Predatory Potential of Coccinella septempunctata L. against Four Aphid Species

Muhammad Arshad1*, Hafiz Azhar Ali Khan2*, Faisal Hafeez3, Ravaid Sherazi1 and Naeem Iqbal4

1Department of Entomology, University of Agriculture, Faisalabad, Pakistan

2Institute of Agricultural Sciences, University of the Punjab, Lahore, Pakistan

3Entomological Research Institute, Ayub Agricultural Research Institute, Faisalabad, Pakistan

4Department of Plant Protection, Faculty of Agricultural Sciences, Ghazi University, Dera Ghazi Khan, Pakistan

ABSTRACT

The relationship between a coccinellid beetle (Coccinella septempunctata L.) and four different aphid species (spinach aphid, Aphis fabae Scopoli; coriander aphid, Hyadaphis coriandri (Das); cabbage aphid, Brevicoryne brassicae L.; pea aphid, Acyrthosiphon pisum Harris) was evaluated in the laboratory in no choice and free choice feeding assays. In the no choice feeding assay, the stages of beetle (adults, 3rd and 4th instar) consumed more aphids than early stages (1st and 2nd instar). In the free choice feeding assay, the consumption of pea aphid (77.647) was statistically high followed by spinach (66.276), coriander (66.14) and cabbage (61.48) aphids. Manly’s preference index suggest that pea aphid was the most preferred (by all stages of C. septempunctata) aphid species followed by coriander, and the cabbage aphid was the least preferred species. The results of the present study revealed predatory potential of C. septempunctata against different aphid species under the laboratory conditions. The results could be helpful in designing biological management strategies for aphids.

Article Information

Received 01 March 2016

Revised 13 May 2016

Accepted 30 July 2016

Available online 28 March 2017

Authors’ Contributions

MA and FH conceived and designed the study. RS and NI performed the experiments and collected raw data. MA, FH and HAAK analyzed the data, and wrote the articles.

Key words

Feeding potential, Biological control, Vegetable aphid, Ladybird beetle, Predator-prey relationship, IPM.

DOI: http://dx.doi.org/10.17582/journal.pjz/2017.49.2.623.627

* Corresponding author: [email protected];

[email protected]

0030-9923/2017/0002-0623 $ 9.00/0

Copyright 2017 Zoological Society of Pakistan

INTRODUCTION

Vegetables are herbaceous plants, comprised chiefly of mineral contents, carbohydrates and vitamins (Robinson, 1990). The vegetables like cabbage, pea and spinach are not only sources of energy for body building and maintenance but also curative and repair the body. In Pakistan, vegetables are always grown at huge risk because these mainly attacked/damaged by sucking and chewing insect pests. Sucking insect pests play a substantial part as yield declining agent. Out of all insect species, aphids are considered as notorious pest of different vegetables (Aheer et al., 2008; Minks and Harewijn, 1987; Ahmad et al., 2016). Aphids insert their proboscis into phloem vessel and suck the cell sap from different parts of the plants. Resultantly, the affected leaves turn pale yellow and start to wilt. Aphids also secrete honey dew due to which sooty mold appear on the leaves (Kindler et al., 1995).

Different chemicals are available for the control of aphids (Messelink et al., 2013) but these chemicals have negative effects on the environment (Khan et al., 2015, 2016). Therefore, there is a need to explore alternate measures for the management of aphids. Bio-control agents like spiders, syrphids and coccinellid species are commonly present in the environment. These agents have been reported as potential candidates for the management of aphids (Singh et al., 2001).

Coccinellid beetle, Coccinella septempunctata L., (Coccinellidae: Coleoptera) is a multicultural having extensive dispersal power with the ability to predate aphids and many soft bodied insects of valuable vegetables (Ali and Rizvi, 2009). In the same preview, C. septempunctata consumed more aphids (Soni et al., 2004) than Brumoides suturalis, Cheilomenes sexmaculata, Menochilus sexmaculatus. Both young ones (grubs) and adults of C. septempunctata consume about 40-173 aphids daily (Akram et al., 1996; Suhail et al., 1999). There are some Coccinellid beetles that have preference only to consume certain aphid species but others attack many species because of their capacity to survive (Habeck et al., 1990). Biological control agents (Coccinellids) consist of an important constituent of many incorporated pest management programs but many synthetic pesticides affect them negatively (Moddue and Blackwell, 1993). To avoid such harmful effects, there is a need to use the natural enemies. The present studies were therefore conducted to determine the predatory potential of C. septempunctata against spinach, coriander, cabbage and pea aphids under the laboratory conditions.

MATERIALS AND METHODS

Insects

The C. septempunctata adults were collected from vegetable fields (University of Agriculture, Faisalabad and Ayub Agricultural Research Area) and placed in plastic cups and vials under controlled conditions in the Insect Biodiversity and Biosystematic laboratory, Department of Entomology, University of Agriculture, Faisalabad. The mates were placed in separate cups with mouth of the cups covered with muslin cloth. Eggs were placed in petri dishes and maintained in the laboratory conditions set at 25±2°C and 62±5% relative humidity. Four aphid species, Aphis fabae Scopoli, Hyadaphis coriandri (Das), Brevicoryne brassicae L. and Acyrthosiphon pisum Harris were collected from spinach, coriander, cabbage and pea, respectively, and identified using an online database for aphids taxonomic identification (http://aphid.aphidnet.org/).

No choice assay

Newly hatched grubs of C. septempunctata were placed singly in separate cup with a Whatmann-No 1 filter paper. Counted numbers of aphids (200 nymphs of 3rd / 4th instar) of each species were provided in each cup daily. Predatory potential was calculated by counting left over aphids in the cups. The grubs were also checked daily for their moulting. Similarly duration of 2nd, 3rd and 4th instars were noted by observing the sheded skin of the beetle grubs. This practice continued till pupation. The same was continued for adults. Average consumption rate was calculated by formula (aphid consumed/aphid offered × 100).

Free choice assay

Four aphid species were offered to each life stage (such as 1st, 2nd, 3rd, 4th instar and adult) of C. septempunctata. The experiment was carried out using free choice feeding tests. During this test, a single instar/stage of C. septempunctata were released separately into plastic jars (10 × 05 inch) lined with muslin cloth (for aeration), and maintained under the laboratory conditions set at 25 ± 2˚C and 62±5 % relative humidity. A mixture of 300 nymphs of each aphid species (spinach, coriander, cabbage and pea) was introduced in each jar and fresh leaves of each vegetable were provided for aphids. Daily consumption was calculated by subtracting the number of aphids left from number of individuals brushed in the jar. The numbers of aphids consumed were counted after every 24 h till the end of each instar/stage of C. septempunctata.

Statistical analysis

The normality of data was checked by applying Kolmogorov-Smirnov test before statistical analysis. The difference in predatory potential of C. septempunctata (four instars of grubs and one adult stage) was compared by using two-way analysis of variance (ANOVA) with the help of computer based software “Statistix v8.1” (Analytical Software, 2005), and a least significant difference test (α = 0.05) was employed to separate the means (Khan et al., 2012). A paired t-test was applied to compare the predatory potential of every stage of C. septempunctata against different aphid species. The preference of different aphid species was estimated by calculating the Manly’s Preference Index (αP) in free choice assay (Manly et al., 1972).

Where; np and rp were the initial numbers of different aphid species (i.e., 200), rp and ru were the consumed after 24 h duration, respectively. The preference of C. septempunctata (four instars of grubs and one adult stage) were calculated separately. This index gives the value from 0 to 1, where 0.5 indicates no preference. However, we tested our null hypothesis of no preference for a specific aphid species by a t-test.

RESULTS

The results indicated that consumption rate (during no choice assay) of different instars and adults C. septempunctata on different aphid species (spinach, coriander, cabbage and pea) is almost similar with each other (Fig. 1). However, 1st, 2nd and 3rd instar grub took three days to complete its stage and shifted to the next one, whereas 4th instar and adults took two and five days respectively. Feeding/consumption was increased with the age of test insect. In addition to this, consumption of 1st instar grub was similar to in all aphid species. In case of 2nd instar, the consumption was almost equal for first two day but considerably different on the last day i.e. spinach, cabbage, coriander and pea (19.4, 19.8, 24.4 and 27.4, respectively). This feeding / consumption of pea aphid preference continued to the 3rd and 4th instar. The pupal stage arrived and lasts for four days. In the continuation of adult life span, consumption was increased rapidly with spinach and coriander aphid but gradually for cabbage and pea. The feeding pace of adults on coriander aphid was maximum (100.8, 116.2, 148, 152.8 and 160.2) followed by spinach and pea aphids (on 12th to 16th day, respectively), whereas cabbage aphid was consumed less in number during all five days, respectively (Fig. 1).

In the choice feeding tests, higher consumption of aphid was observed at each successive instar. However, the consumption of pea aphid was statistically higher in 1st (3.46), 2nd (6.46), 3rd (12.90), 4th (24.13) and adults (30.68) of C. septempunctata followed by spinach, coriander and pea (Table I).

Table I.- Consumption of aphid species by different life stages of C. septempunctata under free choice bioassay.

When 3rd instar aphid species (i.e. spinach vs. coriander, spinach vs. cabbage, spinach vs. pea, coriander vs. cabbage, coriander vs. pea, cabbage vs. pea) were offered to different life stages (first, second, third, and fourth instar, and adult) of C. septempunctata simultaneously, the beetle consumed all aphid species but preferred pea, coriander and spinach respectively (Fig. 2). Index values > 0.5 represents preference for aphid species (written after vs. in Figure 2; positive switching), while those < 0.5 represent non preference for aphid species (written before “vs.” in Figure 2; negative switching). The first instar grub of C. septempunctata showed marked preference of pea aphid over spinach (t=-2.89, df=4, P= 0.05), coriander (t=-5.25, df=4, P=0.03) and cabbage (t=-4.25, df=4, P=0.05). Likewise second instar grub also showed significantly higher preference for coriander aphid over spinach and cabbage (t=3.61, df=4, P=0.05; t=3.52, df=4, P=0.05, respectively), and pea over cabbage (t=-3.25, df=4, P=0.05). When the third instar grub was compared for predation potential for various aphids species, pea aphid was consumed significantly greater over (t=-5.9, df=4, P=0.01). In case of fourth instar grub, pea aphid was consumed greater over spinach, coriander and cabbage whereas spinach and cabbage aphid were preferred over coriander. However, adults of C. septempunctata under comparison of predation potential showed that spinach aphid was greatly preferred over cabbage and pea, whereas coriander preferred over cabbage and pea, and pea preferred over cabbage.

DISCUSSION

Ecosystem is made up of living and non-living environment. However, non-living environment i.e. ecology directly derive population fluctuations and energy flow by means of different food webs. In the same way, predators pose direct impact on prey population by consumption (Peckarsky et al., 2008; Arshad et al., 2015). Feeding of insects has some economical worth, so it is vital to identify the number of prey killed while determining the effects of predators in fluctuation of prey (Messina and Sorenson, 2001).

Our results suggest that C. septempunctata has great potential against aphids. Moreover, different stages also had significant effect on consumption rate. Our findings are partial agreement with scientists working sub-tropical regions (Sharma and Joshi, 2010; Singh and Singh, 2013) who found that C. septempunctata showed more preference to Lipaphis erysimi (under no choice assay). A steady increase in consumption/predation was observed with successive developmental stages. This difference in predation might be due to recognition of most suitable prey by its respective morphological (Dixon, 2000), physiological and chemical variations (Omkar et al., 2004). The phenomenon by which predators seek, locate and / recognize their suitable/ palatable prey is still unknown. This line of research is wide open and required to resolve complications in recognition and discrimination of prey. The results of Singh and Singh (2013) are in conformity with ours that voracity of C. septempunctata increased with the age and predate all stages (Jindal and Malik, 2006; Bilashini and Singh, 2009). In our experiments, adults consume more aphids than grubs, such investigations are in consonance with judgment of (Singh et al., 1994; Ali and Rizvi, 2007, 2009). In addition to this, the above findings yielded the following order preference: pea aphid > coriander aphid > spinach aphid > cabbage whereas Bilashini et al. (2007) while working in India, yielded this order Lipaphis erysimi > M. persicae > B. brassicae.

CONCLUSIONS

It could be concluded from the present findings that different aphid species had a significant effect on the lifelong consumption by C. septempunctata. However, morphological features of prey (aphids) entice a predator (C. septempunctata) that’s why pea aphid was highly preferred under lab conditions in terms of development and predation as compared with the rest of the aphid species (spinach, coriander and cabbage). Hence, it offers comprehensive information to introduce C. septempunctata in biological-based management plans of aphids.

Statement of conflict of interest

Authors have declared no conflict of interest.

REFERENCES

Aheer, G.M., Ali, A. and Ahmed, M., 2008. Abiotic factors effect on population fluctuation of aphids in wheat. J. agric. Res., 46: 367-371.

Ahmad, T., M.W. Hassan, M. Jamil and J. Iqbal, 2016. Population dynamics of aphids (Hemiptera:Aphididae) on wheat varieties (Triticum aestivum L.) as affected by abiotic conditions in Bahawalpur, Pakistan. Pakistan J. Zool., 48:1039-1044.

Akram, W., Akbar, S. and Mehmood, A., 1996. Studies on the biology and predatory efficiency of Coccinella septempunctata L. with special reference to cabbage. Pak. Entomol., 18: 104-106.

Ali, A. and Rizvi, P.Q., 2007. Development and predatory performance of Coccinella septempunctata L. (Coleoptera: Coccinellidae) on different aphid species. J. biol. Sci., 7: 1478-1483. https://doi.org/10.3923/jbs.2007.1478.1483

Ali, A. and Rizvi, P.Q., 2009. Age and stage specific life-table of Coccinella transversalis with regards to various temperatures. Tunisian J. Pl. Protec., 4: 211-219.

Analytical Software, 2005. Statistix version 8.1: User’s manual. Analytical Software.

Arshad, M, Khan, H.A.A., Rehman, M.A, and Saeed, N.A., 2015. Incidence of insect predators and parasitoids on transgenic Bt cotton in comparison to non-Bt cotton varieties. Pakistan J. Zool., 47: 823-829.

Bilashini, Y. and Singh, T.K., 2009. Studies on population dynamics and feeding potential of Coccinella septempunctata Linnaeus in relation to Lipaphis erysimi (Kaltenbach) on cabbage. Indian J. appl. Ent., 23: 99-103.

Bilashini, Y., Singh, T.K. and Singh, R.K.R., 2007. Biological control potential of Coccinella septempunctata Linnaeus (Coleoptera: Coccinellidae) on major homopteran pests of rapeseed. J. biol. Contr., 2: 157-162.

Dixon, A.F.G., 2000. Insect predator prey dynamics, lady bird beetles and biological control. Cambridge University Press.

Habeck, D.H., Bennet, F.D. and Frank, J.H., 1990. Classical biological control in southern United States. Southern Cooperative Series Bulletin No. 355, IFAS Editorial, University of Florida, Gainesville, FC, pp. 197

Jindal, V.K. and Malik, K., 2006. Feeding potential of Coccinella septempunctata Linn. (Coleoptera: Coccinellidae) on mustard aphid, Lipaphis erysimi Kalt and potato peach aphid, Myzus persicae Sulzer. J. entomol. Res., 30: 291-293.

Khan, H.A.A., Syed, A.H., Akram, W., Raza, S. and Ali, M., 2012. Predatory potential of Chrysoperla carnea and Cryptolaemus montrouzieri larvae on stages of the mealybug, Phenacoccus solenopsis: A threat to cotton in South Asia. J. Insect Sci., 12: 1-12. https://doi.org/10.1673/031.012.7801

Khan, H.A.A., Akram, W., Iqbal, J. and Naeem-Ullah, U., 2015. Thiamethoxam resistance in the house fly, Musca domestica L.: current status, resistance selection, cross-resistance potential and possible biochemical mechanisms. PLoS One, 10: e0125850 .https://doi.org/10.1371/journal.pone.0125850

Khan, H.A.A., Akram, W., Khan, T., Haider, M.S., Iqbal, N. and Zubair, M., 2016. Risk assessment, cross-resistance potential, and biochemical mechanism of reistance to emamectin benzoate in a field strain of house fly (Musca domestica Linnaeus). Chemosphere, 151: 133-137. https://doi.org/10.1016/j.chemosphere.2016.02.077

Kindler, S.D., Springer, T.L. and Jensen, K.B.L., 1995. Detection and characterization of the mechanisms of resistance to Russian wheat aphid (Homoptera: Aphididae) in tall wheat grass. J. econ. Ent., 88: 1503-1509. https://doi.org/10.1093/jee/88.5.1503

Manly, B.F.J., Miller, P. and Cook, L.M., 1972. Analysis of a selective predation experiment. Am. Nat., 106: 719-736. https://doi.org/10.1086/282808

Messina, F.J. and Sorenson, S.M., 2001. Effectiveness of lacewing larvae in reducing Russian wheat aphid populations on susceptible and resistant wheat. Biol. Contr., 21: 19-21. https://doi.org/10.1006/bcon.2000.0914

Messelink, G.J., Bloemhard, C.M., Sabelis, M.W. and Janssen, A., 2013. Biological control of aphids in the presence of thrips and their enemies. BioControl, 58: 45-55. https://doi.org/10.1007/s10526-012-9462-2

Minks, A.K. and Harrewijn, P., 1987. Aphids: their biology, natural enemies, and control. Elsevier, Amsterdam, Tokyo, pp. 171-310.

Moddue, A.J. and Blackwell, A., 1993. Azadirachtin: An update. Insect physiol., 39: 903-924.

Omkar, S.K., Pervez, A. and Mishra, G., 2004. Age specific fecundity and natality lifetable of an aphidophagous ladybird, Cheilomenes sexmaculatus. Biol. Mem., 30: 20-25.

Peckarsky, B.L., Abrams, P.A., Bolnick, D.I., Dill, L.M., Grabowski, J.H., Luttbeg, B., Orrock, J.L., Peacor, S.D., Preisser, E.L., Schmitz, O.J. and Trussell, G.C., 2008. Revisiting the classics: considering nonconsumptive effects in textbook examples of predator-prey interactions. Ecology, 89: 2416-2425. https://doi.org/10.1890/07-1131.1

Robinson, D.S., 1990. Food biochemistry and nutritional value. Longman scientific and technical publisher, NewYork, USA.

Sharma, P.K. and Joshi, P.C., 2010. Feeding potential of seven spotted ladybeetle, Coccinella septempunctata (Linnaeus) on mustard aphid, Lipaphis erysimi (Kaltenbach) and cotton aphid, Aphis gossypii (Glover). Nat. Sci., 8: 198-202.

Singh, K. and Singh, N.N., 2013. Preying capacity of different established predators of the aphid Lipaphis erysimi (Kalt.) infesting rapeseed-mustard crop in laboratory conditions. Pl. Protec. Sci., 49: 84-88.

Singh, S.R., Walters, K.F.A. and Port, G.R., 2001. Behaviour of the adult seven spotted ladybird, C. septempunctata (Coleoptera: Coccinellidae), in response to dimethoate residue on bean plants in the laboratory. Bull. entomol. Res., 91: 221-226.

Singh, V.S., Yadav, R.P. and Singh, R., 1994. Post-embryonic development, survival rate and predation potential of Coccinella septempunctata Linn. in relation of mustard aphid (Lipaphis erysimi Kalt.). J. entomol. Res., 18: 5-10.

Soni, R., Deol, G.S. and Brar, K.S., 2004. Feeding potential of coccinellids on mustard aphid, Lipaphis erysimi (Kalt.). Insect Environ., 10: 15-16.

Suhail, A., Sabir, A.M., Hussain, A. and Saeed, A., 1999. Predatory efficacy of Coccinella septempunctata L. on cotton aphids, Aphis gossypii Golv. Pak. J. biol. Sci., 2: 603-605. https://doi.org/10.3923/pjbs.1999.603.605