Psyche: A Journal of Entomology

Psyche: A Journal of Entomology / 2011 / Article

Research Article | Open Access

Volume 2011 |Article ID 868546 | 7 pages | https://doi.org/10.1155/2011/868546

Foraging Behavior of Praon volucre (Hymenoptera: Braconidae) a Parasitoid of Sitobion avenae (Hemiptera: Aphididae) on Wheat

Academic Editor: Bethia King
Received19 Mar 2011
Revised03 Jun 2011
Accepted14 Jun 2011
Published03 Aug 2011

Abstract

Host stage preference, functional response and, mutual interference of Praon volucre (Haliday) (Hym.: Braconidae) parasitizing the grain aphid, Sitobion avenae (Fabricius) (Hem.: Aphididae), were investigated under laboratory conditions. Host stage preference was evaluated at °C, % relative humidity and a photoperiod of 16:8 h (L : D), under choice and no-choice tests. Functional response was done under five constant temperatures (10, 15, 20, 25, and 30°C), % relative humidity and a photoperiod of 16:8 h. (L : D). Praon volucre parasitized all nymphal instars and adults of the grain aphid but strongly preferred to oviposit into second-instar nymphs in both choice and no-choice conditions. Results of logistic regression revealed a type II functional response for all temperatures tested. The handling time () and searching efficiency () were estimated using the Rogers equation. The maximum estimate of searching efficiency occurred at 15°C and 20°C (both  h−1) and decreased to  h−1 at °C. The minimum estimate of handling time was  h at 25°C and increased to  h at °C. The maximum rate of parasitism was 23.52 aphids/female/day at 25°C. With parasitoid density increasing from 1 to 8, the per capita searching efficiency decreased from 0.12 h−1 to 0.06 h−1. The results suggested that P. voluvre has the potential to be a biocontrol agent of S. avenae. However, evaluation of foraging behavior warrants further investigation under field conditions.

1. Introduction

The grain aphid, Sitobion avenae (Fabricius), is a cosmopolitan species [1]. This aphid causes direct damage by sucking plant sap and indirect damage by either excretion of honeydew or the transmission of viruses. It is found on many different species of Poaceae [2]. Chemical control has been the major tool for the control of aphids. However, biological control strategies are being increasingly applied because of rapid development of insecticides resistance in aphids and because of the effects of pesticides on natural enemies [3]. Parasitoids are important in biological control of cereal aphids [4], and several attempts have been made in introduction [5] and augmentative release of cereal aphid parasitoids [6]. Parasitoids are considered to be especially important in suppressing aphid populations earlier in the season because their appearances precede those of predators [7]. All members of the subfamily Aphidiinae (Hymenoptera: Braconidae) are important parasitoids of aphid species [8]. The genus Praon Haliday is one of the largest Aphidiinae genera with more than 50 described species worldwide [9]. Praon volucre (Haliday) is a parasitoid of S. avenae in Iran [10] Chile [11], Brazil [12], and Sebria [13].

Behavioral responses are one of the most important factors in selecting natural enemies in biological control programs [14]. Host-stage preference affects host-parasitoid population dynamics as the host's development status influences the development and reproduction of the parasitoid [15]. Functional response is the number of successfully attacked hosts as a function of host density [16]. It describes how a predator or parasitoid responds to the changing density of its host, and measuring it helps determine the expected effectiveness of natural enemies [17]. Functional response depends on handling time (: the time that a natural enemy needs to parasitize a single host) and searching efficiency (: the rate at which a parasitoid searches). Functional response is affected by different factors including temperature [1820]. Mutual interference was initially shown by Hassell and Varley [21]. Inverse density dependence between searching efficiency and parasitoid density is known as mutual interference [22]. The purpose of this research was to further investigate host stage preference, mutual interference among adult parasitoids, and the effect of temperature on functional response of P. volucre.

2. Materials and Methods

2.1. Plant and Insect Culture

Seeds of wheat (“Pishtaz” variety) were obtained from the Karaj Cereal Research Department of the Iranian Research Institute of Plant Breeding. The grain aphid and P. volucre were originally collected from the wheat fields in the campus of the Faculty of Agriculture, Tarbiat Modares University in Tehran, Iran, in October 2009. The aphids were reared on wheat seedlings grown in plastic pots (10.5 cm diameter and 9.5 cm height) and covered with transparent cylindrical plastic containers. The colony of aphid parasitoid was reared on S. avenae colonies for 3-4 generations before the parasitoids were used in the experiments. The aphid and its parasitoid colonies were maintained in a growth chamber at °C, % relative humidity and a photoperiod of 16 : 8 h (Light : Dark). All experiments were carried out using seedlings of wheat about 15 cm in height.

2.2. Host Stage Preference

Host-stage preference was determined by both choice and no-choice experiments. In the no-choice tests, 50 individual aphids of a single stage (first, second, third, and fourth instar or adult) were released on a wheat seedling and were exposed to a pair of 1-day-old male and female parasitoids. Our preliminary study showed that the maximum parasitism rate was 15 aphids per female parasitoid per day (unpublished data). To avoid superparasitism, we used 50 aphids per female parasitoid (e.g., more than three times maximum parasitism rate). After 24 h, the parasitoids were removed. The aphids were reared on wheat seedlings until mummies appeared. In the choice tests, all instars were established on a wheat seedling (10 aphids from each instar on each seedling) and were then exposed to a pair of 1-day-old male and female parasitoids for 24 h. Then each instar was held separately until the aphids mummified. Both the choice and the no-choice preference tests were replicated 10 times in cylindrical plastic containers (5 cm diameter and 15 cm height) in the same conditions as above. A streak of honey-water solution (20%) was placed on wheat leaves as a source of carbohydrates and water for the adult parasitoids. Data were checked for normality prior to analysis. The data were analyzed using one-way ANOVA [23]. If significant differences were detected at , means were compared using the Student-Newman-Keuls (SNK) post hoc test.

2.3. Functional Response

The effect of host density on parasitism was investigated at temperatures of 10, 15, 20, 25, and °C, % relative humidity and a photoperiod of 16 : 8 h (Light : Dark). Second-instar nymphs, either 2, 4, 8, 16, 32, or 64 of them, were placed on a wheat seedling (15 cm in height) and placed into a cylindrical plastic container (5 cm diameter and 15 cm height). The top of the container was covered with fine nylon mesh, and the aphids were exposed to a pair of 1-day-old male and female parasitoids for 24 h. Honey-water solution (20%) was provided for adult parasitoids. Host feeding was not determined in this research. The aphids were reared on the plants until mummies were formed. Each aphid density at each temperature was replicated 10 times. To determine the type of functional response, the data were fitted to the logistic regression [19, 24, 25] , , , and are the intercept, linear, quadratic and cubic coefficients, respectively. is the number of hosts parasitized, is the initial host density, and is the proportion of total aphids parasitized. A significant negative or positive linear coefficient () of the logistic regression model indicates type II or III, respectively [24]. After defining the type of functional response, the handling time () and searching efficiency () of a type II response were estimated using Rogers equation [26] as follows: is the number of host parasitized, is the initial host density, is the duration of the experiment ( h), is searching efficiency, is handling time and is the number of parasitoids. Handling time () and searching efficiency () were estimated using non-linear regression and SAS software [23].

2.4. Mutual Interference

In this experiment, 120 second-instar nymphs of S. avenae were placed on wheat seedlings and exposed to groups of 2, 4, 6, and 8 one-day-old mated females. After 24 h, the parasitoids were removed from the cages (5 cm diameter and 15 cm height), and the aphids were held at C, % relative humidity and 16 : 8 h (Light : Dark) photoperiod until mummies were produced. Each parasitoid density was replicated 10 times. The per capita searching efficiency () of the parasitoids at different parasitoid densities was calculated according to the Nicholson equation: is the total number of hosts available (), is the total number of hosts attacked, is the number of parasitoids, and is the duration of the experiment ( h). Searching efficiency was fitted to a linear regression by the least square method, using the inductive model of Hassell and Varley [21]: is the searching efficiency of the parasitoid, is the quest constant (intercept of the regression line), and is the mutual interference constant (slope of the regression line). In this model, includes only the component of interference due to behavioral interactions between parasitoids [27]. Excel software was used to draw figures.

3. Result and Discussion

3.1. Host Stage Preference

Praon volucre parasitized all nymphal instars and adults of the grain aphid but strongly preferred to oviposit into second instar nymphs in both choice preference test (, , ) and no-choice preference test (, , ) (Figure 1). Aphidius rhopalosiphi De Stefani-Perez preferred second-and third-instar nymphs of cereal aphids for oviposition [28]. Our finding was consistent with Diaeretiella rapae (M’Intosh) preferring second-instar nymphs of Brevicoryne brassicae (L.) for oviposition [29]. By contrast, Aphidius matricariae (Haliday) preferred to oviposit into third-instar nymphs of Aphis fabae (Scopoli) [30]. Hagvar and Hofsvang [31] demonstrated the parasitism of an aphid nymphal instar influenced the development and fecundity of the aphids as well as their parasitoids. The parasitoids that parasitized first-instar nymphs of aphids did not mature. Aphidius colemani Viereck females, for example, prefer second instar nymphs of M. persicae, which may maximize fitness gain [32]. It is generally assumed that second- and third-instars nymphs of aphids are preferred by parasitoids because of physiological characteristics. Young host stages provide inadequate food for the successful development of offspring, whereas mortality risk of parasitoid progeny from encapsulation in young host stages is less than in late stages [33]. However, the host stage preference is flexible, and it is influenced by several factors, such as experimental conditions [34], host behavior (particularly aphid defense), and availability of each instar in the field [35]. Host-stage preference is also affected by test duration and host densities [36]. It is well known that host stage selection can affect considerably the population growth of both host and parasitoid and, therefore, can have a definite effect on whether a pest population can be controlled successfully by the parasitoids [31].

3.2. Functional Response

Significant negative linear coefficients of the logistic regression model indicated a type II functional response at all temperatures tested (Table 1, Figure 2). The type of functional response was not affected by temperature, indicating that P. volucre is well adapted to temperature changes. The ability of P. volucre to parasitize grain aphid over a broad range of temperatures makes it as a good candidate for biological control of grain aphid. The proportion of hosts parasitized by P. volucre decreased with increasing host density (Figure 2). Searching efficiency was the highest at 15°C ( h−1), and 20°C ( h−1) and was the lowest at 30°C ( h−1) (Table 2). Handling time decreased with an increase in temperature up to 25°C, then increased at 30°C. Results from this study suggest that this parasitoid could be more effective in reducing populations of P. volucre at 20–25°C than at higher and lower temperatures. The lowest handling time was observed at 25°C ( h). The maximum estimate of parasitism () was at 25°C (23.52 nymphs parasitized/female/day) (Table 2).


Temperatures (°C)Parameters
Intercept ( 𝑃 0 )Linear ( 𝑃 1 )Quadratic ( 𝑃 2 )Cubic ( 𝑃 3 )

100.650 ± 0.38−0.217 ± 0.0610.007 ± 0.002−0.00008 ± 0.0001
150.48 ± 0.37−0.016 ± 0.057−0.001 ± 0.0020.000018 ± 0.0001
202.58 ± 0.496−0.253 ± 0.0690.006 ± 0.002−0.00006 ± 0.0001
251.809 ± 0.426−0.207 ± 0.0620.005 ± 0.0020.00005 ± 0.0001
30−1.167 ± 0.448−0.0004 ± 0.07−0.001 ± 0.0010.000019 ± 0.0001


ParametersTemperatures (°C)
1015202530

Handling time ( 𝑇 )1.95 ± 0.34 (1.25–2.65)1.78 ± 0.21 (1.34–2.22)1.06 ± 0.09 (0.86–1.25)1.02 ± 0.11 (0.79–1.26)5.31 ± 0.82 (3.65–6.96)
Searching efficiency (a)0.02 ± 0.001 (0.01–0.04)0.05 ± 0.001 (0.02–0.08)0.05 ± 0.001 (0.03–0.06)0.03 ± 0.001 (0.02–0.05)0.01 ± 0.001 (0.00–0.02)
Maximum rate of parasitism ( 𝑇 / 𝑇 )12.3013.4822.6423.524.51
Coefficient of determination ( 𝑟 2 )0.790.840.940.930.75

Handling time is defined as the time spent handling the host, parasitizing the host, and also the time spent cleaning and resting. The effect of handling time is to reduce the time available for search for other hosts [37]. The type II functional response is the most frequent in insects [33]. Aphidius uzbekistanicus (Luzhetzki) showed a type II functional response to Metopolophium dirhodum (Walker) [38]. Also type II functional response has been reported by Zamani et al. [39] for A. matricariae and A. colemani on Aphis gossypii Glover, for A. matricariae on A. fabae [30], and for D. rapae on B. brassicae [29]. Praon near occidentale showed a type II functional response on Macrosiphum euphorbiae (Thomas) at 18, 20 and 25°C [40]. Searching efficiency was the highest at 18°C (0.1081 h−1) and handling time was shortest at 25°C (4.89 h). The maximum number of parasitized aphids was 4.9 at 25°C, which was much lower than that of obtained in the present study (23.52 at 25°C). By contrast, Stilmant [41] showed a type III functional response for P. volucre, A. rhopalosiphi, and A. ervi on S. avenae. The handling time, instantaneous attack rate, and maximum number of hosts parasitized by P. volucre were estimated as 0.004 day, 0.493 day−1 and 42.3 nymphs parasitized/parasitoid/day, respectively [41]. The difference between these values may be related to the origin of the populations and different experimental conditions. Type III functional response has been reported for Trioxys pallidus (Haliday) on Chromaphis juglandicola (Kaltenbach) [42], and also for A. colemani and Lysiphlebus testaceipes (Cresson) on Schizaphis graminum (Rondani) [43].

The functional response is affected by the experimental conditions, age of parasitoids, time of exposure, and temperatures [44]. Aphidius uzbekistanicus showed a type III response when parasitizing third-instar nymphs of Hyalopteroides humulis Walker but a type II response when parasitizing M. dirhodum [38]. According to Hofsvang and Hågvar [45], Ephedrus cerasicola Stary exposed to hosts for 1, 6 and 24 h showed type II, type I, and type II functional responses, respectively. Lysiphlebus testaceipes showed type II and type III functional responses at 20°C and 28°C, respectively [17]. In natural field conditions natural enemies can move freely to patches with high densities of hosts, but, in laboratory conditions, natural enemies are forced to remain in a patch for a fixed length of time; therefore, under laboratory conditions the type III functional response is less common than the type II [46]. The reason why type III response is rare in invertebrate predators and parasitoids may be caused by experimental procedures in which the numbers of prey or hosts at low densities is higher than what can be expected in fields [47].

3.3. Mutual Interference

With increasing parasitoid densities from 1 to 8, the per capita parasitism decreased significantly from to (, , ) (Table 3). Accordingly, the per capita searching efficiency () decreased significantly from 0.12 ± 0.01 to 0.06 ± 0.01 as parasitoid density increased from 1 to 8 (, , ). The mean numbers of hosts parasitized increased significantly as the parasitoid density increased (, , ) (Table 3). The equation of linear regression between the logarithm of per capita searching efficiency () and the logarithm of parasitoid density () was (Figure 3). The slope of the regression line (the interference coefficient) was −0.3164. This negative value shows an inverse relationship between parasitoid density and per capita searching efficiency. The negative relationship between per capita searching efficiency and parasitoid density was also documented in D. rapae on B. brassicae [29], and Lipaphis erysimi (Kaltenbach) [48, 49]. This reaction refers to intraspecific competition in the parasitoids. In addition, high parasitoid density causes a higher proportion of male progeny, probably because the females laid unfertilized eggs [50]. The significant reduction of host parasitization per parasitoid with increasing parasitoid density suggests that interference amongst parasitoids also increased at higher parasitoid density. This is probably due to a closed experimental arena and limited time for parasitization and a high probability of mutual interference [30]. In nature, parasitoids may be more attracted to patches of high host density than to patches of low host density [51]. Aggregation of parasitoids in high host density patches increases the probability of encounters between parasitoid individuals. The effect of these encounters (i.e.,mutual interference) is to reduce parasitoid searching efficiency and searching time [37]. Accordingly, in our study, the searching efficiency of P. volucre decreased as the parasitoid density increased (Table 3).


Parasitoid densitiesPer capita parasitismPer capita searching efficiency (a)

1 1 3 . 6 ± 0 . 9 3 a 0 . 1 2 0 6 ± 0 . 0 0 8 a
2 9 . 8 0 ± 0 . 3 8 b 0 . 0 8 9 3 ± 0 . 0 0 3 b
4 8 . 6 5 ± 0 . 0 8 b 0 . 0 8 5 0 ± 0 . 0 0 1 b
6 6 . 5 1 ± 0 . 1 5 c 0 . 0 6 5 8 ± 0 . 0 0 1 c
8 5 . 7 2 ± 0 . 0 6 c 0 . 0 6 0 1 ± 0 . 0 0 1 c

This study provides information on host-parasitoid interactions, which are helpful in management of S. avenae. However, field-based studies are needed to determine P. volucre’s impact on S. avenae and to achieve more realistic results.

Acknowledgments

The authors are most grateful to the Department of Entomology, Tarbiat Modares University for supporting this research. They wish to cordially thank the editor, Prof. Bethia King, and two anonymous reviewers for their constructive comments and suggestions on the earlier version of this paper.

References

  1. W. Kolbe and W. Linke, “Studies of cereal aphids; their occurrence, effect on yield in relation to density levels and their control,” Annals of Applied Biology, vol. 77, pp. 85–87, 1974. View at: Google Scholar
  2. L. Asin and X. Pons, “Effect of high temperature on the growth and reproduction of corn aphids (homoptera: Aphididae) and implications for their population dynamics on the Northeastern Iberian Peninsula,” Environmental Entomology, vol. 30, no. 6, pp. 1127–1134, 2001. View at: Google Scholar
  3. A. Levie, P. Dogot, and T. Hance, “Release of Aphidius rhopalosiphi (Hymenoptera: Aphidiinae) for cereal aphid control: field cage experiments,” European Journal of Entomology, vol. 97, no. 4, pp. 527–531, 2000. View at: Google Scholar
  4. P. Stary, Aphid parasites of Czechoslovakia, Dr. W. Junk Publishers, The Hague, The Netherlands, 1966.
  5. S. E. Halbert, J. B. Johnson, P. L. Graves, P. M. Marsh, and D. Nelson, “Aphidius uzbekistanicus (Hymenoptera: Aphidiidae) established in Idaho,” Pan-Pacific Entomologist, vol. 72, no. 1, pp. 13–16, 1996. View at: Google Scholar
  6. A. Levie, M. A. Legrand, P. Dogot, C. Pels, P. V. Baret, and T. Hance, “Mass releases of Aphidius rhopalosiphi (Hymenoptera: Aphidiinae), and strip management to control of wheat aphids,” Agriculture, Ecosystems and Environment, vol. 105, no. 1-2, pp. 17–21, 2005. View at: Publisher Site | Google Scholar
  7. P. Laska, “A method of comparing the role of aphid parasitoids and predators exemplified by the cabbage aphid, Brevicoryne brassicae,” Acta Entomologica Bohemoslovaca, vol. 81, pp. 81–89, 1984. View at: Google Scholar
  8. T. Hofsvang and E. B. Hagvar, “Ovioposition behavior of Ephedrus cerasicola (Hym. Aphidiidae) parasitizing different instars of its aphid host,” Entomophaga, vol. 31, pp. 261–267, 1986. View at: Google Scholar
  9. N. G. Kavallieratos, Z. Tomanović, P. Starý et al., “Praon Haliday (Hymenoptera: Braconidae: Aphidiinae) of Southeastern Europe: key, host range and phylogenetic relationships,” Zoologischer Anzeiger, vol. 243, no. 3, pp. 181–209, 2005. View at: Publisher Site | Google Scholar
  10. E. Rakhshani, Ž. Tomanović, P. Starý et al., “Distribution and diversity of wheat aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) in Iran,” European Journal of Entomology, vol. 105, no. 5, pp. 863–870, 2008. View at: Google Scholar
  11. P. Stary, “The fate of release parasitoids (Hymenoptera: Braconidae, Aphidiinae) for biological control of aphids in Chile,” Bulletin of Entomological Research, vol. 83, no. 4, pp. 633–639, 1993. View at: Google Scholar
  12. D. N. Gassen and F. J. Tambasco, “Controle Biologico dos pulgoes do trigo no Brasil,” Informe Agropecuario, vol. 9, pp. 49–51, 1983. View at: Google Scholar
  13. Z. Tomanovic and M. Brajkovic, “Aphid parasitoids (Hymenoptera: Aphidiidae) of agroecosystems of the south part of the Pannonian area,” Archives of Biological Sciences, Belgrade, vol. 53, pp. 57–64, 2001. View at: Google Scholar
  14. E. Wajnberg, C. Bernstein, and J. van Alphen, Behavioural Ecology of Insect Parasitoids: From Theoretical Approaches to Field Applications, Wiley-Blackwell, Oxford, UK, 2007.
  15. S. Pandey and R. Singh, “Host size induced variation in progeny sex ratio of an aphid parasitoid Lysiphlebia mirzai,” Entomologia Experimentalis et Applicata, vol. 90, no. 1, pp. 61–67, 1999. View at: Publisher Site | Google Scholar
  16. M. E. Solomon, “The natural control of animal populations,” Journal of Animal Ecology, vol. 18, pp. 1–35, 1949. View at: Google Scholar
  17. C. G. Bazzocchi and G. Burgio, “Functional response of Lysiphlebus testaceipes (Cresson) (Hymenoptera: Braconidae) against Aphis gossypii Glover (Homoptera: Aphididae) at two constant temperatures,” Bollettino dell’Istituto di Entomologia “Guido Grandi” dell’Università degli Studi di Bologna, vol. 54, pp. 13–21, 2001. View at: Google Scholar
  18. M. Coll and R. L. Ridgway, “Functional and numerical responses of Orius insidiosus (Heteroptera: Anthocoridae) to its prey in different vegetable crops,” Annals of the Entomological Society of America, vol. 88, no. 6, pp. 732–738, 1995. View at: Google Scholar
  19. F. J. Messina and J. B. Hanks, “Host plant alters the shape of functional response of an aphid predator (Coleoptera: Coccinellidae),” Environmental Entomology, vol. 27, no. 5, pp. 1196–1202, 1998. View at: Google Scholar
  20. Y. Fathipour, K. Kamali, J. Khalghani, and G. Abdollahi, “Functional response of Trissolcus grandis (Hym., Scelionidae) to different egg densities of Eurygaster integriceps (Het., Scutelleridae) and effects of wheat genotypes on it,” Applied Entomology and Phytopathology, vol. 68, pp. 123–136, 2001. View at: Google Scholar
  21. M. P. Hassell and G. C. Varley, “New inductive population model for insect parasites and its bearing on biological control,” Nature, vol. 223, no. 5211, pp. 1133–1137, 1969. View at: Publisher Site | Google Scholar
  22. J. R. Beddington, “Mutual interference between parasites or predators and its effect on searching efficiency,” Journal of Animal Ecology, vol. 44, pp. 331–340, 1975. View at: Google Scholar
  23. SAS Institute, JMP: A Guide to Statistical and Data Analysis, Version 5.0.1., SAS Institute, Cary, NC, USA, 2003.
  24. S. A. Juliano, “Nonlinear curve fitting: predation and functional response curves,” in Design and Analysis of Ecological Experiment, S. M. Scheiner and J. Gurevitch, Eds., pp. 178–196, Oxford University Press, New York, NY, USA, 2001. View at: Google Scholar
  25. P. De Clercq, J. Mohaghegh, and L. Tirry, “Effect of host plant on the functional response of the predator Podisus nigrispinus (Heteroptera: Pentatomidae),” Biological Control, vol. 18, no. 1, pp. 65–70, 2000. View at: Publisher Site | Google Scholar
  26. D. Rogers, “Random search and insect population models,” Journal of Animal Ecology, vol. 41, pp. 369–383, 1972. View at: Google Scholar
  27. C. A. Free, J. R. Beddington, and J. H. Lawton, “On the inadequacy of simple models of mutual interference for parasitism and predation,” Journal of Animal Ecology, vol. 46, pp. 543–544, 1977. View at: Google Scholar
  28. Y. Shirota, N. Carter, R. Rabbinge, and G. W. Ankersmit, “Biology of Aphidius rhopalosiphi, a parasitoid of cereal aphids,” Entomologia Experimentalis et Applicata, vol. 34, no. 1, pp. 27–34, 1983. View at: Publisher Site | Google Scholar
  29. Y. Fathipour, A. Hosseini, and A. A. Talebi, “Some behavioral characteristics of Diaeretiella rapae (Hym., Aphidiidae), parasitoid of Brevicoryne brassicae (Hom., Aphididae),” Iranian Journal of Agricultural Science, vol. 35, pp. 393–401, 2004. View at: Google Scholar
  30. S. Tahriri, A. A. Talebi, Y. Fathipour, and A. A. Zamani, “Host stage preference, functional response and mutual interference of Aphidius matricariae (Hym.: Braconidae: Aphidiinae) on Aphis fabae (Hom.: Aphididae),” Entomological Science, vol. 10, no. 4, pp. 323–331, 2007. View at: Publisher Site | Google Scholar
  31. E. B. Hagvar and T. Hofsvang, “Aphid parasitoids (Hymenoptera: Aphidiidae): biology, host selection and use in biological control,” Biocontrol News and Information, vol. 12, pp. 13–41, 1991. View at: Google Scholar
  32. M. Barrette, G. M. Wu, J. Brodeur, L. A. Giraldeau, and G. Boivin, “Testing competing measures of profitability for mobile resources,” Oecologia, vol. 158, no. 4, pp. 757–764, 2009. View at: Publisher Site | Google Scholar
  33. J. J. M. Van Alphen and M. A. Jervis, “Foraging behaviour,” in Insect Natural Enemies, Practical Approaches to Their Study and Evaluation, M. Jervis and N. Kidd, Eds., pp. 1–62, Chapman & Hall, London, UK, 1996. View at: Google Scholar
  34. P. Stary, “Aphidiidae,” in Aphid, Their Biology, Natural Enemies and Control, A. K. Minks and P. Harrewijn, Eds., pp. 171–184, Elsevier, Amsterdam, The Netherlands, 1988. View at: Google Scholar
  35. K. A. G. Wyckhuys, L. Stone, N. Desneux, K. A. Hoelmer, K. R. Hopper, and G. E. Heimpel, “Parasitism of the soybean aphid, Aphis glycines by Binodoxys communis: the role of aphid defensive behaviour and parasitoid reproductive performance,” Bulletin of Entomological Research, vol. 98, no. 4, pp. 361–370, 2008. View at: Publisher Site | Google Scholar
  36. M. Mackauer, “Quantitative assessment of Aphidius smithi (Hymenoptera: Aphidiidae): fecundity, intrinsic rate of increase, and functional response,” Canadian Entomologist, vol. 115, pp. 399–415, 1983. View at: Google Scholar
  37. M. P. Hassell, The Dynamics of Arthropod Predator-Prey Systems, Princeton University Press, Princeton, NJ, USA, 1978.
  38. R. D. Dransfield, “Aspect of host parasitoid interactions of two aphid parasitoids, Aphidius urticae (Haliday) and Aphidius uzbekistanicus (Luzhetski) (Hymenoptera: Aphidiidae),” Ecological Entomology, vol. 4, pp. 307–316, 1979. View at: Google Scholar
  39. A. Zamani, A. Talebi, Y. Fathipour, and V. Baniameri, “Temperature-dependent functional response of two aphid parasitoids, Aphidius colemani and Aphidius matricariae (Hymenoptera: Aphidiidae), on the cotton aphid,” Journal of Pest Science, vol. 79, no. 4, pp. 183–188, 2006. View at: Publisher Site | Google Scholar
  40. S. Aragon, F. Cantor, J. Cure, and Y. D. Rodriguez, “Capacidad parasítica de Praon pos. occidentale (Hymenoptera: Braconidae) sobre Macrosiphum euphorbiae (Hemiptera: Aphididae) en condiciones de laboratorio,” Agronomia Colombiana, vol. 21, pp. 142–148, 2007. View at: Google Scholar
  41. D. Stilmant, “The functional response of three major parasitoids of Sitobion avenae: Aphidius rhopalosiphi, A. ervi and P. volucre—how could defferent behaviours conduct to similar results?” OILB/SROP Bulletin, vol. 19, pp. 17–29, 1996. View at: Google Scholar
  42. E. Rakhshani, A. A. Talebi, N. Kavallieratos, and Y. Fathipour, “Host stage preference, juvenile mortality and functional response of Trioxys pallidus (Hymenoptera: Braconidae, Aphidiinae),” Biologia, vol. 59, no. 2, pp. 197–203, 2004. View at: Google Scholar
  43. D. B. Jones, K. L. Giles, R. C. Berberet, T. A. Royer, N. C. Elliott, and M. E. Payton, “Functional responses of an introduced parasitoid and an indigenous parasitoid on greenbug at four temperatures,” Environmental Entomology, vol. 32, no. 3, pp. 425–432, 2003. View at: Google Scholar
  44. M. P. Hassell, J. H. Lawton, and J. R. Beddington, “Sigmoid functional responses by invertebrate predators and parasitoids,” Journal of Animal Ecology, vol. 46, pp. 249–262, 1977. View at: Google Scholar
  45. T. Hofsvang and E. B. Hågvar, “Functional responses to prey density of Ephedrus cerasicola [Hym.: Aphidiidae], an aphidiid parasitoid of Myzus persicae [Hom.: Aphididae],” Entomophaga, vol. 28, no. 4, pp. 317–324, 1983. View at: Publisher Site | Google Scholar
  46. P. Montoya, P. Liedo, B. Benery, J. F. Barrere, J. Cancino, and M. Aluja, “Functional response and superparasitism by Diachasmimoopha longicaudata (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae),” Annals of the Entomological Society of America, vol. 93, pp. 47–54, 2000. View at: Google Scholar
  47. J. C. van Lenteren and K. Bakker, “Functional Responses in Invertebrates,” Netherlands Journal of Zoology, vol. 26, pp. 567–572, 1976. View at: Google Scholar
  48. A. Z. Abidi, A. Kumar, and C. P. Tripathi, “Impact of males on the numerical response of Diaeretiella rapae (M’Intosh) (Hym., Aphidiidae), a parasitoid of Lipaphis erysimi Kalt. (Hem., Aphididae),” Mitteilungen aus dem Museum für Naturkunde in Berlin – Zoologische Reihe, vol. 65, pp. 161–169, 1989. View at: Google Scholar
  49. A. N. Shukla, C. P. M. Tripathi, and R. Singh, “Effect of food plants on the numerical response of Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae), a parasitoid of Lipaphis erysimi kalt. (Hemiptera: Aphididae),” Biological Agriculture and Horticulture, vol. 14, no. 1-4, pp. 71–77, 1997. View at: Google Scholar
  50. W. A. Jones, S. M. Greenberg, and B. Legaspi, “The effect of varying Bemisia argentifolii and Eretmocerus mundus ratios on parasitism,” BioControl, vol. 44, no. 1, pp. 13–28, 1999. View at: Google Scholar
  51. J. K. Waage, “Aggregation in field parasitoid populations: foraging time allocation by a population of Diadegma (Hymenoptera, Ichneumonidae) (Plutella xylostella),” Ecological Entomology, vol. 8, no. 4, pp. 447–453, 1983. View at: Google Scholar

Copyright © 2011 Afrooz Farhad 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.

1867 Views | 736 Downloads | 3 Citations
 PDF  Download Citation  Citation
 Download other formatsMore
 Order printed copiesOrder