

F(115) = 384 P = 021 Time F(151) = 55849 P = 009)

after adjusting for multiple tests with a Dunn-Sidak correction

Aquat Ecol (2010) 44167ndash176 173

123

(Figs 1 2) as it has been noted to affect predation in

previous studies (Saha et al 2007a b) At low

densities in Experiment 2 (40 L vessel) the predators

trended toward disproportionate selection of the

abundant prey species while this pattern was not

evident at the higher densities (5 L vessel) in

Experiment 1 A perplexing result was that at high

densities (Fig 1) and skewed prey ratios (ie 2575

and 7525) mosquitoes appeared to be avoided by

Anisops and D rusticus but these predators posi-

tively selected mosquitoes under the same density

and ratio environment in the 16-day experiment

In these 16-day experiments with contrasting

introductions of prey ratios (Fig 3) the predators

maintained remarkably consistent behavior in spite of

the changing conditions All predators increased their

mosquito consumption in response to greater mos-

quito availability but differences among the preda-

tors emerged D rusticus displayed positive electivity

for mosquitoes while its congener D annulatus

appeared to modestly avoid mosquitoes under these

conditions and Anisops remained a flexible opportu-

nistic predator that responded only to prey ratio The

electivity did not change significantly over time

(Fig 3) nor did it change significantly in response to

the order of introduction of mosquitoes and chiron-

omids in the two different series Such results are in

contrast to the classical experiments with guppies

(Murdoch et al 1975) and Notonecta glauca (Lawton

et al 1974) in which the behavioral imprinting of the

predators was considered an essential factor in prey

switching The stonefly nymphs Isoperla grammat-

ica and Perlodes microcephalus (Elliot 2004) the

larvae of the caddisfly Rhyacophila dorsalis (Elliot

2006) the marine copepods Calanus pacificus (Lan-

dry 1981) and the copepods Mesocyclops thermocyc-

lopoides (Kumar and Rao 2003) are known to switch

to the prey which is present in higher proportion in

the environment Here the opportunistic foraging by

notonectids and belostomatids suggests that these

generalist predators would be able to persist in situ-

ations when one or the other prey (chironomid and

mosquito larvae) is low in abundance and that D

rusticus is liable to focus more reliably on mosquitoes

under a variety of circumstances

If the concept of biological control by a generalist

predator is to be successful in practice the role of

controphic species in regulating the target prey and

predator populations should be evaluated (Blaustein

and Chase 2007) For example controphic species

could compete for resources with the target species

affecting abundance of the target species Capability

of adjustment in such situations through switching to

the more abundant prey would help to maintain the

presence of the predator populations in the commu-

nities (Murdoch et al 1975) It has been noted that

the presence of the water bugs Notonecta maculata

prevents the mosquitoes Culiseta longiareolata from

ovipositing (Eitam and Blaustein 2004) but not the

controphic species Chironomus sp that coexists in

the same habitat (Blaustein et al 2004) In such

situations where the chironomid species will be

present in greater numbers compared to the mosqui-

toes N maculata will not be limited by food and can

maintain its population to further discourage mos-

quito oviposition and population growth Here the

heteropteran predators did not strongly demonstrate

lsquolsquoswitchingrsquorsquo as described by Murdoch (1969) but

they did demonstrate flexibility that would allow

them to adapt to varied situations

The flexible preyndashpredator relationship among

these aquatic organisms also imparts diversity to the

community structure spatially as well as tempo-

rally The water bugs A bouvieri D rusticus and

D annulatus too can be expected to shape the

community structure through opportunistic foraging

at high rates In tropical wetlands and other aquatic

bodies the prey considered heremdashchironomid and

mosquito larvaemdashshare a multitude of other preda-

tors including the water scorpion Laccotrephes

griseus water stick insect Ranatra filiformes the

odonate larvae and the dytiscid beetles in addition to

the minnows and larger fishes Our experimental

inferences derived from these hemipterans are

expected to deviate in such scenarios since the

presence of multiple predators would influence the

behavior and predatory success of these hemipterans

(Sih et al 1998) if a considerable degree of niche

segregation is not achieved

The spatial structure of the environment will also

strongly affect predatorndashprey interactions (Hampton

2004) Predators are not only specialized for different

sized prey but also for different predation styles

inside and outside of vegetation and among the

vertical strata of the water column The predatory

impact of the water bugs considered here needs to be

assessed in structurally and functionally complex

habitats like rice fields temporary pools wetlands

174 Aquat Ecol (2010) 44167ndash176

123

(Figs 1 2) as it has been noted to affect predation in

previous studies (Saha et al 2007a b) At low

densities in Experiment 2 (40 L vessel) the predators

trended toward disproportionate selection of the

abundant prey species while this pattern was not

evident at the higher densities (5 L vessel) in

Experiment 1 A perplexing result was that at high

densities (Fig 1) and skewed prey ratios (ie 2575

and 7525) mosquitoes appeared to be avoided by

Anisops and D rusticus but these predators posi-

tively selected mosquitoes under the same density

and ratio environment in the 16-day experiment

In these 16-day experiments with contrasting

introductions of prey ratios (Fig 3) the predators

maintained remarkably consistent behavior in spite of

the changing conditions All predators increased their

mosquito consumption in response to greater mos-

quito availability but differences among the preda-

tors emerged D rusticus displayed positive electivity

for mosquitoes while its congener D annulatus

appeared to modestly avoid mosquitoes under these

conditions and Anisops remained a flexible opportu-

nistic predator that responded only to prey ratio The

electivity did not change significantly over time

(Fig 3) nor did it change significantly in response to

the order of introduction of mosquitoes and chiron-

omids in the two different series Such results are in

contrast to the classical experiments with guppies

(Murdoch et al 1975) and Notonecta glauca (Lawton

et al 1974) in which the behavioral imprinting of the

predators was considered an essential factor in prey

switching The stonefly nymphs Isoperla grammat-

ica and Perlodes microcephalus (Elliot 2004) the

larvae of the caddisfly Rhyacophila dorsalis (Elliot

2006) the marine copepods Calanus pacificus (Lan-

dry 1981) and the copepods Mesocyclops thermocyc-

lopoides (Kumar and Rao 2003) are known to switch

to the prey which is present in higher proportion in

the environment Here the opportunistic foraging by

notonectids and belostomatids suggests that these

generalist predators would be able to persist in situ-

ations when one or the other prey (chironomid and

mosquito larvae) is low in abundance and that D

rusticus is liable to focus more reliably on mosquitoes

under a variety of circumstances

If the concept of biological control by a generalist

predator is to be successful in practice the role of

controphic species in regulating the target prey and

predator populations should be evaluated (Blaustein

and Chase 2007) For example controphic species

could compete for resources with the target species

affecting abundance of the target species Capability

of adjustment in such situations through switching to

the more abundant prey would help to maintain the

presence of the predator populations in the commu-

nities (Murdoch et al 1975) It has been noted that

the presence of the water bugs Notonecta maculata

prevents the mosquitoes Culiseta longiareolata from

ovipositing (Eitam and Blaustein 2004) but not the

controphic species Chironomus sp that coexists in

the same habitat (Blaustein et al 2004) In such

situations where the chironomid species will be

present in greater numbers compared to the mosqui-

toes N maculata will not be limited by food and can

maintain its population to further discourage mos-

quito oviposition and population growth Here the

heteropteran predators did not strongly demonstrate

lsquolsquoswitchingrsquorsquo as described by Murdoch (1969) but

they did demonstrate flexibility that would allow

them to adapt to varied situations

The flexible preyndashpredator relationship among

these aquatic organisms also imparts diversity to the

community structure spatially as well as tempo-

rally The water bugs A bouvieri D rusticus and

D annulatus too can be expected to shape the

community structure through opportunistic foraging

at high rates In tropical wetlands and other aquatic

bodies the prey considered heremdashchironomid and

mosquito larvaemdashshare a multitude of other preda-

tors including the water scorpion Laccotrephes

griseus water stick insect Ranatra filiformes the

odonate larvae and the dytiscid beetles in addition to

the minnows and larger fishes Our experimental

inferences derived from these hemipterans are

expected to deviate in such scenarios since the

presence of multiple predators would influence the

behavior and predatory success of these hemipterans

(Sih et al 1998) if a considerable degree of niche

segregation is not achieved

The spatial structure of the environment will also

strongly affect predatorndashprey interactions (Hampton

2004) Predators are not only specialized for different

sized prey but also for different predation styles

inside and outside of vegetation and among the

vertical strata of the water column The predatory

impact of the water bugs considered here needs to be

assessed in structurally and functionally complex

habitats like rice fields temporary pools wetlands

174 Aquat Ecol (2010) 44167ndash176

123

and bogs where a milieu of other predators and prey

also contributes to the community structure Such

studies that improve knowledge of food web interac-

tions would inform the use of the water bugs in

community-based long-term management (Sharma

1993 Blaustein and Chase 2007 Kumar et al 2008)

of mosquitoes and nuisance midges

Acknowledgments The authors are grateful to the Director

Zoological Survey of India Kolkata and the respective Heads

Department of Zoology University of Calcutta Kolkata and

The University of Burdwan Burdwan India for the facilities

provided including DST-FIST Thanks to Dr RD Gulati and

the four anonymous reviewers for their comments that

enhanced the manuscript The fellowship provided by the

ZSI Kolkata to N S is thankfully acknowledged

References

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1414

Aditya G Raut SK (2002a) Predation potential of the water

bugs Sphaerodema rusticum on the sewage snails Physaacuta Mem Inst Oswaldo Cruz 97(4)531ndash534

doi101590S0074-02762002000400015

Aditya G Raut SK (2002b) Predation of water bug Sphaero-dema rusticum on the freshwater snails Lymnaea (Radix)luteola and Physa acuta Veliger 45(3)267ndash269

Aditya G Saha GK (2006) Predation of the beetle Rhantussikkimensis (Coleoptera Dytiscidae) on the larvae of

Chironomus Meigen (Diptera Chironomidae) of the

Darjeeling Himalayas of India Limnologica 36(4)251ndash

257 doi101016jlimno200607004

Aditya G Bhattacharyya S Kundu N Saha GK Raut SK

(2004) Predatory efficiency of the water bug Sphaero-dema annulatum on mosquito larvae (Culex quinquefas-ciatus) and its effect on adult emergence Bioresour

Technol 95169ndash172 doi101016jbiortech200402007

Aditya G Bhattacharyya S Kundu N Saha GK (2005) Fre-

quency-dependent prey-selection of predacious water

bugs on Armigeres subalbatus immatures J Vector Borne

Dis 429ndash14

Aditya G Ash A Saha GK (2006) Predatory activity of

Rhantus sikkimensis and larvae of Toxorhynchites splen-dens on mosquito larvae in Darjeeling India J Vector

Borne Dis 43(2)66ndash72

Blaustein L (1992) Larvivorous fishes fail to control mosquitos

in experimental rice plots Hydrobiologia 232219ndash232

Blaustein L (1998) Influence of the predatory backswimmer

Notonecta maculata on invertebrate community structure

Ecol Entomol 23246ndash252 doi101046j1365-2311

199800138x

Blaustein L Chase JM (2007) Interactions between mosquito

larvae and species that share the same trophic level Annu

Rev Entomol 52489ndash507 doi101146annurevento52

110405091431

Blaustein L Kiflawi M Eitam A Mangel M Cohen JE (2004)

Oviposition habitat selection in response to risk of pre-

dation in temporary pools mode of detection and con-

sistency across experimental venue Oecologia 138300ndash

305 doi101007s00442-003-1398-x

Chesson JE (1983) The estimation and analysis of preference

and its relationship to foraging models Ecology 641297ndash

1304 doi1023071937838

Das PK Sivagnaname N Amalraj DD (2006) Population

interactions between Culex vishnui mosquitoes and their

natural enemies in Pondicherry India J Vector Ecol

31(1)84ndash88 doi1033761081-1710(2006)31[84PIBC

VM]20CO2

Efron B Tibshirani R (1991) Statistical data analysis in the

computer age Science 253390ndash395 doi101126

science2535018390

Eitam A Blaustein L (2004) Oviposition habitat selection by

mosquitoes in response to predators (Notonecta maculata)

density Physiol Entomol 29188ndash191 doi101111

j0307-696220040372x

Eitam A Blaustein L Mangel M (2002) Effects of Anisopssardea (Hemiptera Notonectidae) on oviposition habitat

selection by mosquitoes and other dipterans and on

community structure of artificial pools Hydrobiologia

485183ndash189 doi101023A1021315309758

Elliot JM (2004) Prey switching in four species of carnivorous

stoneflies Freshw Biol 49709ndash720 doi101111j1365-

2427200401222x

Elliot JM (2006) Prey switching in Rhyacophila dorsalis(Trichoptera) alters with larval instars Freshw Biol

51913ndash924 doi101111j1365-2427200601549x

Fincke OM Yanoviak SP Hanshu RD (1997) Predation by

odonates depresses mosquito abundance in water filled tree

holes in Panama Oecologia 112(2)244ndash253 doi101007

s004420050307

Gerritsen J Strickler JR (1977) Encounter probabilities and

community structure in zooplankton a mathematical

model J Fish Res Board Can 3473ndash82

Gilbert JJ Burns CW (1999) Some observations on the diet of

backswimmer Anisops wakefieldi (Hemiptera Notonecti-

dae) Hydrobiologia 412111ndash118 doi101023A1003

812718853

Gilbert JJ Burns CW Gilbert CC (1999) Summer distribution

patterns of backswimmer Anisops wakefieldi (Hemiptera

Notonectidae) in a New Zealand pond N Z J Freshwat

Res 33661ndash672

Hampton SE (2004) Habitat overlap of enemies temporal

patterns and role of spatial complexity Oecologia

138475ndash484 doi101007s00442-003-1446-6

Hampton SE Gilbert JJ Burns CW (2000) Direct and indirect

effects of juvenile Buenoa macrotibialis (Hemiptera

Notonectidae) on the zooplankton of a shallow pond

Limnol Oceanogr 451006ndash1012

Hassell MP Southwood TRE (1978) Foraging strategies of

insects Annu Rev Ecol Syst 975ndash98 doi101146

annureves09110178000451

Hati AK (1988) Studies on four predacious arthropods for

biological control of mosquitoes Bicovas 125ndash40

Aquat Ecol (2010) 44167ndash176 175

123

Kumar R Rao R (1999) Effect of algal food on animal prey

consumption in the omnivorous copepod Mesocyclopsthermocyclopoides Int Rev Hydrobiol 84419ndash426

Kumar R Rao R (2003) Predation on mosquito larvae by

Mesocyclops thermocyclopoides (Copepoda Cyclopoida)

in presence of alternate prey Int Rev Hydrobiol 88570ndash

581 doi101002iroh200310631

Kumar R Muhid P Dahms H Tseng L Hwang J (2008)

Potential of three aquatic predators to control mosquitoes

in the presence of alternative prey a comparative exper-

imental assessment Mar Freshw Res 59817ndash835 doi

101071MF07143

Landry MR (1981) Switching between herbivory and carnivory

by the planktonic marine copepod Calanus pacificus Mar

Biol (Berl) 6577ndash82 doi101007BF00397070

Lawton JH Beddington JR Bonser R (1974) Switching in

invertebrate predators In Usher MB Williamson MH

(eds) Ecological stability Chapman amp Hall London pp

141ndash158

Lundkvist E Landin J Jackson M Svensson C (2003) Diving

beetles (Dytiscidae) as predators of mosquito larvae

(Culicidae) in field experiments and in laboratory tests of

prey preference Bull Entomol Res 93219ndash226

doi101079BER2003237

Mogi M Memah V Miyagi I Toma T Sembel DT (1995)

Mosquito and aquatic predator abundance in irrigated and

rain fed rice fields in north Sulawesi Indonesia J Med

Entomol 32361ndash367

Mogi M Sunahara T Selemo M (1999) Mosquito and aquatic

predator communities in ground pools on lands deforested

for rice field development in central Sulawesi Indonesia

J Am Mosq Control Assoc 15(2)92ndash97

Murdoch WW (1969) Switching in general predatorsmdashexperi-

ments on predator specificity and stability of prey popula-

tions Ecol Monogr 39(4)335ndash354 doi1023071942352

Murdoch WW Avery S Smyth MEB (1975) Switching in

predatory fish Ecology 561094ndash1105 doi102307

1936149

Murdoch WW Chesson J Chesson PL (1985) Biological

control in theory and practice Am Nat 125344ndash366

doi101086284347

Nishi R Venkatesan P (1997) Influence of vegetation on the

predatory performance of Anisops bouvieri Kirkaldy J

Ecotoxicol Environ Monit 7121ndash124

Oaten A Murdoch WW (1975) Predator switching functional

response and stability Am Nat 109299ndash318 doi101086

282999

Panickar KN Rajagopalan PK (1977) biological control

potential of Anisops bouvieri (Kirkaldy) Indian J Med

Res 66772ndash776

Potvin C Lechowicz MJ Tardif S (1990) The statistical

analysis of ecophysiological response curves obtained

from experiments involving repeated measures Ecology

71(4)1389ndash1400 doi1023071938276

Rao TR Kumar R (2002) Patterns of prey selectivity in the

cyclopoid copepod Mesocyclops thermocyclopoides

Aquat Ecol 36411ndash424 doi101023A1016509016852

Raut SK Saha TC Mukhopadhyay B (1988) Predacious water

bugs in control of vector snails Bicovas I175ndash185

Rey JR OrsquoConnell S Suarez S Menendez Z Lounibos LP

Byer G (2004) Laboratory and field studies of Macrocy-clops albidus (Crustacea Copepoda) for biological con-

trol of mosquitoes in artificial containers in a subtropical

environment J Vector Ecol 29124ndash134

Roy JK Raut SK (1994) Factors influencing predation of the

water bugs Sphaerodema annulatum (Fab) and S rusti-cum (Fab) on the disease transmitting snails Lymnaea(Radix) luteola (Lamarck) Mem Inst Oswaldo Cruz

8911ndash20

Saha TC Raut SK (1992) Bioecology of the water-bug Sph-aerodema annulatum Fabricius (Heteroptera Belostom-

atidae) Arch Hydrobiol 124(2)239ndash253

Saha N Aditya G Bal A Saha GK (2007a) A comparative

study of predation of three aquatic heteropteran bugs on

Culex quinquefasciatus larvae Limnology 8(1)73ndash80

doi101007s10201-006-0197-6

Saha N Aditya G Bal A Saha GK (2007b) Comparative

studies on functional response of common heteropteran

bugs of East Calcutta Wetlands Kolkata India Int Rev

Hydrobiol 92(3)242ndash257 doi101002iroh200610939

Scott MA Murdoch WW (1983) Selective predation by the

backswimmer Notonecta Limnol Oceanogr 28352ndash366

Sharma VP (1993) Ecosystem approach to malaria control

Proc Nat Acad Sci India Sec B-Biol Sc 63(I)47ndash55

Sih A Englund G Wooster D (1998) Emergent impacts of

multiple predators on prey Trends Ecol Evol 13350ndash355

doi101016S0169-5347(98)01437-2

Stav G Blaustein L Margalit Y (2005) Individual and interac-

tive effects of a predator and controphic species on mos-

quito populations Ecol Appl 15(2)587ndash598 doi101890

03-5191

Sunish IP Reuben R (2002) Factors influencing the abundance

of Japanese encephalitis vectors in rice fields in IndiamdashII

Biotic Med Vet Entomol 161ndash9 doi101046j1365-

2915200200325x

Symondson WOC Sunderland KD Greenstone MH (2002) Can

generalist predators be effective biocontrol agents Annu

Rev Entomol 47561ndash594 doi101146annurevento

47091201145240

Victor TJ Reuben R (1999) Population dynamics of mosquito

immatures and the succession of aquatic insects in rice

fields in Madurai South India Indian J Malariol 3619ndash32

Victor TJ Marimithu S Sivaramakrishnan KG (1991) Aquatic

macrophytes and the associated mosquitoes in and around

Madurai city (Tamil Nadu) Indian J Malariol 28151ndash155

Von Kogel F (1987) Zur Biologie und Okologie von Rhantus

consputus STRM Ent Arb Mus 355ndash19

Waage JK Greathead DJ Brown R Paterson RRM Haskell

PT Cook RJ Krishnaiah K (1988) Biological control

challenges and opportunities Philos Trans R Soc Lond B

Biol Sci 318111ndash128 doi101098rstb19880001

Zar JH (1999) Biostatistical analysis IV Singapore Pearson

Education (Singapore) Pte Ltd New Delhi (Indian

Branch)

176 Aquat Ecol (2010) 44167ndash176

123