Comparative Functional and Numeric Response of Two Coccinellids (Coccinella septempunctata and Cheilomenes sexmaculata) Preying Cowpea Aphid (Aphis craccivora)

 

The cowpea aphid, Aphis craccivora Koch (Hemiptera: Aphididae), a plant lice known to commonly attack plants from bean family (Minks and Harrewijn, 1989; Sadeghi et al., 2009). It is one of the important pestiferous hemipteran insect that causes loss by sucking sap from phloem (Chhangani et al., 2021). They also act a vector for many viral diseases via faba bean necrotic yellow virus, broad bean yellow mosaic virus and bean leaf roll virus (Weigand and Bishara, 1991). The fungus developed on aphids’ honeydew secretion also hinders the photosynthesis process, resulting in severe damage to the plant (Klingler et al., 2001, Smith and Boyko, 2007). The parthenogenetic development coupled with high fecundity and short generation resulted in increased biotic potential of the pest (Klingler et al., 2001), which makes it important to control the enormous population damaging the crop. The fortunate increased awareness towards environmental and human health hazards from chemicals has prevailed upon biological control of the insect pests.
       
The common predaceous coleopteran coccinellids are most efficient aphidophagous predators for the biological control of the aphids. In nature, they play a maleficent role in controlling the prolific aphid population. They are the most successful and pioneer agent of the biological control with use of Australian ladybird beetle Rhodolia cardinalis in California in 1888 against scale insect, devastating Californian citrus industry (Dixon, 2000). Both grubs and adults voraciously feed primarily on aphids and other soft bodied insects, which in turn makes them important key in suppressing the aphid population in field. From India, 57 genera comprising of 261 species of predaceous coccinellids have been catalogued (Omkar and Pervez, 2004); out of which 12 genera of aphidophagous coccinellids have been reported from Southern Rajasthan (Jat, 2008). Coccinella septempunctata Linnaeus and Cheilomenes sexmaculata Fabricius were the relatively more dominant in the different cropping patterns in Udaipur region of Southern Rajasthan (Swaminathan et al., 2016).
       
Bio- ecological studies are pre-requisite for maximum and efficient utilisation of the aphidophagous beetle in the arena of biological control. Predatory potential is the basic factor regulating population dynamics of predator-prey system. Function response curve helps to workout basic mechanism governing their interaction and thus enhance biological control strategies. To emphasis the predator effects into action threshold, it requires the estimation of functional response for predator species. Functional response is estimated by establishing the linear regression relationship between the number of prey consumed per predator and the prey densities (Solomon, 1949). Handling time and attack rate, which infers the foraging efficiency are the key parameters for describing the response curve (Hassell, 1978). The fundamental aspect of the study is to further evaluate and compare the predatory traits of Coccinella septempunctata Linnaeus and Cheilomenes sexmaculata Fabricius under insitu condition through assessment of: (i) Functional response of the coccinellids to increasing prey densities (ii) Numeric response of the coccinellids to prey densities.

Rearing of Coccinella septempunctata Linnaeus and Cheilomenes sexmaculata Fabricius 
 
The nucleus culture of the aphidophagous coccinellids was maintained under laboratory conditions at Rajasthan College of Agriculture, MPUAT, Udaipur, Rajasthan for the experiment. The field collected adult predators were brought to the laboratory to maintain a stock culture under ambient conditions of temperature and humidity (25±2^oC, 70±5%).
       
The mating pairs were kept in glass jars (500ml capacity) covered with muslin cloth and fastened with rubber bands. The predators were reared on leaves of cowpea infested with aphids. The eggs laid on cowpea leaves (20) were transferred onto fresh leaves in separate glass jars till the first instar grubs emerge, which were then be provisioned cowpea aphids as food daily. The leaves were changed every two days to maintain succulence for aphid growth. The cowpea pea plants were sown in small pots and were placed in aluminium insect cages having 15 cm × 15 cm × 15 cm size.
 
Experimental conditions
 
The predatory potential of coccinellid grubs and adults were evaluated at six different prey densities (aphids per arena): 25, 50, 75, 100, 125, 150 and 200 with 5 replications. Healthy second instar grubs were separated with the help of a camel hair brush after the first moult and transferred on to tender cowpea plants grown in small pots kept under caged condition individually. To evaluate the predation potential, adult coccinellid beetles, were starved for 6h and individually transferred to the pot plants with known numbers of aphid prey at different aphid prey densities. Observations on the consumption of aphids were recorded in each replicate under the different treatments after 24 h. The experiment continued for one week; wherever required, aphids will be replenished. The functional response at different prey densities computed using the linear interpretation of Holling’s Equation (Holling, 1959) for the grubs and adult coccinellid beetles; likewise, the numerical response was analyzed for the adult coccinellids by observing the fecundity at different prey densities.
 
Data analyses
 
The proportion of prey killed at different densities were plotted to evaluate the type of response curve using logistic regression (by SAS software). As Type I and Type II responses are difficult to distinguish as articulated by most of the researchers (Trexler et al., 1988); makes it necessary to determine the functional curve by considering the proportion of prey eaten (N_a/N_o) as a function of prey offered (N_o) (Juliano 2001). Once the functional curve were plotted, coefficients for Type II response were calculated using the linear interpretation of Holling’s Equation (Holling, 1959):
   
Where,
H = Number of prey consumed.
Ha= Average prey killed.
a= Attack rate.
T= Exposure time for predation and
T_h= Handling time associated with each prey consumed.
 
After using the above Hollings equation for Type II response, it was subject to linear regression to work out the intercept and slope to estimate time for prey handling and area examined by the predator.
   
Numeric response was also observed at different prey densities 25, 50, 75, 100, 125, 150 and 200 with 5 replications in a completely randomised design. The equation suggested by Omkar and Pervez (2004) was used to determine the conversion efficiency of prey consumption (ECI) into biomass (egg) at different densities.

Functional response of C. septempunctata and Ch. sexmaculata with respect to their prey,  A. craccivora
 
During our study the prey consumption varied with prey densities. The prey consumption by grubs of C. septempunctata ranged from 23.71 to 85.17 cowpea aphid (Table 1); whereas, grubs of Ch. sexmaculata consumed an average of 20.8 to 71.94 aphids (Table 3). The consumption by adult C. septempunctata ranged from 23.02 to 87.82 (Table 2); whereas, for adult Ch. sexmaculata it ranged from 20.6 to 71.28 aphids (Table 4). In all the cases the maximum predation was observed at prey density of 150 cowpea aphids per experimental arena. From the observations presented in Tables (1) to (4), it can be inferred that in general cowpea aphid consumption increased with increasing prey densities up to the density of 150 aphids, but the mean consumption, expressed as a per cent value, showed a decreasing rate of increase.
 

 

 

 

       
The linear regression trend line showed an intercept of 32.15 with a slope of 0.030 for the adult, while an intercept of 30.54 with a slope of 0.032 for the grubs of C. septempunctata (Fig 1 and 3). Similarly, an increasing rate of feeding at decreasing rate was observed for grubs and adults of C. septempunctata (Fig 2 and 4). In case of Ch. sexmaculata, for the adults the intercept was 35.54 with a slope of 0.034 and for the grubs the intercept was 35.19 having a slope of 0.034 (Fig 5 and 7). The graphs between feeding propensity and prey density for grubs and adults of Ch. sexmaculata also showed an increasing trend with prey density (Fig 6 and 8).
 

 

 

 

 

 

 

 

       
The intercept and slope values were used to calculate the handling time for predation and area of predation corresponding to it. The handling time ranged from 5.04 h to 5.71 h, calculated by linear regression method. Adults of C. septempunctata required minimum time to act upon their prey (5.04 h) searching an area of 6.99 sq. m.; while, the grubs needed 5.3 h to search an area of 7.36 sq m. The adults and grubs of Ch. sexmaculata required somewhat similar time (5.71 h) to search an arena of 6.33 and 6.39 sq m area respectively; however, the time required for consumption happened to be relatively more for Ch. sexmaculata in comparison to that for C. septempunctata.
       
Our results with regard to the predator-prey relationship of the adults and grubs of both the coccinellids: C. septempunctata and Ch. sexmaculata, showed an increasing prey consumption rate by the respective predators reaching a level of satiation at a prey density of 150 aphids per day, where the rising graph levelled between the prey density provided and the mean prey consumed. This typically showed the Type II functional response of predator-prey relationship as explained by Holling (1959).   
       
Omkar and Pervez (2004) observed that prey consumption per predator significantly decreased with an increase in a constant prey density in case of a ladybeetle, Propylea dissecta. The decrease in prey consumption per predator was curvilinear when fitted with predator density. Type II functional responses are evidenced by an initial decrease in the proportion of prey eaten with increasing prey offered (Trexler et al., 1988 and Juliano, 1993). Although three types of functional responses described by Holling (1959) may occur in coccinellids (Hodek and Honek, 1996), but it is evident that Type II response is a more common predatory response reported for many coccinellids, such as Cheilelomenes vicina Mulsant (Ofuya, 1988), Scymnus hoffmanni (Ding-Xin, 1986), C. septempunctata (Kumar et al., 2001), S. levaillanti Mulsant (Uygum and Athhan  2000), S. creperus Mulsant (Wells et al., 2001), Harmonia axyridis (Lee and Kang 2004), P. dissecta (Omkar and Pervez, 2004; Pervez and Omkar,  2005), C. sexmaculata, C. transversalis (Pervez and Omkar, 2005) and Hippodamia variegata (Goeze) (Farhadi et al., 2010).
 
Numerical response of C. septempunctata and Ch. sexmaculata on cowpea aphids
 
The numerical response in terms of conversion efficiency was observed to be more in case of C. septempunctata (71. 5% to 94.4%) as compared to that for Ch. sexmaculata (69% to 92.8%). The fecundity in both the cases increased with the increased prey densities that eventually decreased after reaching the maximum egg laying capacity at prey density of 125 aphids (Table 5).
 

       
Hodek and Honek (1996) observed a decreased ECI at higher prey densities with a possible suggestion that well-fed females laid large number of eggs, besides investing much in maintenance and metabolic costs. Previous studies explain the efficient fitness of the predator exposed to high prey densities in terms of growth. Besides prey density, other factors such as temporary prey isolation (Evans and Dixon, 1986) and body size (Agarwala and Yasuda, 2000) also influence egg production.

The authors sincerely thank the Head, Department of Entomology, Dean, Rajasthan College of Agriculture and Director Research, MPUAT, Udaipur for providing the necessary facilities to conduct the research. I am very thankful to, Dr. Latika Sharma, Asstt. Professor, Department of Economics for help in statistical analysis and hereby acknowledge the IASRI for NIAP-ICAR project on Statistical Analysis Software SAS for National Agriculture Research System.