Research Article  Open Access
Sara Zarghami, Mohammad Saeed Mossadegh, Farhan Kocheili, Hossein Allahyari, Arash Rasekh, "Functional Responses of Nephus arcuatus Kapur (Coleoptera: Coccinellidae), the Most Important Predator of Spherical Mealybug Nipaecoccus viridis (Newstead)", Psyche: A Journal of Entomology, vol. 2016, Article ID 9417496, 9 pages, 2016. https://doi.org/10.1155/2016/9417496
Functional Responses of Nephus arcuatus Kapur (Coleoptera: Coccinellidae), the Most Important Predator of Spherical Mealybug Nipaecoccus viridis (Newstead)
Abstract
Nephus arcuatus Kapur is an important predator of Nipaecoccus viridis (Newstead), in citrus orchards of southwestern Iran. This study examined the feeding efficiency of all stages of N. arcuatus at different densities of N. viridis eggs by estimating their functional responses. First and 2nd instar larvae as well as adult males exhibited a type II functional response. Attack rate and handling time were estimated to be 0.2749 h^{−1} and 5.4252 h, respectively, for 1st instars, 0.5142 h^{−1} and 1.1995 h for 2nd instars, and 0.4726 h^{−1} and 0.7765 h for adult males. In contrast, 3rd and 4th instar larvae and adult females of N. arcuatus exhibited a type III functional response. Constant and handling time were estimated to be 0.0142 and 0.4064 h for 3rd instars, respectively, 0.00660 and 0.1492 h for 4th instars, and 0.00859 and 0.2850 h for adult females. The functional response of these six developmental stages differed in handling time. Based on maximum predation rate, 4th instar larvae were the most predatory (160.9 eggs/d) followed by adult females (84.2 eggs/d). These findings suggest that N. arcuatus is a promising biocontrol agent of N. viridis eggs especially for 4th instar larvae and adult females.
1. Introduction
The spherical mealybug, Nipaecoccus viridis (Newstead) (Hemiptera: Pseudococcidae), is one of the most important citrus pests in southern and southwestern Iran [1]. This polyphagous pest attacks over 193 plant species throughout tropical and subtropical regions and a large part of the Pacific Basin [2–4]. Chemical control of N. viridis, as with other mealybugs, often becomes ineffective due to their cryptic life style in protected locations as well as the presence of a mealy wax that covers its eggs and body [5]. Therefore, biological control using natural enemies has the potential to be an effective alternative method to manage this pest [6–8].
The coccidophagous coccinellid, Nephus arcuatus Kapur (Coleoptera: Coccinellidae), is a newly recorded predatory beetle indigenous to the warmer regions of Iran [9]. Until recently, it had only been reported in Yemen and Saudi Arabia [10]. This small coccinellid occurs widely and abundantly in citrus orchards in Dezful, southwestern Iran (personal observation). Recent investigations on the biology and consumption capacity of this predator confirm its potential for the control of N. viridis in the citrus orchards [11, 12]. However, more studies are needed to develop this predator within a successful biological management programme.
Prior to using a natural enemy in a biological control programme, it is essential to evaluate its predatory capacity. One of the criteria for determining the efficiency of a predator is the ability of the predator to change its feeding behaviour in response to changes in prey density, that is, its functional response, defined as the number of prey eaten per predator as a function of prey density [13, 14]. Several types of functional response curve have been described, including a linear increase (type I), an increase decelerating to a plateau (type II), or a sigmoidal increase (type III) in which predators cause a constant (I), negative (II), or positive (III) densitydependent mortality of their prey [13, 15, 16]. The functional response curve can be described by evaluating two parameters, the coefficient of attack rate () and the handling time (). The coefficient of attack rate estimates the steepness of the increase in predation with increasing prey density and the handling time helps estimate the satiation threshold [16]. Information on these variables can provide insights into the efficiency of a predator in regulating prey populations, clarifying evolutionary relationships, and predicting the predator’s effectiveness as a biological control agent [16–18].
This study aimed to determine the relative efficiency of different larval instars and of both female and male adults of N. arcuatus as biological control agents of N. viridis. We achieved this by evaluating the effect of N. viridis density on the number of prey consumed by each life stage of N. arcuatus to determine the shape of their functional response to prey density, their attack rate coefficients, and handling times.
2. Materials and Methods
2.1. Prey and Predator Cultures
N. viridis mealybugs were collected from Citrus sinensis L. trees in an orchard in Dezful (48°30′E, 32°20′N), Khuzestan Province, southwestern Iran, in the autumn of 2011. They were then massreared on sprouting potato (Solanum tuberosum L.) shoots, in rearing boxes (24 × 16 × 10 cm) that were tightly covered by a fine mesh net. N. arcuatus adults were collected from the same orchard and reared on sprouted potatoes infested with N. viridis for two generations before being used in experiments. The stock colonies of both N. arcuatus and N. viridis were maintained in an incubator at °C, % RH, and 14L : 10D photoperiod.
2.2. Functional Response Assessments
To obtain a cohort of N. arcuatus for experiments, 50 pairs of adult N. arcuatus were transferred from the stock culture into a colony of N. viridis (mixed developmental stages on 10–12 sprouted potato plants) in a plastic box (20 × 13 × 8 cm) covered with a fine mesh net for ventilation; predator oviposition was allowed to proceed for 12 h after which time the adult predators were removed. Developing predator larvae were observed every 12 h and, over time, developed into cohorts of 1st, 2nd, 3rd, and 4th instar larvae and mated adults males and females (10dayolds) for use in experiments. Before each developmental stage was evaluated, replicate individuals were kept without food for 12 h in a micro tube (1.5 mL) in order to standardize their hunger level. Thereafter, each predator was introduced into a plastic container (9 × 7 × 3 cm) containing different densities of eggs of N. viridis which were the preferred prey for the developmental stage of N. arcuatus [19]. Each container had a 20 mm diameter hole in the middle of the lid, which was covered by a piece of fine net to provide ventilation. The densities of N. viridis eggs were as follows: 2, 4, 6, 8, 10, 14, and 18 eggs for 1st instar larvae; 2, 4, 8, 16, 20, 30, 40, and 50 eggs for 2nd instar larvae; 2, 4, 8, 16, 20, 40, 60, 80, 100, and 120 eggs for 3rd instar larvae; 2, 4, 8, 16, 32, 60, 100, 140, 180, and 220 eggs for 4th instar larvae; 2, 4, 8, 16, 40, 65, 90, and 115 eggs for adult females; and 2, 4, 8, 16, 20, 35, 50, 60, and 80 eggs for adult males. These densities were selected based on preliminary tests of the consumption capacity of different stages of N. arcuatus. After 24 h, predators were removed and the number of eggs consumed was recorded. There were between 10 and 21 replicates for each treatment; greater replication was used for some prey densities to achieve precise information. Experimental conditions were based on optimal temperature for N. arcuatus activity: °C, % RH, and 14L : 10D photoperiod [11].
2.3. Statistical Analysis
The functional responses of N. arcuatus were analyzed in two steps [20]. In the first step, the type (shape) of functional response was described by determining how well the data fitted to a type I, II, or III functional response, using a polynomial logistic regression of the proportion of prey consumed () as follows:where is the number of prey consumed, is the initial prey density, and the parameters , , , and are the constant, linear, quadratic, and cubic parameters related to the slope of the curve. The above parameters were estimated using the CATMOD procedure in SAS software [20, 21]. The data sets for each developmental stage of N. arcuatus were fitted individually to (1) and the types of functional response were determined by examining the signs of and . If was positive and was negative, a type III functional response was evident. However, if was negative the functional response type was a type II [20].
In the second step, a nonlinear least squares regression (PROC NLIN [21]) was used to estimate the functional response parameters ( and either for type II functional response or , , and for type III functional response) using Rogers’s random predator equation which is the most appropriate type II functional response in situations with prey depletion [22]:where is the total time that predator and prey are exposed to each other (24 h); is the attack rate; and is the handling time in hours [20, 23].
For modeling the type III functional response, attack rate () in (2) was substituted in (3) with a function of prey density [16, 24]. In the simplest generalized form, attack rate (3) is a function of the initial number of prey:where , , and are constants that must be estimated. The simplest form arises when is a function of initial density, as in The functional response parameters for 1st instar and 2nd instar larvae and adult males were obtained using (2) (for type II). However, the functional response parameters for 3rd instar and 4th instar larvae and adult females were obtained using (3) and (4) (for type III).
Differences in estimates of attack rates and handling were analyzed using (5) (type II) or (6) (type III) with an indicator variable as follows [20]: where is an indicator variable that takes the value 0 for the first data sets and the value 1 for the second data sets. For a type II response (5), the parameters and estimate the differences between the data sets in the values of the parameters and , respectively. Specifically, the attack rate for one stage is , and that for another stage is . If the parameters and are significantly different from zero, then and , for the two data sets, are different. For the type III response (6), the parameters and estimate the differences between the two data sets being compared with the values of and , respectively. Specifically, the handling time for one stage is , and that for another stage is [20].
The maximum predation rate (), which represents the maximum number of prey that can be consumed by an individual during 24 h, was calculated using the estimated [25].
3. Results
The polynomial logistic regression analysis of the proportion of N. viridis consumed by 1st and 2nd instar larvae and by adult male N. arcuatus yielded estimated parameters that indicate a type II functional response for these predator stages (Table 1). The linear coefficient was negative for these stages; that is, the proportion of prey consumed declined monotonically with an increase in the initial number of prey offered, which indicates a type II functional response (Figures 1 and 2). Therefore, (2) was used to estimate and . Estimated parameters showed that the 1st instar larva of N. arcuatus had the smallest attack rate and handling time compared with 2nd instar larva and adult males (Table 2). The asymptotic 95% confidence interval for included 0 but that for did not, which means that there is a significant difference between and and that these three groups have a different functional response, with a significant difference in handling time, but not in attack rate (Table 3).


 
Significant difference parameters shown in bold face. 
Results of the polynomial logistic regression for 3rd and 4th instar larvae and adult female N. arcuatus indicate a type III functional response for these predator stages. The linear coefficient, , was positive, and the quadratic coefficient, , was negative for these stages (Table 1). Thus, the proportion of prey consumed is positively density dependent, which indicates a type III functional response (Figures 1 and 2). Therefore, (3) was substituted for (2), and the two data sets were fitted to a type III functional response curve. Results of the nonlinear least square regression indicated that parameters and were not significantly different from 0 (not shown): therefore, they were removed from the model, and a reduced model was used [20]. Similarity relationships between and in these data sets () enabled the use of model (6) for data analysis. Both the estimated value and were smallest for 4th instar larvae followed by adult females. The asymptotic 95% confidence interval for and showed that there was a significant difference between and , while there is no significant difference between and (Table 4). Thus, there is a significant difference between and and these three groups also have a different functional response, with a significant difference in handling time, but not in constant (Table 3). For these three groups the relationships between the attack rate and the initial number of prey were linear (), and the rate of successful attack () ranged from 0.0284 to 1.704 h^{−1} for 3rd instar larvae; from 0.0132 to 1.452 h^{−1} for 4th instar larvae; and from 0.0172 to 0.6872 h^{−1} for adult females.
 
Significant difference parameters shown in bold face. 
The value of the coefficient of determination ( = 1 − residual sum of squares/corrected total sum of squares) indicated that Rogers’s random predator equations ((2) and (4)) adequately described the functional responses of all stages of N. arcuatus (see values for , Table 2).
The maximum number of N. viridis eggs that could be eaten by all stages of N. arcuatus increased with larval instar and adult females consumed more N. viridis eggs than adult males (Table 2). This parameter was highest for 4th instar larva followed by adult females and 3rd instar larva.
4. Discussion
The warm, dry climate of southwestern Iran provides suitable conditions for activity of the mealybug, N. viridis, in orchards [1]. In these regions, as in many countries, Cryptolaemus montrouzieri Mulsant is released to control mealybugs in orchards. However, probably due to warm summers and the symbiotic relationship between ants and mealybugs, this predator has not been able to establish permanent populations and must be massreared and released on a yearly basis to control N. viridis [8]. In contrast, N. arcuatus is the most abundant predator in orchards from spring to fall and often controls N. viridis in citrus orchards (personal observation). Zarghami et al. [11] studied the effect of temperature on the population growth and life table parameters of N. arcuatus as a predator of N. viridis and noted that N. arcuatus could develop at a wide range of temperatures (20–35°C), with an optimal temperature of 30°C. They reported that when N. arcuatus was provided with two prey species (N. viridis and P. citri), prey stage, prey size, and previous feeding experience had no effect on prey selection by this predator [12]. Moreover, N. arcuatus is considered to be the most effective predator of other mealybugs including Maconellicoccus hirsutus (Green) and Phenacoccus solenopsis Tinsley due to its large populations and extended periods of activity, especially during the hot summer months [26, 27].
The current study is the first to assess the efficiency of all stages of N. arcuatus as a predator of N. viridis. We found that different developmental stages of N. arcuatus had different types of functional responses. The 1st and 2nd instar larvae as well as adult males exhibited a type II functional response. In contrast, the 3rd and 4th instar larvae and adult females exhibited a type III functional response. This is in accordance with observations for other insects species where the type of functional response and its parameters are affected by developmental stage [28–30]. For example, Bayoumy [28] found that the functional responses of 2nd instar larvae (type II), 4th instar larvae (type III), and adult females (type III) of Nephus includens (Kirsch) to Aphis gossypii Glover were markedly different. However, Tang et al. [31] and Milonas et al. [32] reported that functional responses of Nephus ryuguus (Kamiya) feeding on Oracella acuta (Lobdell) and N. includens feeding on Planococcus citri (Risso) or Planococcus ficus (Signoret), respectively, did not differ depending on developmental stage.
The most common functional response for coccinellids is type II and has been found in many studies: larvae and adults of N. ryuguus feeding on O. acuta [31]; larvae of Propylea dissecta (Mulsant) feeding on Aphis gossypii Glover [33]; all four larval instars and adults of Hippodamia variegata (Goeze) feeding on Aphis fabae Scopoli [34]; and 2nd instar and 4th instar larvae of N. includens feeding on P. ficus and P. citri [32]. In contrast, a type III functional response appears to be relatively rare among coccinellids [18, 28, 30, 35]. A predator with a type II functional response has the potential to destabilize the preypredatory population because it causes inverse densitydependent mortality in the prey population. In contrast, a predator with a type III functional response could contribute more to regulating the density of the prey population than a predator with a type II response and is, theoretically, more capable of suppressing prey populations compared to stages exhibiting a type II response [13, 36, 37]. The three postulated mechanisms for type III functional responses in predators are as follows: (1) the concentration of a predator’s hunting efforts in a highdensity patch [38]; (2) switching in a multiple prey system [36]; and (3) learning [37, 39]. Our experiment with N. arcuatus was a shortterm, single species test and so the first mechanism is most likely to be responsible for the type III functional response we observed. It is probable that these stages, by showing a type III response, have the ability to regulate prey population during outbreaks of N. viridis in citrus orchards.
Our results indicate that estimated attack rates did not change significantly among the different developmental stages of N. arcuatus with similar functional response curves observed for all stages. The attack rate determines how steeply the functional response curve rises with increasing prey density. Thus, the results revealed that the steepness did not differ among different developmental stages of N. arcuatus and that the different developmental stages had similar abilities to respond to increasing prey densities. In contrast, the prey handling times increased as the larval age of this predator increased, and also females had longer handling times than adult males. In other words, the 1st instar larva of N. arcuatus spent more time and 4th instar larvae and adult females spent less time to consume N. viridis eggs than other developmental stages. Handling time is a general term that reflects the cumulative effect of time taken during capturing, killing, subduing, and digesting prey [40]. Thus, being larger is an advantage to 4th instar larvae and adult females in subduing, consuming, and digesting more prey. Farhadi et al. [34] observed similar results for H. variegata feeding on A. fabae. Moreover, Bayoumy [28] reported that the functional response of 4th instar larvae and adult females of N. includens to A. gossypii differed in handling time.
The maximum predation rate per day () was highest for 4th instar larvae due to their greater requirements for food and energy to grow and attain the critical weight for pupation [41] or to achieve a higher search rate [28]. The second highest predation rate was for 3rd instar larvae and the third highest for adult females. These three developmental stages can, therefore, be considered as the most efficient predatory stages of N. arcuatus. The voracity of females may be as much as 2.6 times that of adult males. This difference may be correlated with their larger size and high nutrient requirement for egg production and oviposition [42]. The greater voracity of 4th instar larvae compared with adults is also frequently observed in other coccinellid species, for example, P. dissecta [33], H. variegata [34], and N. includens [28]. However, Tang et al. [31] observed that adults of N. ryuguus had higher predation rates than 4th instar larvae when preying on O. acuta.
Our results also clearly confirm that all stages of N. arcuatus show a high predation rate when feeding on N. viridis eggs. Muştu and Kilinçer [43] reported that the 4th instar larvae and adults of the related species N. kreissli consumed 23.5 and 47.3 eggs of P. ficus in 24 h, respectively. Zarghami et al. [19] observed that the males and females of N. arcuatus consumed 32.6 and 76.7 eggs of P. citri in 24 h. Thus, based on this voracity and the ability of N. arcuatus to survive and reproduce at temperatures around 30°C [11], this species could be efficient in controlling mealybugs in warm regions.
5. Conclusion
In conclusion, with respect to type of functional response observed and parameter estimated for all developmental stages of N. arcuatus, the most effective predators are, in descending order, 4th instar larvae, adult females, and then 3rd instar larvae. This laboratory study indicates that N. arcuatus could be an effective biocontrol agent. Specifically, a mass release of the abovementioned stages of N. arcuatus might provide efficient pest management especially in initial field infestations with N. viridis eggs. Clearly, empirical data obtained under laboratory conditions cannot be directly extrapolated to field conditions; thus further studies especially on the effect of prey age, prey size, and prey species on functional response, numerical response, longterm predation capacity, and mealybug population suppression under field conditions are needed to evaluate the possibilities for using N. arcuatus in inoculative/inundative biological control strategies.
Competing Interests
The authors declare that they have no competing interests.
Acknowledgments
The authors wish to express their sincere gratitude to Dr. Judith Pell from J. K. Pell Consulting, UK, who kindly revised and madevery useful comments and advice for improving the paper and Dr. F. R. Hunter Fujita from Reading University, UK, also kindly made final useful comments.
References
 M. Moghaddam, “An annotated checklist of the scale insects of Iran (Hemiptera, Sternorrhyncha, Coccoidea) with new records and distribution data,” ZooKeys, vol. 334, pp. 1–92, 2013. View at: Publisher Site  Google Scholar
 Y. BenDov, D. R. Miller, and G. A. P. Gibson, “ScaleNet,” 2013, http://www.sel.barc.usda.gov/scalenet/scalenet.htm. View at: Google Scholar
 J. R. Nechols, “The spherical mealybug,” in Biological Control in the Western United States, J. R. Nechols, L. A. Anders, J. W. Beardsley, R. D. Goeden, and C. G. Jackson, Eds., Accomplishments and Benefits of Regional Research Project W84, 1964–1989, pp. 164–165, University of California Press, Division of Agricultural and Natural Resources, New York, NY, USA, 1995. View at: Google Scholar
 N. S. Sharaf and D. E. Meyerdirk, “A review of the biology, ecology and control of Nipaecoccus viridis (Homoptera: Pseudococcidae),” Miscellaneous Publications of the Entomological Society of America, vol. 66, pp. 1–18, 1987. View at: Google Scholar
 A. L. Joyce, M. S. Hoddle, T. S. Bellows, and D. González, “Oviposition behavior of Coccidoxenoides peregrinus, a parasitoid of Planococcus ficus,” Entomologia Experimentalis et Applicata, vol. 98, no. 2, pp. 49–57, 2001. View at: Publisher Site  Google Scholar
 M. Mani and A. Krishnamoorthy, “Biological suppression of the mealybugs Planococcus citri (Risso), Ferrisia virgata (Cockerell) and Nipaecoccus viridis (Newstead) on pummelo with Cryptolaemus montrouzieri Mulsant in India,” Journal of Biological Control, vol. 22, no. 1, pp. 169–172, 2008. View at: Google Scholar
 D. E. Meyerdirk, S. Khasimuddin, and M. Bashir, “Importation, colonization and establishment of Anagyrus indicus (Hym.: Encyrtidae) on Nipaecoccus viridis (Hom.: Pseudococcidae) in Jordan,” Entomophaga, vol. 33, pp. 229–237, 1988. View at: Google Scholar
 M. S. Mossadegh, R. Eslami Zadeh, and M. Esfandiari, “Biological study of mealybugs Nipaecoccus viridis (News.) and possibility of its biological control by Cryptolaemus montrouzieri Mul. in citrus orchards of North Khuzestan,” in Proceedings of the 18th Iranian Plant Protection Congress, p. 35, Hamedan, Iran, August 2008. View at: Google Scholar
 I. Löbl and A. Smetana, Eds., Catalogue of Palearctic Coleoptera. Vol. 4: Elateroidea, Derodontoidea, Bostrichoidea, Lymexyloidea, Cleroidea and Cucujoidea, Apollo Books, Stenstrup, Denmark, 2007.
 A. A. C. Ramindo and A. van Harten, “An annotated checklist of the Coccinellidae (Insecta: Coleoptera) of Yemen,” Fauna of Arabia, vol. 18, pp. 211–243, 2000. View at: Google Scholar
 S. Zarghami, F. Kocheili, M. S. Mossadegh, H. Allahyari, and A. Rasekh, “Effect of temperature on population growth and life table parameters of Nephus arcuatus (Coleoptera: Coccinellidae),” European Journal of Entomology, vol. 111, pp. 199–206, 2014. View at: Google Scholar
 S. Zarghami, F. Kocheili, M. S. Mossadegh, H. Allahyari, and A. Rasekh, “Prey preference and consumption capacity of Nephus arcuatus (Coleoptera: Coccinellidae): the influence of prey stage, prey size and feeding experience,” Biocontrol Science and Technology, vol. 24, no. 9, pp. 1062–1072, 2014. View at: Publisher Site  Google Scholar
 C. S. Holling, “The components of predation as revealed by a study of smallmammal predation of the European pine sawfly,” The Canadian Entomologist, vol. 91, no. 05, pp. 293–320, 1959. View at: Publisher Site  Google Scholar
 M. E. Solomon, “The natural control of animal populations,” The Journal of Animal Ecology, vol. 18, no. 1, pp. 1–35, 1949. View at: Publisher Site  Google Scholar
 M. P. Hassell, J. H. Lawton, and J. R. Beddington, “Sigmoid functional responses by invertebrate predators and parasitoids,” The Journal of Animal Ecology, vol. 46, no. 1, pp. 249–262, 1977. View at: Publisher Site  Google Scholar
 A. Pervez and Omkar, “Functional responses of coccinellid predators: an illustration of a logistic approach,” Journal of Insect Science, vol. 5, pp. 1–6, 2005. View at: Google Scholar
 M. A. Houck and R. E. Strauss, “The comparative study of functional responses: experimental design and statistical interpretation,” The Canadian Entomologist, vol. 117, no. 05, pp. 617–629, 1985. View at: Publisher Site  Google Scholar
 R. A. Sarmento, A. Pallini, M. Venzon, O. F. F. De Souza, A. J. MolinaRugama, and C. L. De Oliveira, “Functional response of the predator Eriopis connexa (Coleoptera: Coccinellidae) to different prey types,” Brazilian Archives of Biology and Technology, vol. 50, no. 1, pp. 121–126, 2007. View at: Publisher Site  Google Scholar
 S. Zarghami, M. S. Mossadegh, F. Kocheili, H. Allahyari, and A. Rasekh, “Prey stage preference and functional response of the coccinellid, Nephus arcuatus Kapur in response to Nipaecoccus viridis (News.),” Plant Pests Research, vol. 4, pp. 73–86, 2014. View at: Google Scholar
 S. A. Juliano, “Nonlinear curve fitting: predation and functional response curve,” in Design and Analysis of Ecological Experiments, S. M. Scheiner and J. Gurevitch, Eds., pp. 178–216, Oxford University Press, New York, NY, USA, 2001. View at: Google Scholar
 SAS Institute, JMP: A Guide to Statistical and Data Analysis, Version 9.1, SAS Institute, Cary, NC, USA, 2003.
 D. Rogers, “Random search and insect population models,” The Journal of Animal Ecology, vol. 41, no. 2, pp. 369–383, 1972. View at: Publisher Site  Google Scholar
 J. C. Trexler, C. E. McCulloch, and J. Travis, “How can the functional reponse best be determined?” Oecologia, vol. 76, no. 2, pp. 206–214, 1988. View at: Publisher Site  Google Scholar
 M. P. Hassell, The Dynamics of Arthropod Predator Prey Systems, Princeton University Press, Princeton, NJ, USA, 1978. View at: MathSciNet
 M. P. Hassell, The Spatial and Temporal Dynamics of Host Parasitoid Interactions, Oxford University Press, Oxford, UK, 2000.
 M. S. Alizadeh, M. S. Mossadegh, and M. Esfandiari, “Natural enemies of Maconelilcoccus hirstus (Green) (Hemiptera: Pseudococcidae) and their population fluctuations in Ahvaz, southwest of Iran,” Journal of Crop Protection, vol. 2, pp. 13–21, 2013. View at: Google Scholar
 M. S. Mossadegh, Sh. Vafaei, S. Zarghami et al., “Natural enemies of Phenacoccus solenopsis Tinsely (Sternorrhycha: Coccoidea: Pseudococcidae) in Khuzestan, Iran,” in Proceedings of the 20th Iranian Plant Protection Congress, p. 216, Shiraz, Iran, September 2012. View at: Google Scholar
 M. H. Bayoumy, “Foraging behavior of the coccinellid Nephus includens (coleoptera: Coccinellidae) in response to Aphis gossypii (hemiptera: Aphididae) with particular emphasis on larval parasitism,” Environmental Entomology, vol. 40, no. 4, pp. 835–843, 2011. View at: Publisher Site  Google Scholar
 R. L. Koch, W. D. Hutchison, R. C. Venette, and G. E. Heimpel, “Susceptibility of immature monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae: Danainae), to predation by Harmonia axyridis (Coleoptera: Coccinellidae),” Biological Control, vol. 28, no. 2, pp. 265–270, 2003. View at: Publisher Site  Google Scholar
 S. Zarghami, M. S. Mossadegh, F. Kocheili, H. Allahyari, and A. Rasekh, “Functional and numerical responses of Nephus arcuatus Kapur feeding on Nipaecoccus viridis (Newstead),” Agricultural Pest Management, vol. 2, pp. 48–59, 2015. View at: Google Scholar
 L. Tang, X. Zhag, C. Tang, C. Zheng, and X. Lu, “Study on functional response of Nephus ryuguus (Kamiya) to Oracella acuta (Lobdell),” Natural Enemies of Insects, vol. 27, pp. 27–31, 2005. View at: Google Scholar
 P. G. Milonas, D. C. H. Kontodimas, and A. F. Martinou, “A predator's functional response: influence of prey species and size,” Biological Control, vol. 59, no. 2, pp. 141–146, 2011. View at: Publisher Site  Google Scholar
 Omkar and A. Pervez, “Functional and numerical responses of Propylea dissecta (Col., Coccinellidae),” Journal of Applied Entomology, vol. 128, no. 2, pp. 140–146, 2004. View at: Publisher Site  Google Scholar
 R. Farhadi, H. Allahyari, and S. A. Juliano, “Functional response of larval and adult stages of Hippodamia variegata (Coleoptera: Coccinellidae) to different densities of Aphis fabae (Hemiptera: Aphididae),” Environmental Entomology, vol. 39, no. 5, pp. 1586–1592, 2010. View at: Publisher Site  Google Scholar
 A. A. Işikber, “Functional response of two coccinellid predators, Scymnus levaillanti and Cycloneda sanguinea, to the cotton aphid, Aphis gossypii,” Turkish Journal of Agriculture and Forestry, vol. 29, no. 5, pp. 347–355, 2005. View at: Google Scholar
 W. W. Murdoch, “Switching in general predators: experiments on predator specificity and stability of prey populations,” Ecological Monographs, vol. 39, no. 4, pp. 335–364, 1969. View at: Publisher Site  Google Scholar
 W. W. Murdoch and A. Oaten, “Predation and Population Stability,” Advances in Ecological Research C, vol. 9, pp. 1–131, 1975. View at: Publisher Site  Google Scholar
 M. B. Hertlein and K. Thorarinsson, “Variable patch times and the functional response of Leptopilina boulardi (Hymenoptera: Eucoilidae),” Environmental Entomology, vol. 16, no. 3, pp. 593–598, 1987. View at: Publisher Site  Google Scholar
 C. S. Holling, “The functional response of predators to prey density and its role in mimicry and population regulation,” Memoirs of the Entomological Society of Canada, vol. 97, no. 45, pp. 1–60, 1965. View at: Publisher Site  Google Scholar
 R. Veeravel and P. Baskaran, “Searching behaviour of two coccinellid predators, Coccinella transversalis fab. and Cheilomenes sexmaculatus fab., on egg plant infested with Aphis gossypii Glov.,” Insect Science and Its Application, vol. 17, no. 34, pp. 363–368, 1997. View at: Google Scholar
 I. Hodek and A. Honek, Ecology of Coccinellidae, Kluwer Academic Publishers, Dordrecht, The Netherlands, 1996.
 R. A. F. Van Den Meiracker and M. W. Sabelis, “Do functional responses of predatory arthropods reach a plateau? A case study of Orius insidiosus with western flower thrips as prey,” Entomologia Experimentalis et Applicata, vol. 90, no. 3, pp. 323–329, 1999. View at: Publisher Site  Google Scholar
 M. Muştu and N. Kilinçer, “Life table and some feeding features of Nephus kreissli fed on Planococcus ficus,” Phytoparasitica, vol. 41, no. 2, pp. 203–211, 2013. View at: Publisher Site  Google Scholar
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Copyright © 2016 Sara Zarghami et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.