comparative study of functional response of common hemipteran bugs of east calcutta wetlands, india

© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 1434-2944/07/306-242

NABANEETA SAHA1, 2, GAUTAM ADITYA1, 3, ANIMESH BAL2 and GOUTAM KUMAR SAHA*, 1

1Department of Zoology, University of Calcutta, 35, Ballygunge Circular Road, Kolkata 700019. India; e-mail: [email protected]

2Zoological Survey of India, M Block, New Alipore, Kolkata 700053. India3Department of Zoology, The University of Burdwan, Golapbag, Burdwan 713104. India

Comparative Study of Functional Response of Common Hemipteran Bugs of East Calcutta Wetlands, India

key words: mutual interference, Anisops bouvieri, Diplonychus rusticus, D. annulatus, Culex quinquefasciatus, larvae

Abstract

The common and abundant hemipteran water bugs Anisops bouvieri, Diplonychus rusticus, D. annu-latus, of the wetlands of East Kolkata are known predators of a wide range of aquatic insects includingthe mosquito larvae. In the laboratory their predation were assessed in respect to short term and longterm periods using the larvae of Culex quinquefasciatus to reveal their possible role in regulating thedipteran population in nature. The attack rate (a) and handling time (Th) of these predators varied withrespect to the prey size. For the backswimmers A. bouvieri the values for a and Th for the small preywere 5.47 L and 18.72 min respectively, while in case of the belostomatid bugs, the values for the samewere 5.37 L and 8.64 min (for D. rusticus), 5.81 L and 20.16 min (for D. annulatus). The predation ratevaried with prey and predator densities for both the prey sizes. It was revealed that on an average A. bou-vieri can kill and consume 10–82 and 6–44, D. rusticus 10–118 and 10–84 and D. annulatus 10–70and 10–138 small and large sized prey per day, respectively. However the mutual interference (m)values of the three predators varied with the prey size and ranged between 0.053–0.326 for A. bouvieri,0.0381–0.066 for D. rusticus and 0.0556–0.115 for D. annulatus, respectively. In the long term exper-iments A. bouvieri killed between 6 –119 small preys and 3–31 large preys, D. rusticus killed 50–94small preys and 50–96 large preys and D. annulatum were found to kill between 14–74 small prey and50–131 large prey per day, respectively. The clearance rates were found to be proportional to the preda-tor density as well to the prey size and density, and differed between the predator species significant-ly. These data are supportive of qualifying the water bugs, A. bouvieri, D. rusticus, and D. annulatusas potential biological resources in regulating the population of mosquito larvae in the wet-lands.

1. Introduction

The eastern fringe of the city of Kolkata is characterized by the perennial East Calcuttawetlands already incorporated in the list of Ramsar. Certain portions are commerciallyexploited for sewage fed fisheries and prawn cultures. The rest of the wetlands is free fromhuman interference and hosts a greater amount of biodiversity compared to similar wetlandsin the state. Fragmentary records of different species inhabiting these wetlands suggest thatinsect diversity at both taxonomic and ecological level is very high (IWMED, 2004). Thisincludes dipterans like mosquitoes and chironomids and the Hemipterans, particularly thebelostomatids and the notonectids (NANDI et al., 1993; KHAN and GHOSH, 2001). Controph-ic chironomid and the mosquito larvae share the belostomatids and notonectids as predators

Internat. Rev. Hydrobiol. 92 2007 3 242–257

DOI: 10.1002/iroh.200610939

* Corresponding author

in the food chains of these and other aquatic insect communities (BLAUSTEIN, 1998; KIFLAWI

et al., 2003; PRAMANIK and RAUT, 2003; ADITYA et al., 2004; BLAUSTEIN and CHASE, 2007).In recent survey of East Calcutta wetlands the belostomatid bugs Diplonychus (= Sphaerode-ma) annulatus FABRICIUS 1906 and D. rusticus FABRICIUS 1906 (Heteroptera: Belostomati-dae) and the backswimmers Anisops bouvieri KIRKALDY 1904 (Heteroptera: Notonectidae)were found abundant along with different species of mosquito immatures, particularly Culexquinquefasciatus SAY 1823. The continuous presence of mosquitoes in the city can be attrib-uted to the access of varied types of habitats available throughout the year. The wetlandscan be expected as principal source of mosquitoes. The vastness of the wetlands and theperennial nature is in support of this. Even droughts induce increments in mosquito popula-tion in wetlands (CHASE and KNIGHT, 2003). Traditional methods of control may interferewith the maintenance of non-target species of these wetlands. On the other side, this wet-land has been threatened by agriculture and pisciculture.

The use of a suitable predator and natural enemy to regulate the population of immaturemosquitoes can reduce the menace. In other mosquito breeding habitats, like temporarypools and cemented tanks, predators like the dytiscid beetles Rhantus signatus signatus(FISCHER et al., 2000; CAMPOS et al., 2004) and R. sikkimensis (ADITYA et al., 2006a, 2006b),the notonectid bugs Notonecta maculata and Anisops sardea (MURDOCH et al., 1984;BLAUSTEIN, 1998; EITAM et al., 2002; KIFLAWI et al., 2003; EITAM and BLAUSTEIN, 2004) areknown to regulate the mosquito populations and even influence their oviposition habitatselection. Thus they are involved in structuring the aquatic insect communities. TheHemipteran water bugs considered in the present study can be expected to play a similarrole as predators of dipteran immatures.

In view of these facts, the evaluation of the predatory nature of the water bugs can formthe basic framework to substantiate them as biological resource against mosquitoes. Earlierstudies have revealed that the presence of D. annulatus and D. rusticus in aquatic habitatscan suppress the population of mosquitoes through predation (ADITYA et al., 2004; PRA-MANIK and RAUT, 2003, 2005). Similar evidence has been recorded for A. bouvieri from thetemporary pools and ponds (NISHI and VENKATESAN, 1989, 1997). In aquatic habitats likerice fields, wetlands and temporary pools, interactions between these preys and predators arecommon (SUNISH and REUBEN 2002; DAS et al., 2006) and this can be explored in order toframe a proper strategy for mosquito pest regulation by biological means from the commu-nity viewpoint (BLAUSTEIN and CHASE, 2007). In the present study an attempt has been madeto compare the predatory nature of these common Hemipteran water bugs, on the mosquitolarvae, in the context of their presence in the same guild. Interpretation on their possible rolein regulation of mosquito population and influence as predators in aquatic communities canbe made from the present study.

2. Methods

2.1. Collection of Water Bugs and Mosquito Larvae

The adult water bugs were collected from the wetlands along the Eastern Metropolitan Bypass,Kolkata, India with an insect net of 200 µ mesh size seven days prior to the experiments and maintainedseparately in the laboratory for acclimatization within glass aquaria containing pond water, adequateamounts of mosquito larvae as food and some specimens of aquatic plants like Vallisneria spiralis,Chara vulgaris to provide resting sites to the insects.

Mosquito larvae were collected from the drains of Ballygunge Science College campus, Kolkata,India. In the experiments two sizes of the prey were considered. The IV instar larvae (4.5–6.0 mm) ofCx. quinquefasciatus (large prey) were separated from the heterogeneous population by proper sieving.The smaller instars obtained after sieving were maintained for growth to IV instar stage following Ent-

Functional Response of Hemipteran Bugs 243

© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com

guide No. 3 (www.pherec.org). The small sized prey larvae to be used in the experiments were obtainedfrom field collected egg rafts. Ten to fifteen rafts were cautiously placed within enamel trays of12″ × 8″ × 4″ capacity containing de-chlorinated tap water. After hatching the 0-day old larvae were pro-vided with yeast granules as food and water was changed every 24 h. The 3–4 day old larvae(1.5–2.5 mm in length, 0.8–1.2 mg wet weight) were considered as the small sized prey and used in theexperiments. The larger preys (IV instar larvae) were 1.6–2.2 mg in weight (wet).

Prior to using any predator individual in the experiments, they were fed to satiation followed by 24h of starvation. In all the experiments controls without predators were set with equal numbers of preda-tors as that of the test sets. The estimation of predation by the bugs was made through the followingexperiments in the laboratory at a room temperature of 25–30 °C.

2.2. Experimental Design

2.2.1. Determination of Attack Rates and Handling Times

To an adult morph of each species of water bug, 10, 50, 100, 200 larvae of Cx. quinquefasciatuswere supplied per 5 L in plastic trays and were allowed to predate for a period of 24 h. Nine replicatesfor each prey density as well as prey size were carried out to record the rate of predation and note the functional response (type II). The functional response was analysed using the Holling Disc Equa-tion:

Ha = a · H · T/(1 + a · H · Th).

The above equation was transformed into a linear regression after FOX and MURDOCH (1978) to obtainthe values of a and Th,

1/Ha = 1/a · 1/(H · T) + Th/T

Which is equivalent to y = αx + �, where 1/a = α and Th/T = �, and a = constant, the attack rate of the predators (a is the instantaneous rate of discovering prey by onepredator), Th = handling time (time from which a prey is grasped by the predator to the time when it was con-sumed or the left over abandoned), T = total time of predation, Ha = total prey killed, H = prey density.

2.2.2. Determination of Numerical Response

In this experiment, 100, 200 and 400 Cx. quinquefasciatus larvae per 5 L were provided to either a single or two or four predators for a period of 24 h and predation rate was noted. Nine replicates of the experiment for each of the predator densities as well as prey sizes and densities were carried out.

The attack rate and handling time of each individual insect was calculated at multiple predator den-sities. Chi-square test were applied to justify differences in attack rate and handling time, if any, betweendifferent predator species and prey size class.

The data obtained from this experiment was also used to evaluate the mutual interference betweenpredators when present in multiple numbers using the formula (HASSELL and VARLEY, 1969) presentedbelow:

ai = A · P –m

244 N. SAHA et al.


where ai = attack rate when P = i, andA = attack rate for a single predator (P = 1),P = predator density;m = the mutual interference constant.

The equation was transformed logarithmically to:

ln a = –m · ln P + ln A

and ‘m’ was calculated.When multiple predators of the same species are considered the value of mutual interference is

expected to remain constant for a particular time period, provided other factors influencing predationremains constant. The difference in the levels of intraspecific interference also provides an idea aboutthe spatial distribution of predators in the field (ELLIOT, 2003a, 2003b).

2.2.3. Determination of Long-Term Prey Consumptions

For a long term study on predation rate, for 9 consecutive days, 2 or 4 adult morphs of water bugswere kept in a plastic bucket of 16 L capacity, 50 mosquito larvae were given as food for the first threedays, 100 for the next three days and 200 for the last three days. 9 replicates for each of the predatordensities as well as prey sizes were carried out (except for the A. bouvieri – II instar larvae combina-tion, where 6 repeats were done). The rate of predation was noted and the prey density was reset every24 h. Data obtained from the experiments were used to calculate the Clearance rate (CR) followingGILBERT and BURNS (1999) with required modifications, as stated below.

CR = V · ln (PC – PE) /T · N

Where V = volume of water (in litres), andT = time (in days),N = number of predators,PE = number of preys left after time T,PC = number of preys at the start of the experiment.

Clearance Rate (numbers · L · d–1 · predator–1) is an index of predation, which reflects the amount ofspace and time utilized in prey capture, killing, and consumption by the predator.

In the experimental and control containers, three long leaves of Vallisneria spiralis and two twigs ofJussiaea repens were provided to simulate the natural conditions. The plant parts formed the prey andpredator refuge. Sieved pond water was used in this experiment (pH 8.5–9 and water temperature of23.6–28.9 °C), carried out between July and September 2005.

2.3. Statistical Analyses

The data obtained on the rate of predation in experiments I and II were subjected to regression analy-sis. Also, with respect to the prey sizes the handling times and the attack rates of the predators werecompared with Chi-square tests. Results of numerical response were subjected to two-way ANOVAwith respect to prey and predator densities. Predation rate obtained from long-term experiments weresubjected to 4-way repeated measures ANOVA with predator species, predator density and prey size asbetween-subject factors and days as within-subject factor. The interactions between predator species,predator density and prey size and prey density were also tested for Clearance Rate data following ZAR

(1999).



3. Results

3.1. Attack Rates and Handling Times: Effect of Prey Density

The average prey consumption rate ranged between 8.55–35.44, 10–79.67, 10–104.33 forIV instar and 10–68.66, 10–97.67, 10–59.0 for II instar Cx. quinquefasciatus larvae in casesof A. bouvieri, D. rusticus and D. annulatus, respectively (Table 1). Handling time (Th) andattack rate (a) of the predators when present individually or in multiple numbers are repre-sented in Table 2. In case of A. bouvieri the attack rate decreased from 7.57 to 5.33 L withrespect to predator density in case of large preys. Compared to this the attack rate did notdiffer much for small prey and ranged between 5.31 to 5.74 L depending on predator den-sity. In case of the other two predators D. annulatus and D. rusticus the values rangedbetween, 5.1 to 5.74 L irrespective of small and large preys. In general, both the parameters(a and Th) were negatively correlated with predator density at a constant prey density(Figs. 1, 2). The attack rate did not exhibit any significant variation between predators for

246 N. SAHA et al.


Table 1. Analysis of Functional Response of A. bouvieri, D. rusticus and D. annulatusagainst the mosquito larvae. (n = 9 trials per prey density per prey size). T = 1 day.

Prey Anisops bouvieri Diplonychus rusticus Diplonychus annulatusdensity[number 5 1/HT Range, Mean 1/Ha Range, Mean 1/Ha Range, Mean 1/Ha

L–1] (H) (± SE) of (SE) of (± SE) ofprey killed prey killed prey killed

(Ha) (Ha) (Ha)

A. Prey size : Small Mosquito larvae

10 0.1–– 10–10 0.1––– 10–10 0.1––– 10–10 0.1–––10 ± 0 10 ± 0 10 ± 0

50 0.02– 22–34 0.0327 42–52 0.0204 19–41 0.020430.55 ± 1.23 49.00 ± 0.88 30.11 ± 2.81

100 0.01– 29–61, 0.0220 47–89, 0.0153 29–51, 0.015345.44 ± 4.43) 65.11 ± 5.25 38.78 ± 2.13

200 0.005 40–88 0.0159 71–91 0.0118 36–62 0.011862.88 ± 5.92 84.56 ± 3.15 50.00 ± 3.31

400 0.002 42–82 0.0145 77–118 0.0102 35–70 0.010268.66 ± 4.5 97.67 ± 4.60 59.00 ± 3.64

B. Prey size: Large mosquito larvae

10 0.1––– 6–10 0.1169 10–10 0.1––– 10–10 0.1–––8.55 ± 0.52 10 ± 0 10 ± 0

50 0.02–❚4–6 0.1071 46–50 0.2006 19–31 0.0372

9.33 ± 1.17 49.22 ± 0.52 26.88 ± 2.15

100 0.01–– 7–15 0.0957 38–55 0.0205 29–44 0.027310.44 ± 0.86 48.78 ± 1.91 36.56 ± 1.68

200 0.005– 9–45 0.0370 49–74 0.0149 40–74 0.015527.00 ± 4.44 67.11 ± 2.71 64.33 ± 3.57

400 0.0025 27–44 0.0282 69–84 0.0125 69–138 0.009535.44 ± 2.06 79.67 ± 2.31 104.33 ± 7.69



Table 2. Table showing transformations of the Holling Disc Equation into linear regres-sions 1/Ha = 1/a .1/Ht + Th/T equivalent to y = ax + b where, 1/a = a and Th/T = b. Attackrate (a, in litres) and Handling Time (Th, in mins) are calculated at three predator densities

(numbers 5 L–1).

Predator 1 predator 5 L–1 2 predators 5 L–1 4 predators 5 L–1

speciesRegression a Th Regression a Th Regression a Th

Equation Equation Equation

A. Prey size: Small Mosquito larvae

A. bouvieri y = 0.87x + 0.013 5.74 18.72 y = 0.90x + 0.008 5.53 12.09 y = 0.94x + 0.005 5.31 7.38r2 = 0.99 r2 = 0.996 r2 = 0.99P < 0.001 P < 0.001 P < 0.001

D. rusticus y = 0.93x + 0.0006 5.37 8.64 y = 0.95x + 0.003 5.23 5.57 y = 0.96x + 0.002 5.18 4.28r2 = 0.99 r2 = 0.997 r2 = 0.99P < 0.001 P < 0.001 P < 0.001

D. annulatus y = 0.86x + 0.014 5.81 7.38 y = 0.89x + 0.013 4.28 4.95 y = 0.93x + 0.006 5.37 9.05r2 = 0.999 r2 = 0.999 r2 = 0.994P < 0.001 P < 0.001 P < 0.001


A. bouvieri y = 0.66x + 0.059 7.57 84.96 y = 0.84x + 0.17 5.89 24.72 y = 0.93x + 0.006 5.33 8.64r2 = 0.24 r2 = 0.947 r2 = 0.997

N. S. P < 0.001 P < 0.001

D. rusticus y = 0.90x + 0.009 5.54 12.96 y = 0.94x + 0.004 5.29 7.15 y = 0.97x + 0.002 5.14 3.31r2 = 0.98 r2 = 0.995 r2 = 0.997P < 0.001 P < 0.001 P < 0.001

D. annulatus y = 0.87x + 0.013 5.74 19.87 y = 0.94x + 0.006 5.27 8.68 y = 0.95x + 0.003 5.21 5.18r2 = 0.947 r2 = 0.993 r2 = 0.997P < 0.001 P < 0.001 P < 0.001

Figure 1. The Attack Rate (a) as a function of the water bugs A. bouvieri, D. rusticus and D. annula-tus density, against – a. II instar and b. IV instar of Cx. quinquefasciatus larvae.

both prey sizes. Handling times, on the other hand, varied significantly between the preda-tors for the IV instar larvae only (for large prey �2 = 80.39, P < 0.001). For the belostom-atids, the handling time varied between the two prey sizes was not statistically significant.However it varied significantly with prey sizes in for A. bouvieri (�2 = 42.53, P < 0.001,df. = 1).

3.2. Numerical Response: Effect of Predator Density

The rates of predation with respect to numerical responses are presented in Table 3. Formost of the prey and predator combinations – species, densities and sizes, significant dif-ferences were noted in terms of prey consumption as revealed by the 2-way ANOVA. Con-sidering the small preys, in case of A. bouvieri the difference between prey densities wassignificant; F = 36.35, P < 0.003; between predator densities; F = 60.81, P < 0.001; forD. rusticus: between prey densities; F = 34.79, P < 0.002; between predator densities;F = 18.74, P < 0.009; for D. annulatus; between prey densities; F = 25.87, P < 0.005;between predator densities; F = 30.90, P < 0.003. In contrast, in the case of large preys forA. bouvieri the difference between prey densities was not significant; F = 5.62, N.S, but wassignificant between predator densities, F = 57.63, P < 0.001; for D. rusticus: between preydensities; F = 22.61, P < 0.006; between predator densities; F = 31.5, P < 0.003; forD. annulatus; between prey densities; F = 14.17, P < 0.015. However between predator den-sities the difference was not significant, F = 6.35. Although the overall prey consumptionrates increased in presence of multiple predators, the increase was not proportional due tomutual interference (Table 4).

3.3.1. Long-Term Prey Consumptions

In the long-term experiments, the rate of predation varied from 2–48, 49–78, 50–111 IVinstar Cx. quinquefasciatus larvae per day at predator density of 2 per 5 L for A. bouvieri,D. rusticus, and D. annulatus, respectively (Fig. 3). The values for small prey were 30–48,50–96 and 19–71 larvae per day, respectively. At the predator density of 4 per 5 L, the waterbugs A. bouvieri, D. rusticus and D. annulatus were found to predate upon 4–28, 50–96,

248 N. SAHA et al.


Figure 2. The Handling Time (Th) as a function of the water bugs A. bouvieri, D. rusticus and D. annu-latus density, against – a. II instar and b. IV instar of Cx. quinquefasciatus larvae.



Tab

le3.

The

Num

eric

al r

espo

nse.

Ran

ge,

Mea

n±

SE o

f pr

ey c

onsu

med

by

A.

bouv

ieri

, D

.rus

ticu

san

d D

. an

nula

tus

in a

24

h pe

riod

(n

=9

tria

ls p

re p

rey

size

per

pre

y de

nsity

per

pre

dato

r de

nsity

).

Pre

dato

rA

niso

ps b

ouvi

eri

Dip

lony

chus

rus

ticus

Dip

lony

chus

ann

ulat

usde

nsit

y(n

umbe

r P

rey

dens

ity

(num

ber

5 L

–1)

5 L

–1)

100

200

400

100

200

400

100

200

400

A.

Pre

y si

ze:

Smal

l M

osqu

ito

larv

ae

129

–61

40–

8842

–82

47–

8971

–96

77–1

1829

–51

36–

6235

–70

45.4

4±

4.43

62.8

8±

5.92

68.8

8±

4.5–

65.1

1±

5.25

84.5

6±

3.15

97.6

7±

4.60

39.7

8±

2.13

50.0

±3.

3159

.00

±3.

64

249

–70

62–

8159

–89

62–

9185

–112

106

–147

39–5

955

–79

65–8

261

.66

±3.

3673

.83

±3.

9275

.16

±5.

3179

.83

±4.

3297

.67

±4.

1412

5±

6.30

48.6

7±

3.25

66.1

7±

3.50

75.8

3±

2.88

451

–87

81–1

0180

–119

89–1

0081

–118

119

–155

49–7

069

–94

89–1

1072

.16

±5.

6291

.33

±3.

1697

.16

±6.

1795

.67

±2.

0110

2.17

±5.

7513

6.33

±5.

9860

.50

±3.

0582

.33

±82

.33

98.5

±3.

47

B.

Pre

y si

ze:

Lar

ge m

osqu

ito

larv

ae

17–

159

–45

27–

4438

–55

49–7

469

–84

29–9

440

–74

69–1

3810

.44

±0.

8627

.00

±4.

4435

.44

±2.

0648

.78

±1.

9167

.11

±2.

7179

.67

±2.

1336

.56

±1.

6864

.33

±3.

5710

4.33

±7.

69

229

–54

40–

6735

–86

43–7

957

–118

112–

139

57–7

694

–120

110

–188

41.6

6±

2.93

36.1

1±

5.88

61.8

8±

7.29

64.0

0±

5.96

89.6

7±

9.75

125.

67±

4.32

63.3

3±

2.73

109.

67±

4.80

167.

00±

11.9

2

461

–96

60–1

3688

–97

89–1

0010

8–14

213

0–1

5970

–86

101–

135

103

–151

78.4

4±

3.83

91.1

1±

8.75

92.8

8±

1.14

93.6

7±

1.61

126.

67±

4.70

143.

67±

4.96

78.3

3±

2.35

116.

83±

5.87

123.

00±

8.34

50–132 IV instar and 44–88, 50–96, 48–74 II instar larvae per day, respectively. The resultsof a 4-way repeated measures ANOVA indicated that predation rate varied significantly withdays, prey size, prey density, predator species, predator density as well as with the interac-tions between these factors (Table 5).

3.3.2. Clearance Rates

Clearance rate was found to differ significantly with prey size, prey density, predatorspecies, and predator density and with majority of the possible combinations between thesefactors (Table 6). Since the interaction between predator species were found to be signifi-cant, the CR of different predators were subjected to separate one-way ANOVAs and sub-sequent post-hoc Tukey Test which further confirmed the variation between A. bouvieri-D.rusticus (P < 0.001) and A. bouvieri-D. annulatus (P < 0.001) but not between D. rusticus-D. annulatus (P > 0.05) for the large sized prey. However, the variation was not significantbetween the belostomatid bugs for the small sized prey larvae (P > 0.05) (Fig. 4).

4. Discussion

It is evident that the water bugs exhibited differential levels of predation with respect tothe same sized prey. The pattern of predation related to the variables like prey and predatordensities were identical, yet the number of prey killed by the predator species varied. Thebelostomatid bugs D. annulatus killed maximum numbers of large preys while the back-swimmers A. bouvieri predated the least numbers of preys, irrespective of the size. Also, the belostomatid bugs preferred larger than the smaller preys, revealed by their rate of pre-dation, both in the long-term and short-term experiments. These differences can be attrib-uted to the body size, and other predatory adaptations associated with the life history traits.The biomass (wet weight in mg) of II instar larvae was 0.9 mg, whereas that of the IV instarlarvae was 1.9 mg. Thus the difference in energy gain is obvious. Despite this the back-swimmers chose to feed the II instars at a greater rate than the IV instars perhaps due tolimitation in prey handling capability. Predators of smaller size like the copepods Mesocy-clops thermocyclopoides also showed a preference of II instar mosquito larvae compared tothe larger ones (RAO and KUMAR, 2002; KUMAR and RAO, 2003).

250 N. SAHA et al.


Table 4. Mutual interference (m) at 2 and 4 predators per 5 litres of pond water for A. bouvieri, D. rusticus and D. annulatus.

2 predators 5 L–1 4 predators 5 L–1

A. Prey size: Small Mosquito larvae

A. bouvieri 0.0537 0.0561D. rusticus 0.0381 0.0259D. annulatus 0.0556 0.0568


A. bouvieri 0.362– 0.253–D. rusticus 0.066– 0.057–D. annulatus 0.115– 0.064–

The backswimmers, A. bouvieri and other species, are associated primarily with the shal-low, littoral regions or deeper open water zones in ponds and other aquatic bodies (STREAMS,1987, 1992; NISHI and VENKATESAN, 1997; GILBERT et al., 1999). Also, they show a dielactivity in the spatial distribution in their habitats (GILBERT et al., 1999; HAMPTON, 2004).Compared to this the belostomatid water bugs D. rusticus and D. annulatus are associatedprimarily with the aquatic macrophytes and show diving and swimming ability into the deepwaters (RAO, 1981; RAUT and SAHA, 1989, 1992; PAL et al., 1998; ADITYA et al., 2004;



Figure 3. Number (mean ± SE) of small (a, c, e) and large (b, d, f) mosquito larvae consumed day–1

for nine consecutive days (D1 to D9) with 50, 100 and 200 prey 5 L–1 of pond water for the first, second and last three days by the water bugs A. bouvieri, D. rusticus and D. annulatus.

PRAMANIK and RAUT, 2005). Due to this difference in the microhabitats, difference in preyselection can be expected. Further the mouthparts and the shape of the body in these waterbugs are different. While the backswimmers have a smaller piercing apparatus, the belostom-atids have a long bent rostrum, which might contribute to the difference in handling of aprey item. This can be correlated to the differential rate of predation of small and large prey.Also, prey profitability (biomass of prey in mg/handling time by the predator) was differentfor the smaller and the larger sizes of the preys. For A. bouvieri the values were 0.05 mgmin–1 and 0.02 mg min–1 for the II and IV instar larvae, respectively. While for the belostom-atids D. rusticus and D. annulatus the values were 0.1 and 0.12 mg min–1 for the II instarand 0.15 and 0.1 mg min–1 for the IV instar preys, respectively. Thus, the backswimmerswould target more on the II instars and the belostomatids would prefer to have the IV instarCx. quinquefasciatus as preys, keeping apart other factors that contribute to prey selection(HAMPTON, 2004; ADITYA et al., 2005).

During the experiments it was observed that the backswimmers most of the time occu-pied the central part of the trays avoiding the little amount of complexity in form of theaquatic stems and twigs while the belostomatids between active foraging took refuge in thetwigs. During prey searching, these bugs chased the preys horizontally as well as vertically(seldom) in the space compared to the backswimmers that caught the preys on the move justbelow the water level (personal observation). Further, attributes like predation rhythm (PRA-MANIK and RAUT, 2005), and size dependent predation (DUDGEON, 1990) and fluctuation inpredation rhythm (DIEGUEZ and GILBERT, 2003; ELLIOT, 2005) can be the reasons for theobserved variation in predation by the water bugs.

In general, arthropod predation follows certain common rules that are quantified in termsof the attack rate and handling time (HASSELL et al., 1976). The attack rate reflects prey-

252 N. SAHA et al.


Table 5. Results of 4-way repeated measures ANOVA with days as within subject factorand prey density, predator density, predator species and prey size as between subject factorson the predation rates of A. bouvieri, D. annulatus, and D. rusticus for 9 consecutive

days. All F-Values are significant at P < 0.01. SS: Sum of squares; MS: Mean square.

Source of variation SS df MS F

A. Within subject contrasts.

Days 22780.80 1 22780.80 398.90Days · Prey size 3743.00 1 3743.00 65.54Days · Predator species 6006.80 2 3003.40 52.59Day · predator density 5129.90 1 5129.90 89.83Day · prey size · predator species 456.30 2 228.19 3.96Days · prey size · predator density 406.37 1 406.37 7.10Days · Predator species · predator density 9163.76 2 981.85 17.19Day · prey size · predator species · predator density 4646.82 2 2323.41 40.68Error 5139.28 90 57.10

B. Between subject contrasts.

Prey size 4014.37 1 4014.37 62.35Predator species 163482.50 1 81741.20 ,1269.70Predator density 30865.50 1 30865.50 479.44Prey size · predator species 74178.39 2 37089.19 576.12Prey size · predator density 2355.70 1 2355.70 36.59Predator species · predator density 1138.80 2 569.40 8.84Prey size · predator species · predator density 7924.80 2 3962.40 61.50Error 5793.90 90 64.30

searching capability within the space in unit time. Between the prey sizes the difference inthe attack rates varied significantly in case of the backswimmers while in the belostomatidbugs the difference was not pronounced. The difference in the attack rates can be partly dueto the prey size selection and can largely be attributed to the exploitation of the space bythe water bugs that are obviously functions of the species-specific predatory adaptations. Themosquito larvae are metapneustic in nature and for most of the time they were associatedwith the interface between the water and the wall of the containers or with the floating twigsand did not show a uniform pattern of availability in the space. Rarely during the periods ofrest by the predators these larvae were observed to reach the middle part of the trays. The



Figure 4. Clearance rate (CR) values at three prey densities (number 5 L–1) for small (I, II) and large(III, IV) mosquito larvae prey at 2 (I, II) and 4 (III, IV) predators 5 L –1 of pond water of the waterbugs A. bouvieri, D. rusticus and D. annulatus. Values in each graph indicate F values (one-way

ANOVA between predator species).

backswimmers had a contrasting behaviour using the space in respect to these preys, whilethe belostomatids could take a benefit from this situation.

The mutual interference constants for the species were different and reflected the degreeof suppression of prey consumption due to presence of other conspecific predators. In anoth-er sense this is an indicator of aggregation from the part of the predator individuals that tar-get the same patch of prey (ELLIOT, 2003a). For the mosquito larvae the spatial distributionin the habitats can vary from random to clumped and was rarely uniform. Similar observa-tions were made for the belostomatids but not for the notonectids under field conditions (per-sonal observation). In contrast to this the mutual interference of other predatory aquaticinsects like stoneflies, caddisflies feeding on chironomid larvae increased with predator den-sity thus exhibiting a uniform or random dispersal pattern (ELLIOT, 2003a, 2003b, 2005).

The rates of predation of the three bugs during the course of long-term experimentsincreased with the increasing numbers of prey provided. Between the predator species, thedifference in rate of predation was prominent, with A. bouvieri showing a preference moretowards the smaller instars and the belostomatids preferring the larger instar larvae. This dif-ference is quantified in terms of clearance rates, which reflected the ability of the predatorsto regulate the mosquito larvae in the real time situation. The values of clearance rates asobserved here are expected to vary due to the spatial heterogeneity and to multiple preyitems in nature. Nonetheless, as predators, the performance of the three water bugs can beexpected to vary due to morphological features and other ecological adaptations.

The role of many aquatic Hemipteran predators likes Notonecta glauca, N. maculata, A.sardea, Bouenoa sp. (MURDOCH et al., 1984; BLAUSTEIN, 1998; EITAM et al., 2002; KIFLAWI

et al., 2003; EITAM and BLAUSTEIN, 2004; HAMPTON, 2004) in structuring and regulatinginsect communites are well established. The presence of the predator N. maculata, leads todifferential level of oviposition in the mosquitoes Culiseta longiareolata. Also, dytiscid bee-tles, Rhantus signatus signatus as predators were noted together with the dipteran larvae intemporary pools in Buenos Aires, Argentina (FISCHER et al., 2000; CAMPOS et al., 2004). Thewater bugs studied here are expected to play a similar role in structuring the aquatic insectcommunities of the wetlands. However, in nature the presence of multiple prey items can

254 N. SAHA et al.


Table 6. Results of multivariate ANOVA on the effects of interactions of prey density,predator density, prey size and predator species on the Clearance rates of the hemipteranbugs. All F-values are significant at P < 0.001, except those marked with * (P > 0.05).

SS: Sum of squares; MS: Mean square.

Source of variation SS df MS F

Prey size 0.816 1 0.816 45.94Predator species 19.02 2 9.5 535.62Predator density 250.1 1 250.1 14084.9Prey density 2.91 2 1.45 82.08Prey size · Predator species 6.7 2 3.39 191.2Prey size · Predator density 0.001 1 0.001 0.073*Prey size · Prey density 0.03 2 0.015 798Predator species · Predator density 3.73 2 1.8 105.04Predator species · Prey density 0.66 4 0.165 9.28Predator density · Prey density 0.257 2 0.128 7.23Prey size · Predator species · Predator density 0.528 2 0.264 14.86Prey size · Predator density · Prey density 0.06 2 0.03 0.149*Predator species · Predator density · Prey density 0.591 4 0.148 8.318Prey size · Predator species · Predator density · Prey density 1.22 8 0.153 8.603Error 4.77 269 0.0178

influence the dietary preferences of the water bugs, and the trends in the results obtainedhere may differ.

As such, many predators of mosquito larvae are on records but a few succeed to the levelof potential biological control agent of mosquitoes like the larvae of Toxorhynchites (COLLINS

and BLACKWELL, 2000) or the fishes like Poecilia. Habitat specificity, prey preference andabundance in nature are important criteria for selection and qualification as a potential bio-logical control agent. In this respect the water bugs N. maculata (BLAUSTEIN et al., 2004)and the dytiscid beetles Colymbetes paykulli (LUNDKVIST et al., 2003), Rhantus consputus(KÖGEL, 1987) showed a positive preference for mosquito larvae against other dipteran orarthropod preys. The water bugs Sphaerodema (=Diplonychus) nepoides were found to pre-fer mosquito larvae to a range of other preys (VICTOR and UGWOKE, 1987). Similarly, inIndia the copepods Mesocyclops thermocyclopoides have been found to predate and preferthe smaller instars of Anopheles stephensi and Cx. quinquefasciatus larvae against clado-cerans (RAO and KUMAR, 2002; KUMAR and RAO, 2003). Also the prey preference of A. bou-vieri, D. rusticus and D. annulatus need to be further evaluated to understand their role inspecies regulation in aquatic communities or as a biological resource against the mosquitoes.

5. Acknowledgement

The guidance, cooperation and advice received from Prof. NORBERT WALZ in preparing this manu-script are acknowledged with regards and gratitude. The authors are grateful to the respective Heads,Department of Zoology, University of Calcutta, Kolkata and The University of Burdwan, Burdwan, aswell as the Director, Zoological Survey of India, Kolkata, India, for the facilities provided. The fel-lowship provided by the ZSI, Kolkata, to N. S. is thankfully acknowledged. Also, the help from twoanonymous reviewers in modifying the earlier version of the manuscript is thankfully acknowledged.

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Manuscript received October 30th, 2006; revised February 8th, 2007; accepted February 12th, 2007



comparative study of functional response of common hemipteran bugs of east calcutta wetlands, india

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