Pure Appl. Biol., 5(4): 671-681, December, 2016 http://dx.doi.org/10.19045/bspab.2016.50069
Research Article
Functional response of Coccinella septempunctata L. (Coleoptera: Coccinellidae) on Ommatissus lybicus (Homoptera: Tropiduchidae)
Arif Shah1*, Muhammad Qasim Kakar2, Atta Ullah2, Abdul Razaq2, Nikos E. Papanikolaou3, Toheed Iqbal4 and Habib Ullah5 1. Balochistan Agriculture College Quetta, Pakistan 2. Department of Agriculture (Extension) Balochistan, Pakistan 3. Biodiversity Conservation Laboratory, Department of Environmental Sciences, University of the Aegeen, Mytilene 81100, Greece. 4. Department of Entomology, University of Agriculture, Peshawar, Pakistan 5. Department of Agriculture (Research) Balochistan, Pakistan *Corresponding author’s email: [email protected] Citation Arif Shah, Muhammad Qasim Kakar, Atta Ullah, Abdul Razaq, Nikos E. Papanikolaou, Toheed Iqbal, and Habib Ullah. Functional response of Coccinella septempunctata L. (Coleoptera: Coccinellidae) on Ommatissus lybicus (Homoptera: Tropiduchidae). Pure and Applied Biology. Vol. 5, Issue 4, pp671-681. http://dx.doi.org/10.19045/bspab.2016.50069 Received: 26/05/2016 Revised: 02/06/2016 Accepted: 10/06/2016 Online First: 17/06/2016 Abstract Dubas bug, Ommatissus lybicus (Homoptera: Tropiduchidae), is a major insect pest of date palm. Adult and nymph stages suck sap from all green parts and cause direct and indirect damage. Large number of predators feed on it; however, no information is available on their consumption rate and functional response using this prey. We aim to find out consumption rate of Coccinella septempunctata with an objective how adult female and fourth nymphal instars of C. septempunctata responds to 1st and 3rd instar nymphs of O. lybicus at various density levels under controlled condition. Both stages of C. septempunctata exhibited a type II functional response. Handling times and attack rates were significantly different between adult female and larval stage indicating that predator responds differentially to prey stage offered at same density. Estimated handling time of C. septempunctata adult female and fourth instar (in bracket) at 24 hours were 0.563(0.692) and 1.008(1.492) and estimated attack rate were 0.020 (0.014) and 0.003(0.002) on first and third instar nymphs of prey, respectively, which conclude that adult is more voracious stage than larva. However, further field studies on predator and prey stage specific in the presence of honeydew droplets on leaflets are still needed to quantify biocontrol efficiency of predator. Keywords: Bivoltine; Coccinella septempunctata; Dubas bug; Honeydew; Predation Introduction [2-5]. In Pakistan, it was first recorded in Dubas bug, Ommatissus lybicusis 1999 in district Panjgur of Balochistan [6]. (Homoptera: Tropiduchidae), an important Adult and nymph stages of O. lybicus suck sucking pest of date palm on the Arab the phloem sap from all green parts of date peninsula [1]. This monophagous and palm and cause direct and indirect damage bivoltine pest is recorded in several by puncturing the tissue and secretion of countries in the near East and North Africa honeydew droplets on leaflets which
Published by Bolan Society for Pure and Applied Biology 671 Shah et al. results in poor photosynthetic activity [1, functional response of C. septempunctata 7] and may cause yield losses up to 50% in raising the following questions (i) Does Iraq [8]. In Pakistan yield losses ranged the predation rate of adult female and 4th from 35-80% but susceptible cultivars may instar larval stages of C. septempunctata fail to produce [6]. vary when fed on same density of same or Coccinellids, commonly known as different prey stages? (ii) Do the functional ladybirds, feed on a large number of prey response curves of adult and larva vary and have been getting importance as when fed on same prey stage? biocontrol agents [9-11]. Adults and larvae Materials and methods of most species of coccinellids are the The study was conducted for the four potential predators of a variety of prey consecutive generations in spring and [11]. Coccinella septempunctata L., is one summer 2009-10, in district Panjgur of the potential predators of aphids in India (26`59.165°N 064`05.880°E Alt. 3200ft) [12]. of Balochistan. The functional response of predator is a Predator’s selection and identification key factor in the population dynamics of In order to select the most efficient predator–prey systems. It illustrated the predator a preliminary study on rate at which a predator kills its prey at consumption rate of C. septempunctata, on different levels of density [13]. The different life forms of dubas bug was effectiveness of the predators is directly carried out in Petri dishes (experiment related to the type of functional response arena) in summer generation (2nd) in the [14, 15] and such information is critical for year 2008. Based on comparatively high implementing natural enemies consumption rate C. septempunctata was conservation and augmentation of natural selected for the present study. biological control program [16]. Type of Frond and cage size selection functional response is of immense Number of fully expanded fronds of practical importance in estimating the bio- Kehraba cultivar with ten (10) middle efficacy of predatory insect, however leaflets; five on each side were selected. ecologists usually face difficulties in Both cut ends (sides) of frond were determining functional response when the covered with wet cotton to reduce water curve lies between Type II and III. Hence losses and keep the turgidity of leaflets suitable analysis that can best determine during the course of experiment. A single the functional response is intensely frond was placed in each cages (20x17x3 required [17]. inch) with a wooden frame and covered by In Panjgur, coccinellids spp., Chrysopa muslin cloth in order to maintain the prey spp., black ants sp. and spider spp. are and predator similar to natural/field commonly found predators in date palm conditions. agro-ecosystem where these predators Prey stage selection and culture were observed to feed on nymphs and Two developmental stages (1st and 3rd adult stages of dubas bug [6]. instar nymphs) of dubas bug (prey) were Adults of coccinellids, C. septempunctata, chosen. In order to test the predation rate C. undecimpunctata L., Chilocorus and determine the functional response of bipustulatus L. and larvae of Chrysoperla both stages of predator on each carnea Steph. feed upon the nymphs and developmental stage of prey at a time, a adults stages of O. lybicus [3, 4, 18]. number of 1st instar nymphs of dubas bug However, no information is available on were collected with aspirator and consumption rate and functional response maintained as stock population. When of any predator who is attacking this pest. more than 90% of the stock population of The aim of this study was to test the prey reached to 3rd instar, required consumption rate and evaluate the numbers of 1st instar nymphs were
672 Pure Appl. Biol., 5(4): 671-681, December, 2016 http://dx.doi.org/10.19045/bspab.2016.50069 collected from field and offered to the P2 < 0, the proportion of prey consumed is predator. Similarly, stock population of C. positively density dependent, thus septempunctata was maintained on describing a type III functional response. If Medicago sativa and fed with aphids. P1 < 0, the proportion of prey consumed Estimating consumption rate and declines with initial prey density functional response suggesting a type II functional response Consumption rate and functional response [19]. Later on, the functional response of fourth instar and adult female of C. parameters were estimated using Roger’s septempunctata were determined by random predator equation (Rogers 1972). offering the 1st and 3rd instar nymphs of For Type II response the equation will be dubas bug at different density levels (1, 5, followed:
10, 20, 40, and 60 bugs per leaflet or a Ne N01 expaTh Ne T (2) total of 10, 50, 100, 200, 400 and 600 bugs Where, Ne is number of prey consumed per cage). Each life stage of predator and and N0 is initial prey density, a is the density level of prey was released attack rate, T is the total time of exposure, randomly into the single cage to each and Th is the handling time. Random predator stage. Similarly, control cages predator equation overcomes the problem received corresponding prey density level of prey depletion. Data fitting was and developmental stages but no predator. performed using nonlinear least square Both stages of predators were starved for method on SAS Version 9.0 (Procedure 24 hours before introducing into the cages. NLIN) [19]. Exposure time of prey to predator was 24 For Type III response equation will be hours and without replacement of prey. followed: Following 24 hours, mean number of Ne = No {1- exp [(d + bNo)((ThNeT)/(1+cNo)]} (3) killed/consumed prey were counted in both where b, c and d are constants. treated and control cages. The experiment The data on prey consumption by fourth was conducted controlled conditions instar and adult female C. septempunctata (temperature 30±2 °C, R.H. 20±2 % and at different prey stage level were subjected photoperiod 16L:8D) replicated five times. to one-way ANOVA and the comparison Data analysis of means was done using Tukey’s HSD The logistic regression model [19] was test using statistical software, SAS. The used to determine the shape of the number of first and third instar nymphs of functional response prior to fitting the data dubas bug at different density levels for functional response analysis. This consumed by fourth instar and adult model helps distinguishing between Type female of C. septempunctata in 24 hours II and Type III [17]. The relationship were analyzed using two-way ANOVA by between the proportion of prey consumed using “prey stage” and “prey density” level (Ne / N0) and number of prey present (N0) as independent factor and “prey was determined by fitting the data to a consumed” as dependent factor using polynomial function (equation 1) using statistical software, SAS. statistical software SAS, Version 9.0 Results (Procedure CATMOD) on personal Consumption Rate (average of four seasons) computer. C. septempunctata (adult female) vs. Dubas bug first and third instar nymph exp P P N P N 2 P N 3 0 1 0 2 0 3 0 (1) Consumption rate of adult female C. Ne N0 2 3 1 expP0 P1N0 P2 N0 P3 N0 septempunctata fed on first (F=162.98; Where Po, P1, P2, and P3 were the intercept, P<0.0001; d.f. = 5, 29) and third linear, quadratic and cubic coefficients, (F=121.19; P<0.0001; d.f. = 5, 29; Table- respectively, which were estimated using 1) instars of dubas bug increased maximum likelihood method. If P1 > 0 and significantly with increase in prey density
673 Shah et al. levels. Comparison of means revealed that figure. 1). Prey consumption by fourth prey consumption was significant at all the instar of C. septempunctata increased density levels except at prey densities, 400 significantly with increase in densities of and 600 of first instar nymph when adult first (F=205.82; P<0.0001; d.f. = 5, 29) female was used as predator (Tukey’s and third (F=121.93; P<0.0001; d.f. = 5, range = 4.31). 29) instar nymphs of dubas bug. Mean C. septempunctata (grub) vs. Dubas bug values also varied significantly at all the first and third instar nymph density levels except at prey densities, 400 Almost similar trend was observed when and 600 of first instar nymph when fourth fourth instar C. septempunctata was used instar C. septempunctata was used as as predator at different densities of first predator (Tukey’s range = 4.31). and third instars of dubas bug (table 2 and
Table 1. Mean number (±SE) of first and third instar nymphs of O. lybicus, consumed (in 24 hours) by adult female C. septempunctata at different prey densities (average of four seasons: spring and summer, 2009-10) Treatment Dubas bug development stage Density /cage First instar Third Instar Control 0.00±00.00 f 0.00±0.00 f 10 bugs 1.45±0.14 e 0.75±0.11 f 50 bugs 7.50±0.27 d 3.95±0.21 e 100 bugs 15.45±0.21 c 8.10±0.35 d 200 bugs 22.00±1.14 b 12.05±0.57 c 400 bugs 27.55±0.62 a 16.70±0.90 b 600 bug 29.40±0.43 a 19.00±0.86 a F-value 162.98* 121.19* *Means followed by different letters in the same column are significantly different at P<0.001; Tukey’s Range = 4.31)
Table 2. Mean number (±SE) of first and third instar nymphs of O. lybicus, consumed (in 24 hours) by fourth instar C. septempunctata at different prey densities (average of four seasons: spring and summer, 2009-10) Treatment Dubas bug development stage Density/cage First instar Third Instar Control 0.00±0.00 e 0.00±0.00 f 10 bugs 1.00±0.07 e 0.60±0.20 f 50 bugs 5.70±0.16 d 3.35±0.29 e 100 bugs 12.60±0.37 c 6.00±0.37 d 200 bugs 19.75±0.63 b 11.35±0.32 c 400 bugs 26.25±0.64 a 16.15±0.40 b 600 bug 28.80±0.85 a 18.25±0.32 a F-value 205.82* 121.93* *Means followed by different letters in the same column are significantly different at P<0.001; d.f. = 5, 29; Tukey’s Range = 4.31)
674 Pure Appl. Biol., 5(4): 671-681, December, 2016 http://dx.doi.org/10.19045/bspab.2016.50069
Comparative consumption rate of of both developmental stages of C. fourth instar and adult female C. septempunctata was significantly high septempunctata feeding on 1st than 3rd instar nymphs of Significant difference was observed in the dubas bug. Similarly, irrespective of prey predation rate of adult female and fourth stage the overall functional response curve instar larva of C. septempunctata feeding of adult was higher than the grub, whereas on the same density and prey stage with at higher prey density the prey consumed same environmental conditions. by both developmental stages was at par Irrespective of prey density, mean (fig. 3). Two- way ANOVA revealed a predation per 24 hours of adult and grub significant main effect of “prey stage” (F= stages of C. septempunctata was recorded 314.79; P<0.0001; d.f. = 1) and “prey as 13.66 and 12.48 prey, respectively (Fig. density” (F= 278.93; P<0.0001; d.f. = 5) 3). when adult female C. septempunctata was Functional response searching. The interaction between “prey Parameter estimated for logistic stage” and “prey density” was also found regression of proportion of prey killed to be significant (F= 20.87; P<0.001; d.f. = (Ne/No) against the number of prey 5). Similarly, main effect of “prey stage” offered (No) for the adult female and 4th (F= 584.64; P<0.0001; d.f. = 1) and “prey instar grub of C. septempunctata feeding density” (F= 321.23; P<0.0001; d.f. = 5) on first and 3rd instar nymphs of dubas bug was also significant when fourth instar C. displayed type II functional response, i.e. septempunctata was searching. The significant linear parameter P1 < 0 (table 3 interaction between “prey stage” and “prey and fig. 1 and 2). density” was also found to be significant Figure 1 and 2 illustrated that functional (F= 37.71; P<0.001; d.f. = 5). response curves and predation percentage 35
30
25
20
15
10
prey consumedprey 5
0 0 100 200 300 400 500 600 700
Prey density Adult Vs. 1st instar Adult Vs. 3rd instar Grub Vs. 1st Instar Grub Vs. 3rd instar
Figure 1. Functional response of adult female and fourth instar C. septempunctata (obtained from the predicted values of prey consumed by PROC-NLIN procedure of SAS), preying upon 1st and 3rd instar nymphs of dubas bug offered at different density levels (average of four seasons, 2009-10)
675 Shah et al.
0.18 0.16 0.14 0.12 0.10 0.08 0.06 0.04
Proportional prey killed prey Proportional 0.02 0.00 0 100 200 300 400 500 600 700 Prey density
Adult Vs. 1st instar Adult Vs. 3rd instar Grub Vs. 1st Instar Grub Vs. 3rd instar
Figure 2. Functional response of C. septempunctata adult and grub preying upon 1st and 3rd instar nymphs of dubas bug offered at different density levels (average of four seasons, 2009-10) 30
25
20
15
10
Preyconsumed 5
0 10 50 100 200 400 600 Prey density C. septempuntata(Grub) C. septempuntata(Adult)
Figure 3. Comparative functional response of C. septempunctata adult and grub at different densities of dubas bug (irrespective of life stages)
Handling time and search rate septempunctata spent shortest time, Prey stage significantly affected the followed by fourth instar feeding on 1st handling time and it increased with instar nymphs of dubas bug. Similarly increasing prey size. Adult female C. search rate of predator decreased when
676 Pure Appl. Biol., 5(4): 671-681, December, 2016 http://dx.doi.org/10.19045/bspab.2016.50069 prey stage developed. Regardless of prey septempunctata was shorter than adult stage overall search rate of fourth instar C. (table 4).
Table 3. Functional response model based on analysis of maximum likelihood estimates of parameters (±SE) using proportional prey killed as function of initial prey densities by C. septempunctata (average of four seasons: spring and summer 2009-10) Predator Prey Intercept Linear Quadratic Cubic Best Fitted stage stage (P0) (P1) (P2) (P3) model -1.655 -0.004 -0.000081 0.000000096 Adult 1st Instar ±0.25 ±0.053 ±0. 000001 ±0.000000001 Type II Female -2.529 -0.004 0.000062 0.000000046 3rd Instar ±0.33 ±0.003 ±0. 000001 ±0.000000002 Type II Fourth -1.868 -0.004 -0.000025 0.000000023 Instar 1st Instar ±0.263 ±0.004 ±0. 000001 ±0.000000001 Type II -3.037 -0.002 0.000045 0.000000014 3rd Instar ±0.413 ±0.005 ±0. 00001 ±0.000000001 Type II
Table 4. Estimated attack rate (a’) and handling time (Th) of C. septempunctata on two life stages and seven densities of dubas bug, O. lybicus (average of four seasons; spring and summer 2009-10) Predator Dubas Parameter Estimated SE t value Pr(>|t|) Stage stage a' 0.02 0.002 8.621 0.00 1st Instar Th 0.563 0.024 23.020 0.00 (Adult a' 0.003 0.0001 8.050 0.00 female) 3rd Instar 1.008 0.121 8.300 0.00 Th a' 0.011 0.001 8.335 0.00 Average Th 0.785 0.027 15.66 0.00 a' 0.014 0.001 9.917 0.00 1st Instar Th 0.692 0.029 23.840 0.00 (4h instar a' 0.002 0.0001 6.563 0.00 3rd Instar grub) Th 1.492 0.227 6.571 0.00 a' 0.008 0.0001 8.240 0.00 Average Th 1.092 0.128 15.205 0.00 2 a’(cm /hour), Th (days or hours/prey) , Predation time for predators was 24 hours
Discussion septempunctata. Predation rate increased Developmental stage of dubas bug with increasing prey density, while significantly influenced the consumption percentage of predation was inversely rate of both stages of C. septempunctata. proportional to prey density level. The This may be due to difference in body size more predation at higher density could be and mobility of and 3rd instar nymphs of due to more chance for predator for dubas bug. Similar results were indicated searching and killing of prey than lower by [20], who found that prey size and prey density. Generally these hunger level of predators affected the investigations are in line with [21-23]. At predation ratio. Density level of prey high prey density predation frequency of significantly affected the predation rate of ladybirds decrease with predation time 4th instar grub and adult of C. however, it was not observed at low prey
677 Shah et al. density [22]. C. septempunctata consumed instar nymphs of dubas bug. Predators more than 50% of prey during the first displayed such type of functional response three hours exposed for 24 hours [24]. In consumed higher number of prey with other study, [25] reported that 4th instar high prey availability, but the rate of grub of seven spotted beetle consumed 2.8 predation/consumption decreased with and 2.55 aphids (Lipaphis erysimi Kalt.) increasing prey density and plateau in under laboratory and field conditions functional response curve indicated offered at density level of 10 aphids, predator saturation. Similar type of respectively. It is assumed that this response (FR II) has been reported for C. difference may be on account of difference septempunctata preyed on: Lipaphis in prey species, experimental arena, erysimi (Kaltenbach) [32], green apple prevailing environmental condition during aphid Aphis pomi De Geer [33], Aphis experiment and difference in geographical glycines [34]. provenance of C. septempunctata species. Predators demonstrate similar functional Adult C. septempunctata consumed response curve cannot be deemed to significantly more dubas bug than 4th respond in the same way in term of instar grub when offered at the same handling time and search rate [12]. Present density, stage and under the same results showed that handling time of both environmental condition. This was stages of C. septempunctata varied probably due to comparatively poor visual significantly and it increased with prey perception of 4th instar larvae of C. (dubas) developmental stage, which septempunctata than adult, which detect indicates that predator have different the prey at distance of about 1.0 cm and abilities to response against different prey 0.7 cm, respectively [26]. Coccinella stage/size. Being the first study no septempunctata finds the first prey (patch) reference is available to compare the result only under light conditions (at a distance of present study with earlier work. of 7 mm) and upon coming in contact However, generally these results are in line under dark conditions [27]. Generally, with [35] who found that handling time present results are in consonance with the includes time it takes to: chase, kill, findings of [28] who found that larvae of subdue and eat/digest a prey item, once the C. septempunctata spent longer time in prey is located. While this study disagree finding a prey and adapted to search for with [36] who reported that handling time aggregated prey. Our findings is in close of Exochomus nigromaculatus decrease agreement with those of [29], who claimed with developmental stage of H. pruni. This that adult C. septempunctata had a lesser discrepancy may be due to dissimilarity in prey handling time with high attack rate prey and predator: species, size, than the fourth instars. Food consumption development stage, degree of predator of C. septempuctata grub increased with hunger and most importantly some development of instars [30], while, [21] environmental variables. reported that C. septempunctata grub Search rate (a) and handling time (Th) of feeding rate was two fold greater than both stages of C. septempunctata was those of adult feeding on aphid species. significantly high preying on 1st instar This variation may be due to feeding nymphs of dubas bug compared to 3rd behavior /preference of predator which instar nymphs; indicated comparatively may change under different environmental more mobility of 3rd instar than 1st instar variables [31]. dubas bug. Other possibly reasons may be Present study showed that both due to variation in prey distribution [28], developmental stages of C. effect of temperature on predation and septempunctata, illustrated type II search rate of predator [37, 38]. While functional response feeding on 1st and 3rd higher handling time of both stages on 3rd
678 Pure Appl. Biol., 5(4): 671-681, December, 2016 http://dx.doi.org/10.19045/bspab.2016.50069 instar nymphs showed that both stages of Arabic). Project for palm and date predator need more time to grasp 3rd instar Research Centre in the near east and than 1st instar. North Africa. FAO Bulletin, Baghda. In comparison, adult had significantly 126p shorter handling time and higher search 3. Gharib A (1966). Ommatissus rate compared to grub, they take less time binotatus Fieb.Var. lybicus Berg. App to process the food and take comparatively Entomo and Phytopatho 24: 37-47. more time to locate the prey (may be due 4. Hussain AA (1963). Biology and to mobility), which showed that C. control of dubas bug Ommatissus septempunctata adult is more efficient in binotatus var. lybicus de-Berg. terms of food processing. (Homoptera: Tropiduchida) infesting Based on present result of consumption date palm in Iraq. Bull Entomol Res rate, functional response, handling time 53: 737-745. and attack rate between two stages of 5. Klein M & Venezian A (1985). The predator that varied significantly we can dubas date Tropiduchid, Ommatissus conclude that though both development binotatus lybicus, a threat to date palm stages of C. septempunctata illustrated in Israel. Phytoparastica 13: 95-101. type II functional response but adult is the 6. GOB (2006). Project proposal for the most efficient than grub. Functional control of dubas bug in Panjgur response of predators can be affected by district. Agric. Extension Dept. different biotic and a-biotic factors. Balochistan Report. However, field studies on predator and 7. Hussain AA (1974). Dates palm and prey stage, sex specific, temperature and Dates with their pests in Iraq. host plant in the presence of honeydew University of Baghdad Ministry of droplets on leaflets are still needed to Higher Education and Scientific quantify biocontrol efficiency of predator. Research Iraq. 166 pp. Authors’ contributions 8. Kranz J, Schmutterer H & Koch W Conceived and designed the experiments: (1978). Diseases, pests, and weeds in A Shah, MQ Kakar & T Iqbal, Performed tropical crops. Soil Sci 125: 272. the experiments: A Shah & H Ullah, 9. Işıkber AA & Copland MJW (2003). Analyzed the data: NE Papanikolaou & A Effects of various aphid foods on Shah, Contributed reagents/ materials/ Cycloneda sanguinea. Entomol Exp analysis tools: A Shah, A Ullah & A Appl 102: 93-97. Razaq, Wrote the paper: A Shah. 10. Obrycki JJ & Kring TT (1998). Acknowledgement Predaceous Coccinellidae in biological This study was completed with the control. Ann Rev Entomol 43: 295-321. Financial Assistance of Pakistan Science 11. Oliveira EE, Oliveira CL, Sarmento Foundation, Islamabad under the Project RA, Rezende LM & Fadini MAM No. PSF/Res/B-ACD/Agr (379). (2004). Aspectos biológicos do References predador Cycloneda sanguinea 1. Mokhtar AM, & Al-Nabhani SS (Coleoptera: Coccinellidae) alimentado (2010). Temperature-dependent com Tetranychus evansi (Acari: development of dubas bug, Tetranychidae) Macrosiphum Ommatissus lybicus (Hemiptera: euphorbiae (Homoptera: Aphididae). Tropiduchidae), an endemic pest of Biosci J 21: 33-39. date palm, Phoenix dactylifera. Eur J 12. Pervez A & Omkar (2005). Functional Entomol 107: 681–685. responses of coccinellid predators: An 2. El-Haidri HS & AL-Hafidh EMT illustration of a logistic approach. J (1986). Palm and date arthropods pests Insect Sci 5: 1-6. in the Near-East and North Africa, (in
679 Shah et al.
13. Murdoch WW & Oaten A (1975). Aphidid and Cicadellid (Hemipteran) Predation and population stability. Adv Pests. Int J Agric Bio 13: 427-430. Ecol Res 9: 1-131. 22. Yasuda H & Ishikawa H (1999). 14. Holling CS (1959). Some Effects of prey density and spatial characteristics of simple type of distribution on prey consumption of predation and parasitism. Can Entomol the adult predatory ladybird beetle. J 91: 385-398. Appl Entomol 123: 585–589. 15. Holling CS (1965). The functional 23. Rai S, Singh NN & Shankar U (2010). response of predators to prey density Functional response of grub and adult and its role in mimicry and population of Coccinella septempunctata (L.) and regulation. Mem Entomol Soc Can 45: Coccinella transversalis (Fabr.) on 3-60. mustard aphid, Lipaphis erysimi 16. Parajulee MN, Shrestha RB, Leser JF, (Kalt.). Arch Phytopathol 43: 1829- Wester DB & Blanco CA (2006). 1835. Evaluation of the functional response 24. Shukla AN, Singh R & Tripathi CPM of selected arthropod predators on (1990). Effect of Predation Period on bollworm eggs in the laboratory and the Functional Fesponse of Coccinella effect of temperature on their predation septempunctata L. (Coleoptera, efficiency. Environ Entomol 35: 379- Coccinellidae), a predator of Lipaphis 386. erysimi Kalt (Hemiptera, Aphididae). J 17. Trexler JC, Charles EM & Travis J Advance Zool 11: 27–32. (1988). How can the functional 25. Solangi BK, Lohar MK, Abro GH & response best be determined? Talpur MA (2007). Searching ability Oecologia. 76: 206–214. and feeding potential of larvae, 7- 18. Bassim HA (2003). Biological spotted beetle Coccinella performance of dubas bug Ommatissus septempunctata Linn. Under laboratory lybicus De Berg. (Homoptera: and field conditions. Sarhad J Agric Tropiduchidae) under field conditions 23: 705-711. and predicting of its appearance by 26. Stubbs M (1980). Another look at using degree-day model. M.Sc. Thesis. prey detection by Coccinellids. Department of Plant Protection, Ecological Entomol 5: 179–182. College of Agriculture, University of 27. Nakamuta K (1984). Visual orientation Baghdad, Abu Ghraib, Baghdad, Iraq. of a ladybeetle, Coccinella 19. Juliano SA (2001). Nonlinear curve septempunctata L. (Coleoptera: fitting: Predation and Functional Coccinellidae), towards its prey. App response curve. In: S.M. Scheiner and Entomol Zool 19: 82-86. J. Gurevitch (eds.) “Design and 28. Murakami Y & Tsubaki Y (1984). Analysis of Ecological Experiments, Searching efficiency of the lady beetle Second Edition”. Oxford University Coccinella septempunctata larvae in Press. p. 178-196. uniform and patchy environments. J 20. Frazer BD & McGregor RR (1992). Ethology 2: 1-6. Temperature-dependent survival and 29. Gupta RK, Pervez A, Guroo MA, & hatching rate of eggs of seven species Srivastava K (2012). Stage-specific of Coccinellidae. Can Entomol 124: functional response of an 305-312. aphidophagous ladybird, Coccinella 21. Inayat TP, Rana SA, Rana N, Ruby T, septempunctata (Coleoptera: Sadiqui MJI & Abbas MN (2011). Coccinellidae), to two aphid species. Predation Rate in Selected Coccinellid Int J Trop Insect Sci 32: 136-141. (Coleoptera) Predators on some Major 30. Sattar M, Hamed M & Nadeem S (2008). Biology of Coccinella
680 Pure Appl. Biol., 5(4): 671-681, December, 2016 http://dx.doi.org/10.19045/bspab.2016.50069
septempunctata Linn. (Coleoptera: (2009). Predation by Coccinella Coccinellidae) and its predatory septempunctata and Harmonia axyridis potential on cotton aphids, Aphis (Coleoptera: Coccinellidae) on Aphis gossypii glover (Hemiptera: glycines (Homoptera: Aphididae). Aphididae). Pak J Zool 40: 239-242. Environ Entomol 38: 708-714. 31. Khan MR & Khan MR (2010). The 35. Veeravel R & Baskaran P (1997). relationship between temperature and Functional and Numerical Responses functional response of Coccinella of Coccinella transversalis Fab. and septempunctata(L) (Coleoptera: Cheilomenes sexmaculatus Fab. Coccinellidae). Pak J Zool 42: 461- Feeding on the Melon Aphid, Aphis 466. gossypii Glov. Int J Trop Insect Sci 17: 32. Omkar & Srivastava S (2003). 335-339. Functional Response of the Seven 36. Atlıhan R & Özgökçe MS (2002). spotted Lady Beetle, Coccinella Development, fecundity and prey Septempunctata Linnaeus on the consumption of Exochomus Mustard Aphid, Lipaphis Erysimi nigromaculatus feeding on (Kaltenbach). Intl J Trop Insect Sci 23: Hyalopterus pruni Phytoparasitic 30: 149-152. 443-450. 33. Khan AA & Mir RA (2008). 37. Menon S, Hansen JE, Nazarenko L & Functional response of four predaceous Luo Y (2002). Climate effects of black coccinellids, Adalia tetraspilota carbon aerosols in China and (Hope), Coccinella septempunctata L., India. Science 297: 2250-2253. Calvia punctata (Mulsant) and 38. Xia JY, Rabbinge R, & Van Der Werf, Hippodamia variegata (Goeze) feeding W (2003). Multistage functional on the green apple aphid, Aphis pomi responses in a ladybeetle-aphid system: De Geer (Homoptera: Aphididae). J scaling up from the laboratory to the Biolog Control 22: 291-298. field. Environ Entomol 32(1):151-162. 34. Xue Y, Bahlai CA, Frewin A, Sears MK, Schaafsma AW & Hallett RH
681