Temperature-dependent Functional Response of Cryptolaemus montrouzieri (Col.: Coccinellidae) to the Citrus Mealybug, Planococcus citri (Hem.: Pseudococcidae)

Document Type : Research Article

Authors

• M. Hassanpour
• M. Moradi

Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran

10.22067/jpp.v33i3.79292

Abstract

Introduction: The citrus mealy bug,  Planococcus citri (Risso) is one of the major pests of citrus and many other orchards crops, as well as ornamental plants in subtropical and tropical regions of the world, including Iran. Due to the harmful effects of chemical pesticides on biological control agents and non-target organisms, along with developing resistance to various pesticides by the pests, there has been an increasing interest in integrating biological control methods in the pest management programs. The predatory ladybird, Cryptolaemus montrouzieri Mulsant is one of the most widely used biological control agents. It is an important natural enemy of many species of mealybugs such as P. citri. Functional response of a predator that refers to the number of prey consumed per predator as a function of a prey density is the important characteristic of predator–prey interactions. Temperature can affects the consumption behaviour of the predators. The aim of the present study is to evaluate the effects of temperature on the functional response of C. montrouzieri to different densities of P. citri. Improving our understanding about predator-prey interactions between C. montrouzieri and P. citri may be helpful to optimize biological control of the mealy bug.
Materials and Methods: The colony of P. citri was collected from bitter orange in Mehmansara region, Ghaemshahr, Mazandaran province, and was reared on pumpkin, Cucurbita maxima. The laboratory colony of C. montrouzieri was obtained from Baharan Dasht Sahel insectarium in Sari, Mazandaran province, and was reared on P. citri. The functional response experiments were performed with fourth instar larvae and adult females of C. montrouzieri to the adult female of P. citri. The experiments were conducted at the temperatures of 18, 23, 27, 32 and 37±1 °C, 60±10% RH and L16:D8 h. Prey in densities of 3, 5, 7, 10, 15 and 30 was offered to the predators. The predators used for the experiments were < 48 h old and were starved for 24 h before starting the tests. A single bitter orange leaf disc (3 cm2) was centred upside down in each ventilated Petri dish (10 cm diameter). Ten replicates were conducted for each prey density. After 24 h, the predators were removed from the experimental arena and the number of consumed prey was recorded and they were not replaced during the functional response tests. The type of the functional response was determined by logistic regression analysis (SAS/STAT, CATMOD-procedure) of the proportion of prey killed in relation to prey offered. To determine the type of functional response, the sign of the linear coefficient was estimated by the logistic regression. The negative sign is evident to a functional response type II, whereas a positive sign reveals a type III functional response. Parameters of attack rate and handling time were estimated using the PROC NLIN procedure of SAS and compared through the indicator variable method. 
Results and Discussion: The logistic regression for fourth instar larvae and adult females of C. montrouzieri to P. citri at all temperatures showed a negative linear parameter and the proportion of prey eaten by the predators declined with increasing prey density. This suggested that fourth instar larvae and females of C. montrouzieri exhibited a type II functional response to change in P. citri density at all tested temperatures. The highest attack rate and lowest handling time of fourth instar larvae were estimated at 37 and 27 °C, respectively. Whereas the highest attack rate and lowest handling time of adult females were estimated at 37 and 32 °C, respectively. At the same temperature, the attack rate estimated for the adult female was higher than that of the larval instar of the predator, showing higher predation potential of adult female in compared to the fourth larval instar of the predator. Theoretical maximum attack rates (T/Th) for fourth larval instar of the predator at above-mentioned temperatures were respectively estimated 8.20, 28.81, 43.80, 19.82 and 14.44 and for adult female predator were 9.70, 9.17, 9.10, 18.47 and 17.92, respectively.          
Conclusion: Temperature affected significantly functional response parameters of fourth instar larvae and adult females of C. montrouzieri to P. citri densities. Although the last instar larvae and adult females of C. montrouzieri showed high predation potential at all temperatures, adult females of the predator was more voracious compared to the last instar larvae of the predator especially at higher temperatures.

Keywords

• temperature
• Functional response
• Cryptolaemus montrouzieri
• Planococcus citri

20.1001.1.20084749.1398.33.3.3.8

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References

1-Abdollahi Ahi, G., Afshari, A., Baniameri, V., Dadpour Moghanloo, H., Assadeh, Gh. And Yazdanian, M. 2012. Functional response of Cryptolaemus montrouzieri Mulsant (Col.: Coccinellidae) to citrus mealybug, Planococcus citri (Risso) (Hom.: Pseudococcidae) under laboratory conditions. Plant Protection (Scientific Journal of Agriculture), 35:1-14.(in Persian)

2- Allahyari, H., Fard, P.A. and Nozari, J. 2004. Effects of host on functional response of offspring in two populations of Trissolcus grandis on the Sunn pest. Journal of Applied Entomology, 128:39-43.

3- Ardestani, M., Tusi, M, and Khaledi, K. 2010. Surveying orange domestic marketing in North of Iran. Agricultural Economics and Development, 18:47-68. (in Persian)

4- Asghari, F., Samih, M.A., Mahdian, K., Basirat, M. and Izadi, H. 2010. Functional response of Hippodamia varigata (Goeze), predator of common pistachio psylla, under laboratory conditions. 19th Iranian Plant Protection Congress, 1-3 August, Tehran, Iran. (in Persian)

5- Atif, J.Y.M., Naser, K.S.A., Elsherif, M.E. and Al- Humiari, A.A. 2011. Functional response of the Adult predator of Cryptolaemus montrouzieri (Mulsant), reared on the third nymphal instar of Planococcus citri (Risso). Egyption Journal of Pest Control, 21:267-270.

6- Bernal, J.S., Bellows, T.S. and Gonzalez, D. 1994. Functional response of Diaeretiella rapae (M’ Intosh) (Hym.: Aphidiidae) to Diuraphis noxia (Mordvilko) (Hom.: Aphididae) hosts. Journal of Applied Entomology, 118:300-309.

7- Campbell, A., Frazer, B.D., Gilbert, N., Gutierrez, A.P. and Makauer, M. 1974. Temperature requirements of some aphids and their parasites. Journal of Applied Ecology, 11:431-438.

8- Delfosse, E.S. 2005. Risk and ethics in biological contral. Biological Control, 35:319-329.

9- Ding-Xu, L., Juan, T. and Zuo-Rui, S. 2007. Functional response of the predator Scolothrips takahashito howthorn spider mite, Tetranychus viennensis: Effect of age and temperature. Biocontrol, 52:47-67.

10- Emami, M. S., Sahragard, A. and Hajizade, J. 1999. Effect of different temperatures on development of Scymnus syriacus (Col.: Coccinellidae). Journal of Applied Entomology and Phytopathology, 17:35-40.

11- Esmaeili, M. 2007. The most important pests of fruit trees. Publishing Center Sepehr.(in Persian)

12- Farhadi, R., Allahyari, H. and Juliano, S.A. 2010. Functional response of larval and adult stages of Hippodamia variegata (Col.: Coccinellidae) to different densities of Aphis fabae (Hem.: Aphididae). Environmental Entomology, 39:1586-1592.(in Persian)

13- Flinn, P.W. and Hagstrum, D.W. 2002. Temperature-mediated functional response of Theocolax elegans (Hymenoptera: Pteromalidae) parasitizing Rhyzopertha dominica (Coleoptera: Bostrichidae) in stored wheat. Journal of Stored Products Research, 38: 185-190.

14- Ghafoor, A., Saba, I., Khan, S. and Farooq, H. 2011. Predatory potential of Cryptolaemus montrouzieri for cotton mealybug under laboratory conditions. Journal of Animal and Plant Sciences, 21:90-93.

15- Gill, H.K., Goyal, G. and Gillett-Kaufman, J. 2012. Citrus mealybug, Planococcus citri (Risso) (Insecta: Hemiptera: Pseudococcidae). EENY-537. Entomology and Nematology, Florida Cooperative Extension Service. University of Florida IFAS.

16- Gotoh, T., Nozawa, M. and Yamaguchi, K. 2004. Prey consumption response of three acarophagous species to egg of the two-spotted spider mite in the laboratory. Laboratory of Applied Entomology and Zoology. Faculty of Agriculture, Ibraki University, 39: 97-105.

17- Hassanpour, M., Bagheri, M., Golizadeh, A. and Farrokhi, S. 2016. Functional response of Nesidiocoris tenuis (Hemiptera: Miridae) to Trialeurodes vaporariorum (Hemiptera: Aleyrodidae): Effect of different host plants. Biocontrol Science and Technology, 26: 1489-1503.

18- Hassanpour, M., Maghami, R., Rafiee Dastjerdi, H. and Golizadeh, A. 2015. Predation activity of Chrysoperla carnea (Neuroptera: Chrysopidae) upon Aphis fabae (Hemiptera: Aphididae): Effect of different hunger levels. Journal of Asia-Pacific Entomology, 18: 297-302.

19- Hassell, M. 1982. Patterns of parasitism by insect parasites in patchy environments. Ecological Entomology, 7:365-377.

20- Hodek, I. and Honek, A. 1996. Ecology of coccinellidae. Kluwer Academic Publishers. Dordrecht, 464.

21- Holling, C. S. 1959. Some characteristics of simple types of predation and parasitism. Canadian Entomologist, 91:385-398.

22- Huffaker, C., Berryman, A. and Turchin, P. 1999. Dynamics and regulation of insect populations. p. 269-305. In Huffaker, C.B. and Gutierrez, A.P. (ed.) Ecological Entomology. 2nd ed. Wiley, New York.

23- Imani, Z., Shishebor, P.and Mosadegh, M.S. 2010. Functional response of Stethorus gilvifrons Mulsant (Col.: Coccinellidae) to different developmental stages of Eutetranychus orientalis (Acari: Tetranychidae). Scientific Journal of Agriculture, 33:1-10.(in Persian)

24- Jafari, S., Fathipour, Y. and Faraji, F. 2012. The influence of temperature on the functional response and prey consumption of Neoseiulus barkeri (Acari: Phytoseiidae) on Tetranychus urticae (Acari: Tetranychidae). Journal of Entomological Society of Iran, 31:39-52. (in Persian)

25- Jalali, M.A., Tirry, L. and De Clercq, P. 2010. Effect of temperature on the functional response of Adalia bipunctata to Myzus persicae. BioControl, 55:261-269.

26- Jeschke, J.M., Kopp, M. and Tollrian, R. 2004. Consumer- food systems: why type I functional responses are exclusive to filter feeders. Biology Review, 79:337-349.

27- Juliano, S.A. 2001. Non-linear curve-fitting: predation and functional response curves, p. 178-196. In Scheiner, S.M. and Gurevitch, J. (ed.) Design and Analysis of Ecological Experiments. 2nd ed. Chapman and Hall, New York.

28- Kalyebi, A., Overholt, W.A., Schulthess, F., Mueke, J.M., Hassan, S.A. and Sithanonthan, S. 2005. Functional response of six indigenous trichogrammatid egg parasitoids (Hymenoptera: Trichogrammatidae) in Kenya: influence of temperature and relative humidity. Biological Control, 32:164-171.

29- Kareiva, P. 1990. The special dimension in pest-enemy interaction. p. 213-227. In Mackauer,M., Ehler, L. E. and Roland, J. (ed.) Critical Issues in Biological Control. Intercept, Anover, Hants.

30- Kaur, H. and Virk, J.S. 2012. Feeding potential of Cryptolaemus montrouzieri against the mealybug Phenacoccus solenopsis. Phytoparasitica, 40:131-136.

31- Kontodimas, D.C. and Stathas, G.J. 2005. Phenology, fecundity and life table parameters of the predator Hippodamia variegata reared on Dysaphis crataegi. BioControl 50, 223–233.

32- Madadi, H., Enkegard, A., Brosgaard, H.F., Kharrazi-Pakdel, A., Ashouri, A. and Mohaghegh-Neishabouri, J. 2007.Host plant effects on the functional response of Neoseiulus cucumeris to onion thrips larvae. Journal of Applied Entomology, 131:728-733.

33- Mahdian, K., Vantornhout, I., Tirry, L. and De Clercq, P. 2006. Effects of temperature on predation by the stinkbugs Picromerus bidens and Podisus maculiventris (Heteroptera: Pentatomidae) on noctuid caterpillar. Bulletin of Entomological research, 96:489-496.

34- Malkeshi, S.H. 2010. Mass rearing of Cryptolaemus montrouzieri (Mulsant) with the farmers participation for biological control of mealybug, Pseudococcus viburni at tea orchards in Guilan and Mazandaran provinces. Iranian Research Institute of Plant Protection, Final report of project, approved number: 04-16-16-87088, 77

35- Moayeri, H.R.S., Madadi, H., Pouraskar, H. and Enkegaard, A. 2013. Temperature dependent functional response of Diaeretiella rapae (Hymenoptera: Aphidiidae) to the Cabbage aphid, Brevicoryne brassicae (Hemiptera: Aphididae). European Journal of Entomology, 110:109-113.

36- Moghaddam, M. 2017. The scale insects of citrus in Iran. (Identification, Biology, Natural Enemies and Distribution). Iranian Research Institute of Plant Protection, 179.(in Persian)

37- Mohajeri Parizi, A., Madadi, H., Allahyari, H. and Mehrnejad, M.R. 2010. Functional response of different developmental stages of Hippodamia variegata to the fourth instar nymphs of Aphis gossypii in microcosm condition. 19th Iranian Plant Protection Congress, 1-3 August, Tehran, Iran. (in Persian)

38- Mohasesian, E., Ranjbar Aghdam, H. and Pakyari, H. 2015. Temperature-dependent functional response of mealybug destroyer, Cryptolaemus montrouzieri on citrus mealybug, Planococcus citri. BioControl in Plant Protection, 2:1-11. (in Persian with English abstract)

39- Murdoch, W.W. 1973. The functional response of predators. Journal of Applied Ecology, 14:335-347.

40- Mossadegh, M.S., Eslamizadeh, R. and Esfandiari, M. 2008. Biological study of mealybug Nipaecoccus viridis (New.) and possibility of its biological control by Cryptolaemus montrouzieri Mulsant in citrus orchards of North Khuzestan. Proceeding of 18th Iranian Plant Protection Congress, Hamedan, Iran.(in Persian)

41- Munyaneza, J. and Obrycki, J.J. 1994. Functional response of Coleomegilla maculata (Col.: Coccinellidae) to Colorado potato beetle eggs (Col.: Chrysomelidae).Biological Control, 8: 215-224.

42- Nazari, A., Hajizadeh, J. and Sahragard, A. 2004. Functional response of Exochomus nigromaculatus (Col.: Coccinellidae) to different densities of Aphis nerii and Aphis craccivora. Entomology and Phytopathology, 72:85-94.(in Persian)

43- O’Neil, P.J. 1989. Comparison between laboratory and field measurements of the functional response of Podisus maculiventris (Heteroptera: Pentatomidae0. Journal of the Kansas Entomological Society, 62:148-155.

44- Omkar, O. and Pervez, A. 2016. Ladybird Beetles.p. 281–310. In Omkar (ed) Ecofriendly PestManagement for Food Security. Academic Press.

45- Pakyari, H., Fathipour, Y., Rezapanah, M. and Kamali, K. 2009. Temperature-dependent functional response of Scolothrips longicornis (Thysanoptera: Thripidae) preying on Tetranychus urticae. Journal of Asia-Pacific Entomology, 12:23-26.

46- Parajulee, M.N., Phllips, T.W. and Hogg, D.B. 1994. Functional response of Lyctocoris campestris (F.) adults: effects of predator sex, prey species, and experimental habitat. Bilogical Control, 4:80-87.

47- Pervez, A. and Omkar, O. 2005. Functional response of coccinellid predators on illustration of a logistic approach. Journal of Insect Science, 5:1-6.

48- Rahimi, R., Mahdian, K. and Shahidi Nouqani, S. 2010. Temperature-dependent functional response of Coccinula elegantula on Aphis gossypii. Journal of Greenhouse Culture Science and Technology, 7:125-133.(in Persian)

49- Rogers, D.J. 1972. Random search and insect population models. Journal of animal Ecology, 41:369-383.

50- Sadeghi, A. 1991. An investigation on the coccinellids fauna of alfalfa fields and determination of species at Karaj. M.Sc. dissertation, Faculty of Agriculture, University of Tehran, Iran. (in Persian with English abstract)

51- Saljoqi, A.U.R., Nasir, M., Khan, J., Ehsan-Ul-Haq, M., Salim, M., Nadeem, Z., Huma, H., Saeed, G., Ahmad, B. and Sadur-Rehman, Z. 2015. Functional response study of Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae) fed on cotton mealybug, Phenacoccus solenopsis Tinsley under laboratory conditions. Journal of Entomology and Zoology of Studies. 3:411-415.

52- SAS Institute Inc. 2004. SAS/ STAT User’s guide, version 9.1, vols 1 and 2. Cary, NC: SAS Institute Inc.

53- Seko, T. and Miura, K. 2008. Functional response of the lady beetle Harmonia axyridis Pallas (Col.: Coccinelidae) on the aphids Myzus persicae Sulzer (Hom.: Aphididae). Applied Entomology and Zoology, 43:341-345.

54- Skrivin, D.J. and Fenlon, J.S. 2003. The effect of temperature on the functional response of Phytoseiulus persimilis (Acari: Phytoseiidae). Experimental of Applied Acarplogy, 31:37-49.

55- Sohrabi, F. and Shishebor, P. 2007. Functional and numerical response of Stethorus gilvifrons Mulsant feeding on strawberry spider mite, Tetranychus turkestani Ugarov and Nikolski. Pakistan Journal of Biological Sciences. 10: 4563-4566.

56- Solomon, M.E. 1949. The natural control of animal population. Journal of Animal Ecology, 18:1-35.

57- Tazerouni, Z., Talebi, A.A. and Rakhshani, E. 2012. Temperature-dependent functional response of Diaretiella rapae (Hymenoptera: Braconidae), a parasitoid of Diuraphis noxia (Hemiptera: Aphididae). Journal of the Entomological research Society, 14:31-40.

58- Van Alphen, J.J.M. and Jervis, M.A. 1996. Foraging behavior. p. 1-62. In Jervis, M. and Kidd, N. (ed.) Insect Natural Enemies, Practical Approaches to their study and Evaluation. Chapman and Hall, London, U. K.

59- Zamani, A.A., Talebi, A.A., Fathipour, Y. and Baniameri, V. 2006.Temperature-dependent functional response of two aphid parasitoids, Aphidius colemani and Aphidius matricariae (Hymenoptera: Aphidiidae), on the cotton aphid. Journal of Pest Science, 79:183-188.