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Consumption, developmental and reproductive attributes of two con-generic ladybird predators under variable prey supply
Biological Control 74 (2014) 36–44
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Consumption, developmental and reproductive attributes of two con-generic ladybird predators under variable prey supply Mahadev Bista, Omkar ⇑ Ladybird Research Laboratory, Department of Zoology, University of Lucknow, Lucknow 226 007, India
h i g h l i g h t s
g r a p h i c a l a b s t r a c t
Evaluated performance of two
con-generic ladybirds on three prey biomasses. Larvae developed fastest and survived maximum on high prey biomass. Middle aged adults consumed and reproduced maximally on high prey biomass. Females consume prey to increase body biomass at early & late reproductive phases. Females invest more on oviposition during their reproductive phase.
a r t i c l e
i n f o
Article history: Received 16 May 2013 Accepted 1 April 2014 Available online 6 April 2014 Keywords: Ladybird Prey quantity Conversion efficiency Consumption rate Fecundity Egg fertility
a b s t r a c t Availability of aphid prey in habitat is often heterogeneous in space and time and its deprivation causes severe effects on life attributes of ladybird predators. Sometimes ladybirds locate high prey biomass while on certain occasions prey biomass may be either medium/low or altogether absent. Present study has been designed in view of three prey biomass conditions in nature, viz. low, medium and high, selecting Coccinella septempunctata and Coccinella transversalis as experimental ladybirds. Results revealed that consumption, developmental and reproductive attributes of both ladybirds changed in response to prey availability. On high prey biomass larvae had higher consumption and growth rates, developed faster and had low mortality, while emerging adults were large in size, had high consumption rates and utilized prey biomass maximally on production of eggs, self maintenance and survival. In contrast low prey biomass reduced chances of larval survival and emerging adults were small in size, had poor prey consumption rates, low fecundity, egg fertility and short life span. Females exhibited triangular fecundity and egg fertility functions and plateau shaped prey consumption rate function with age, indicating towards their highest reproductive performance during middle age on three prey biomasses; being highest on high prey biomass. On three prey biomasses, females had higher body biomass conversion efficiency during pre- and post-oviposition periods and higher egg biomass conversion efficiency during oviposition period; being highest on high prey biomass. Thus middle aged ladybirds reared on high prey biomass may suppress pest populations better than those reared on low/medium prey biomass. Ó 2014 Elsevier Inc. All rights reserved.
1. Introduction ⇑ Corresponding author. Mobile: +91 9415757747. E-mail address: [email protected] (Omkar). http://dx.doi.org/10.1016/j.biocontrol.2014.04.001 1049-9644/Ó 2014 Elsevier Inc. All rights reserved.
Prey availability is often heterogeneous in space and time and its deprivation causes severe effects on the life attributes of
M. Bista, Omkar / Biological Control 74 (2014) 36–44
ladybirds (Phoofolo et al., 2008; Santos-Cividanes et al., 2011) which forage in unstable habitats with variable prey density (Agarwala et al., 2001). Studies have shown that reduced prey consumption (Phoofolo et al., 2008) and/or prey deprivation severely affect the development and survival of ladybirds (Omkar and Pervez, 2003; Schuder et al., 2004; Atlihan and Guldal, 2009), and the developmental rate and the size of offspring (Agarwala et al., 2001; Seagraves, 2009). Under limited prey conditions the larvae develop slowly and the surviving adults are smaller in size. Further prey deprivation negatively affects the reproductive attributes of ladybirds (Dmitriew and Rowe, 2011). Under prey deprived conditions the pre-reproductive periods of adults are considerably prolonged and their reproductive phase, fecundity (Agarwala et al., 2008, 2009), oviposition rate and clutch size are highly reduced (Dixon, 2000; Ware et al., 2008). It therefore appears that there is a strong selection pressure in the natural populations of ladybird predators for survival, reproduction and offspring performance under limited prey resource. Moreover, the prey abundance/ deprivation not only affect the parents but also have trans-generational effects (Omkar et al., 2010); and the individuals that acquire abundant resource transfer their resources to offspring and enhance offspring fitness (Qvarnström and Price, 2001; Bonduriansky and Head, 2007). There are a few studies that have evaluated the stage and age specific consumption attributes in larval and/or adult stages (Schuder et al., 2004; Mishra et al., 2012), but not much work has been done on the comparative consumption and reproductive attributes of ladybirds under high prey/ low prey biomass conditions. The present study has been aimed to: (i) assess the impact of prey quantity (low, medium and high biomass) on the larval consumption (consumption rate, conversion efficiency and/or relative growth rate) and immature development of two congeneric ladybirds, viz. Coccinella septempunctata (L.) and Coccinella transversalis F., (ii) evaluate their reproductive attributes under variable prey quantities, (iii) understand how these ladybirds compensate for the reduction in prey supply in terms of consumption, survival and reproduction, and (iv) facilitate the mass multiplication of these ladybirds for the augmentative biocontrol of aphid pests. C. septempunctata, though of Palearctic origin, is ubiquitous owing to its euryphagous nature, is large in size and has wide adaptability to different climatic conditions and food habitats (Hodek and Michaud, 2008). On the other hand C. transversalis is another large sized aphidophagous ladybird of Oriental region, native to India and found conspicuously in South Asia (Omkar et al., 2005a). Both the ladybirds co-exist as predators of numerous aphid species that infest the local agricultural crops of India. Because of wide prey range and association with a variety of aphid species, both ladybirds are recognized as effective biocontrol agents in the aphid management program.
2. Materials and methods 2.1. Stock maintenance Adults of C. septempunctata (C7) and C. transversalis (Ct) (n = 40) were collected from the fields of Lucknow, India (26°500 N, 80°540 E), paired and reared in plastic Petri dishes (14.5 1.5 cm2) under constant abiotic conditions (27 ± 2 °C; 65 ± 5% RH; 14L:10D photoperiod) in Environmental Test Chambers (ETC.; CH-6S Remi Instruments, Mumbai, India). They were provided with ad libitum aphid, Aphis craccivora Koch infested on cowpea (Vicia faba Linnaeus; Fabaceae) plants maintained in polyhouse (28 ± 1 °C; 65 ± 5% RH and 14L:10D photoperiod). The eggs laid were collected every 24 h, observed for hatching and the neonates obtained were used in the experiment.
37
2.2. Experimental design 2.2.1. Effect on consumption and developmental attributes Neonates of both the ladybird predators were weighed 12 h after hatching using an electronic balance (Sartorius CP225-D; 0.01 mg precision) and kept individually in plastic Petri dishes (abiotic conditions similar to stock). They were reared on any one of the following diets throughout their development (i.e. first instar to adult emergence), viz. (i) low prey condition (25 mg 60 third instars of A. craccivora), (ii) medium prey condition (50 mg 120 third instars of A. craccivora), and (iii) high prey condition (75 mg 180 third instars of A. craccivora). Prior to experimentation, prey biomasses (low, medium and high) were standardized on the prey consumption ability of: (i) late third/early fourth instars of C7 and Ct (most voracious stages amongst larvae and their prey consumption ability directly influence the adult reproductive performance; Mishra et al., 2012; Michaud, 2000, 2005), and (ii) 8–12 day old females (at this age females of C7 and Ct are highly voracious; Mishra et al., 2012). When fed on low prey, no aphid was left after 24 h. Under medium prey condition, larvae/females left scanty aphid biomass (2.00 ± 1.0 mg) in Petri dishes and under high prey supply, larvae/ females left surplus aphid biomass (8.00 ± 2.00 mg) after 24 h. The larvae were separated from the remaining biomass of prey (consisting of live and dead aphids as well as aphid parts and faecal matter) every 24 h and the remaining biomass was measured before providing a fresh amount to the larvae. Also the Petri dishes were examined every 24 h for the presence of larval moults (indicative of the next developmental stage), and once the moults were detected the biomass of larvae was measured. The durations of different immature stages were recorded on each prey quantity. The numbers of larvae surviving on each prey quantity were also recorded. The observations were made once daily, i.e. at 24 h interval. A mortality life table was constructed according to Morris and Miller (1954), where: (i) x is the developmental stage, i.e. all four larval instars, prepupae, pupae and adults; (ii) lx is the number of individuals entering the stage x; (iii) dx is the number of individuals dying within the stage x; (iv) 100qx is the apparent mortality, dx as a percentage of lx; (v) 100rx is the real mortality, dx as a percentage of the original cohort size; (vi) k-Value is a dimensionless measure of the mortality within the age interval x, calculated as the difference between the log values of the number of surviving individuals in subsequent stages; (vii) Sx is the survival rate of a stage, calculated from the number of individuals surviving the present stage number versus the number in the previous stage; (viii) K (kappa) is the sum of k-values; (ix) Mortality: survivor ratio (MSR). This shows the increase in the population that would have occurred if the mortality in the particular stage (x) had not occurred. This was calculated for a particular stage as: MSR = [mortality in the particular stage/lx of subsequent stage]; (x) Indispensable mortality (IM). The mortality that would not occur in a population, if the factor causing it is not allowed to operate and was calculated as: IM = [total number of adults emerged] [MSR of the particular stage]. Sex ratio was calculated as the ratio of the total number of females to the total number of adults (Omkar et al., 2009), while generation survival was calculated as the ratio of number of females to the number of first instars (modified after Harcourt,
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M. Bista, Omkar / Biological Control 74 (2014) 36–44
1969). Consumption rate, conversion efficiency and relative growth rate of larvae were calculated using the following formulae: 1. Consumption
rate
(mg-day1)
(Lucas
et
al.,
2004) =
Dixon,
2000) =
Aphid biomass consumed ðmgÞ by the larval instar Duration of larval instar ðdaysÞ
2. Conversion
efficiency
(modified
after
Increase in biomass ðmgÞduring a particular larval stage Aphid biomass consumedðmgÞby the larval instar
3. Relative growth rate (day1) (modified after Dixon, 2000) = lnðbody biomassðmgÞof succeeding larval stageÞlnðbody biomass ðmgÞof preceding larval stage Duration of larval stageðdaysÞ
The newly emerged adults were reared on the same diet under similar conditions. The adults were allowed to mate and ten mating pairs per prey quantity per ladybird species were separated for conducting the experiments on reproductive attributes. 2.2.2. Effect on reproductive attributes Every 24 h the males and females of each mating pairs were allowed to mate for 2 h. Thereafter they were separated and reared individually in Petri dishes (size as above) on the same prey quantity as provided to them during their larval stages. The biomass of adult females and remaining aphid prey were taken every 24 h and before providing them fresh prey. Pre-oviposition, oviposition and post-oviposition periods, daily oviposition and percent egg fertility were also recorded prior to the prey replenishment. Egg biomass conversion efficiency (Omkar et al., 2005b) was calculated as the ratio of egg biomass (mg) laid to that of aphid prey biomass (mg) consumed. Consumption rate was calculated as the daily aphid biomass (mg) consumed by the females, whereas the conversion efficiency was calculated as the daily increase in biomass (mg) of females per aphid biomass (mg) consumed (modified after Lucas et al., 2004 and Dixon, 2000). To assess the reduction in biomass of different diets in both the experiments (consumption, developmental and reproductive attributes) in absence of a predator (control), measured amount of these diets (i.e. 25, 50 and 75 mg, respectively) were placed individually in Petri dishes, kept under similar abiotic conditions for 24 h and then weighed. The average loss, if any, in biomass of these diets, based on 5 replicates, was used in statistical analyses of the data. 2.3. Statistical analysis The data obtained in the study were checked for normal distribution using Kolmogorov–Smirnoff test for normality and Bartlett’s test for homogeneity of variances. All percent data were subjected to arcsine square root transformation prior to subjecting to further analysis. The experimental data on larval consumption attributes, i.e. consumption rate, conversion efficiency and relative growth rate, were individually subjected to three-way ANOVA followed by Tukey’s post hoc comparison of means at 5% level, where ladybird species, prey quantity, larval stages and their interaction (ladybird species prey quantity larval stages) were the independent factors, and larval consumption attributes were the dependent factors. However, the independent factors, viz. mean body mass of newly emerged adults and total developmental duration of immature stages per ladybird species were individually subjected to one-way ANOVA with prey quantity acting as the dependent factor, followed by Tukey’s post hoc comparison of means. Moreover, generation survival and sex ratio per ladybird species were individually subjected to v2-test, followed by Tukey’s post hoc comparison of means at 5% level. For both the ladybird species, the reproductive periods (viz. preoviposition, oviposition and post-oviposition periods), fecundity
and egg fertility of females, and female and male longevities were individually subjected to two-way ANOVA, followed by Tukey’s post hoc comparison of means, where ladybird species, prey quantity and their interaction (ladybird species prey quantity) were independent factors and reproductive periods, fecundity, egg fertility, and female and male longevities were dependent factors. Further, age-specific consumption rate, fecundity, egg fertility, body biomass and egg biomass conversion efficiencies per prey quantity per ladybird species were individually regressed against mean reproductive age, followed by two-way ANCOVA with ladybird species, prey quantity and their interaction (ladybird species prey quantity) as independent factors and age as a covariate. All statistical analyses were performed on MINITAB 16 (Minitab Inc., State College, PA, USA). 3. Results 3.1. Effect on predatory and developmental attributes Results of three-way ANOVA revealed significant influence of ladybird species (F = 45.65; P < 0.0001; df = 1, 239), prey quantity (F = 272.33; P < 0.0001; df = 2, 239) and larval stage (F = 137.65; P < 0.0001; df = 3, 239) on the consumption rate of larvae; but the effect of their interactions (Fladybird species prey quantity larval stage = 0.24; P = 0.964; df = 6, 239) on consumption rate was insignificant. The conversion efficiency and relative growth rate of larvae were significantly influenced by the prey quantity (F = 14.23; P < 0.0001; df = 2, 239 and F = 13.42; P < 0.0001; df = 2, 239, respectively), larval stage (F = 232.67; P < 0.0001; df = 3, 239 and F = 162.56; P < 0.0001; df = 3, 239, respectively) and the interaction between ladybird species, prey quantity and larval stage (F = 5.36; P < 0.0001; df = 6, 239 and F = 5.22; P < 0.0001; df = 6, 239, respectively). Although the relative growth rate significantly differed between ladybird species (F = 14.50; P < 0.0001; df = 1, 239), but the conversion efficiency did not (F = 1.67; P = 0.198; df = 1, 239). In both the ladybird species, larval consumption rate was highest on high prey biomass and lowest on low prey biomass. Also the larvae had higher relative growth rates on high prey biomass than on low prey biomass, but their conversion efficiencies were lower than the larvae reared on low prey biomass (Fig. 1). Amongst the larval stages of both the ladybird species, higher consumption rate was recorded for the fourth instars than the early (first, second and third) instars on the three prey conditions provided; whereas higher conversion efficiencies and relative growth rates were recorded for the early instars than the fourth instars. One-way ANOVA further revealed significant influence of prey quantity on the total developmental duration of immature stages and mean body mass of newly emerged adults. Also, the v2-values exemplified significant influence of prey quantity on generation survival and sex ratio. In both C. septempunctata and C. transversalis, the total developmental durations of immature stages were shortest on high prey biomass and longest on low prey biomass. Also the mean body mass of newly emerged adults, generation survival and sex ratio were highest on high prey biomass and lowest on low prey biomass (Table 1). In C. septempunctata and C. transversalis the apparent and real mortalities, k-values, MSR and IM values, and overall mortality prior to adult stage (kappa values) were lowest on high prey biomass and highest on low prey biomass. However, the survival rates were highest on high prey biomass and lowest on low prey biomass (Tables 2 and 3). 3.2. Effect on reproductive attributes In adult females, two-way ANCOVA revealed significant influence of the ladybird species and the prey quantity on consumption
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M. Bista, Omkar / Biological Control 74 (2014) 36–44
Fig. 1. Conversion efficiency, relative growth rate and consumption rate of Coccinella septempunctata (C7) and Coccinella transversalis (Ct) larvae under the three different prey conditions (values are means ± SE; small and large letters represent comparison of means between larval stages per prey condition and among prey conditions per larval stage, respectively).
Table 1 Effects of quantity of prey on total developmental duration of immature stages, mean body mass of newly emerged adults, generation survival and sex ratio of Coccinella septempunctata (C7) and Coccinella transversalis (Ct) (n = 100 per ladybird species). Ladybird species
C7
Prey quantity
Low Medium High
One-way ANOVA
Ct
One-way ANOVA
Low Medium High
Total developmental duration (days)
Mean body mass of newly emerged adults
Generation survival
Sex ratio
17.73 ± 0.30a 25.43 ± 0.25b 26.07 ± 0.27c
0.26 ± 0.04a 0.44 ± 0.05b 0.46 ± 0.05b
0.46 ± 0.05a 0.60 ± 0.05b 0.63 ± 0.05b
F = 12.50 P < 0.0001 df = 2, 116
F = 294.81 P < 0.0001 df = 2, 87
v2 = 10.232 P = 0.006 df = 2
v2 = 6.694 P = 0.035 df = 2
14.00 ± 0.10c 12.22 ± 0.10b 11.11 ± 0.14a
18.82 ± 0.32a 21.70 ± 0.20b 24.50 ± 0.11c
12.38 ± 0.23a 16.17 ± 0.24b 17.96 ± 0.24c
0.25 ± 0.04a 0.45 ± 0.05b 0.54 ± 0.05b
0.45 ± 0.05a 0.62 ± 0.05b 0.64 ± 0.05b
F = 94.56 P < 0.0001 df = 2, 210
F = 15.51 P < 0.0001 df = 2, 122
F = 149.01 P < 0.0001 df = 2, 88
v2 = 18.173
v2 = 2.30 P = 0.012 df = 2
Females (mg)
Males (mg)
13.67 ± 0.16c 12.00 ± 0.17b 9.33 ± 0.05a
25.39 ± 0.18a 31.01 ± 0.37b 32.98 ± 0.45c
F = 100.38 P < 0.0001 df = 2, 203
P < 0.0001 df = 2
Values are means ± SE; F-values/v2-values are significant at P < 0.05. Small letters represent comparison of means among prey quantities per ladybird species.
rate (FANCOVA (Ladybird species Prey quantity) = 18.70; P < 0.0001; df = 2, 629) and the mean body mass (FANCOVA (Ladybird species Quantity) = 16.72; P < 0.0001; df = 2, 629). The influence was age dependent (FANCOVA (Age) = 587.40; P < 0.0001; df = 1, 629 and FANCOVA (Age) = 226.56; P < 0.0001; df = 1, 629, respectively). The aphid prey consumption by females initially increased at an early age, reached a peak at middle age and then declined at old age (plateau shaped). Mean body mass of adult females increased with age on the three diets. The values of consumption rates and mean body mass were highest on high prey biomass and lowest on low prey biomass (Fig. 2). Results revealed significant influence of ladybird species, prey quantity and their interaction on pre-oviposition period and female longevity. The post-oviposition period was not influenced by the prey quantity, although the effects of ladybird species and the interaction between ladybird species and prey quantity were significant. The oviposition period and fecundity were influenced by the prey quantity, but neither by the ladybird species nor by
the interaction between ladybird species and prey quantity. However, the egg fertility was significantly influenced by the ladybird species and prey quantity but not by their interaction. Moreover, the male longevity was not significantly influenced by the ladybird species, though the influence of prey quantity and the interaction between ladybird species and prey quantity was significant. On high prey biomass the pre-oviposition periods of both the ladybird species were shortest and their oviposition periods were longest. Also the females had highest fecundity and egg fertility; and males and females of both the ladybirds lived longest on high prey biomass (Table 4). Further, the age specific fecundity and egg fertility were not influenced by the ladybird species (FANCOVA (Ladybird species) = 1.97; P = 0.161; df = 1, 629 and FANCOVA (Ladybird species) = 0.01; P = 0.925; df = 1, 629, respectively) or the interaction between ladybird species and prey quantity (FANCOVA (Ladybird species Prey quantity) = 1.64; P = 0.195; df = 2, 629 and FANCOVA (Ladybird species Prey quantity) = 1.35; P = 0.260; df = 2, 629, respectively). However, the individual effect
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M. Bista, Omkar / Biological Control 74 (2014) 36–44
Table 2 Effect of prey quantity on mortality life-table of Coccinella septempunctata (n = 100). Prey quantity
Developmental stage (x)
No. of individuals entering stage x (lx)
No. of individuals dying within stage x (dx)
Apparent mortality (100qx)
Real mortality (100rx)
Survival rate (Sx)
kValue
MSR
IM
Low prey
Instars
First Second Third Fourth
100 86 76 68 64 60 56
14 10 8 4 4 4 Kappa = 0.252
14.00 11.63 10.53 5.88 6.25 6.67
14.00 10.00 8.00 4.00 4.00 4.00
0.86 0.88 0.89 0.94 0.94 0.93
0.066 0.054 0.048 0.026 0.028 0.030
0.14 0.12 0.11 0.06 0.06 0.07
7.84 6.51 5.89 3.29 3.50 3.73
First Second Third Fourth
100 90 85 82 78 76 73
10 5 3 4 2 3 Kappa = 0.137
10.00 5.56 3.53 4.88 2.56 3.95
10.00 5.00 3.00 4.00 2.00 3.00
0.90 0.94 0.96 0.95 0.97 0.96
0.046 0.025 0.016 0.022 0.011 0.017
0.10 0.06 0.04 0.05 0.03 0.04
7.30 4.06 2.58 3.56 1.87 2.88
First Second Third Fourth
100 92 88 84 80 77 75
8 4 4 4 3 2 Kappa = 0.125
8.00 4.35 4.55 4.76 3.75 2.60
8.00 4.00 4.00 4.00 3.00 2.00
0.92 0.96 0.95 0.95 0.96 0.97
0.036 0.019 0.020 0.021 0.017 0.011
0.08 0.04 0.05 0.05 0.04 0.03
6.00 3.26 3.41 3.57 2.81 1.95
Pre-pupa Pupa Adults Medium prey
Instars
Pre-pupa Pupa Adults High prey
Instars
Pre-pupa Pupa Adults
MSR and IM represent mortality-survivor ratio and indispensable mortality, respectively.
Table 3 Effect of prey quantity on mortality life-table of Coccinella transversalis (n = 100). Prey quantity
Developmental stage (x)
No. of individuals entering stage x (lx)
No. of individuals dying within stage x (dx)
Apparent mortality (100qx)
Real mortality (100rx)
Survival rate (Sx)
kValue
MSR
IM
Low prey
Instars
First Second Third Fourth
100 88 78 70 65 60 57
12 10 8 5 5 3 Kappa = 0.244
12.00 11.36 10.26 7.14 7.69 5.00
12.00 10.00 8.00 5.00 5.00 3.00
0.88 0.89 0.90 0.93 0.92 0.95
0.056 0.052 0.047 0.032 0.035 0.022
0.12 0.11 0.10 0.07 0.08 0.05
6.84 6.48 5.85 4.07 4.38 2.85
First Second Third Fourth
100 92 86 83 79 77 75
8 6 3 4 2 2 Kappa = 0.125
8.00 6.52 3.49 4.82 2.53 2.60
8.00 6.00 3.00 4.00 2.00 2.00
0.92 0.93 0.97 0.95 0.97 0.97
0.036 0.029 0.015 0.021 0.011 0.011
0.08 0.07 0.03 0.05 0.03 0.03
6.00 4.89 2.62 3.61 1.90 1.95
First Second Third Fourth
100 95 91 87 84 81 79
5 4 4 3 2 2 Kappa = 0.102
5.00 4.21 4.40 3.45 3.57 2.47
5.00 4.00 4.00 3.00 3.00 2.00
0.95 0.96 0.96 0.97 0.96 0.98
0.022 0.019 0.020 0.015 0.016 0.010
0.05 0.04 0.04 0.03 0.04 0.02
3.95 3.33 3.47 2.72 2.82 1.95
Pre-pupa Pupa Adults Medium prey
Instars
Pre-pupa Pupa Adults High prey
Instars
Pre-pupa Pupa Adults
MSR and IM represent mortality- survivor ratio and indispensable mortality, respectively.
of prey quantity (FANCOVA (Prey quantity) = 41.93; P < 0.0001; df = 2, 629 and FANCOVA (Prey quantity) = 24.71; P < 0.0001; df = 2, 629, respectively) was significant and was age dependent (FANCOVA (Age) = 167.81; P < 0.0001; df = 1, 629 and FANCOVA (Age) = 217.96; P < 0.0001; df = 1, 629, respectively). The fecundity increased with increase in adult age, reached a peak and thereafter declined with further advancement in age, i.e. a triangular fecundity trend, on different prey supply. The egg fertility also revealed similar trend. The maximum fecundity and egg fertility were obtained when the females of C. septempunctata (between 45–48 days on low prey biomass, 42–45 days on medium prey biomass and 39–42 days on high prey biomass) and C. transversalis (between 35–40 days on low prey
biomass, 28–31 days on medium prey biomass and 25–30 days on high prey biomass) were middle aged (Fig. 3). The body biomass conversion efficiency of adult females was significantly influenced by the ladybird species (FANCOVA (Ladybird species) = 5.05; P = 0.025; df = 1, 629) and the prey quantity (FANCOVA (Prey quantity) = 3.20; P = 0.041; df = 2, 629), but not by their interaction (FANCOVA (Ladybird species Prey quantity) = 2.12; P = 0.121; df = 2, 629). It was age dependent (FANCOVA (Age) = 95.22; P < 0.0001; df = 1, 629). However, the egg biomass conversion efficiency was influenced by the prey quantity (FANCOVA (Prey quantity) = 5.63; P = 0.004; df = 2, 629); but neither influenced by the ladybird species (FANCOVA (Ladybird species) = 0.29; P = 0.587; df = 1, 629) nor
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M. Bista, Omkar / Biological Control 74 (2014) 36–44
Fig. 2. Age specific consumption rate and mean body mass of Coccinella septempunctata (C7) and Coccinella transversalis (Ct) adult females under the three different prey conditions (r2-values significant at P < 0.05).
Table 4 Effect of quantity of prey on the reproductive attributes of Coccinella septempunctata (C7) and Coccinella transversalis (Ct) (n = 10 per ladybird species). Ladybird species
Prey quantity
Pre-oviposition period (days)
Oviposition period (days)
Post oviposition period (days)
Fecundity (No. of eggs)
Egg fertility (%)
Female longevity (days)
Male longevity (days)
C7
Low Medium High
19.00 ± 0.60c 12.50 ± 0.43b 11.30 ± 0.65a
40.30 ± 0.52a 52.70 ± 1.12b 54.50 ± 0.50c
10.40 ± 0.54a 11.90 ± 0.64a 11.80 ± 0.49a
784.90 ± 30.15a 1439.90 ± 44.20b 1546.60 ± 41.61c
81.23 ± 1.34a 87.17 ± 0.94b 89.17 ± 0.98c
69.70 ± 2.07a 77.10 ± 2.26b 77.60 ± 1.23b
64.90 ± 1.45a 70.50 ± 1.88ab 71.10 ± 1.46b
Ct
Low Medium High
9.20 ± 0.13c 7.00 ± 0.26b 6.40 ± 0.16a
38.50 ± 0.54a 52.70 ± 0.84b 55.10 ± 0.72c
11.10 ± 0.41a 10.10 ± 0.53a 8.80 ± 0.33a
794.60 ± 30.84a 1561.30 ± 44.91b 1604.10 ± 45.61b
82.72 ± 0.67a 89.87 ± 0.87b 90.82 ± 0.80b
58.80 ± 1.60a 69.80 ± 1.26b 70.30 ± 1.30b
56.20 ± 1.75a 64.20 ± 1.58b 65.80 ± 1.48b
Ladybird species
F = 380.16 P < 0.0001 df = 1, 59
F = 0.44 P = 0.511 df = 1, 59
F = 11.27 P = 0.001 df = 1, 59
F = 3.65 P = 0.061 df = 1, 59
F = 6.20 P = 0.016 df = 1, 59
F = 11.19 P = 0.001 df = 1, 59
F = 2.20 P = 0.144 df = 1, 59
Prey quantity
F = 88.13 P < 0.0001 df = 2, 59
F = 254.30 P < 0.0001 df = 2, 59
F = 1.01 P = 0.370 df = 2, 59
F = 231.57 P < 0.0001 df = 2, 59
F = 38.81 P < 0.0001 df = 2, 59
F = 444.41 P < 0.0001 df = 2, 59
F = 486.00 P < 0.0001 df = 2, 59
Interaction
F = 19.97 P < 0.0001 df = 2, 59
F = 1.42 P = 0.250 df = 2, 59
F = 7.16 P = 0.002 df = 2, 59
F = 0.97 P = 0.387 df = 2, 59
F = 0.21 P < 0.810 df = 2, 59
F = 38.71 P < 0.0001 df = 2, 59
F = 53.03 P < 0.0001 df = 2, 59
Values are means ± SE Small letters represent comparison of means among prey quantities within each ladybird species.
by their interaction (FANCOVA (Ladybird species Prey quantity) = 0.49; P = 0.611; df = 2, 629). It was also age dependent (FANCOVA (Age) = 195.05; P < 0.0001; df = 1, 629). The body biomass conversion efficiency was higher during pre- and post-oviposition periods in both the ladybirds on three different diets; being highest on high prey biomass and lowest on low prey biomass. In contrast, the egg biomass conversion efficiency was lower during pre- and post-
oviposition periods in both the ladybirds. It was highest on the high prey biomass and lowest on the low prey biomass (Fig. 4). 4. Discussion In the present study, larval stages of both C. septempunctata and C. transversalis had higher consumption rates and relative growth
42
M. Bista, Omkar / Biological Control 74 (2014) 36–44
Fig. 3. Age specific fecundity and egg fertility of Coccinella septempunctata (C7) and Coccinella transversalis (Ct) adult females under the three different prey conditions (r2values significant at P < 0.05).
rates, but shorter developmental durations when fed on high prey biomass while the reverse was true on low prey biomass. It is assumed that when high prey biomass is available for feeding, the larvae consume maximum prey biomass to enhance their growth rates. Further, on account of their higher growth rates, they quickly acquire the threshold biomass necessary for pupation and complete their development earlier than the larvae feeding on low prey biomass. The present findings are in agreement with many earlier studies in ladybirds (Schuder et al., 2004; Agarwala et al., 2008; Atlihan and Guldal, 2009; Omkar et al., 2010; Maurice and Ashwani, 2011). Further, despite lower consumption rate, relative growth rate and prolonged developmental durations, the larvae of both the ladybirds have shown higher conversion efficiencies under low prey biomass condition in the present study. Probably, the slowing down of larval development and increase in conversion efficiency under low prey biomass condition are amongst the several mechanisms displayed by the larvae to compensate for a shortage of
food, as also reported earlier by Schuder et al. (2004) in the larvae of Adalia bipunctata L. Increased generation survival, higher sex ratio, emergence of heavier adults and decreased larval mortality on high prey biomass in the present study further reveal that when surplus prey is available, ladybirds possibly exploit the prey population maximally to increase their population and enhance their progeny fitness. Contrary to it, the availability of low prey biomass probably retards the population growth of ladybirds, increases their larval mortality and reduces their progeny fitness. Amongst the larval stages, a higher consumption rate of fourth instars over the early instars on the three prey conditions provided is possibly owing to their large size and increased energy requirements to fulfill their increased metabolic costs. In contrast, the higher conversion efficiencies and relative growth rates of early instars over the fourth instars may be attributed to their small size, low metabolic costs and low energy needs (Mishra et al., 2012).
M. Bista, Omkar / Biological Control 74 (2014) 36–44
43
Fig. 4. Age specific body biomass conversion efficiency and egg biomass conversion efficiency of Coccinella septempunctata (C7) and Coccinella transversalis (Ct) adult females under the three different prey conditions (r2-values significant at P < 0.05).
In the present study, adult females showed highest consumption rates, maximum mean body mass gain, shortest pre- and post-oviposition periods, longest oviposition periods and highest fecundity and egg fertility on high prey biomass. These may be owing to: (i) the large size of adults at emergence on high prey biomass (Boggs and Freeman, 2005; Agarwala et al., 2008) and their higher reproductive rates related with their large size (Salavert et al., 2011; Omkar and Afaq, 2013; Bista and Omkar, 2013), and (ii) the availability of surplus prey for consumption and to fulfill the high energy requirements associated with large size. The longer pre-oviposition and shorter oviposition periods under low prey biomass condition may be attributed to the late ripening of ovarioles due to poor availability of nutrients, as also reported earlier by Omkar and Pervez (2003) in Propylea dissecta (Mulsant) and Omkar et al. (2010) in Anegleis cardoni (Weise). Lower consumption rates, fecundity and egg fertility may be ascribed to the small size of emerging adults on low prey biomass. Under the three prey supply conditions, the prey consumption rates by adult females of C. septempunctata and C. transversalis initially increased with age, reached a peak and thereafter declined. This initial increase in consumption rate may be ascribed to their high energy requirements for gonadal development and sexual
maturity. The process of senescence is possibly responsible for decline in prey consumption by adult females at later age (Dixon and Agarwala, 2002). However, no decline in mean body mass of adult females under three prey supply conditions with increase in age supports the findings of Mishra et al. (2012) in ladybirds. Perhaps despite reduced prey consumption rates, older females use their entire nutrients in maintaining their body biomass once egg laying is ceased. Further, both the ladybirds exhibited a triangular fecundity and egg fertility function on the three prey biomasses. The oviposition in adult females occurred during earlier and later phases of middle age under high and low prey biomass conditions, respectively. The findings thus reveal that the middle aged individuals invest most of their energy in reproduction than young or old aged individuals, as also reported in earlier studies (Pandey and Omkar, 2013; Bista and Omkar, 2013). However, the investment is higher on high prey biomass than on low prey biomass. Higher body biomass conversion efficiency during pre- and post-oviposition periods, and higher egg biomass conversion efficiency during oviposition period on the three prey biomasses indicate that prior to egg laying or once the reproduction ceases, the ladybirds invest their energy for maintenance and survival,
44
M. Bista, Omkar / Biological Control 74 (2014) 36–44
maturation of gonads and body mass gains. However, during reproductive period they possibly partition their energy on the production of eggs, self maintenance and survival, and the investment is higher when ladybirds are fed on high prey biomass. But under low prey biomass condition, they probably utilize less resources obtained from poor prey consumption to their self-maintenance and egg production, as also reported by Legaspi and Legaspi (1998), Omkar and Pervez (2003) and Evans (2003). In brief, the consumption, developmental and reproductive attributes of C. septempunctata and C. transversalis change in response to aphid prey availability. On high prey biomass the larvae have high consumption and growth rates, fast development and low mortality, while the emerging adults are large in size, consume more aphid prey and utilize the prey biomass maximally on the production of eggs, self maintenance and survival. In contrast, the availability of low aphid prey biomass reduces the chances of larval survival, and those that emerged as adults are small in size, have poor prey consumption rates, low fecundity, egg fertility and short life span. Further, age-based consumption and reproductive attributes reveal that middle aged ladybirds reared on high prey biomass may suppress the pest population better than those reared on low/medium prey biomass. References Agarwala, B.K., Bardhanroy, P., Yasuda, H., Takizawa, T., 2001. Prey consumption and oviposition of the aphidophagous predator Menochilus sexmaculatus (Coleoptera: Coccinellidae) in relation to prey density and adult size. Environ. Entomol. 30, 1182–1187. Agarwala, B.K., Singh, T.K., Lokeshwari, R.K., Sharmila, M., 2009. Functional response and reproductive attributes of the aphidophagous ladybird beetle, Harmonia dimidiate (F.) in oak trees of sericultural importance. J. Asia Pac. Entomol. 12, 179–182. Agarwala, B.K., Yasuda, H., Sato, S., 2008. Life history response of a predatory ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) to food stress. Appl. Entomol. Zool. 43 (2), 183–189. Atlihan, R., Guldal, H., 2009. Prey density-dependent feeding activity and life history of Scymnus subvillosus. Phytoparasitica 37, 35–41. Bista, M., Omkar, 2013. Effects of body size and prey quality on reproductive attributes of two aphidophagous ladybird beetles (Coleoptera: Coccinellidae). Can. Entomol. 145, 566–576. Boggs, C.L., Freeman, K.D., 2005. Larval food limitation in butterflies: effects on adult resource allocation and fitness. Oecologia 144, 353–361. Bonduriansky, R.A., Head, M., 2007. Maternal and paternal condition effects on offspring phenotype in Telostylinus angusticollis (Diptera: Neriidae). J. Evol. Biol. 20, 2379–2388. Dixon, A.F.G., 2000. Insect Predator-Prey Dynamics: Ladybird Beetles and Biological Control. Cambridge University Press, Cambridge, pp. 257. Dixon, A.F.G., Agarwala, B.K., 2002. Triangular fecundity function and ageing in ladybird beetles. Ecol. Entomol. 27, 433–440. Dmitriew, C., Rowe, L., 2011. The effects of larval nutrition on reproductive performance in a food-limited adult environment. PLoS ONE 6 (3), e17399. http://dx.doi.org/10.1371/journal.pone.001 7399. Evans, E.W., 2003. Searching and reproductive behaviour of female aphidophagous ladybirds (Coleoptera: Coccinellidae): a review. Eur. J. Entomol. 100, 1–10. Harcourt, D.G., 1969. The development and use of life tables in the study of natural insect populations. Annu. Rev. Entomol. 14, 175–196.
Hodek, I., Michaud, J.P., 2008. Why is Coccinella septempunctata so successful? Eur. J. Entomol. 105, 1–12. Legaspi, J.C., Legaspi, B.C., 1998. Life history trade-offs in insects, with emphasis on Podisus maculiventris (Heteroptera: Pentatomidae). In: Coll, M., Ruberson, J.R. (Eds.), Predatory Heteroptera: Their Ecology and Use in Biological Control. Thomas Say Publications in Entomology, Laham, pp. 71–87. Lucas, E., Demougeot, S., Vincent, C., Coderre, D., 2004. Predation upon the obliquebanded leafroller, Choristoneura rosaceana (Lepidoptera: Tortricidae), by two aphidophagous coccinellids (Coleoptera: Coccinellidae) in the presence and absence of aphids. Eur. J. Entomol. 101, 37–41. Maurice, N., Ashwani, K., 2011. Effect of quantity and consumption of food on body weight and development of two species of ladybird beetles. Ann. Plant Prot. Sci. 19 (1), 59–62. Michaud, J.P., 2000. Development and reproduction of ladybeetles (Coleoptera: Coccinellidae) on the citrus aphids Aphis spiraecola Patch and Toxoptera citricida (Kirkaldy) (Homoptera: Aphididae). Biol. Control 18, 287–297. Michaud, J.P., 2005. On the assessment of prey suitability in aphidophagous Coccinellidae. Eur. J. Entomol. 102, 385–390. Mishra, G., Omkar, Pandey, B., Pandey, G., 2012. Stage and age specific predation in four aphidophagous ladybird beetles. Biocontrol Sci. Tech. 22, 463–476. Morris, R.E., Miller, C.A., 1954. The development of life-tables for the spruce budworm. Can. J. Zool. 32, 283–301. Omkar, Afaq, U., 2013. Evaluation of Darwin’s fecundity advantage hypothesis in Parthenium beetle. Zygogramma bicolorata Pallister. Insect Sci. 20 (4), 531–540. Omkar, Kumar, G., Sahu, J., 2009. Performance of a predatory ladybird beetle, Anegleis cardoni (Coleoptera: Coccinellidae) on three aphid species. Eur. J. Entomol. 106, 565–572. Omkar, Pervez, A., 2003. Influence of prey deprivation on biological attributes of pale morphs of the ladybeetle, Propylea dissecta (Mulsant). Insect Sci. Appl. 23 (2), 143–148. Omkar, Mishra, G., Srivastava, S., Gupta, A.K., Singh, S.K., 2005a. Reproductive performance of four aphidophagous ladybirds on cowpea aphid, Aphis craccivora Koch. J. Appl. Entomol. 129 (4), 217–220. Omkar, Pervez, A., Mishra, G., Srivastava, S., Singh, S.K., Gupta, A.K., 2005b. Intrinsic advantages of Cheilomenes sexmaculata over two coexisting Coccinella species (Coleoptera: Coccinellidae). Insect Sci. 12, 179–184. Omkar, Sahu, J., Kumar, G., 2010. Effect of prey quantity in a ladybird beetle, Anegleis cardoni (Weise) (Coleoptera: Coccinellidae). Int. J. Trop. Insect Sci. 30 (1), 48–56. Pandey, P., Omkar, 2013. Age based mate choice improves reproductive performance and offspring attributes in Parthenium beetle, Zygogramma bicolorata (Coleoptera: Chrysomelidae). Can. Entomol. 145, 292–301. Phoofolo, M.W., Giles, K.L., Elliott, N.C., 2008. Larval life history responses to food deprivation in three species of predatory lady beetles (Coleoptera: Coccinellidae). Environ. Entomol. 37, 315–322. Qvarnström, A., Price, T.D., 2001. Maternal effects, paternal effects and sexual selection. Trends Ecol. Evol. 16, 95–100. Salavert, V., Zamora-Munoz, C., Ruizrodriguez, M., Soler, J.J., 2011. Female-biased size dimorphism in a diapausing caddisfly, Mesophylax aspersus: effect of fecundity and natural and sexual selection. Ecol. Entomol. 36, 389–395. Santos-Cividanes, T.M., dos Anjos, A.C.R., Cividanes, F.J., Dias, P.C., 2011. Effects of food deprivation on the development of Coleomegilla maculata (De Geer) (Coleoptera: Coccinellidae). Neotrop. Entomol. 40 (1), 112–116. Schuder, I., Hommes, M., Larink, O., 2004. The influence of temperature and food supply on the development of Adalia bipunctata (Coleoptera: Coccinellidae). Eur. J. Entomol. 101, 379–384. Seagraves, M.P., 2009. Lady beetle oviposition behavior in response to the trophic environment. Biol. Control 51, 313–322. Ware, R.L., Yguel, B., Majerus, M.E.N., 2008. Effects of larval diet on female reproductive output of the European coccinellid Adalia bipunctata and the invasive species Harmonia axyridis (Coleoptera: Coccinellidae). Eur. J. Entomol. 105, 437–443.
Contents lists available at ScienceDirect
Biological Control journal homepage: www.elsevier.com/locate/ybcon
Consumption, developmental and reproductive attributes of two con-generic ladybird predators under variable prey supply Mahadev Bista, Omkar ⇑ Ladybird Research Laboratory, Department of Zoology, University of Lucknow, Lucknow 226 007, India
h i g h l i g h t s
g r a p h i c a l a b s t r a c t
Evaluated performance of two
con-generic ladybirds on three prey biomasses. Larvae developed fastest and survived maximum on high prey biomass. Middle aged adults consumed and reproduced maximally on high prey biomass. Females consume prey to increase body biomass at early & late reproductive phases. Females invest more on oviposition during their reproductive phase.
a r t i c l e
i n f o
Article history: Received 16 May 2013 Accepted 1 April 2014 Available online 6 April 2014 Keywords: Ladybird Prey quantity Conversion efficiency Consumption rate Fecundity Egg fertility
a b s t r a c t Availability of aphid prey in habitat is often heterogeneous in space and time and its deprivation causes severe effects on life attributes of ladybird predators. Sometimes ladybirds locate high prey biomass while on certain occasions prey biomass may be either medium/low or altogether absent. Present study has been designed in view of three prey biomass conditions in nature, viz. low, medium and high, selecting Coccinella septempunctata and Coccinella transversalis as experimental ladybirds. Results revealed that consumption, developmental and reproductive attributes of both ladybirds changed in response to prey availability. On high prey biomass larvae had higher consumption and growth rates, developed faster and had low mortality, while emerging adults were large in size, had high consumption rates and utilized prey biomass maximally on production of eggs, self maintenance and survival. In contrast low prey biomass reduced chances of larval survival and emerging adults were small in size, had poor prey consumption rates, low fecundity, egg fertility and short life span. Females exhibited triangular fecundity and egg fertility functions and plateau shaped prey consumption rate function with age, indicating towards their highest reproductive performance during middle age on three prey biomasses; being highest on high prey biomass. On three prey biomasses, females had higher body biomass conversion efficiency during pre- and post-oviposition periods and higher egg biomass conversion efficiency during oviposition period; being highest on high prey biomass. Thus middle aged ladybirds reared on high prey biomass may suppress pest populations better than those reared on low/medium prey biomass. Ó 2014 Elsevier Inc. All rights reserved.
1. Introduction ⇑ Corresponding author. Mobile: +91 9415757747. E-mail address: [email protected] (Omkar). http://dx.doi.org/10.1016/j.biocontrol.2014.04.001 1049-9644/Ó 2014 Elsevier Inc. All rights reserved.
Prey availability is often heterogeneous in space and time and its deprivation causes severe effects on the life attributes of
M. Bista, Omkar / Biological Control 74 (2014) 36–44
ladybirds (Phoofolo et al., 2008; Santos-Cividanes et al., 2011) which forage in unstable habitats with variable prey density (Agarwala et al., 2001). Studies have shown that reduced prey consumption (Phoofolo et al., 2008) and/or prey deprivation severely affect the development and survival of ladybirds (Omkar and Pervez, 2003; Schuder et al., 2004; Atlihan and Guldal, 2009), and the developmental rate and the size of offspring (Agarwala et al., 2001; Seagraves, 2009). Under limited prey conditions the larvae develop slowly and the surviving adults are smaller in size. Further prey deprivation negatively affects the reproductive attributes of ladybirds (Dmitriew and Rowe, 2011). Under prey deprived conditions the pre-reproductive periods of adults are considerably prolonged and their reproductive phase, fecundity (Agarwala et al., 2008, 2009), oviposition rate and clutch size are highly reduced (Dixon, 2000; Ware et al., 2008). It therefore appears that there is a strong selection pressure in the natural populations of ladybird predators for survival, reproduction and offspring performance under limited prey resource. Moreover, the prey abundance/ deprivation not only affect the parents but also have trans-generational effects (Omkar et al., 2010); and the individuals that acquire abundant resource transfer their resources to offspring and enhance offspring fitness (Qvarnström and Price, 2001; Bonduriansky and Head, 2007). There are a few studies that have evaluated the stage and age specific consumption attributes in larval and/or adult stages (Schuder et al., 2004; Mishra et al., 2012), but not much work has been done on the comparative consumption and reproductive attributes of ladybirds under high prey/ low prey biomass conditions. The present study has been aimed to: (i) assess the impact of prey quantity (low, medium and high biomass) on the larval consumption (consumption rate, conversion efficiency and/or relative growth rate) and immature development of two congeneric ladybirds, viz. Coccinella septempunctata (L.) and Coccinella transversalis F., (ii) evaluate their reproductive attributes under variable prey quantities, (iii) understand how these ladybirds compensate for the reduction in prey supply in terms of consumption, survival and reproduction, and (iv) facilitate the mass multiplication of these ladybirds for the augmentative biocontrol of aphid pests. C. septempunctata, though of Palearctic origin, is ubiquitous owing to its euryphagous nature, is large in size and has wide adaptability to different climatic conditions and food habitats (Hodek and Michaud, 2008). On the other hand C. transversalis is another large sized aphidophagous ladybird of Oriental region, native to India and found conspicuously in South Asia (Omkar et al., 2005a). Both the ladybirds co-exist as predators of numerous aphid species that infest the local agricultural crops of India. Because of wide prey range and association with a variety of aphid species, both ladybirds are recognized as effective biocontrol agents in the aphid management program.
2. Materials and methods 2.1. Stock maintenance Adults of C. septempunctata (C7) and C. transversalis (Ct) (n = 40) were collected from the fields of Lucknow, India (26°500 N, 80°540 E), paired and reared in plastic Petri dishes (14.5 1.5 cm2) under constant abiotic conditions (27 ± 2 °C; 65 ± 5% RH; 14L:10D photoperiod) in Environmental Test Chambers (ETC.; CH-6S Remi Instruments, Mumbai, India). They were provided with ad libitum aphid, Aphis craccivora Koch infested on cowpea (Vicia faba Linnaeus; Fabaceae) plants maintained in polyhouse (28 ± 1 °C; 65 ± 5% RH and 14L:10D photoperiod). The eggs laid were collected every 24 h, observed for hatching and the neonates obtained were used in the experiment.
37
2.2. Experimental design 2.2.1. Effect on consumption and developmental attributes Neonates of both the ladybird predators were weighed 12 h after hatching using an electronic balance (Sartorius CP225-D; 0.01 mg precision) and kept individually in plastic Petri dishes (abiotic conditions similar to stock). They were reared on any one of the following diets throughout their development (i.e. first instar to adult emergence), viz. (i) low prey condition (25 mg 60 third instars of A. craccivora), (ii) medium prey condition (50 mg 120 third instars of A. craccivora), and (iii) high prey condition (75 mg 180 third instars of A. craccivora). Prior to experimentation, prey biomasses (low, medium and high) were standardized on the prey consumption ability of: (i) late third/early fourth instars of C7 and Ct (most voracious stages amongst larvae and their prey consumption ability directly influence the adult reproductive performance; Mishra et al., 2012; Michaud, 2000, 2005), and (ii) 8–12 day old females (at this age females of C7 and Ct are highly voracious; Mishra et al., 2012). When fed on low prey, no aphid was left after 24 h. Under medium prey condition, larvae/females left scanty aphid biomass (2.00 ± 1.0 mg) in Petri dishes and under high prey supply, larvae/ females left surplus aphid biomass (8.00 ± 2.00 mg) after 24 h. The larvae were separated from the remaining biomass of prey (consisting of live and dead aphids as well as aphid parts and faecal matter) every 24 h and the remaining biomass was measured before providing a fresh amount to the larvae. Also the Petri dishes were examined every 24 h for the presence of larval moults (indicative of the next developmental stage), and once the moults were detected the biomass of larvae was measured. The durations of different immature stages were recorded on each prey quantity. The numbers of larvae surviving on each prey quantity were also recorded. The observations were made once daily, i.e. at 24 h interval. A mortality life table was constructed according to Morris and Miller (1954), where: (i) x is the developmental stage, i.e. all four larval instars, prepupae, pupae and adults; (ii) lx is the number of individuals entering the stage x; (iii) dx is the number of individuals dying within the stage x; (iv) 100qx is the apparent mortality, dx as a percentage of lx; (v) 100rx is the real mortality, dx as a percentage of the original cohort size; (vi) k-Value is a dimensionless measure of the mortality within the age interval x, calculated as the difference between the log values of the number of surviving individuals in subsequent stages; (vii) Sx is the survival rate of a stage, calculated from the number of individuals surviving the present stage number versus the number in the previous stage; (viii) K (kappa) is the sum of k-values; (ix) Mortality: survivor ratio (MSR). This shows the increase in the population that would have occurred if the mortality in the particular stage (x) had not occurred. This was calculated for a particular stage as: MSR = [mortality in the particular stage/lx of subsequent stage]; (x) Indispensable mortality (IM). The mortality that would not occur in a population, if the factor causing it is not allowed to operate and was calculated as: IM = [total number of adults emerged] [MSR of the particular stage]. Sex ratio was calculated as the ratio of the total number of females to the total number of adults (Omkar et al., 2009), while generation survival was calculated as the ratio of number of females to the number of first instars (modified after Harcourt,
38
M. Bista, Omkar / Biological Control 74 (2014) 36–44
1969). Consumption rate, conversion efficiency and relative growth rate of larvae were calculated using the following formulae: 1. Consumption
rate
(mg-day1)
(Lucas
et
al.,
2004) =
Dixon,
2000) =
Aphid biomass consumed ðmgÞ by the larval instar Duration of larval instar ðdaysÞ
2. Conversion
efficiency
(modified
after
Increase in biomass ðmgÞduring a particular larval stage Aphid biomass consumedðmgÞby the larval instar
3. Relative growth rate (day1) (modified after Dixon, 2000) = lnðbody biomassðmgÞof succeeding larval stageÞlnðbody biomass ðmgÞof preceding larval stage Duration of larval stageðdaysÞ
The newly emerged adults were reared on the same diet under similar conditions. The adults were allowed to mate and ten mating pairs per prey quantity per ladybird species were separated for conducting the experiments on reproductive attributes. 2.2.2. Effect on reproductive attributes Every 24 h the males and females of each mating pairs were allowed to mate for 2 h. Thereafter they were separated and reared individually in Petri dishes (size as above) on the same prey quantity as provided to them during their larval stages. The biomass of adult females and remaining aphid prey were taken every 24 h and before providing them fresh prey. Pre-oviposition, oviposition and post-oviposition periods, daily oviposition and percent egg fertility were also recorded prior to the prey replenishment. Egg biomass conversion efficiency (Omkar et al., 2005b) was calculated as the ratio of egg biomass (mg) laid to that of aphid prey biomass (mg) consumed. Consumption rate was calculated as the daily aphid biomass (mg) consumed by the females, whereas the conversion efficiency was calculated as the daily increase in biomass (mg) of females per aphid biomass (mg) consumed (modified after Lucas et al., 2004 and Dixon, 2000). To assess the reduction in biomass of different diets in both the experiments (consumption, developmental and reproductive attributes) in absence of a predator (control), measured amount of these diets (i.e. 25, 50 and 75 mg, respectively) were placed individually in Petri dishes, kept under similar abiotic conditions for 24 h and then weighed. The average loss, if any, in biomass of these diets, based on 5 replicates, was used in statistical analyses of the data. 2.3. Statistical analysis The data obtained in the study were checked for normal distribution using Kolmogorov–Smirnoff test for normality and Bartlett’s test for homogeneity of variances. All percent data were subjected to arcsine square root transformation prior to subjecting to further analysis. The experimental data on larval consumption attributes, i.e. consumption rate, conversion efficiency and relative growth rate, were individually subjected to three-way ANOVA followed by Tukey’s post hoc comparison of means at 5% level, where ladybird species, prey quantity, larval stages and their interaction (ladybird species prey quantity larval stages) were the independent factors, and larval consumption attributes were the dependent factors. However, the independent factors, viz. mean body mass of newly emerged adults and total developmental duration of immature stages per ladybird species were individually subjected to one-way ANOVA with prey quantity acting as the dependent factor, followed by Tukey’s post hoc comparison of means. Moreover, generation survival and sex ratio per ladybird species were individually subjected to v2-test, followed by Tukey’s post hoc comparison of means at 5% level. For both the ladybird species, the reproductive periods (viz. preoviposition, oviposition and post-oviposition periods), fecundity
and egg fertility of females, and female and male longevities were individually subjected to two-way ANOVA, followed by Tukey’s post hoc comparison of means, where ladybird species, prey quantity and their interaction (ladybird species prey quantity) were independent factors and reproductive periods, fecundity, egg fertility, and female and male longevities were dependent factors. Further, age-specific consumption rate, fecundity, egg fertility, body biomass and egg biomass conversion efficiencies per prey quantity per ladybird species were individually regressed against mean reproductive age, followed by two-way ANCOVA with ladybird species, prey quantity and their interaction (ladybird species prey quantity) as independent factors and age as a covariate. All statistical analyses were performed on MINITAB 16 (Minitab Inc., State College, PA, USA). 3. Results 3.1. Effect on predatory and developmental attributes Results of three-way ANOVA revealed significant influence of ladybird species (F = 45.65; P < 0.0001; df = 1, 239), prey quantity (F = 272.33; P < 0.0001; df = 2, 239) and larval stage (F = 137.65; P < 0.0001; df = 3, 239) on the consumption rate of larvae; but the effect of their interactions (Fladybird species prey quantity larval stage = 0.24; P = 0.964; df = 6, 239) on consumption rate was insignificant. The conversion efficiency and relative growth rate of larvae were significantly influenced by the prey quantity (F = 14.23; P < 0.0001; df = 2, 239 and F = 13.42; P < 0.0001; df = 2, 239, respectively), larval stage (F = 232.67; P < 0.0001; df = 3, 239 and F = 162.56; P < 0.0001; df = 3, 239, respectively) and the interaction between ladybird species, prey quantity and larval stage (F = 5.36; P < 0.0001; df = 6, 239 and F = 5.22; P < 0.0001; df = 6, 239, respectively). Although the relative growth rate significantly differed between ladybird species (F = 14.50; P < 0.0001; df = 1, 239), but the conversion efficiency did not (F = 1.67; P = 0.198; df = 1, 239). In both the ladybird species, larval consumption rate was highest on high prey biomass and lowest on low prey biomass. Also the larvae had higher relative growth rates on high prey biomass than on low prey biomass, but their conversion efficiencies were lower than the larvae reared on low prey biomass (Fig. 1). Amongst the larval stages of both the ladybird species, higher consumption rate was recorded for the fourth instars than the early (first, second and third) instars on the three prey conditions provided; whereas higher conversion efficiencies and relative growth rates were recorded for the early instars than the fourth instars. One-way ANOVA further revealed significant influence of prey quantity on the total developmental duration of immature stages and mean body mass of newly emerged adults. Also, the v2-values exemplified significant influence of prey quantity on generation survival and sex ratio. In both C. septempunctata and C. transversalis, the total developmental durations of immature stages were shortest on high prey biomass and longest on low prey biomass. Also the mean body mass of newly emerged adults, generation survival and sex ratio were highest on high prey biomass and lowest on low prey biomass (Table 1). In C. septempunctata and C. transversalis the apparent and real mortalities, k-values, MSR and IM values, and overall mortality prior to adult stage (kappa values) were lowest on high prey biomass and highest on low prey biomass. However, the survival rates were highest on high prey biomass and lowest on low prey biomass (Tables 2 and 3). 3.2. Effect on reproductive attributes In adult females, two-way ANCOVA revealed significant influence of the ladybird species and the prey quantity on consumption
39
M. Bista, Omkar / Biological Control 74 (2014) 36–44
Fig. 1. Conversion efficiency, relative growth rate and consumption rate of Coccinella septempunctata (C7) and Coccinella transversalis (Ct) larvae under the three different prey conditions (values are means ± SE; small and large letters represent comparison of means between larval stages per prey condition and among prey conditions per larval stage, respectively).
Table 1 Effects of quantity of prey on total developmental duration of immature stages, mean body mass of newly emerged adults, generation survival and sex ratio of Coccinella septempunctata (C7) and Coccinella transversalis (Ct) (n = 100 per ladybird species). Ladybird species
C7
Prey quantity
Low Medium High
One-way ANOVA
Ct
One-way ANOVA
Low Medium High
Total developmental duration (days)
Mean body mass of newly emerged adults
Generation survival
Sex ratio
17.73 ± 0.30a 25.43 ± 0.25b 26.07 ± 0.27c
0.26 ± 0.04a 0.44 ± 0.05b 0.46 ± 0.05b
0.46 ± 0.05a 0.60 ± 0.05b 0.63 ± 0.05b
F = 12.50 P < 0.0001 df = 2, 116
F = 294.81 P < 0.0001 df = 2, 87
v2 = 10.232 P = 0.006 df = 2
v2 = 6.694 P = 0.035 df = 2
14.00 ± 0.10c 12.22 ± 0.10b 11.11 ± 0.14a
18.82 ± 0.32a 21.70 ± 0.20b 24.50 ± 0.11c
12.38 ± 0.23a 16.17 ± 0.24b 17.96 ± 0.24c
0.25 ± 0.04a 0.45 ± 0.05b 0.54 ± 0.05b
0.45 ± 0.05a 0.62 ± 0.05b 0.64 ± 0.05b
F = 94.56 P < 0.0001 df = 2, 210
F = 15.51 P < 0.0001 df = 2, 122
F = 149.01 P < 0.0001 df = 2, 88
v2 = 18.173
v2 = 2.30 P = 0.012 df = 2
Females (mg)
Males (mg)
13.67 ± 0.16c 12.00 ± 0.17b 9.33 ± 0.05a
25.39 ± 0.18a 31.01 ± 0.37b 32.98 ± 0.45c
F = 100.38 P < 0.0001 df = 2, 203
P < 0.0001 df = 2
Values are means ± SE; F-values/v2-values are significant at P < 0.05. Small letters represent comparison of means among prey quantities per ladybird species.
rate (FANCOVA (Ladybird species Prey quantity) = 18.70; P < 0.0001; df = 2, 629) and the mean body mass (FANCOVA (Ladybird species Quantity) = 16.72; P < 0.0001; df = 2, 629). The influence was age dependent (FANCOVA (Age) = 587.40; P < 0.0001; df = 1, 629 and FANCOVA (Age) = 226.56; P < 0.0001; df = 1, 629, respectively). The aphid prey consumption by females initially increased at an early age, reached a peak at middle age and then declined at old age (plateau shaped). Mean body mass of adult females increased with age on the three diets. The values of consumption rates and mean body mass were highest on high prey biomass and lowest on low prey biomass (Fig. 2). Results revealed significant influence of ladybird species, prey quantity and their interaction on pre-oviposition period and female longevity. The post-oviposition period was not influenced by the prey quantity, although the effects of ladybird species and the interaction between ladybird species and prey quantity were significant. The oviposition period and fecundity were influenced by the prey quantity, but neither by the ladybird species nor by
the interaction between ladybird species and prey quantity. However, the egg fertility was significantly influenced by the ladybird species and prey quantity but not by their interaction. Moreover, the male longevity was not significantly influenced by the ladybird species, though the influence of prey quantity and the interaction between ladybird species and prey quantity was significant. On high prey biomass the pre-oviposition periods of both the ladybird species were shortest and their oviposition periods were longest. Also the females had highest fecundity and egg fertility; and males and females of both the ladybirds lived longest on high prey biomass (Table 4). Further, the age specific fecundity and egg fertility were not influenced by the ladybird species (FANCOVA (Ladybird species) = 1.97; P = 0.161; df = 1, 629 and FANCOVA (Ladybird species) = 0.01; P = 0.925; df = 1, 629, respectively) or the interaction between ladybird species and prey quantity (FANCOVA (Ladybird species Prey quantity) = 1.64; P = 0.195; df = 2, 629 and FANCOVA (Ladybird species Prey quantity) = 1.35; P = 0.260; df = 2, 629, respectively). However, the individual effect
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Table 2 Effect of prey quantity on mortality life-table of Coccinella septempunctata (n = 100). Prey quantity
Developmental stage (x)
No. of individuals entering stage x (lx)
No. of individuals dying within stage x (dx)
Apparent mortality (100qx)
Real mortality (100rx)
Survival rate (Sx)
kValue
MSR
IM
Low prey
Instars
First Second Third Fourth
100 86 76 68 64 60 56
14 10 8 4 4 4 Kappa = 0.252
14.00 11.63 10.53 5.88 6.25 6.67
14.00 10.00 8.00 4.00 4.00 4.00
0.86 0.88 0.89 0.94 0.94 0.93
0.066 0.054 0.048 0.026 0.028 0.030
0.14 0.12 0.11 0.06 0.06 0.07
7.84 6.51 5.89 3.29 3.50 3.73
First Second Third Fourth
100 90 85 82 78 76 73
10 5 3 4 2 3 Kappa = 0.137
10.00 5.56 3.53 4.88 2.56 3.95
10.00 5.00 3.00 4.00 2.00 3.00
0.90 0.94 0.96 0.95 0.97 0.96
0.046 0.025 0.016 0.022 0.011 0.017
0.10 0.06 0.04 0.05 0.03 0.04
7.30 4.06 2.58 3.56 1.87 2.88
First Second Third Fourth
100 92 88 84 80 77 75
8 4 4 4 3 2 Kappa = 0.125
8.00 4.35 4.55 4.76 3.75 2.60
8.00 4.00 4.00 4.00 3.00 2.00
0.92 0.96 0.95 0.95 0.96 0.97
0.036 0.019 0.020 0.021 0.017 0.011
0.08 0.04 0.05 0.05 0.04 0.03
6.00 3.26 3.41 3.57 2.81 1.95
Pre-pupa Pupa Adults Medium prey
Instars
Pre-pupa Pupa Adults High prey
Instars
Pre-pupa Pupa Adults
MSR and IM represent mortality-survivor ratio and indispensable mortality, respectively.
Table 3 Effect of prey quantity on mortality life-table of Coccinella transversalis (n = 100). Prey quantity
Developmental stage (x)
No. of individuals entering stage x (lx)
No. of individuals dying within stage x (dx)
Apparent mortality (100qx)
Real mortality (100rx)
Survival rate (Sx)
kValue
MSR
IM
Low prey
Instars
First Second Third Fourth
100 88 78 70 65 60 57
12 10 8 5 5 3 Kappa = 0.244
12.00 11.36 10.26 7.14 7.69 5.00
12.00 10.00 8.00 5.00 5.00 3.00
0.88 0.89 0.90 0.93 0.92 0.95
0.056 0.052 0.047 0.032 0.035 0.022
0.12 0.11 0.10 0.07 0.08 0.05
6.84 6.48 5.85 4.07 4.38 2.85
First Second Third Fourth
100 92 86 83 79 77 75
8 6 3 4 2 2 Kappa = 0.125
8.00 6.52 3.49 4.82 2.53 2.60
8.00 6.00 3.00 4.00 2.00 2.00
0.92 0.93 0.97 0.95 0.97 0.97
0.036 0.029 0.015 0.021 0.011 0.011
0.08 0.07 0.03 0.05 0.03 0.03
6.00 4.89 2.62 3.61 1.90 1.95
First Second Third Fourth
100 95 91 87 84 81 79
5 4 4 3 2 2 Kappa = 0.102
5.00 4.21 4.40 3.45 3.57 2.47
5.00 4.00 4.00 3.00 3.00 2.00
0.95 0.96 0.96 0.97 0.96 0.98
0.022 0.019 0.020 0.015 0.016 0.010
0.05 0.04 0.04 0.03 0.04 0.02
3.95 3.33 3.47 2.72 2.82 1.95
Pre-pupa Pupa Adults Medium prey
Instars
Pre-pupa Pupa Adults High prey
Instars
Pre-pupa Pupa Adults
MSR and IM represent mortality- survivor ratio and indispensable mortality, respectively.
of prey quantity (FANCOVA (Prey quantity) = 41.93; P < 0.0001; df = 2, 629 and FANCOVA (Prey quantity) = 24.71; P < 0.0001; df = 2, 629, respectively) was significant and was age dependent (FANCOVA (Age) = 167.81; P < 0.0001; df = 1, 629 and FANCOVA (Age) = 217.96; P < 0.0001; df = 1, 629, respectively). The fecundity increased with increase in adult age, reached a peak and thereafter declined with further advancement in age, i.e. a triangular fecundity trend, on different prey supply. The egg fertility also revealed similar trend. The maximum fecundity and egg fertility were obtained when the females of C. septempunctata (between 45–48 days on low prey biomass, 42–45 days on medium prey biomass and 39–42 days on high prey biomass) and C. transversalis (between 35–40 days on low prey
biomass, 28–31 days on medium prey biomass and 25–30 days on high prey biomass) were middle aged (Fig. 3). The body biomass conversion efficiency of adult females was significantly influenced by the ladybird species (FANCOVA (Ladybird species) = 5.05; P = 0.025; df = 1, 629) and the prey quantity (FANCOVA (Prey quantity) = 3.20; P = 0.041; df = 2, 629), but not by their interaction (FANCOVA (Ladybird species Prey quantity) = 2.12; P = 0.121; df = 2, 629). It was age dependent (FANCOVA (Age) = 95.22; P < 0.0001; df = 1, 629). However, the egg biomass conversion efficiency was influenced by the prey quantity (FANCOVA (Prey quantity) = 5.63; P = 0.004; df = 2, 629); but neither influenced by the ladybird species (FANCOVA (Ladybird species) = 0.29; P = 0.587; df = 1, 629) nor
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Fig. 2. Age specific consumption rate and mean body mass of Coccinella septempunctata (C7) and Coccinella transversalis (Ct) adult females under the three different prey conditions (r2-values significant at P < 0.05).
Table 4 Effect of quantity of prey on the reproductive attributes of Coccinella septempunctata (C7) and Coccinella transversalis (Ct) (n = 10 per ladybird species). Ladybird species
Prey quantity
Pre-oviposition period (days)
Oviposition period (days)
Post oviposition period (days)
Fecundity (No. of eggs)
Egg fertility (%)
Female longevity (days)
Male longevity (days)
C7
Low Medium High
19.00 ± 0.60c 12.50 ± 0.43b 11.30 ± 0.65a
40.30 ± 0.52a 52.70 ± 1.12b 54.50 ± 0.50c
10.40 ± 0.54a 11.90 ± 0.64a 11.80 ± 0.49a
784.90 ± 30.15a 1439.90 ± 44.20b 1546.60 ± 41.61c
81.23 ± 1.34a 87.17 ± 0.94b 89.17 ± 0.98c
69.70 ± 2.07a 77.10 ± 2.26b 77.60 ± 1.23b
64.90 ± 1.45a 70.50 ± 1.88ab 71.10 ± 1.46b
Ct
Low Medium High
9.20 ± 0.13c 7.00 ± 0.26b 6.40 ± 0.16a
38.50 ± 0.54a 52.70 ± 0.84b 55.10 ± 0.72c
11.10 ± 0.41a 10.10 ± 0.53a 8.80 ± 0.33a
794.60 ± 30.84a 1561.30 ± 44.91b 1604.10 ± 45.61b
82.72 ± 0.67a 89.87 ± 0.87b 90.82 ± 0.80b
58.80 ± 1.60a 69.80 ± 1.26b 70.30 ± 1.30b
56.20 ± 1.75a 64.20 ± 1.58b 65.80 ± 1.48b
Ladybird species
F = 380.16 P < 0.0001 df = 1, 59
F = 0.44 P = 0.511 df = 1, 59
F = 11.27 P = 0.001 df = 1, 59
F = 3.65 P = 0.061 df = 1, 59
F = 6.20 P = 0.016 df = 1, 59
F = 11.19 P = 0.001 df = 1, 59
F = 2.20 P = 0.144 df = 1, 59
Prey quantity
F = 88.13 P < 0.0001 df = 2, 59
F = 254.30 P < 0.0001 df = 2, 59
F = 1.01 P = 0.370 df = 2, 59
F = 231.57 P < 0.0001 df = 2, 59
F = 38.81 P < 0.0001 df = 2, 59
F = 444.41 P < 0.0001 df = 2, 59
F = 486.00 P < 0.0001 df = 2, 59
Interaction
F = 19.97 P < 0.0001 df = 2, 59
F = 1.42 P = 0.250 df = 2, 59
F = 7.16 P = 0.002 df = 2, 59
F = 0.97 P = 0.387 df = 2, 59
F = 0.21 P < 0.810 df = 2, 59
F = 38.71 P < 0.0001 df = 2, 59
F = 53.03 P < 0.0001 df = 2, 59
Values are means ± SE Small letters represent comparison of means among prey quantities within each ladybird species.
by their interaction (FANCOVA (Ladybird species Prey quantity) = 0.49; P = 0.611; df = 2, 629). It was also age dependent (FANCOVA (Age) = 195.05; P < 0.0001; df = 1, 629). The body biomass conversion efficiency was higher during pre- and post-oviposition periods in both the ladybirds on three different diets; being highest on high prey biomass and lowest on low prey biomass. In contrast, the egg biomass conversion efficiency was lower during pre- and post-
oviposition periods in both the ladybirds. It was highest on the high prey biomass and lowest on the low prey biomass (Fig. 4). 4. Discussion In the present study, larval stages of both C. septempunctata and C. transversalis had higher consumption rates and relative growth
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Fig. 3. Age specific fecundity and egg fertility of Coccinella septempunctata (C7) and Coccinella transversalis (Ct) adult females under the three different prey conditions (r2values significant at P < 0.05).
rates, but shorter developmental durations when fed on high prey biomass while the reverse was true on low prey biomass. It is assumed that when high prey biomass is available for feeding, the larvae consume maximum prey biomass to enhance their growth rates. Further, on account of their higher growth rates, they quickly acquire the threshold biomass necessary for pupation and complete their development earlier than the larvae feeding on low prey biomass. The present findings are in agreement with many earlier studies in ladybirds (Schuder et al., 2004; Agarwala et al., 2008; Atlihan and Guldal, 2009; Omkar et al., 2010; Maurice and Ashwani, 2011). Further, despite lower consumption rate, relative growth rate and prolonged developmental durations, the larvae of both the ladybirds have shown higher conversion efficiencies under low prey biomass condition in the present study. Probably, the slowing down of larval development and increase in conversion efficiency under low prey biomass condition are amongst the several mechanisms displayed by the larvae to compensate for a shortage of
food, as also reported earlier by Schuder et al. (2004) in the larvae of Adalia bipunctata L. Increased generation survival, higher sex ratio, emergence of heavier adults and decreased larval mortality on high prey biomass in the present study further reveal that when surplus prey is available, ladybirds possibly exploit the prey population maximally to increase their population and enhance their progeny fitness. Contrary to it, the availability of low prey biomass probably retards the population growth of ladybirds, increases their larval mortality and reduces their progeny fitness. Amongst the larval stages, a higher consumption rate of fourth instars over the early instars on the three prey conditions provided is possibly owing to their large size and increased energy requirements to fulfill their increased metabolic costs. In contrast, the higher conversion efficiencies and relative growth rates of early instars over the fourth instars may be attributed to their small size, low metabolic costs and low energy needs (Mishra et al., 2012).
M. Bista, Omkar / Biological Control 74 (2014) 36–44
43
Fig. 4. Age specific body biomass conversion efficiency and egg biomass conversion efficiency of Coccinella septempunctata (C7) and Coccinella transversalis (Ct) adult females under the three different prey conditions (r2-values significant at P < 0.05).
In the present study, adult females showed highest consumption rates, maximum mean body mass gain, shortest pre- and post-oviposition periods, longest oviposition periods and highest fecundity and egg fertility on high prey biomass. These may be owing to: (i) the large size of adults at emergence on high prey biomass (Boggs and Freeman, 2005; Agarwala et al., 2008) and their higher reproductive rates related with their large size (Salavert et al., 2011; Omkar and Afaq, 2013; Bista and Omkar, 2013), and (ii) the availability of surplus prey for consumption and to fulfill the high energy requirements associated with large size. The longer pre-oviposition and shorter oviposition periods under low prey biomass condition may be attributed to the late ripening of ovarioles due to poor availability of nutrients, as also reported earlier by Omkar and Pervez (2003) in Propylea dissecta (Mulsant) and Omkar et al. (2010) in Anegleis cardoni (Weise). Lower consumption rates, fecundity and egg fertility may be ascribed to the small size of emerging adults on low prey biomass. Under the three prey supply conditions, the prey consumption rates by adult females of C. septempunctata and C. transversalis initially increased with age, reached a peak and thereafter declined. This initial increase in consumption rate may be ascribed to their high energy requirements for gonadal development and sexual
maturity. The process of senescence is possibly responsible for decline in prey consumption by adult females at later age (Dixon and Agarwala, 2002). However, no decline in mean body mass of adult females under three prey supply conditions with increase in age supports the findings of Mishra et al. (2012) in ladybirds. Perhaps despite reduced prey consumption rates, older females use their entire nutrients in maintaining their body biomass once egg laying is ceased. Further, both the ladybirds exhibited a triangular fecundity and egg fertility function on the three prey biomasses. The oviposition in adult females occurred during earlier and later phases of middle age under high and low prey biomass conditions, respectively. The findings thus reveal that the middle aged individuals invest most of their energy in reproduction than young or old aged individuals, as also reported in earlier studies (Pandey and Omkar, 2013; Bista and Omkar, 2013). However, the investment is higher on high prey biomass than on low prey biomass. Higher body biomass conversion efficiency during pre- and post-oviposition periods, and higher egg biomass conversion efficiency during oviposition period on the three prey biomasses indicate that prior to egg laying or once the reproduction ceases, the ladybirds invest their energy for maintenance and survival,
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maturation of gonads and body mass gains. However, during reproductive period they possibly partition their energy on the production of eggs, self maintenance and survival, and the investment is higher when ladybirds are fed on high prey biomass. But under low prey biomass condition, they probably utilize less resources obtained from poor prey consumption to their self-maintenance and egg production, as also reported by Legaspi and Legaspi (1998), Omkar and Pervez (2003) and Evans (2003). In brief, the consumption, developmental and reproductive attributes of C. septempunctata and C. transversalis change in response to aphid prey availability. On high prey biomass the larvae have high consumption and growth rates, fast development and low mortality, while the emerging adults are large in size, consume more aphid prey and utilize the prey biomass maximally on the production of eggs, self maintenance and survival. In contrast, the availability of low aphid prey biomass reduces the chances of larval survival, and those that emerged as adults are small in size, have poor prey consumption rates, low fecundity, egg fertility and short life span. Further, age-based consumption and reproductive attributes reveal that middle aged ladybirds reared on high prey biomass may suppress the pest population better than those reared on low/medium prey biomass. References Agarwala, B.K., Bardhanroy, P., Yasuda, H., Takizawa, T., 2001. Prey consumption and oviposition of the aphidophagous predator Menochilus sexmaculatus (Coleoptera: Coccinellidae) in relation to prey density and adult size. Environ. Entomol. 30, 1182–1187. Agarwala, B.K., Singh, T.K., Lokeshwari, R.K., Sharmila, M., 2009. Functional response and reproductive attributes of the aphidophagous ladybird beetle, Harmonia dimidiate (F.) in oak trees of sericultural importance. J. Asia Pac. Entomol. 12, 179–182. Agarwala, B.K., Yasuda, H., Sato, S., 2008. Life history response of a predatory ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) to food stress. Appl. Entomol. Zool. 43 (2), 183–189. Atlihan, R., Guldal, H., 2009. Prey density-dependent feeding activity and life history of Scymnus subvillosus. Phytoparasitica 37, 35–41. Bista, M., Omkar, 2013. Effects of body size and prey quality on reproductive attributes of two aphidophagous ladybird beetles (Coleoptera: Coccinellidae). Can. Entomol. 145, 566–576. Boggs, C.L., Freeman, K.D., 2005. Larval food limitation in butterflies: effects on adult resource allocation and fitness. Oecologia 144, 353–361. Bonduriansky, R.A., Head, M., 2007. Maternal and paternal condition effects on offspring phenotype in Telostylinus angusticollis (Diptera: Neriidae). J. Evol. Biol. 20, 2379–2388. Dixon, A.F.G., 2000. Insect Predator-Prey Dynamics: Ladybird Beetles and Biological Control. Cambridge University Press, Cambridge, pp. 257. Dixon, A.F.G., Agarwala, B.K., 2002. Triangular fecundity function and ageing in ladybird beetles. Ecol. Entomol. 27, 433–440. Dmitriew, C., Rowe, L., 2011. The effects of larval nutrition on reproductive performance in a food-limited adult environment. PLoS ONE 6 (3), e17399. http://dx.doi.org/10.1371/journal.pone.001 7399. Evans, E.W., 2003. Searching and reproductive behaviour of female aphidophagous ladybirds (Coleoptera: Coccinellidae): a review. Eur. J. Entomol. 100, 1–10. Harcourt, D.G., 1969. The development and use of life tables in the study of natural insect populations. Annu. Rev. Entomol. 14, 175–196.
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