- Open Access
Demographic parameters of the predaceous ladybird, Hippodamia variegata (Goeze), on the aphid species, Aphis craccivora (Koch), reared on four host plants
© The Author(s) 2018
- Received: 2 June 2018
- Accepted: 31 October 2018
- Published: 23 November 2018
The reproductive and demographic attributes of the aphidophagous ladybird, Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae), when fed on the aphid species, Aphis craccivora (Koch), reared on four host plants, viz. Dolichos lablab L., Vigna unguiculata L. Walp, Cajanus cajan (L.) Millsp., and Ranunculus sceleratus L., were investigated in the laboratory to find host suitability for the production of the ladybird. Results indicated that there was a significant effect of host plant on both reproductive and demographic parameters of the predator. The host plant suitability was in the rank order D. lablab = V. unguiculata > C. cajan > R. sceleratus. This ladybird started reproducing very early and laid a high number of eggs for a longer period of time when the adults were fed on aphids raised on D. lablab and V. unguiculata. Both the fecundity and percent egg hatching increased significantly in the case of the abovementioned two host plants. Similar host plant effects were found on demographic parameters of H. variegata, with significantly high values of net reproductive rate (rm), short generation (Tc), and doubling times (D.T.) on D. lablab and V. unguiculata. Age-specific fecundity of H. variegata at all host plant treatments was triangular in function with an initial increase in ovipositional rate with age, followed by attainment of peak and gradual decline till egg laying ceases. These peaks were higher on the host plant treatments, D. lablab and V. unguiculata. Sub-optimal values of both reproductive and demographic parameters were found on the host plant, R. sceleratus. Thus, it could be concluded that both D. lablab and V. unguiculata were the suitable host plants to raise aphid, A. craccivora, for the augmentative rearing of the ladybird, H. variegata.
- Hippodamia variegata
- Aphis craccivora
- Demographic analysis
- Prey suitability
- Host plants
Predaceous coccinellids, popularly known as ladybirds (Coleoptera: Coccinellidae), are important biocontrol agents of numerous crop pests, viz. aphids, mealybugs, whiteflies, thrips, and other tiny soft-bodied insects (Dixon 2000 and Hodek et al. 2012). Their augmentative rearing in the laboratory depends largely on the prey food and the abiotic factors (Omkar and Pervez 2016). Hodek and Evans (2012) expanded the classical idea of food relationship in ladybirds in terms of essential food (that supports both development and reproduction), alternative food (that supports only survival), and rejected food (that is toxic and unpalatable). The degree of essential prey food varies among aphidophagous ladybirds, as they develop and reproduce optimally, when fed on certain aphids, viz. Aphis craccivora (Koch) and Aphis gossypii (Glover) (Pervez and Omkar 2004 and Omkar and Mishra 2005), whereas their development and reproduction are negatively affected, when fed on aphids containing toxic biochemical constituents. Among aphids, A. craccivora is one of the major crop pests infesting over 400 host plants, and the grain legumes are the major target crops (Blackman and Eastop 2000). A. craccivora is a major pest of Indian bean, [Lablab purpureus (L.) Sweet = Dolichos lablab L.], cowpea, Vigna unguiculata L. Walp (Karungi et al. 2000), and pigeon pea [Cajanus cajan (L.) Millsp.]. It also infests poison buttercup, Ranunculus sceleratus L. (Pervez and Kumar 2017).
Hippodamia variegata (Goeze) is a cosmopolitan, eurytopic, predaceous ladybird beetle with Palaearctic origin (Franzmann 2002 and Omkar and Pervez 2004) occurring abundantly in aphid prevalent hilly agro-ecosystems of North India. It is a polymorphic ladybird with an immense biocontrol potential (Honek et al. 2012). For the mass multiplication of this ladybird, a thorough understanding of its reproductive and demographic parameters is a prerequisite. These aspects have been investigated, using aphid prey cultured on only one host plant (Lanzoni et al. 2004; Farhadi et al. 2011 and Jafari 2011).
Aphid–host plant association also affects the prey suitability (Francis et al. 2000, 2004 and Pervez and Chandra 2018), as aphids reared on different host plants seem to bear different effects on the bio-attributes of H. variegata (Wu et al. 2010). Moghaddam et al. (2016) studied age-stage, two-sex life table of H. variegata feeding on the English grain aphid, Sitobion avenae (Fabricius), reared on four host plants. Rakhshan and Ahmad (2013) observed that A. craccivora reared on different host plants had significant effects on growth and development of predaceous ladybirds. In addition, consumption of A. craccivora was also varied when the ladybird was fed on prey raised from different host plants (Rakhshan and Ahmad 2015). The presence of allelochemicals and the morphology of different plants also affect the biocontrol potential of ladybirds.
Thus, the present study was designed to determine the demographic attributes of H. variegata on A. craccivora infesting four host plants, viz. D. lablab, V. unguiculata, C. cajan, and R. sceleratus, in the laboratory to determine host suitability for the mass multiplication of the ladybird.
Collecting and rearing of H. variegata and aphid species
Adults of H. variegata were collected from the suburbs of a hilly region of Uttarakhand, India (30.2937° N, 79.5603° E), and brought to the laboratory. These were sexed and paired in Petri dishes (2.0 cm height × 9.0 cm diameter) in four sets (each containing 10 replicates for each host plant and each Petri dish had a pair of H. variegata) provided daily with a sufficient quantity of A. craccivora infested on (i) D. lablab, (ii) V. unguiculata, (iii) C. cajan, and (iv) R. sceleratus. The host plants were inoculated with the aphid, A. craccivora, and grown in a small crop-field, present in the college campus, Kashipur, India. The Petri dishes were kept in the Environmental Test Chamber (REMI Instruments, India), maintained at controlled abiotic conditions of 25 ± 1 °C, 65 ± 5% R.H, and 12L:12D. A preliminary experiment revealed that H. variegata reproduced best at 12L:12D photoperiod. Similarly, 27 °C was found to be the best temperature for laboratory rearing of the ladybird understudy (Maia et al. 2014). The F1 eggs laid by the female ladybirds in each Petri dish were isolated in other dishes (size as above) to be used in the experiments.
Reproduction and demographic analysis
The F1 eggs taken from the above stock were reared from egg-hatch to adult-emergence, using A. craccivora as prey obtained from the respective host plants (which were provided to the parents). The developmental duration and the number of adults that survived in each aphid–host plant combination were recorded (n = 10). After emergence, the adults were sexed and isolated in Petri dishes (space and diet as above). The adult male and female ladybirds were paired together in four sets and provided daily with a sufficient quantity of A. craccivora infested on (i) D. lablab, (ii) V. unguiculata, (iii) C. cajan, and (iv) R. sceleratus and observed daily for mating and oviposition for their lifetime until the death of female ladybird (n = 10). The data on pre-oviposition and oviposition periods, fecundity, and percent egg viability were recorded. The data for normality, using the Kolmogorov–Smirnoff test, and homogeneity of variance, using Bartlett’s test via statistical software, SAS version 9.0, were tested, as well were the data of pre-oviposition and oviposition periods, daily oviposition, fecundity, and percent egg viability of H. variegata, when fed on A. craccivora raised on four host plants, to one-way ANOVA, using SAS, version 9.0. The age-specific fecundity of H. variegata was plotted by subjecting the data on mean reproductive age (i.e., mean values of ovipositional period) and daily oviposition to polynomial regression analysis using SAS, 9.0 (2002).
The demographic parameters, viz. net reproductive rate (Ro), intrinsic (rm) and finite (λ) rates of increase, generation (Tc), and doubling times (D.T.) were estimated, using the jackknife method given by Maia et al. (2000, 2014) on SAS, 9.0 (2002). This method evaluates the pseudo-values of the demographic parameters, which helped to obtain their mean values and standard errors in each group. The box and whisker plots to illustrate the dispersion of pseudo-values within each group were constructed. This is directly related to the uncertainty of their estimates.
Reproductive parameters of H. variegata when fed on aphid, A. craccivora, infested on four host plants
Pre-oviposition period (days ± S.E.)
Oviposition period (days ± S.E.)
Fecundity (eggs per female ± S.E.)
Egg viability (%)
3.50 ± 0.22c (3–5)
45.70 ± 1.86a (35–54)
915.50 ± 23.16a (821–1064)
94.73 ± 0.55a (91.45–97.25)
3.40 ± 0.22c (3–5)
42.20 ± 1.50ab (39–50)
923.50 ± 22.57a (800–1062)
94.32 ± 0.77a (88.51–96.25)
4.80 ± 0.29b (3–6)
39.00 ± 1.90b (30–49)
755.80 ± 22.42b (643–846)
83.54 ± 1.67b (75.62–91.13)
8.40 ± 0.31a (7–10)
25.20 ± 1.53c (18–32)
337.30 ± 16.66c (229–440)
71.97 ± 1.86c (64.03–79.48)
Ovipositional period was significantly (F = 165.50; P < 0.0001; df = 3, 36) prolonged, when H. variegata was provided by the aphid infested on D. lablab and V. unguiculata, and shortened in the case of R. sceleratus. Lanzoni et al. (2004) found a shorter ovipositional period of 32.2 ± 3.2 days, while Jafari (2011) reported 43 ± 0.21 days. This period ranged from 24.37 ± 0.28 to 36.68 ± 0.19 days, when H. variegata was fed on S. avenae, infesting four host plants (Moghaddam et al. 2016). The ovipositional period extended to 45.70 ± 1.86 days, when the predator was fed on aphids reared on D. lablab, which was much longer than those periods reported earlier. Seemingly, nutrients from these host plants support oviposition for a longer time.
The fecundity of H. variegata was significantly (F = 66.42; P < 0.0001; df = 3, 36) higher when the host plants were V. unguiculata (923.50 ± 22.57 eggs) and D. lablab (915.50 ± 23.16 eggs), while it was minimal on R. sceleratus (337.30 ± 16.66 eggs). Previous studies recorded a fecundity ranging from 362.47 to 587.31 eggs on S. avenae (Moghaddam et al. 2016) and 599.29 to 667.12 eggs on A. gossypii (Wu et al. 2010), reared on multiple hosts. Comparing the fecundities, A. craccivora infesting V. unguiculata or D. lablab was recommended for the augmentative growth of the predator. Obtained data are in close agreement with the other reports on fecundity, i.e., 841.7 eggs on M. persicae (Lanzoni et al. 2004) and 943.90 eggs on A. fabae (Jafari 2011). Ladybirds fed on high-quality aphid diets had more ovarioles than those raised on inferior diets (Hodek et al. 2012). Egg viability in H. variegata was significantly (F = 27.54; P < 0.0001; df 3, 36) higher when the aphid was reared on D. lablab (94.73%) and V. unguiculata (94.32%) and lower in the case of R. sceleratus. The egg viability ranged from 72.11 to 86.5% on A. gossypii (Lanzoni et al. 2004).
Demographic attributes of H. variegata when fed on aphid, A. craccivora, infested on four host plants
457.93 ± 11.59a (431.72–484.15)
0.18 ± 0.0031a (0.1771–.1910)
1.20 ± 0.0037a (1.1938–1.2105)
33.27 ± 0.5259b (32.081–34.461)
3.76 ± 0.06c (3.6216–3.9060)
450.21 ± 11.00a (425.31–475.09)
0.19 ± 0.0035a (0.1778–.1937)
1.20 ± 0.0042a (1.1945–1.2136)
32.87 ± 0.7058b (31.288–34.482)
3.72 ± 0.07c (3.572–3.8895)
261.20 ± 7.75b (243.68–278.73)
0.15 ± 0.0031a (0.1469–.1538)
1.16 ± 0.0018a (1.1583–1.1663)
37.00 ± 0.4450a (35.997–38.011)
4.60 ± 0.05a (4.5041–4.7128)
82.16 ± 4.06c (72.99–91.35)
0.16 ± 0.0036a (0.1491–.1654)
1.17 ± 0.0042a (1.1607–1.1798)
28.00 ± 0.7849c (26.256–29.807)
4.40 ± 0.10b (4.1791–4.6333)
It could be concluded that A. craccivora infesting D. lablab and V. unguiculata could be used as the best option for mass multiplication of H. variegata. In addition, its augmentative releases as a biocontrol agent against A. craccivora, infesting the plants above, are recommended as it can easily multiply faster than on other hosts.
The authors are thankful to Dr. Barbara Castleton, ESL Instructor, South Seattle College, Seattle, WA, USA, for improving the language of the manuscript. AP thanks SERB, Department of Science and Technology, New Delhi, for financial assistance (EMR/2016/006296).
Present study has been funded by Science and Engineering Research Board, Department of Science and Technology, Government of India, in the form of Major Research Project (EMR/2016/006296). AP is Project Investigator in the said project.
Availability of data and materials
Not applicable. Authors’ cannot submit the raw data as they will further be used to developing suitable rearing techniques.
AP has planned the outline of this research and designed the methodology. He drafted the manuscript and did certain portion of statistical analysis. PA assisted in maintaining the laboratory culture and performing the experiments. HB helped in further drafting the manuscript and performing certain statistical analysis. All the authors read and approved the final manuscript.
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