INTRODUCTION. Joumal oj Aphidology. 19: The Aphidologtcal Society. India ISSN

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1 Joumal oj Aphidology. 19: The Aphidologtcal Society. India ISSN FEEDING POTENTIAL AND ITS EFFECT ON DEVELOPMENT OF AN APHID PREDATOR, EPISYRPHUS BALTEATUS (DE GEER) (DIPTERA: SYRPHIDAE) VIs-A-VIS VARIABLE PREY DENSITY Raina N. Samuel, I.J. Dass & R. Singhl Department of Zoology, St. Andrew's College, Gorakhpur , U.P., India. laphid Biocontrol Laboratory, Department of Zoology, DDU Gorakhpur University, Gorakhpur , U.P., India. .rsmgh gpussyahoo.corn Abstract : Feeding potential of an aphid predator. the larvae of Ephisyrphus balteatus (De Geer) (Diptera: Syrphidae) and its effect on its development was studied at different preypredator ratio as aphids are usually patchily distributed. and hence patches of different aphid numbers are simultaneously available to the individual predator. Two aphid species. viz., Lipapiiis erysimi (Kalt.) (reared on mustard, Brassica campestris and cabbage, B. oleracea var. capitata) and Macrosiphoniella sanbomi Gillette (reared on chrysanthemum) were provided to the predatory larvae as food resource. The results show a positive density-dependent predation rate which corresponded to the Holling's type I functional response. Amount of food consumed by the larvae determine the larval and pupal duration and even their survival. The larvae of E. balteatus required at least 20 aphids/day for proper growth and development; 80 aphids/day was found to be the optimum number at which the larvae consumed aphids for their complete development and emergence: and normal duration of adult longevity was of days. In field, it was observed that the adult females of E. balteatus also determine whether to deposit. based on the patch-size of the prey. They have been found to oviposit very judiciously accounting the number of preys to avoid shortage of food to their young ones. In other words, the gravid females demonstrated a positive density-dependent response to aphid colony size in terms of oviposition behaviour. Key words: Episurphiis balteatus, density-dependent predation, feeding potential, predation rate, functional response. INTRODUCTION Syrphids are one of the most important predators of many economically important aphid species and are known to regulate the prey population effectively (Tamaki et al ; Pollard. 1969; Chamber et al., 1983; Tenhumberg, 1995). The larvae of hover fly, Episyrphus balteatus (De Geer) (Diptera:Syrphidae) are natural aphidivores in feeding habit. All adult syrphids. however. are melhphagous, i.e., they feed on nectar and pollen, the protein from the latter being essential for the maturation of gametes in both sexes (Gilbert, 1981). Aphidophagous syrphids are high performance insects and although strong fliers, fare relatively poorly when weather is cold, wet or windy (Lewis, 1965). Aphid colonies are ephemeral sources: they can appear quickly and just as suddenly disappear due to predation, parasitism, fungal eptzootics, declining host plant quality, changes in weather, or dispersal. Therefore, it is important for the predators to locate aphid infestations quickly. Because of their strong flight and

2 94 Raina N. Samuel. J.J. Dass & R. Singh ability to hover and inspect foliage for aphids. syrphids are especially adept at this. Economically, the predaceous larvae of E. balteatus are notable in being important enemies of aphids, mainly Aphis gossypii Glover, A. Koch Lipaphis erysimi (Kalt.], Myzus persicae (Sulzer], and Macrosiphoniella sanbomi Gillette serving as common accepted food of the predator. In its about 14 day development period, one larva sucks several hundred aphids. Prey finding of first instar larvae exhibited directed search over short distance (several millimeters) guided by olfactory cues from aphids, but not from honeydew (Bargen & Poehling, 1996; Bargen et al., 1997, 1998). Impressive images of the "tricks" a larva uses to overcome its prey have also been captured, for example, it "ties up" a whole colony with its secretion and bit-by-bit sucks them dry. Prey density-dependent predation is considered an important condition for the stability of predator-prey interactions and the success of biocontrol. The present programme of investigation on prey consumption and its effect on development of an aphid predator, E. balteatus in relation to variable prey density was undertaken chiefly to comprehend and realise more precisely the hitherto unknown role, significance and limitation of this predator in biocontrol programmes of the aphids. MATERIALS & METHODS The stock cultures of E. balteatus and aphids, L. erysimi and M. sanbomi were collected from the experimental plot of 7.40 x 5.50 m dimension, located in the botanical garden of the institution. The production process consisted of three separate steps viz., raising of host plants of mustard. Brassica campestris Linn., cabbage, Brassica oleracea, L. var. capitata and Chrysanthemum sp.. rearing of aphids as food for the predator and rearing of E. balteatus in the laboratory. and these three steps were followed simultaneously. The performance of the predator was evaluated by studying its predation rate at variable prey-predator ratio. To enquire into this aspect, three different series of trials were arranged. In the first series, a single newborn larva «24 h) of E. balteatus in each case was individually allowed to continue its post-embryonic development to adult on 5, 10, 20, 40, 60, 80, 100 and 120 aphids provided per day, in separate glass tubes (4xlO cm) covered at the top by a piece of muslin cloth fastened by elastic bands. At each prey density level five replicates were arranged. In this trial the aphids provided to the larvae were of L. erysimi reared on mustard plants. In each of these maggot's rearing tube, prey consumption was recorded and the number of fresh aphids as specified for each replicate were replenished daily. The larvae underwent pupation and were allowed to metamorphose into adults. Developmental ability of each maggot, based on its life cycle parameters i.e., larval, pupal durations, their emergence into adult male or female, adult longevity and progeny sex ratio, t.e., proportion of males in the population was determined in relation to the programmed effect of prey density in each of predator's rearing regime. In the second and third series of trials all the experimental details remained unchanged except the prey aphids were L. erysimi fed on cabbage and M. sanbomi fed on chrysanthemum plants, respectively. The experiments were conducted at 22 ± 1 C temperature and 60-75% RH. RESULTS Data regarding the influence of variable prey-predator ratio on predation rate of E. balteatus and its effect on the developmental parameters of the predator i.e.. its larval and pupal durations, adult longevity and progeny sex ratio are displayed in Table 1-3. In the first set of trials where the larvae were fed on chrysanthemum aphid,

3 Table: I. Effect of prey density on feeding potential, larval period, pupal period, larval and pupal per cent mortality, adult longevity and progeny sex ratio of Episyrphus balteatus when fed on Macrosiphoniella sanbomi reared on Chrysanthemum sps. Data are expressed as mean ± S.E..,.. LARVAL PERIOD PUPAL PERIOD ADULT. ""' - Mean Mean Mean Mean Mean pupal Mean adult Il.W consumption Per cent Per cent Sex «onsurn pilon consumption larval period period In longevity In c during larval mortality mortality ratio In Itrst 5 days per day in days days days period ± ± ± ± ± 0.2d ± :t: ± ± 0.2d ± ± ± ± 0.3e ± 0.2a 1.75 ± 0.3a ± ± ± ±0.2b ±0.2a 1.8 ± 0.3a ± ± ± ± 0.3a 0 7.8±0.la 15.8 ± 0.8 b ± ± 1.4 4'13.4 ± ±0.4b ± 0.2a 16.6 ± 0.3b ± ± ± ±0.4b ±0.2a 17.2 ± 0.5 h 0.8 Regression (y = a + b x) a b r p < < < 'Tj ro ro 0- S'!1C\ '0 oe+ ro ::l Co o-,. ::l" 0: '0 0- o [ii' \t:: "ti [ I Note: Entire data is based on observations collected from 5 separately arranged replicates per trial. Mean values superscripted by common letter do not vary significantly. a: Intercept, b: Slope, r: correlation coefficient, P: Level of significance. to (]I

4 to OJ 96 Raina N. Samuel, I.J. Dass & R. Singh Table 2: Effect of prey density on the feeding potential, larval period, pupal period, larval and pupal per cent mortality, adult longevity and progeny sex ratio of Episyrphus balteatus when fed on Lipaphis erysimi reared on mustard Brassica campestris. Data are expressed as mean ± S.E. LARVAL PERIOD PUPAL PERIOD ADULT - Mean Mean Mean Mean Mean pupal Mean adult o..w consumption Per cent Per cent Sex consumption consumption larval period period in longevity in Q during larval mortality mortality ratio In flrst 5 days per day in days days days period ± ± ± ± ± 0.25d ± ± ± ± 0.15c ± 0.2a 2.0 ± 0.2a ± ± ± ± 0.2c - 8.2±0.la 2.0 ± 0.3a ± ± ± ±0.2a - 7.2±0.la 4.4 ±0.4b ± ± ± ± Oa a 17.8±0.7c ± ± ± ± o a 17.8 ± 0.4c ± ± ± ± 0.2b a 18.2 ± 0.3 c 0.2 Rezresston tv = a + b xl a b r p <0.001 <0.001 < r.n 8.:?-... c... o [Jl R> ;:0 r.n s Note: Entire data is based on observations collected from 5 separately arranged replicates per trial. Mean values superscripted by common letter do not vury significantly. II: Intercept, b: Slope, r: correlation coefficient, P: Level of significance.

5 Table 3: Effect of prey density on the feeding potential, larval period, pupal period, larval and pupal mortality, adult longevity and progeny sex ratio of Episyrphus balteatus when fed on Lipaphis erysimi reared on cabbage, Brassica oleracea var. capitata, Data are expressed as mean ± S.E. B. S (1Q ><t LARVAL PERIOD PUPAL PERIOD ADULT Mean Mean Mean Mean Mean pupal Mean adult o... consumption Per cent Per cent Sex consumption consumption larval period period in longevity in 0 during larval mortality mortality ratio in first 5 days per day in days days days period 5 24.B ± ± * 224.0* BO 23.0* d ± ± O.le - B.O + 0.4h a B ±0.3a Oa 3.B +0.3h ± ± ± ± 0.2a - 6.B±0.la 5.0 ± 0.3h 0.6 BO ± O.la o ± O.4e ± B ±0.3h a 20.6 ± O.4e ± B + 0.3e a 21.2 ± 0.8e 0.4 ReI! ession (v = a + b xl a b r B p < < < Note: Entire data is based on observations collected from 5 separately arranged replicates per trial. Mean values superscripted by common letter do not vary Significantly. a: Intercept. b: Slope. r: correlation coefflcient,p: Levelof significance. '1:l o sg. E ọ...,. e: 0- '1:l 0- S!"1 fii' \.t:: 1: f co --.J

6 98 Raina N. Samuel, I.J. Dass & R. Singh M. sanbomi reared on chrysanthemum, an increase in prey density exhibited a corresponding increase in mean consumption in first five days, mean consumption per day and mean consumption during total larval period (Table 1). The observation on the functional response (Diraviam & Viraktamath, 1991) of E. balteatus on M. sanborru showed that the predator responded positively to the increasing prey density t.e., a positive correlation was evident between the two. A linear relationship between feeding potential/predation rate and prey density was clearly exhibited under three observed conditions (Table 1) which demonstrated that the prey density has a Significant influence on the rate of prey consumption which corresponds to the type I functional response of Holling (1959). Effect of variable prey density on the life history parameters of E. balteatus showed that an increase in prey density resulted in progressive decrease in mean larval period. At lowest prey density level t.e., 5 aphids per day, none of the larvae developed to pupal stage. However, with increase in prey number, the larvae completed development to pupae with 600Al and 8oo/o success when 10 and 20 aphids were given per day, respectively. Moreover, when the food supply increased beyond 20 aphids/day, all the larvae developed to pupae (Table 1). The shortest mean larval period was recorded at prey density of 80 aphids/day and the same number of aphids was also found to be optimum for a single day consumption as any increase in prey density above SO aphids/day began to show an upward trend in mean larval duration. The pupal duration did not show any noticeable change except that below 20 aphids/day there was 100% pupal mortality. The adult survived hardly for 2 days if during the larval period they were given less than 60 aphids to feed per day. Ho.. ewr. if they were provided SO aphids vday or above the adult longevity showed its normal duration i.e., days. The progeny sex ratio (proportion of males in the population) was always more than 0.5 at higher prey density (Table 1). In the second set of trials where the larvae were fed on mustard aphids, L. erysimi fed on mustard plant, an increase in prey density showed a corresponding increase in mean consumption in first five days, mean consumption per day and mean consumption during larval duration (Table 2). The findings on the functional response of E. balteatus on L. erysimi reared on mustard revealed that the predator responded positively to increasing prey density i.e., a positive correlation was exhibited between the two like the first set of experiment. A linear relationship between feeding potential and prey density was explicitly evident under three observed conditions (Table 2). These findings revealed that the prey density has a significant effect on the rate of prey consumption. Effect of variable prey density on lifecycle parameters of E. balteatus showed the same trend as observed for earlier set, i.e.. a progressive increase in prey density resulted in corresponding decrease in mean larval period but not the pupal period. At 5 aphids/day all larvae died before pupation, however, SO% (10-20 aphids/day) and 100% larvae reached pupal stage when they were given 40 aphids/day and above (Table 2). The shortest mean larval period was of 7 days, observed at 80 aphids/day and an increase the number above it, began to show an increase in mean larval duration. The pupal mortality was 100% if the.larvae were given less than 10 aphids/day, 25% at 20 aphids/day and cent percent at 40 and above aphids/day. The adult survived for 2-4 days at less than 60 aphids per day, but at SO aphids/day and above they lived for 17- IS days (Table 2). The progeny sex ratio except at 100 aphids/day (O.S) was less than 0.5 at all prey densities (Table 2). In the third set of trials where the syrphid larvae were exposed to L. enjsimi

7 Feeding potential of an aphid predator, Episyrplw.s balteatus 99 reared on cabbage, an increase in prey density did show a corresponding increase in mean consumption in first five days and mean consumption per day from 5 aphids per day to 120 aphids per day like earlier two trials. The higher level of mean prey consumption at 10 and 20 aphids per day may be attributed to lengthening in larval duration and not due to higher predation rate (Table 3). The functional response of E. balteatus on L. erysimi reared on cabbage, revealed that the predator responded positively to increasing prey density i.e., a positive linear correlation was exhibited between the two (Table 3). These findings vindicated the view, established earlier that prey density has a significant effect on the rate of prey consumption. Influence of variable prey density on developmental ability of E. balteatus unlike previous trials showed a mixed trend. At lowest prey density level I.e., 5 aphids/day, larval mortality was 100% and at 10 aphids/day it was 80 per cent while no larval mortality was observed at 20 aphids/day and above. There was a lengthening in larval duration at 10 and 20 aphids/day (23.0 and 9.2 days, respectively). but from aphids/day, there was shortening in mean larval duration (6-7 days), which again began to increase from 100 aphids/day onwards (8-10 days). The pupal mortality was 100% at 10 aphids/day, while no mortality was observed above it. The mean pupal duration was maximum of 8 days at 20 aphids/day and minimum of 6.4 days at 120 aphids/day. The mean adult longevity at prey densities from 20 to 60 aphids/day ranged from 2 to 5 days but from 80 to 120 aphids/day, the mean adult longevity ranged from days (Table 3). The progeny sex ratio varied from 0.2 (40 and 100 aphids/day) to 0.8 (20 aphids/day) without showing any relationship with prey density. A comparison of mean feeding potential of E. balrearus larvae in first five days on L. erysimi reared on mustard and cabbage. and.'1. sanbomi reared on chrysanthemum revealed that there was no significant difference between them when the prey density level was less than optimum i.e., from 5 to 40 aphids/day/ predator but when prey density level reached the threshold limits i.e., from 60 to 120 aphids/day the difference in feeding potential became significant at 1% level in favour of prey aphids reared on cabbage [Table 3). Progeny sex ratio is highly variable with food plant, aphid species and its number exposed to the prey. DISCUSSION Predation is an example of interspecific interaction between two populations or species, which results in negative effects on the growth and survival of one of the populations or species. The results demonstrated that the predatory larvae of E. balteatus showed a positive response to a programmed increase in prey density by increasing their predation rate, a desirable attribute of any bioagent. Hairston et al (1960) suggested that population regulation at the herbivore level (primary consumer) is fundamentally different from that at other trophic levels. The populations of producers, carnivores and decomposers are limited by their respective resources in the classical density-dependent fashion, and therefore, interspecific competition must necessarily exist among members of these three groups. In contrast, herbivores are seldom food-limited, but appear most often to be predation-limited, and therefore, not likely to compete for common resources. Undoubtedly, the generalisation appears to be far too sweeping (Singh. 2003). The best way to be objective is to consider predation from the population rather than from the individual stand point. Predators certainly kill their prey and depress them in some measure at least the growth rate of population or reduce the total population size.

8 100 Raina N. Samuel, I.J. Dass & R. Singh The decrease in food resource below the optimum amount always increases the larval duration, therefore, in spite of low predation rate, they consume considerably high amount of preys. The data displayed in Table 1-3 show that all the three food resources are almost equally acceptable to the predator, however, the survival of the developing stages is better on L. erysimi-b. o/eracea var. capiiaia even at lower prey densities (20 aphids/day). Similarly, the adults also survived for more days when the larvae were fed this food resource. Therefore, for mass rearing of E. balteatus these results should be taken into account in order to enhance the production of insects and optimize the fitness of adult sysphids at the release site. In nature, however, the prey selection of E. balteatus highly depends on the capability of the females to select aphid species and respective host plants that can provide the larvae with qualified food. Acknowledgements: We (RNS and IJD) thank to the authorities of st. Andrew's College, Gorakhpur for providing necessary working facilities. One of the authors (IJD) is also grateful to U.G.C., New Delhi for providing financial assistance (No. F.6-102/2002 (MRP/NRCB)). REFERENCES Bargen, H. & Poehling, H.M. (1996). Mechanismen der Beutefindung von Epistjrptuis balteatus Deg. 50. Deutsche Pflanzenschutztagung in Munster, September Mitteilungen aus der Biologischen Bundesanstalt fur Land-und Forstwirtschaft, Heft 321. p Bargen, H.. Saudhoff, K. & Poehling. H.M. (1997). Mechanismen der Beutefindung von Episyrphus bolteatus, Entomologen Tagung Bayreuth. p Marz Bargen, H.. Saudhof. K. & Poehling. H.. (1998) Prey finding of larvae and adult females of Episyrphus balteatus. Ent. Exp. Appl. 87: Chambers. R. J.. Sunderland. K.D.. Wynt. I. J. & Vickerman. C. P. (1983). The effect of predator exclusion and caging of cereal aphids in the winter wheat. J. Appl. Econ. 20: Gilbert. F. S. (1981). The foraging ecology of hover flies (Diptera: Syrphidae): Morphology of the mouthparts in relation to feeding on nectar and pollen in some common urban species. Ecol. Ent. 6: Hairston, N.G., Smith. F.E. & Slobodkin, L.B. (1960). Community structure, population control and competition. Amer. Nat. 94: Holling. C.S. (1959). Some characteristics of simple type of predation and parasitism. Can. Ent. 91: Lewis. T. (1965). The effects of an artificial windbreak on the aerial distri-bution of flying insects. Ann. Appl. Bioi. 55: Pollard. E. (1969). The effect of removal of arthropod predators on an infestation of Brevicoryne brassicae (Linn.) (Hemiptera: Aphtdtdae) on brussel sprouts. Ent. Exp. Appl. 12: Singh. R. (2003). Tritrophic interactions with reference to biological control of insect pests. Biological Mem. 29: Tamaki, G.. Lndts, B. J. & Weeks. R. (1967). Autumn populations of green peach aphid on peach trees and the role of syrphid flies in their control. J. Econ. Ent. 60: Tenhumberg, B. (1995). Estimating predatory efficiency of Episyrphus balteatus (Diptera: Syrphidae) in cereal fields. Env. Ent, 24:

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