(J BioI. COlllrol, 22(2): 291-298, 2008 )

Functional response of four predaceous coccinellids, Adalia tetraspilota (Hope), septempunctata L., Calvia punctata (Mulsant) and Hippodamia variegata (Goeze) feeding on the green apple aphid~ Aphis pom; De Geer (Homoptera: Aphididae)

A. A. KHAN and R. A. MIR Division of Entomology Sher-e-Kashmir University ofAgricultural Sciences and Technology of Kashmir, Shalimar, Sri nagar 191121, Jammu and Kashmir, India, E-mail: akhtaralikhan47@rediffil1aiLcom

ABSTRA CT: Functional responses of four coccinellids, I'iz., Adalia tetraspilota (Hope), Coccillella septempullctata L, Calvia plt/letllta (Mulsant) and Hippo(lamiu variegata (Goeze), were evaluated under laboratory conditions to find out how these predators responded to density of the prey species, green apple aphid Aphis pOllli Oe Geer, All the coccinellid species exhibited a convex (Type II) functional response determined by a non-linear model. The non-linear reciprocal transformation of Hollings, disc equation was used to estimate the parameter values of the model. The large predator, C. septempllllctata was seen to eat more aphids due to its greater voracity as compared to the smaller species C. p'lllctata, H, vtlriegattl and A. tetra~1}ilota. C. sepfCltlpllllctala had higher search rate than C. p"Hetllta, H. variegata and A. letraspilola, whereas the handling time showed the opposite trend as the search rate. The results suggest C. septem/lllllctata is the best predator for the biocontrol of Aphis pomi. Further field-based studies are required to confirm this hypothesis.

KEY WORDS: Adalia tetraspilo/a, Aphis pOl1li, Calvill PilI/cia ta , Coccinella sepfemplll/{;tata. fUllctional respollse, handling time, Jiippodamia varieglltll. search rate,

INTRODUCTION numerical response (the change in predator density resulting from a change in prey density) (Solomon, It is well documented that ladybird 1949). Holling (1959, 1965 and 1966) and Trexler et are very efficient predators ofseveral aphid species al. (1988) reviewed the literature on the functional (Trouve et al., 1997; Cardoso and Lazzari, 2003). response of predator to prey density. They The factors that influence the feeding process and classified the functional responses into three main efficiency of these predators as biological control types: an increasing linear relationship (Type I), a agents are voracity (maximum number of prey curvilinear or a decelerating curve (Type II), or a consumed by the predator), functional response sigmoidal relationship (Type 111). Two other types (the change in the number of prey consumed per of functional response have been reported: Type predator in response to changing prey density) and IV (Luck, 1985) and Type V (Sabelis, 1992).

291 KHAN and MIR

Coccinellids usually show a Type II (curvilinear experiments were taken either from the culture or curve) functional response as reported, for example, directly from the field. The adults were placed for adult female Adalia hiplIllctala (Roche, 1998); indi vidually in vials and starved for 24 hrs prior to Hippodamia cOl1vergclIs (Wells and McPherson, an experiment in order to minimize differences in 1999); Cocccllii/a sepfempullctata (Ninkovic and individual hunger levels (Nakamura, 1977). Pettersson, 2003); Propylea dissecta, C. Thereafter, they were introduced singly into a transversalis and Cheilomenes sexmacu/ata separate plastic jar (height 20cm, diameter 15cl11) (Parvez and Ol11kar, 2005), C. septelllplillctata and together with 2,4,8,16,32,64,128 or 256mediuI11 size Chi/ocorlls iflfemalis (Khan and Zaki, 2007); and . aphids on excised apple leaves stuck to agar medium Eriopis ('Of1nexa (Sarmento ct. al., 2007). and covered with a muslin cloth. The test predators were randomly assigned to one of the eight aphid Type H functional response curves can be density treatments. One treatment (the control) was characterized by two parameters: the predator's also allocated for estimating the natural mortality search rate or searching efficiency (a) and its of aphids. At each aphid density, three replicates handling time (Th) (Hassell et al., 1976). The were used for each coccinellid species. After 24 coefficient of searching efficiency determines the hrs, the numbers of aphids consumed by the steepness of the functional response with different predators were recorded by counting the increasing prey density, while handling time aphids remaining alive in each jar. detenTlincs the satiation threshold (Hassell, 1978). Adalia tetraspilota, Coccillella septempuflctata, Data analysis Ca/via pUl1cta/a and Hippodamia variegata are aphidophagolls ladybird beetles abundant in the Search rates (a) are measured in units of horticultural ecosystems of Kashmir, India. Little surface area of habitat for a standard cylindrical jar information is available on the functional responses (size 20 cm height and 15 cm diameter) for standard of these cocciniJlid species to changes in the time (cm2h-l) and handling time (Th) were ill h. The densities of Aphis pomi. Thus, the present study probabilities are generated under the null was designed to investigate the suitability of these hypothesis that the fit of equation 3 to data is due coccinellids as biological control agents against to chance. Aphis pOllli. which is an important apple pest in Kashmir. The number of aphids that have been preyed at the different densities were analyzed for each MATERIALS AND METHODS predator species separately using a non-linear least square programme (R Development Core Team, Experimental arena and test 2005). Usually, it is difficult distinguish between Type H and III functional responses as mentioned Laboratory cultures of the four predatory by many workers (Mills, 1982; Trexler et al., 1988). coccinellid species (Adalia tetraspilota, Hence, prior to fitting the data to a particular Coccillella septempul1ctata, Calvia pUllctata, Holling's Disc equation (1959, 1965) that is Type II Hippodamia variegata) and the aphid Aphis pom; functional response: were established from collections during 2007 in an apple orchard belonging to Sher-e-Kashmir University ofAgricultural Sciences and Technology N = a(N IV)T, " l+aT,,(NIV)·······························(I) of Kashmir, Shalimar Campus, Srinagar-19112 I (Jammu and Kashmir), India. The coccillellid and aphid cultures were maintained in a cu1ture room at where, Na is the number of prey consumed by one 25± 5°C temperature, 60 ± 10% relative humidity predator during a time period T. N is the initial prey and a photoperiod of l4 hour light: 10 hour dark. density; V is the volume of th~ experimental cage and a and T" is as above. However, the above The adult coccinelllds used for the equation describes the instantaneous predation

292 Functional response or lour eoccincllids

rates and does not account for the change in prey RESULTS AND DISCUSSION density during an experiment due to predation (Hassel et aI., 1976; Royama, 1971; Rogers, 1972; The functional response of a predator McArdle and Lawton, 1979). In contrast, the offers an excellent framework for considering the "random predator equation (2)" of Rogers (1972) potential action ofbioagents in inundative releases takes prey exploitation il1to consideration. It is (Burgio et al., 2005, Waage und Greathead, 19S5). derived from As seen from Fig. I, the functional responses ofA. tetraspi/ota. C. septelll{)llIlclata, C. jJ//IIC{(1W and H. l'ariegafa to the density of Aphis pomi were dN a(N/V) typically of Type II with a steep initial rise in lit l+aTI;(N/V) ...... (2) predation rates as the prey density increased (Table 1 ). C. septempullc!ata .\. consumption increased to Wbich integrates to: 26.06 aphids per day (Fig. \b) which was higher than that orc pllllclala (21.73), H l'CJriega!a ( 19.73) and A. tetraspi/ofa (18.40) (Fig. I c, Fig. I d and Fig. 1a). A Type II functional response has been repol·tcd N" = (~ )(1- exp(- a(I; - T"NJL ...... (3) for other coccinellid species, e.g. larva oflJarl/uJllic. a.\)'ridis (Mogi, 19(9), C. sepfellljJllllcfa/a (Sinha Equation 3 now allows a and I'll to be calculuted by et al., 1982, Khan and Zaki, 20(7), A. hipllllcta{a itemtion from experiments in which the consumed (Roche, \998), /-lippodwllia co"vergem (Cardoso prey individuals are not replaced. In order to avoid and Lazzari, 2003), C. transversalis (Pcrvcz and the errors incurred by applying the linear regression Ol11kar, 20(5), c. l4ernalis (Khan and Zaki, 20(7) method to estimate a and Th as suggested by and Eriopis COl1lleXa (Sarmento et al., 2(07). Rogers (1972), we used the non-linear function (n Is) The larger species, C. seplempullc/o{a provided by the R-software (R Development Core followed by C. pun elata, were shown to consume Team, 2005). more Aphis pomi than JI. variegata and A.

Table1. Parameter values of Holling's disc equation estimated from functional response experiments with predaceous ladybird beetles feeding on green apple aphid, A./Jomi.

Predatory coccinellids Parameter Estimate SO t value ratp

Adalia tetraspilota =At. Coccinella septempullctata= Cs. Calvia pUJ/ctata= Cpo Hippodamia Fareigala =Hv.

293 KHAN and MIR

tetraspilota. Isikber (2004) reported that the large Regrettably, the non-linear model for functional species eye/olleda sanguinea consumed more response of predaceous coccinelids is least Aphis gossipyii than the small species SCYIJII1I1S documented. levaillanti. Similarly, Hemptinne et al., (1996), in an The search rate (a) and handling time (Th) experimental study of two-spotted ladybeetle, estimated for the four coccinellid predators are Ada/ia hiplinetata, on Aeyrthosiphol1 pislIlJ1 found presented in Table I and Figs. 2 and 3 which show that at high prey densities, females ate more aphids that C. septempul1ctata had the highest search rate, than males to meet growth and reproductive followed by C. pIll/ctata, H. variegata and A. requirements. A comparison offunctional response tetraspilota. The handling times of the predators curves revealed that C. septempullctata responded were just the opposite of the search rates with A. more vigorously to lower densities of A. pomi than tetraspilota being the highest and C. pUllctata the C. {JuJletata and H. I'ariegata did. However, the number of prey consumed per time unit increases, smallest. The effect of different sized coccinellids on the rate of successful encounters ,vith A. pomi but the proportion of prey killed declines with prey is shown in Fig.2. Obviously, the search rate is density if the functional response is Type II. The determined by the movement speed, reactive result indicates that C. septempulle/ata has a higher functional response than any of the three other distance at which a predator responds to the prey species at all the densities ofprey. Pervez and Omkar of presence and prey and the proportion of attacks (2005) reported that the functional response of C. that are sllccessful (Holl ing, 1965). The search rate IrollsFcrsahs showed an earlier and steeper increase and the handling time are the parametel's that reflect than that of Cheiloll1cncs sexmaclilata when the the significance of these responses. The fact that density densities of two aphids, A. craceivora and these parameters differed significantly among the Afl'z/lS persicae increased and the former species coccinellid species when exposed to A. pond also approachcd a higher level of predation than indicates that the four predatol' species possess the latter. different capacities to pursue prey at increasing aphid densities. It also shows that coccineHids The results show that a Type [I curvilinear manifesting similar qualitative response cUI'ves may curve provides an adequate description of the data. not necessarily have the same quantitative impact The upper asymptote of the relationship showed on the prey. The values of different parameters indicates the maximum possible predation rate. A varied due to the differences in size, greediness, non-linear model was further lIsed to detect whether satiation time, hunger levels, digestive power, the functional response fitted the data better than searching speed, etc. (Ofuya and Akinbohungbe, a Type III. Such a response could indicate that the 1988; Omkar and Pervez, 2004). predator improved its perfom1ance due to switching or learning. Although the logistic model (Juliano, Of the four coccinellids, C seplempullctata 200 1) easily illuminates the delicate differences in was the one that responded most to increasing Type II and Type III, it fails to distinguish them densities of A. pomi, followed by C. pune/ata, H from a linearly rising curve (Type O. The variegata and A. tetra.\pilola. This result is forcibly experimental data, particularly C septemplilletata supported by empirical data of the reproductive feeding on A. ponli at low density, seem to satisfy a biology of C. septempullctata, which acquires Type I functional response; the data were more greater values in adaptation and reproductiol1l1sing closely fitted to equation 2. The differences among A. pomi than the other species of coccinellids. predator responses at lower and higher prey Handling time differs signi ficantly among predatory densities may lead to wrong predictions. coccinellids. The observed handling time is the Henceforth, efforts must be invested in fitting an accumulative impact of time taken during searching analogous logistic model so as to distinguish Type and capturing, preying, overpowering and I from I I and i I I (Pervez and Omkar, 2005). digesting the prey {Omkar' and Pe/'vez, 2003}. The

294 --~-<.------"~ \:::::, ~ ", ~~ ~I m ~ ;/ " z ':6 U ,1' ", I " ~1 ~ ~ ;/ .:::; ~ - 8 >- ~ -1', :e? ::L "- ! I '" ~ 0 50 100 150 200 250 0 50 100 150 200 2'50

Prey density(N) Prey densily(I'j)

(a) (b)

0 "-' N '"

0 N ;c? 0J OJ Z z is' U '" ~ co / c ;::> 8 :3 :;:,... ij) ! a' Ct: :1 ct .,-, / ~ "III 50 100 0 50 100 150 200 250 0 150 200 250 Prey aensity(N) Prey densit1(N)

(C) (d)

Fig. 1. The mean number of A. pomi eaten by individual predaceous ladybird beetles (a) Adalia tetraspilota (b) Coccinella septempunctata (c) Calvia punctata (d) Hippodamia variegata. All curves are Type II functional responses fitted by Holling's disc equation model (Holling, 1959) using the parameter values given in Table 1. signi fic

295 KIIAl'. ;Jllll Mil<

3.5 3 2.5 .-.. ~ '-' ~ 2 ....~ ..c 1.5 ~ 0 '" 1 0.5 0 At Cs Cp Hv Ladybird beetles

Fig. 2. The search rate (a) for predacaceous ladybird beetles preying on Aphis pomi. Exact numerical values are given in Table 1.

1.4

1.2

1

0.8 ~ 41 E 0.6 +i 0'> .S: 0.4 '6 c ('!I :r: 0.2

0 At Cs Cp Hv Ladybird beetles

Fig. 3. Thebandling time (Th) for predaceous ladybird beetles preying on Aphis pomi. Exact numerical values are given in Table 1. tool for investigating the type and shape of management of A. pomi. However, further field functional responses. All the four coccinellids studies are required in order to reveal the predator's showed Type II functional responses, which varied capacity under natural conditions. quantitatively among the species feeding on single A. pomi. The highest search rate and lowest ACKNOWLEDGEMENT handling time was exhibited by C. septempunctata followed by C. punctata. H. variegata and A. This research has been funded by leAR, New Ictraspilota. C. septempunctata has the efficiency Delhi, under the Horticulture Technology Mission to become un important biocontrol agent for the Project entitled "Mass production and supply or

296 FUllctionul response 0 r four eoccincllids

bioagents for the management of horticultural Juliano, S. A. 1993. Nonlinear curve fitting: predation pests". We are grateful to Dr. Athar Ali Khan and functional response curves. pp. 159-181. In: Associate Professor, Division of Agriculturai Design and A lIall's is ofEcological E,perimcllts (Eds. Statistics, for his assistance with the statistical S. M. Scheiner and J. Gureritch), Chapman and HaH, New York. analyses. REFERENCES Khan, A. A. and Zaki, F. A. 2007. Predation rates of Coccil1ella septempullctata Linnaeus and Chi/ocorlls Burgio, G., Santi. F. and Maini, S. 2005. Intra-guild i1!fernalis Muisant on aphids. Asial1 JOllrnal ofBio preda t ion and cannibal ism between Harmonia Sciences, 2( I): 53-55. axyridis and Adalia biplIl1ctata adults and larvae: laboratory experiments. Bulletin ojJllScc/olog): 58(2): Luck, R. F. 1985. Princip les of predation, pp. 135-140. 497-530. In: Ec%gv and Entoillology (Eds. C. B. Huffaker and R. L. Rabb), Wiley, New York. Cardoso, J. T. and Lazzari, S. M. N. 2003. Consumption of CinclI'a spp. (Hemiptera: Aphididae) by McArdle, B. H. and Lawton, J. II. 1979. Effects of prey eye/oneda sal/guinea (Linnaeus, 1763) and size and predator instar on the predation of Dapllll fa Hippodamia convergens Guerin-Meneville, 1942 by Notonecta. Ecological Entomology. 4: 267-275. (Coleoptera: ). Revista Brasileria de Elltomologia. 47: 443-446. Mills, N. J. 1982. Satiation and the funetiollnl response: A test of a new model. Ecological Entomology, 7: Hassell, M. P. 1978. The Dynamics of Arthropod 305-315. predator-Prey S.vslems. Princeton University Press. Mogi, M. 1969. Predation response of the larvae of Harmonia axyrfdis Pallas (Coccinellidae) to the Hassell, 1\.1. P., Lawton, 1. H. and Beddington, J. R. 1976. different prey densities. Japanese Journal (~lApplf{'d The components of arthropod predation. i. The prey Entomology and Zoology. 13: 9-16. death rate. Journal ofAnimal Ecology, 45: 135-164. Nakamura, K. i 977. A model for the functional response Hemptinne. J. L., Dixon, A. F. G and Lognay, G 1996. ofa predator to varying prey densities based on the Search behaviour and mate recognition by males of feeding ecology of wolf spiders. Bu/letin of the Natiol1allnstilutcO{Agricultural Sciences (Tokyo), the two-spotted ladybird , Adalia bipunctata. Series C 31: 29-89. Ecological Entomology, 21: 165-170.

Ninkovic. Y. and Pettersson, 1. 2003. Searching behaviour Holling, C. S. 1959. Some characteristics of simple types of the seven spotted ladybird, Coccillella of predation and parasitism. Canadian septempullctata-effects of plant-plant odour Entomologist. 91: 385-398. interaction. Gikos, 100: 65-70. Holl ing, C. S. 1965. The functional response of predators Ofuya. T. I. and Akingbohungbe, A.E.1988. Functional to prey density and its role in mimicry and and numerical responses of Cheilomcllcs lunata population regulation. Memoirs ofthe Elltomological (Fabricius) (Coleoptera: Coccinel1idae) feeding on Society ofCanada. 45: 3-60. the cowpea aphid, Aphis craccivora Koch (Homoptera: Aphididae). Illsect Science and its Holling, C. S. 1966. The functional response of Application, 9: 543-546. invertebrate predators to prey density. Memoirs oj tile Ecological Society ofCall ada. 48: 1-86. Omkar and Pervez, A. 2003. Ecology and biocontrol potential of a scale predator. Chilocorus Iligrillls. lsikber, A. A. 2005. Functional responses of two Biocolltrol Science alld Technology, 13: 379-390. coccinellid predators, Sc.vmllllS levaillanti and Cyclolleda .mnguinea, to the cotton aphid. Aphis Omkar and Pervez, A. 2004. Functional and numerical gossypii. T/lrkey Journal oj Agriculture. 29: 347- responses of Prop'vim dissecta (Col., Coccinellidac). 355.

297 KHAN and MIR

JOllma{ OfApplied Entomology, 128: 140-146. Brazilian Archives ofBiolog~' {lnd Technology, 50: 45-50. Pervez, A. and Omkar, 2005. Functional responses of Coccinellid predators: An illustration of a logistic Sinha, T. B., Pandey, R. K., Singh, R, Trirathi, C. P. M. approach. Journal of/nsee! Science, 5: 319-325. and Kumar, A. 1982. The functional response of Coccil/ella seplemplillctatll Linn., a Coccinellid R Development Core Team 2005. R: A language and predator of mustard aphid, Upaphis cr\'sillli Kalt. environment for statistical computing. R Foundation EIl(OmOIl, 7: 7-10. for Statistical Computing, Vienna, Austria. ISBN 3- 900051-07-0, URL http://www.R-project.org. Solomon, M. E. 1949. The natural control of population. Journal o.fAllimal Ec%g\". 18: J-35. Roche, J. P. 1998. The functional response of increases Trexler, 1. c., Me Culloch, C. E. and Travis, J. 1988. in aphid density in female two-spotted lady beetles, How can the functional response best be Adalia hiplIlIetata. Animal Behaviour Bulletil1, 3: determined? Deco/agia, 76: 206-214. 411-413. Trouve, c., Ledee, S., Ferran, A. and Bnm, J. 1997. Rogers, D. 1972. Random search and insect population Biological control of the damson-hop aphid, models. Journal ofAnimal Ecology, 41: 369-383. PllOrodoJl 11lII11uli (Homoptcra: Aphididae), using the lady beetle, Harmonia (uyridis (Coleoptera: Royama, T. 1971. A comparative study of models for Coccinellidae). Elltomoplwga, 42: 57-62. predation and parasitism. Researches all population Ecology supplement. J: 1-9 I . Waage, J. K. and Greathead. 0, J, 1988. Biological control: Challenges aud opportunities. P/iilosophical Sabel is, M. W. 1992. Predatory , pp. 225- IraJ/sactiollS ofl/ie Royal Saci<'fY (~rL()l1doll, B 318: 264. In: Nalural Enemies: The Population Biology II 1-128. of Predators, Parasites and Diseases (Ed. M. J. Crawley), Blackwell, Oxford. Wells, M. L. and Me Pherson, R. M. 1999. Population dynamics of three coccinellids ill Iluc-cured tobacco Sarmento, R. A., Pallini, A. Venzon, M., Souza, O. F. E, and fUllctional response of Hippodumi a cO/ll'ergens Molina-Rugama,A. J. and Limade Oliveira, C. 2007. (Coleoptera: Coccinellidae) fceding onlobacco aphid FUllctional response ofthe predator Eriopis COllllexa (Homptera: Aphididae). Em'irolllllcllwi EI/toll/ology, (Coleoptera: Coccinellidae) to different prey type. 28: 768-773.

(Received: 28.09.2007; Revised: 03.11.2007~ Accepted: 21.11.2007)

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