Abstract
The functional responses of two coccinellid-predators, viz. Propylea dissecta (Mulsant) and Menochilus sexmaculatus (Fabricius) sharing common aphid-prey, Aphis gossypii (Glover) were investigated in various heterospecific and conspecific combinations in laboratory conditions. The third and fourth instar larvae, along with adults (males and females) of the above coccinellids were fed on increasing densities (from 25 to 600) of A. gossypii, after releasing a couple of conspecifics or heterospecific coccinellids of the same stage in a microhabitat. Their cumulative prey consumption was quantified at predator species, predatory stage and prey densities levels. Despite a Type II response by predators in each combination, high proportion of prey was consumed at low and middle densities. Heterospecific females consumed prey with a maximum attack rate (0.0024) with the least handling time (0.1831 hour) than conspecific ones. Adult female P. dissecta was smaller than M. sexmaculatus but together they consumed more aphids than the two females of M. sexmaculatus due to the least interference, which supports releases of dual-predators for aphid biocontrol. Amongst larvae, duo fourth instars M. sexmaculatus had an attack rate of 0.0015 and handling time of 0.1879 hour. We conclude that duo release of adult M. sexmaculatus and P. dissecta benefits more than their single releases for the biocontrol of A. gossypii. In addition, conspecific fourth instars M. sexmaculatus were better predators in various larval combinations.
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References
Atlihan R, Kaydan MB, Yarımbatman A, Oku H (2010) Functional response of the coccinellid predator Adalia fasciatopunctata revelierei to walnut aphid (Callaphis juglandis). Phytoparasitica 38:23–29. https://doi.org/10.1007/s12600-009-0075-y
Bayoumy MH, Osman MA, Michaud JP (2014) Host plant mediates foraging behavior and mutual interference among adult Stethorus gilvifrons (Coleoptera: Coccinellidae) preying on Tetranychus urticae (Acari: Tetranychidae). Environ Entomol 43(5):1309–1318. https://doi.org/10.1603/EN14134
Bayoumy MH, Awadalla HS (2018) Foraging responses of Coccinella septempunctata, Hippodamia variegata and Chrysoperla carnea to changing in density of two aphid species. Biocont Sci Technol 28:226–241. https://doi.org/10.1080/09583157.2018.1437597
Bayoumy MH, Ramadan MM (2018) When predators avoid predation by their con- and heterospecific competitors: non-consumptive effects mediate foraging behavior and prey handling time of predators. J Econ Entomol 111:1577–1586. https://doi.org/10.1093/jee/toy122
Boopathi T, Singh SB, Dutta SK, Dayal V, Singh AR, Chowdhury S, Ramakrishna Y, Shakuntala I, Lalhruaipuii K (2020) Biology, predatory potential, life table, and field evaluation of Propylea dissecta (Coleoptera: Coccinellidae), against Lipaphis erysimi (Hemiptera: Aphididae) on broccoli. J Econ Entomol 113:88–97. https://doi.org/10.1093/jee/toz272
Cabral S, Soares AO, Garcia P (2009) Predation by Coccinella undecimpunctata (Coleoptera: Coccinellidae) on Myzus persicae Sulzer (Homoptera: Aphididae): Effect of prey density. Biol Cont 50:25–29. https://doi.org/10.1016/j.biocontrol.2009.01.020
Carmo-Sousa M, Moreno A, Plaza M, Garzo E, Fereres A (2016) Cucurbit aphid-borne yellows virus (CABYV) modifies the alighting, settling and probing behaviour of its vector Aphis gossypii favouring its own spread. Ann Appl Biol 169:284–297. https://doi.org/10.1111/aab.12300
Chaudhary DD, Kumar B, Mishra G, Omkar (2015) Resource partitioning in a ladybird, Menochilus sexmaculatus: function of body size and prey density. Bull Ent Res 105:121–128. https://doi.org/10.1017/S0007485314000844
DeClercq P, Mohaghegh J, Trriy L (2000) Effect of host plant on the functional response of the predator Podisus nigrispinus (Heteroptera: Pentatomidae). Biol Cont 18:65–70. https://doi.org/10.1006/bcon.1999.0808
Dehkordi SD, Sahragard A, Hajizadeh J (2012) Comparison of functional response of two and one individual female predator, Hippodamia variegata Goeze (Coleoptera: Coccinellidae) to different densities of Aphis gossypii Glover (Hemiptera: Aphididae) under laboratory conditions. Mun Entomol Zool 7:998–1005
Farhadi R, Allahyari H, Juliano SA (2010) Functional response of larval and adult stages of Hippodamia variegata (Coleoptera: Coccinellidae) to different densities of Aphis fabae (Hemiptera: Aphididae). Environ Entomol 39:1586–1592. https://doi.org/10.1603/EN09285
Fatemi S, Samih MA (2017) Functional response of six - spotted zigzag ladybird, Menochilus sexmaculatus (Fabricius) (Col.: Coccinellidae) to pomegranate green aphid, Aphis punicae Pass. (Hem.: Aphididae) at different temperatures. J Plant Protect 31:179–190. https://doi.org/10.22067/jpp.v0i0.41174
Feng Y, Zhou ZX, An MR, Yu XL, Liu TX (2018) The effects of prey distribution and digestion on functional response of Harmonia axyridis (Coleoptera: Coccinellidae). Biol Cont 124:74–81. https://doi.org/10.1016/j.biocontrol.2018.04.009
Ghosh S, Agarwala BK (2018) Inter-specific relationship of size and walking speed in predaceous ladybirds (Insecta: Coleoptera: Coccinellidae). Curr Sci 115:141–146
Gupta RK, Pervez A, Guroo MA, Srivastava K (2012) Stage specific functional response of an aphidophagous ladybird, Coccinella septempunctata (Coleoptera: Coccinellidae), to two aphid species. Int J Trop Insect Sci 32:136–141. https://doi.org/10.1017/S1742758412000227
Hameed Y, Hamid MF, Ahmad N, Sarmad M, Zaka SM, Saeed Q, Khan MAZ, Abbas K, Shahzaib M, Zakria M (2021) Influence of three aphid species for determining the stage-specific functional response of the coccinellid beetle Menochilus sexmaculatus (F.). J Kansas Entomol Soc 93:185–195. https://doi.org/10.2317/0022-8567-93.3.185
Hautier L, San Martin G, Jansen J-P, Branquart E, Grégoire J-C (2017) Spiny prey, fortunate prey, dorsal spines are an asset in intraguild interactions among lady beetles. Frontiers Ecol Evol 5:135. https://doi.org/10.3389/fevo.2017.00135
Hodek I, van Emden HF, Honek I (2012) Ecology and behaviour of the ladybird beetles (Coccinellidae). Wiley-Blackwell, Oxford, UK
Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398
Holling CS (1965) Functional response of predators to prey density and its role in mimicry and population regulation. Mem Entomol Soc Canada 45:3–60
Islam Y, Shah FM, Shah MA, Khan MM, Rasheed MA, Rehman SU, Ali S, Zhou X (2020) Temperature-dependent functional response of Harmonia axyridis (Coleoptera: Coccinellidae) on the eggs of Spodoptera litura (Lepidoptera: Noctuidae) in laboratory. Insects 11:583. https://doi.org/10.3390/insects11090583
Jalali MA, Ziaaddini M (2017) Effects of host plant morphological features on the functional response of Adalia bipunctata (Coleoptera: Coccinellidae) to Myzus persicae (Hemiptera: Aphididae). Int J Pest Manag 63:309–315. https://doi.org/10.1080/09670874.2016.1258502
Juliano SA (2001) Nonlinear curve fitting: predation and functional response curves. In: Cheiner SM, Gurven J (eds) Design and Analysis of Ecological Experiments, 2nd edn. Chapman and Hall, London, pp 178–196
Khalil RE, Shaheen FAH, Abdel-Hady AA, Saleh AA (2020) Functional Responses of Coccinella undecimpunctata and Chrysoperla carnea to their Aphid Prey under Semi-Field Conditions. J Plant Protect Pathol Mansoura Univ 11:89–95. https://doi.org/10.21608/jppp.2020.78912
Khan AA (2017) Functional response of four syrphid predators associated with mealy cabbage aphid, Brevicoryne brassicae L. on cruciferous vegetables. Int J Curr Microbiol Appl Sci 6:2806–2816
Kindlmann P, Dixon AFG (1999) Generation time ratios-determinants of prey abundance in insect predator-prey interactions. Biol Cont 16:133–138. https://doi.org/10.1006/bcon.1999.0754
Kindlmann P, Stipkova Z, Dixon AFG (2020) Generation time ratio, rather than voracity, determines population dynamics of insect–natural enemy systems, contrary to classical Lotka-Volterra models. Eur J Environ Sci 10:133–140. https://doi.org/10.14712/23361964.2020.15
Kisdi É, Liu S (2006) Evolution of handling time can destroy the coexistence of cycling predators. J Evol Biol 19:49–58. https://doi.org/10.1111/j.1420-9101.2005.00993.x
Köhnke MC, Siekmann I, Seno H, Malchow H (2020) A type IV functional response with different shapes in a predator-prey model. J Theo Biol 505:110419. https://doi.org/10.1016/j.jtbi.2020.110419
Kumar B, Mishra G, Omkar (2014) Functional response and predatory interactions in conspecific and heterospecific combinations of two congeneric species (Coleoptera: Coccinellidae). Eur J Entomol 111:257–265. https://doi.org/10.14411/eje.2014.025
Madadi H, Parizi EM, Allahyari H, Enkegaard A (2011) Assessment of the biological control capability of Hippodamia variegata (Col.: Coccinellidae) using functional response experiments. J Pest Sci 84:447–455. https://doi.org/10.1007/s10340-011-0387-9
Moezipour M, Kafil M, Allahyari H (2008) Functional response of Trichogramma brassicae at different temperatures and relative humidities. Bull Insectol 61:245–250
Omkar, Pervez A (2004a) Predaceous coccinellids in India: predator-prey catalogue. Orient Insects 38:27–61. https://doi.org/10.1080/00305316.2004.10417373
Omkar, Pervez A (2004b) Functional and numerical responses of Propylea dissecta (Mulsant) (Col., Coccinellidae). J Appl Entomol 128:140–146. https://doi.org/10.1111/j.1439-0418.2004.00824.x
Omkar, Pervez A (2011) Functional response of two aphidophagous ladybirds searching in tandem. Biocont Sci Technol 21:101–111. https://doi.org/10.1080/09583157.2010.527319
Papanikolaou DN, Milonas PG, Preston S, Kypraios T (2016) Does mutual interference affect the feeding rate of aphidophagous coccinellids? a modeling perspective. PLoS One 11(1):e0146168. https://doi.org/10.1371/journal.pone.0146168
Pervez A, Chandra S, Kumar R (2021) Effect of dietary history on intraguild predation and cannibalism of ladybirds’ eggs. Int J Trop Insect Sci. https://doi.org/10.1007/s42690-021-00444-4
Pervez A, Kumar R (2017) Preference of the aphidophagous ladybird, Propylea dissecta for two species of aphids reared on toxic host plants. Eur J Environ Sci 7:130–134
Pervez A, Omkar (2004) Prey dependent life attributes of an aphidophagous ladybird beetle, Propylea dissecta (Mulsant). Biocont Sci Technol 14:385–396. https://doi.org/10.1080/09583150410001683547
Pervez A, Omkar (2005) Functional responses of coccinellid predators: An Illustration of a Logistic Approach. J Insect Sci 5:1–6. https://doi.org/10.1093/jis/5.1.5
Pervez A, Omkar (2011) Ecology of an aphidophagous ladybird Propylea: A review. J Asia Pacific Entomol 14:357–365. https://doi.org/10.1016/j.aspen.2011.01.001
Pervez A, Omkar, Harsur MM (2020) Coccinellids on crops: Nature’s gift for farmers. In Chakravarty AK (ed) Innovative Pest Management Approaches for the 21st Century: Harnessing Automated Unmanned Technologies. Springer International Publisher, Singapore, pp 429–460
Rahman T, Roff MNM, Ghani IBA (2010) Within-field distribution of Aphis gossypii and aphidophagous lady beetles in chili, Capsicum annuum. Ent Exper Applic 137:211–219. https://doi.org/10.1111/j.1570-7458.2010.01056.x
Roger D (1972) Random search and insect population models. J Anim Ecol 41:369–383
Sanati S, Goldasteh S, Shirvani A et al (2020) Functional response of Oenopia conglobata contaminata (Coleoptera: Coccinellidae) to Agonoscena pistaciae (Hemiptera: Psyllidae) at two different temperatures. Int J Trop Insect Sci 40:621–628. https://doi.org/10.1007/s42690-020-00108-9
SAS 9.0 (2002) SAS/Stat Version 9 SAS Institute Inc. Cary, NC, USA
Siddiqui A, Kumar A, Kumar N, Tripathi CPM (1999) Prey-predator relationship between Lipaphis erysimi Kalt. (Homoptera Aphididae) and Coccinella septempunctata Linn. (Coleoptera: Coccinellidae): III. Effect of host plants on the searching strategy, mutual interference and killing power of the predator. Biol Agri Hortic 17(1):11–17. https://doi.org/10.1080/01448765.1999.9754820
Singh G, Singh NP, Singh R (2014) Food plants of a major agricultural pest Aphis gossypii Glover (Homoptera: Aphididae) from India: An Updated Checklist. Int J Life Sci Biotech Pharma Res 3:1–26
Sobhani M, Madadi H, Gharali B (2013) Host plant effect on functional response and consumption rate of Episyrphus balteatus (Diptera: Syrphidae. feeding on different densities of Aphis gossypii (Hemiptera: Aphididae). J Crop Protect 2:375–385
Trexlar JC, McCulloch CE, Travis J (1988) How can the functional response best be determined? Oecologia 76:206–214
Uiterwaal SF, de Long JP (2018) Multiple factors, including arena size, shape the functional responses of ladybird beetles. J Appl Ecol 55:2429–2438. https://doi.org/10.1111/1365-2664.13159
Watt KEF (1959) A mathematical model for the effect of densities of attacked and attacking species on the number attacked. Can Ent 91:129–144
Acknowledgements
Authors thank Dr. Agatha Betsy for language improvement, the two anonymous reviewers for their comments and suggestions, and Science and Engineering Research Board, Department of Science and Technology, Govt. of India, New Delhi for financial assistance (Project No. EMR/2016/006296).
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Dr. Ahmad Pervez is the Principal Investigator of a major project funded by the Science and Engineering Research Board, Ministry of Science and Technology, Govt. of India (EMR/2016/006296).
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AP has planned the outline of this research and designed the methodology, drafted the major part of the manuscript, figures and tables. RK and SC assisted in maintaining laboratory culture and performing experiments. All the authors read and approved the final manuscript.
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Pervez, A., Kumar, R. & Chandra, S. Cumulative functional responses of larvae and adults of two aphidophagous ladybirds. Int J Trop Insect Sci 42, 1569–1577 (2022). https://doi.org/10.1007/s42690-021-00678-2
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DOI: https://doi.org/10.1007/s42690-021-00678-2