Introduction
The potato aphid, Macrosiphum euphorbiae (Thomas) (Hemiptera: Aphididae) is a sap sucking pest that infests more than 200 species of plants in 20 distinct families, including herbaceous crops, solanaceous plants, and ornamentals (Venkatesh et al., Reference Venkatesh, Rajna, Suroshe, Joshi and Chander2024). It is also known to infest tomato (Aragon et al. Reference Aragon, Cantor and Rodriguez2007; Machado-Assefh et al., Reference Machado-Assefh, Said-Adamo, Cortéz, Gialdi, Isasmendi, Ortego and Alvarez2023) and can cause crop losses of approximately one ton per acre (Zalom, Reference Zalom2007). Beyond causing direct damage to crop, M. euphorbiae also serves as a vector for numerous plant viruses (Radcliffe and Ragsdale, Reference Radcliffe and Ragsdale2002; Teixeira et al., Reference Teixeira, Sela, Atamian, Bao, Chaudhary, Macwilliams, He, Mantelin, Girke and Kaloshiani2018; Sridhar et al., Reference Sridhar, Kumari, Venkateswarlu, Bhatnagar, Malik, Sharma and Chakrabarti2020; Venkatesh et al., Reference Venkatesh, Rajna, Suroshe, Joshi and Chander2024). Aphids have a remarkable ability to reproduce rapidly and complete their development in a short time, causing their populations to increase quickly. This trait makes them major pests in various crops, whether grown in open fields or under protected conditions. Farmers primarily rely on synthetic chemical insecticides, which can result in serious environmental issues such as pest resurgence, secondary pest outbreaks, and insecticide residues (Nawaz et al., Reference Nawaz, Sufyan, Gogi and Javed2019). To mitigate these effects, enhancing the role of natural enemies, combined with other eco-friendly management practices, offers a sustainable alternative. Biological control using natural enemies is a widely accepted, environmentally sustainable and cost-effective strategy for protecting crops from insect-pests (Sethuraman et al., Reference Sethuraman, Janzen, Weisrock and Obrycki2020). Syrphid flies (Diptera: Syrphidae) are important predators and pollinators, playing a dual role in agriculture. While their adults act as effective pollinators for numerous crops, their larvae exhibit predatory behaviour against aphids (Dunn et al., Reference Dunn, Lequerica, Reid and Latty2020; Rodríguez-Gasol et al., Reference Rodríguez-Gasol, Alins, Veronesi and Wratten2020). These flies are distributed throughout the world and consist of three subfamilies, 180 genera, and around 6,000 described species (Rojo et al., Reference Rojo, Gilbert, Marcos-García, Nieto and Durante2003). The most important syrphid predators of M. euphorbiae are Episyrphus balteatus DeGeer, Episyrphus viridaureus (Weidemann), Sphaerophoria indiana Bigot and Melanostoma spp. Among them, E. viridaureus (Diptera: Syrphidae) has been reported as a major predator of M. euphorbiae on tomato crop in the mid-hills of Himachal Pradesh (Sharma, Reference Sharma2024). It is a yellow-orange fly with black bands on its abdomen, distinguished by two stripes on the second and third sterna (Palial, Reference Palial2023). To enhance the effectiveness of syrphids as biological control predators, their fitness is assessed using age-specific fertility tables, which provides key biological data on survival rates, life expectancy, and reproductive value at different life stages (Tazerouni et al., Reference Tazerouni, Talebi, Fathipour and Soutbaf2016), illustrating the reproductive potential of female insects over time (Chi, Reference Chi1988). These fertility table and population growth parameters are vital for developing efficient pest management strategies, as they help identify the most suitable biocontrol agents. (Herrero et al., Reference Herrero, Dami, Fogliata, Casmuz, Gomez, Gastaminza and Murua2018). The larvae of approximately one-third of all syrphid fly species are voracious feeders on aphids (Dib et al., Reference Dib, Simon, Sauphanor and Capowiez2010; Dunn et al., Reference Dunn, Lequerica, Reid and Latty2020). The efficacy of a biocontrol agent is closely linked to its consumption rate or feeding potential (Sengonca et al., Reference Sengonca, Al-Zyoud and Blaeser2005). Understanding the effects of prey density on predator performance or its functional response is crucial for analysing predator–prey interactions (Gitonga et al., Reference Gitonga, Overholt, Lohr, Magambo and Mueke2002). Functional response curves can show an increasing linear pattern (Type I), a slowing or decelerating curve (Type II), or a sigmoid pattern (Type III). The functional response of a predator is crucial in regulating predator–prey dynamics, representing how the predator’s consumption rate changes with prey density and indicating its effectiveness in controlling the population of prey species (Murdoch and Oaten, Reference Murdoch and Oaten1975). Understanding different parameters like population growth parameters, predatory efficacy, and functional response of an insect predator are essential for assessing its effectiveness as a biocontrol agent and for optimising its use in pest management strategies. However, the study focusing on these parameters for E. viridaureus in relation to M. euphorbiae is scarce. Hence, this study seeks to address this gap by examining the biological attributes, predatory potential, and functional response of E. viridaureus on M. euphorbiae.
Material and methods
The populations of M. euphorbiae were reared on tomato plants both in field conditions and in the Biological Control Laboratory of the Department of Entomology at Dr. Yashwant Singh Parmar University of Horticulture and Forestry, Nauni, Solan, HP, India (30.85°N; 77.16°E). E. viridaureus specimens were collected from the same fields using a sweep net and were reared for two generations on M. euphorbiae, which were raised on tomato plants under controlled conditions: 14:10 h (Light: dark) photoperiod, 25 ± 1°C temperature, and 70 ± 5% relative humidity. After the first generation was completed, the progeny was used for conducting various experiments.
Developmental biology and population growth parameters
Freshly laid eggs of E. viridaureus were collected from the culture of syrphid maintained under controlled conditions and was placed singly in Petri plates of 9 cm diameter and 1.5 cm height. From those eggs, their hatching period was monitored at 24 h intervals. After hatching, larvae were fed a daily count of aphids until pupation, with each developmental stage being recorded. Pairs of adult syrphids that emerged were isolated in glass chimneys for mating and honey solution (10%) along with fresh bloom of tomato (pollen source) was provided to them. The tomato leaflet dipped in a small glass vial containing water, infested with M. euphorbiae was provided for egg laying. After every 24 h, the fecundity was recorded and the leaflet was changed until the adults’ mortality. The experiment included twenty replications. Key developmental indicators such as the total pre-oviposition period (TPOP), adult pre-oviposition period (APOP), and fecundity rate were assessed using age-stage, two-sex life table methodology outlined by Chi (Reference Chi1988), using TWOSEX MS-Chart computer program (Chi, Reference Chi2018). All population growth parameters were computed using the formulae provided below:
sxj = It indicates the likelihood that a newly emerged egg will survive to reach age x and stage j.
fxj = It indicates the number of eggs that hatch from an adult female at age x:
\begin{equation*}l_x=\;\sum_{j=1}^m\;s_{xj}\end{equation*}
\begin{equation*}m_x=\;\frac{\sum_{j=1}^m\;s_{xj\;}\;f_{xj}}{l_x}\end{equation*}Various growth parameters were derived using the above mentioned variables:
1. Net Reproductive rate (R 0): This metric quantifies the total egg production by a female throughout her lifespan. It was determined using the following formula:
\begin{equation*}R_0=\sum_{x=0}^\infty\sum_{j=1}^m\;s_{xj\;}\;f_{xj}\end{equation*}
\begin{equation*}m_x=\;{\textstyle\sum_{x=0}^\infty}\;l_x\end{equation*}where m x: age-specific fecundity, which is the average number of offspring produced by an individual of age x.
2. Gross reproductive rate (GRR): It refers to the total number of female offspring produced by a female over her entire lifespan. It is determined by calculating the sum of female eggs laid by the adult female throughout her life.
\begin{equation*}GRR=\;\sum_{x=0}^\infty m_x\end{equation*}3. True intrinsic rate of increase (r): It is the population’s natural growth rate under optimal environmental conditions with no limitations on resources like food and space. It reflects the potential expansion of the population when the living conditions are ideal.
4. True generation time (T): It represents the average time interval between the birth of parents and birth of their offspring. This metric is determined by the calculation of mean time span separating the two generations.
\begin{equation*}\text{T}=\frac{\ln\,R_0}r\end{equation*}5. Finite rate of natural increase (
$\lambda $): It measures how frequently a population grows within a defined time period. This rate is determined by evaluating the population’s growth over that specific interval.
\begin{equation*}\lambda=e^r\end{equation*}6. Doubling time (DT): It indicates the time period needed for a population to increase twice its original size.
\begin{equation*}\text{DT}=\frac{\ln\,2}r\end{equation*}7. Reproductive value (vxj): It represents the impact an individual of age x and stage j has on the future growth of the population. It quantifies the potential contribution of an individual at a specific age and developmental stage to future population dynamics.
\begin{equation*}v_{xj}=\;\frac{e^{-r(x+1)}}{s_{xj}}\sum_{i=x}^\infty\;e^{-r(i+1)}\;\sum_{y=j}^ms'_{iy\;}f_{iy}\\\end{equation*}8. Age-stage specific life expectancy (exj): It is the expected lifespan or duration an individual at age x and stage j is predicted to live. It was calculated as:
\begin{equation*}e_{xj}=\sum_{i=x}^\infty\overset m{\underset{y=j}{\sum s'_{iy}}}\end{equation*}
Predatory potential and host-kill parameters
The predatory efficiency of the first, second, and third larval instars of E. viridaureus were evaluated against M. euphorbiae. Daily survival and prey consumption were meticulously recorded for each instar, using twenty replicates to ensure reliable data. The analysis was done by a software, CONSUME-MS Chart (Chi, Reference Chi2020), and predator’s host-kill parameters were computed according to the methods outlined by Van Lenteren et al. (Reference Van Lenteren, Bueno, Burgio, Lanzoni, Montes, Silva, de Jong and Hemerik2019).
cxj = average prey intake or consumption rate of an individual at a specific age (x) and developmental stage (j).
sxj = the likelihood that a newly deposited egg will successfully develop to age x and reach developmental stage j.
1. Age-specific predation rate (kx): It refers to the count of prey killed or eliminated by a predator at age x. It was determined as
\begin{equation*}
k_x = \frac{\sum_{j=1}^{\beta} s_{xj} c_{xj}}{\sum_{j=1}^{\beta} s_{xj}}
\end{equation*}2. Age-specific net predation rate (qx): It represents the proportion of individuals that are preyed on at age x, accounting for the age specific survival rate (lx), which indicates the number of individuals that reach age x:
\begin{equation*}{q_x} = {l_x}{k_x}.\end{equation*}3. Net consumption rate (C 0): It represents the total number of hosts eliminated or killed by a predator from age x onward:
\begin{equation*}
C_0 = \sum_{x=0}^{\infty} \sum_{j=1}^{\infty} s_{xj} c_{xj}
\end{equation*}4. Transformation rate (Qp): This rate indicates how many prey individuals a predator must consume to produce one offspring:
\begin{equation*}{Q_{\text{p}}} = \frac{{{C_0}}}{{{R_0}}}.\end{equation*}5. Stable host-kill rate (
$\psi$): It reflects the percentage of individuals at age x and stage j within a stable age distribution (axj):
\begin{equation*}
\Psi = \sum_{x=0}^{\infty} \sum_{j=1}^{\beta} a_{xj} c_{xj}
\end{equation*}6. Finite host-kill rate (ω): To assess the host-killing capability, finite host-kill rate (ω) was determined by the following method:
\begin{equation*}{\omega } = {{ \lambda }}\Psi \end{equation*}
Functional response of E. viridaureus
To study the functional response, different densities of M. euphorbiae, i.e. 3, 5, 10, 15, 20, 25; 5, 10, 15, 20, 25, 30 and 10, 20, 30, 40, 50, 60 were provided to first, second and third larval instar of E. viridaureus. The aphids were housed in 9 cm diameter and 1.5 cm height Petri dishes with tomato leaflets on moist blotting paper, with a controlled environment. Each prey density level was tested in ten separate trials, with the number of aphids eaten recorded after 24 hours. To generate the functional response curve for each larval stage of E. viridaureus, a logistic regression analysis was used to relate the fraction of aphids consumed to the varying prey densities, following this equation:
\begin{equation*}\frac{{{N_a}}}{N} = \frac{{\exp { }\left( {{p_0} + {p_1}{N_0} + {p_2}N_0^2 + {p_3}N_0^3} \right)}}{{1 + \exp { }\left( {{p_0} + {p_1}{N_0} + {p_2}N_0^2 + {p_3}N_0^3} \right)}}\end{equation*}where, Na: count of prey consumed or eaten; N: initial count of prey; p0: intercept; p1: linear coefficient; p2: quadratic coefficient; p3: cubic coefficient.
Roger’s random predator equation (Rogers et al., Reference Rogers, Jackson, Eikenbary and Starks1972) was employed to determine the parameters of functional response according to the functional response type as follows:
\begin{equation*}{N_a} = N\left\{ {1{\text{ }} - {\text{ }}exp{\text{ }}\left[ {a\left( {{T_h}{N_a} - T} \right)} \right]} \right\}{\text{ }}\left( {type{\text{ }}II} \right)\end{equation*}where, Na = number of prey consumed per predator; N = prey density provided; T = length of the experiment (24 h); Th = handling time; a = predation rate coefficient or predator attack rate.
Additionally, parameters such as the attack rate per unit handling time (a/Th) and theoretical maximum predation rate, K = T/Th were computed.
Statistical analysis
Biological and population growth parameters were evaluated with the help of TWOSEX-MS Chart. To ensure the result consistency, the mean values and standard error of the population were derived through the bootstrap method comprising 100,000 replications (Efron and Tibshirani, Reference Efron and Tibshirani1993). Parameters related to predation rate and host-killing for E. viridaureus were determined through CONSUME-MS Chart (Chi, Reference Chi2020). Functional response regression equation was generated with SPSS 2020, and additional functional response parameters were calculated in MS-Excel.
Results
Developmental biology of E. viridaureus on M. euphorbiae
The developmental period of different stages of E. viridaureus was observed on M. euphorbiae which revealed that the mean egg period was 3.00 days whereas the mean larval period for first (L1), second (L2) and third instar (L3) was 2.67, 3.62, and 4.69 days, respectively (Table 1). The pupal period was observed to be 6.62 days whereas the other biological parameters like APOP, oviposition period and TPOP were recorded as 2.71, 6.14, and 23.14 days, respectively. The adult female lived for 10.43 days whereas adult male lived for 8.78 days. The total pre-adult period was recorded as 20.62 days.
Developmental biology of E. viridaureus on M. euphorbiae on tomato
Population growth parameters of E. viridaureus on M. euphorbiae
The population growth parameters of the syrphid, E. viridaureus on M. euphorbiae were assessed by constructing fertility tables based on the critical information of life cycle of E. viridaureus in relation to M. euphorbiae.
Fertility table of E. viridaureus on M. euphorbiae
Age specific fecundity
Egg laying by female adult of E. viridaureus began on the 22nd day of pivotal age and continued until the 30th day with peak fecundity occurring on the 24th day. The initial age specific fecundity (mx) was 1.37 on the first day of oviposition (22nd day) whereas the maximum age specific fecundity was 4.12 eggs on the 24th day. The age-specific fecundity (mx) dropped to zero by the 31st day of pivotal age. The age-stage-specific fecundity (fx) followed a similar trend as mx, with the highest value of 9.43 eggs recorded on the 24th day. The age-specific maternity (lxmx) also peaked on the 24th day, reaching a value of 3.30. (Fig. 1).
Age specific survival rate l (x), female age-specific fecundity f(x), age specific fecundity m(x) and age-specific maternity l(x)m(x) of E. viridaureus on M. euphorbiae.
Age specific survival rate
The survival rate (lx) of E. viridaureus was 100 per cent up to the 4th day and then exhibited a decreasing trend with increasing age. The survival rate (lx) reduced from 90 per cent to 15 per cent from 5th day to 31st day. For the pupal stage, the survival rate remained constant (0.80) from 15th day to 18th day of pivotal age. Similarly, for female and male adults, the survival rate was constant from 22nd day to 28th day for female (0.35) and 22nd to 27th day for male (0.45), respectively (Fig. 2). Also, the peak survival rate in the pre-adult period (egg (1.00), larva (1.00), pupa (0.80)) was more as compared to adult period (male (0.45) and female (0.45) (Fig. 2).
Age-stage specific survival rate (sxj) of E. viridaureus on M. euphorbiae.
Age specific life expectancy
The age-stage specific life expectancy of E. viridaureus decreased with increasing age. It was recorded peaking at the time of birth i.e. 25.40 days (Fig. 3). In the larval stage, the lowest and highest age-stage life expectancy was 16.19 and 22.67 days on 14th and 5th day of pivotal age whereas in the pupal stage, the age-stage specific life expectancy varied between 9.26 and 17.19 days which was more than the adult stage. For male and female adults, the peak age-stage life expectancy was 8.67 days on the 21st day and 11.86 days on the 19th day, respectively (Fig. 3).
Age-stage life expectancy (exj) of E. viridaureus on M. euphorbiae.
Age specific reproductive value
Following the emergence of E. viridaureus, the female age-stage specific reproductive value (vxj increased gradually to 23.13 on the 19th day and reached a maximum of 31.66 on the 22nd and 23rd days of pivotal age (Fig. 4).
Age-stage specific reproductive value (vxj) of E. viridaureus on M. euphorbiae.
Population growth parameters of E. viridaureus on M. euphorbiae
The population growth parameters of E. viridaureus were assessed through its interaction with M. euphorbiae (Table 2). The GRR and net reproductive rate (R₀) were 19.18 and 14.95 offspring per individual, respectively. The intrinsic rate of increase (r) was 0.103 offspring per individual per day, and the finite rate of increase (λ) was 1.108 per day. The true generation time (T) was 25.87 days, and the DT, or the time required for the population to double, was 7.14 days (Table 2).
Population growth parameters of E. viridaureus against M. euphorbiae on tomato
Predatory potential and host-kill parameters of E. viridaureus on M. euphorbiae
Consumption patterns of E. viridaureus increased as larvae progressed through their stages. The first instar larvae (L1) consumed 5.61 aphids daily and a total of 14.55 aphids. In contrast, second instar larvae (L2) had a daily consumption of 24.18 aphids and a total consumption of 85.11 aphids. The third instar larvae (L3) were the most voracious, with daily and total consumption rates of 49.95 and 232.69 aphids, respectively (Table 3).
Predatory potential of E. viridaureous on the potato aphid, M. euphorbiae
The emergence of first larval instar of E. viridaureus began on the 3rd day of pivotal age, with survival extending through the 30th day. The age specific predation rate (kx) commenced at 2.85 aphids per day on the 3rd day and showed a steady increase until peaking on the 12th day of pivotal age, after which it declined and dropped to zero by the 15th day (Fig. 5). Both age specific predation rate (kx) and age specific net predation rate (qx) reached their maximum on the 12th day of pivotal age (kx: 56.81 aphids per day; qx: 45.45 aphids per day) (Fig. 5). The host-kill parameters for E. viridaureus were measured as follows: net predation rate (C0) at 277.30, transformation rate (Qp) at 20.65, stable host-kill rate (
$\psi$) at 11.85 and finite host-kill rate (ω) at 13.14 (Table 4).
Age specific predation rate (kx), net age specific predation rate (qx), and cumulative predation rate (C 0) of E. viridaureus on M. euphorbiae.
Host- Kill parameters of E. viridaureus on the potato aphid, M. euphorbiae
Functional response of E. viridaureus on M. euphorbiae
A logistic regression analysis was conducted to examine the relationship between aphid consumption (Na) and the prey density provided (N). The analysis identified a statistically significant linear coefficient (P1), suggesting a functional response of type-II, throughout all the three larval stages of E. viridaureus (first instar: P1 = − 1.563, t = − 4.620, p = < 0.001; second instar: P1 = − 1.995, t = − 20.663, p = < 0.001; third instar: P1 = − 0.470, t = − 3.194, p = 0.002) (Table 5). All three larval instars of E. viridaureus consumed a comparable number of aphids at higher prey densities, achieving satiety (Fig. 6). The consumption of aphids by the larval instars of E. viridaureus varied significantly with prey density: first instar (F = 59.079; df = 5.54; p < 0.001), second instar (F = 127.793; df = 5.54; p < 0.001) and third instar (F = 141.826; df = 5.54; p < 0.001).
Functional response of E. viridaureus on M. euphorbiae over a period of 24 h.
Parameters of Polynomial regression equation to determine the type of functional response of different instars of E. viridaureus on different densities of M. euphorbiae
Analysis of functional response parameters were also calculated which revealed that the coefficient of attack rate (a) increased (first instar: 0.049 h−1; second instar: 0.339 h−1; third instar: 0.342 h−1) while handling time decreased (first instar: 3.996 h; second instar: 2.841 h; third instar: 0.540 h) with the development of larval stage (Table 6).
Functional response parameters of different stages of E. viridaureus to potato aphid, M. euphorbiae
*Values superscripted by different letters within the column differ significantly with each other (p ≤ 0.05).
Discussion
The present study was focused to study the developmental biology, population growth parameters, predatory efficiency and functional response of E. viridaureus on potato aphid, M. euphorbiae infesting tomato. Notably, this research represents the first detailed study of its kind on this aphid species. In the mid-hills of Himachal Pradesh, M. euphorbiae is one of the damaging aphid species which infests tomato and other solanaceous crops throughout their growing period. E. viridaureus was found to complete its biology on M. euphorbiae with the pre-adult period of 20.62 days. The total larval developmental period was 10.98 days out of which the developmental period for first, second and third instar was 2.67, 3.62, and 4.69 days, respectively. Similarly in findings of Singh et al. (Reference Singh, Thakur, Sharma, Sharma and Nayak2020) and Jalilian (Reference Jalilian2015), larval period of 13.70 and 11.90 days was recorded for E. balteatus on different aphids, viz., Brevicoryne brassicae (Hemiptera: Aphididae) and Aphis pomi (Hemiptera: Aphididae). The same syrphid species, viz., E. viridaureus completed its larval period in 22.00 days on another aphid, Lipaphis erysimi (Hemiptera: Aphididae) which is much higher than our findings (Manpoong et al., Reference Manpoong, Firake, Behere and Rajesh2016). This difference in the larval developmental period may have occurred due to various factors such as role of host plants or nutritional aspect of the offered prey species (Arcaya et al., Reference Arcaya, Pérez-Bañón, Mengual, Zubcoff-Vallejo and Rojo2017; Gilbert, Reference Gilbert2005; Omkar, Reference Omkar2003). Focusing on E. viridaureus, which began laying eggs on the 22nd day and reached peak egg production on the 24th day in our study, the age-specific maternity (mx) was recorded as 1.37 and 4.12 eggs per day on the 22nd and 24th day of pivotal age. The age-stage fecundity (fx) varied from 0.50 on the 30th day to a maximum of 9.43 eggs on the 24th day. The survival rate (lx) of E. viridaureus showed a significant decrease with increasing age. The survival rate (lx) reduced from 90 per cent to 15 per cent from 5th to 31st day of pivotal age. Also, the survival rate exhibited a declining trend as the larvae progressed through successive stages, with overlapping curves observed during the various developmental phases of the syrphid. This intersection or overlap in age-stage specific survival rates may be attributed to the varying developmental rates across different stages such as egg, larva, and pupa (Liu et al., Reference Liu, Cui, Gao, Wang, Cheng and Liu2005; Arcaya et al., Reference Arcaya, Pérez-Bañón, Mengual, Zubcoff-Vallejo and Rojo2017; Palial et al., Reference Palial, Verma, Sharma, Chandel, Kumar, Gupta and Sharma2022). The age-stage life expectancy in our findings was higher in females than males in E. viridaureus which is supported by Palial et al. (Reference Palial, Verma, Sharma, Chandel, Kumar, Gupta and Sharma2022). They also reported higher age-stage life expectancy in females of Scaeva pyrastri (Diptera: Syrphidae) against B. brassicae. Our study recorded the intrinsic rate of increase (r) at 0.103 and the finite rate of increase (λ) at 1.108. Similarly, Campoy et al. (Reference Campoy, Sáez, Pérez‐Bañón and Rojo2020) observed comparable rates while assessing population parameters of the hoverflies Eristalis tenax (Diptera: Syrphidae) (r = 0.05, λ = 1.05) and Eristalinus aeneus (Diptera: Syrphidae) (r = 0.09, λ = 1.09). This study found the GRR, net reproductive rate (R₀), and DT of E. viridaureus to be 19.18, 14.95, and 7.14 days, respectively. These findings are in line with those reported by Palial et al. (Reference Palial, Verma, Sharma, Chandel, Kumar, Gupta and Sharma2022), who examined S. pyrastri on B. brassicae and noted GRR, R₀, and DT values of 18.01, 15.10, and 7.37 days, respectively. In our study, the larvae of E. viridaureus consumed nymphs of M. euphorbiae efficiently and their consumption exhibited an increasing trend as the subsequent larval stage advanced. The consumption by third instar larva (daily consumption: 49.95 aphids; total consumption: 232.69 aphids) was much higher as compared to first (daily consumption: 5.61 aphids; total consumption: 14.55 aphids) and second instar larva (daily consumption: 24.18 aphids; total consumption: 85.11 aphids). This is in corroboration with the observations made by Manpoong et al. (Reference Manpoong, Firake, Behere and Rajesh2016), who found that third instar larvae exhibited the highest feeding efficiency against L. erysimi, with a total intake of 227.67 aphids. However, this study by Manpoong et al. (Reference Manpoong, Firake, Behere and Rajesh2016) revealed that the lifetime consumption of E. viridaureus on L. erysimi was comparatively higher (416.67 aphids) than our study (332.35 aphids). The variations in the consumption may be due to several factors like test environment (Farhadi et al., Reference Farhadi, Allahyari and Juliano2010), suitability of the offered prey (Shah and Khan, Reference Shah and Khan2014), size of predator and prey (Putra and Yasuda, Reference Putra and Yasuda2006) and mobility of prey (Dixon, Reference Dixon2000). In agreement with our study, Devjani and Singh (Reference Devjani, Singh and Goel2006) also reported the highest feeding efficiency in the third instar larvae of E. balteatus (215 aphids) and I. scutellaris (268.20 aphids). This is in alignment with Singh et al. (Reference Singh, Thakur, Sharma, Sharma and Nayak2020), who noted that the third instar larvae of Eupeodes frequens (Diptera: Syrphidae) and E. balteatus consumed 184.4 and 237.3 aphids, respectively. The age specific net predation rate (qx) and age specific predation rate (kx) showed an upward trend with age, reaching their highest values on the 12th day. Other host-kill parameters like net predation rate (C 0), finite host-kill rate (ω) and stable host-kill rate (ψ) were recorded as 277.30, 13.14, and 11.85. Hence, the study pertaining to the biological parameters and predatory potential of E. viridaureus suggests that M. euphorbiae is an appropriate prey species for the former.
The functional response of a predator illustrates how its rate of prey capture and consumption varies with changes in prey density. Present study indicated that at higher prey densities for all three larval stages, the consumption by E. viridaureus decreased and was at par with each other in terms of functional response. This reduction in consumption is likely due to the predator reaching satiation at increased prey densities. (Mills, Reference Mills1982). In this study, all three larval stages of E. viridaureus exhibited a type-II functional response when exposed to different densities of M. euphorbiae. In alignment with our study, a type-II functional response has been observed by other researchers in a related species, E. balteatus (Jalilian et al., Reference Jalilian, Fathipour, Talebi and Sedaratian2011; Amiri-Jami and Sadeghi-Namagh, Reference Amiri-Jami and Sadeghi-Namagh2014). However, Putra and Yasuda (Reference Putra and Yasuda2006) observed contrasting results, reporting a type-II functional response in early instars but a linear (type-I) response in the third larval instars of E. balteatus and E. corollae, likely due to the larger size of the third instar larvae. In contrast with the present findings, but involving different prey and predators, Khatua et al. (Reference Khatua, Mohapatra, Nayak and Dilbyarani2020) documented a type-III response in Eumerus albifrons against A. craccivora. In other study, Sobhani et al. (Reference Sobhani, Madadi and Gharali2013) observed that third instars of E. balteatus exhibited a type-III functional response when feeding on Aphis gossypii. In a similar vein, Tenhumberg (Reference Tenhumberg1995) found a type-III functional response in E. balteatus preying on Metopolophium dirhodum (Hemiptera: Aphididae) and Sitobion avenae (Hemiptera: Aphididae). The variations in the functional response types in different studies may be attributed to several factors like ratio of predator to prey body size (Kalinkat et al., Reference Kalinkat, Schneider, Digel, Guill, Rall and Brose2013), experimental arena (Hemerik and Yano, Reference Hemerik and Yano2011), size of prey (Streams, Reference Streams1994), appetite or size of predator (Putra and Yasuda, Reference Putra and Yasuda2006; Varshney et al., Reference Varshney, Budhlakoti and Ballal2018), and temperature and humidity of the test environment (Ho and Jun, Reference Ho and Jun2004). The attainment of type-II functional response in E. viridaureus against M. euphorbiae may be attributed to the use of small arena such as Petri dishes, which may not accurately simulate the natural interactions between prey and predator, particularly at low prey densities (Van Lenteren and Baker, Reference Van Lenteren and Baker1976). Functional response parameters, such as coefficient of attack rate and handling time reflect the effectiveness of predation across the developmental stages of predator. In E. viridaureus, the attack rate (a) increased with each advancing larval stage, while handling time (T h) decreased. The third instar demonstrated the highest attack rate (0.342 h−1) and the shortest handling time (0.540 h), outperforming the earlier instars. This trend is attributed to the larger size of third instar, which has higher nutritional demands compared to the initial larval stages (Hodek and Honek, Reference Hodek and Honek1996). Additionally, the larger larval instars demonstrate greater mobility compared to the smaller instars, resulting in a higher attack rate and allowing them to subdue and consume their prey more efficiently. In our study, the coefficient of attack rate (a) was comparable between the second and third instar (second instar: 0.339 h−1; third instar: 0.342 h−1) but showed significant difference between the first and second instar (first instar: 0.049 h−1; second instar: 0.339 h−1), as well as between the first and third instar (first instar: 0.049 h−1; third instar: 0.342 h−1). Pervez and Omkar (Reference Pervez and Omkar2004) stated that such differences in functional response parameters can be attributed to variations in few physiological factors, like body size and digestive efficiency of the predator. Handling time serves as a crucial indicator of predation efficiency and rate of consumption, encompassing the entire process of capturing, killing, subduing, and digesting prey (Veeravel and Baskaran, Reference Veeravel and Baskaran1997). It also influences the type of functional response, with shorter handling times leading to a quicker attainment of the curve’s asymptote (Nordlund and Morrison, Reference Nordlund and Morrison1990). A shorter handing time highlights a predator’s efficiency as a biocontrol agent, underscoring its ability to quickly capture and process the prey (Rotheray, Reference Rotheray1989). Our study found that the third instar of E. viridaureus exhibited a significantly shorter handling time (0.540 h) compared to the first (3.996 h) and second instars (2.841 h). Similar findings were reported by Jalilian et al. (Reference Jalilian, Fathipour, Talebi and Sedaratian2011), who observed a lower handling time in the third instar (0.32 h) compared to the second instar (0.51 h) of E. balteatus. Additionally, in larger instars, the predator’s increased search efficiency allows it to capture and handle prey more quickly, resulting in a reduced handling time (Evans, Reference Evans1976).
Hence, the present study indicates that E. viridaureus successfully completed its life cycle on M. euphorbiae and demonstrated significant predatory potential against this aphid. Furthermore, E. viridaureus displayed a type-II functional response to different densities of M. euphorbiae. The observed increase in attack rate and reduction in handling time across its larval instars indicate that E. viridaureus holds promise as an effective component in Integrated Pest Management (IPM) for tomato. Nonetheless, additional field trials are required to validate these findings.
Acknowledgements
Authors are thankful to the Dr. Yashwant Singh Parmar University of Horticulture and Forestry, Nauni, Solan, HP – 173230 for providing necessary facilities to conduct this research.
Author contribution
AB conducted the experiments, collected and analysed the data, and also wrote the manuscript. SCV, PLS, RSC, and VGSC designed the experiments and contributed to improve the manuscript. NC, CS, AS, and PS helped in statistical analysis, reviewed the manuscript and provided necessary corrections. All authors read and approved the final version of the manuscript.
Financial support
Not applicable.
Competing interests
Authors declare no competing interest.
Data availability statement
Data will be made available on valid request to the corresponding author.
Consent for publication
Not applicable.
Ethics approval
All the work was done by taking care of ethical approval.
Consent to participate
Consent was taken from all the authors.
