Functional response estimations of Chrysoperla carnea to different densities of Aphis craccivora and Gynaikothrips ficorum nymphs

Estimativas da resposta funcional de Chrysoperla carnea em diferentes densidades de ninfas de Aphis craccivora e Gynaikothrips ficorum

Abstract

The functional responses of Chrysoperla carnea larvae were evaluated at different seven densities of the 3^rd instar nymphs of Aphis craccivora and Gynaikothrips ficorum in order to find out the relationship between predator densities and its prey by the, and also to find out their capability for biological control of aphids and thrips. Results revealed that all tested larval instars of Ch. carnea exhibited a type II response in relation to the prey. Moreover, the coefficients of attack rate (a) and handling time (T_h) was differed among various growing instars of predator and for the prey species. The 3^rd instar larvae of Ch. carnea manifested the highest attacking rate (1.23 and 1.22) on the 3^rd instar nymphs of A. craccivora and G. ficorum, respectively. In addition it exhibited the highest maximum predation (Na _max) (50.00 and 52.63) on A. craccivora and G. ficorum nymphs, respectively as compared with the other treatments. Accordingly, Ch. carnea could be considered as a promising bio-control agent for A. craccivora and G. ficorum management.

Keywords:  Chrysoperla carnea; functional response; aphids; thrips; predation rate; biological control

Resumo

As respostas funcionais de larvas de Chrysoperla carnea foram avaliadas em sete diferentes densidades de ninfas de 3º instar de Aphis craccivora e Gynaikothrips ficorum, a fim de descobrir a relação entre as densidades de predadores e suas presas, e sua capacidade de controle biológico de pulgões e tripes. Os resultados revelaram que todos os instares larvais testados de Ch. carnea apresentaram resposta de tipo II em relação à presa. Além disso, os coeficientes de taxa de ataque (a) e tempo de manejo (Th) diferiram entre os vários instares de crescimento do predador e para a espécie de presa. As larvas de 3º instar de Ch. carnea manifestaram a maior taxa de ataque (1,23 e 1,22) nas ninfas de 3º instar de A. craccivora e G. ficorum, respectivamente. Além disso, a maior taxa de predação máxima (Na _máx.) (50,00 e 52,63) apresentou-se em ninfas de A. craccivora e G. ficorum, respectivamente, em comparação aos demais tratamentos. Assim, é possível concluir que o Ch. carnea pode ser considerado um agente de biocontrole promissor para o manejo de A. craccivora e G. ficorum.

Palavras-chave:  Chrysoperla carnea; resposta funcional; pulgões; tripes; taxa de predação; controle biológico

1. Introduction

Predation is one of the main important factors for decreasing the insect pest populations. So that, the utilization of predators in insect pest management has got a lot of attention hoping to decrease the using of chemical pesticides (Atlihan et al., 2010). The important factor for the regulating of the population changes in predator-prey densities was predator’s functional response. . It indicated the predator’s efficiency against different prey densities (Murdoch and Oaten, 1975). The functional response of predator was classified to different types, Holling (1959, 1966) reported three types of functional response; I, (increasing the linear relationship), II (a decelerating curve) and III (a sigmoid relationship). The functional response curves can be detected by evaluating different parameters as well as coefficient of attack rate and handling time (time spent in attacking, killing, subduing and digesting). The coefficient of attack rate was estimated the increasing in the predation and the time needed for satiation. Pervez (2005) reported that the regression model was necessary for determining the functional response type.

Several factors were affect the functional response including the size of predator to its prey (Flinn et al., 1985), voracity (Rotheray, 1989), type of prey (Allahyari et al., 2004), the age of predator and the predacious stage (Farhadi et al., 2010). Moreover, Rotheray (1989) added other factors like as predator’s density, time of day, capability of prey for defense and prey’s density affect the efficiency and handling time of a predator. To reach successful control of many pest species, the used of predator's reaction to changes the prey density was extremely important. Additionally, Villa et al. (2016) stated that the Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) larval stage feed on their prey species such as aphids (nymph and adults), while adults feed on nectar, pollen and honeydew. The ability of the predator to feed determined the effectiveness of biocontrol. (Sengonca et al., 2005) and the number of consumed prey/predator individuals depended on the prey density (Holling, 1959; Solomon, 1949). The variations in number of attacked prey density was called the functional response as that reported by Solomon (1949).

The thrips, Gynaikothrips ficorum (Marchal) (Phlaeothripidae) was a pan tropical thrips species feeding multiply in leaf-galls on leaves of Ficus microcarpa L. var. nitida (Alford, 2013), but in case of high abundance of G. ficorum can be fed on other hosts, particularly those of genus Ficus. According to Holling (1965), the functional response of C. carnea on A. craccivora constituted a critical factor to regulate the prey density. For this reason, the present study was implemented to find the type of functional response of the C. carnea larval instar when fed on different densities of the 3^rd instar of A. craccivora and G. ficorum nymph under laboratory in order to assess the potential of C. carnea larvae against the two mentioned prey species.

2. Materials and Methods

2.1. Stock cultures of tested insect species

2.1.1. Aphis craccivora

First stock of A. craccivora individuals was provided on faba bean seedlings by Syngenta Company at Qaha district, Qalubiya Governorate. The obtained seedlings were taken to the laboratory of Insect Rearing at the Faculty of Agriculture at Moshtohor, Benha University for rearing of the aphid individuals on fresh grown faba bean seedlings. Faba bean seeds were sown at 1-2 cm depth in wet sawdust and placed in plastic trays (30 × 15 × 4 cm) or no. 10 pots. Containers were placed in cages covered by muslin screen (70 × 60 × 60 cm). Sawdust containing seeds was, daily, supplied with suitable amount of water until germination and the new seedlings become having 3 or 4 rows of leaves. Rearing of A. craccivora continued at 27 ± 1 °C. and 65 ± 5%RH. Old aphid infested faba bean leaves were cut and gently placed between the new seedlings to start aphid multiplying. The population of Aphis gossypii increased and gave the continuous needed supply of prey for feeding C. carnea larvae and achieving the desired experiments.

2.2. Stock cultures of Gynaikothrips ficorum

The infested Ficus nitida leaves with G. ficorum nymphs on small branches were handpicked from Ficus trees grown in the Faculty of Agriculture, Benha Univ and it were kept in small plastic containers. The 3^rd instar of nymphs were selected for this experiment. For exposing the G. ficorum nymphs to C. carnea larvae, those were taken out from the folded leaves for selection of the 3^rd instar nymphs which were used in this experiment.

2.3. The aphid lion, C. carnea

C. carnea were obtained from the Biological Control Research Laboratory at the Plant Protection Research Institute, Dokki, Giza. it was placed in. plastic containers (30 × 20 × 15 cm) covered by white pieces of muslin cloth. These larvae were released on A. craccivora infesting faba bean seedlings. Surviving of aphid individuals were daily added in each container to replace those consumed by the predaceous larvae. This process was continued until C. carnea cocoons formation. Using a soft brush, cocoons were separated, and placed in new plastic container covered with white pieces of muslin cloth until adults’ emergence. Adults of C. carnea (10 males & 10 females) were placed in plastic containers of the same size as those used for C. carnea rearing but it was covered with a black cloth on which stalks of the deposited eggs were glued. Droplets of semi-artificial diet (2 gm. of dried active yeast + 1 gm. of honey + 1 mL. of distilled water) had been placed in the middle of the cloth cover using a sticker for adults’ feeding. The pieces of black cloth were replaced daily by new ones. Eggs on cloth pieces were daily collected and placed in other plastic containers until hatching. The newly larvae were supplied with adequately numbers of A. craccivora individuals on fresh faba bean seedlings for feeding. So, enough quantities of the prey (aphid nymphs) and larvae of the predator (C. carnea) were always available for achieving the desired experiments.

3. Statistical Analysis

3.1. Functional response

The three C. carnea larval instars fed on 3^rd instar nymphs of A. craccivora and G. ficorum were determined. The larvae were starved, individually, in vials for 24 hours before starting experiments (Nakamura, 1977). the 7^th densities of A. craccivora and G. ficorum (10, 20, 40, 80, 90, 100, and 110) were experimented . The glass tubes were covered with muslin and kept under laboratory conditions (27 ± 1 °C and 65 ± 5 RH). After 24 hours, the numbers of A. craccivora and G. ficorum consumed by each of the three C. carnea larval instars were recorded by counting the number of remaining surviving prey nymphs in each tube. Five replicates of the experiment were performed.

Discrimination of the different types of functional response was exhibited by a particular instar of a predator to a particular prey species in order to fit the data to a particular Hollings’ equation (Holling, 1959, 1966). For determining the type of functional response, a logistic regression model has been used as a tool taking into consideration the proportion of prey eaten (Na/N0) as a function of prey offered (N0) (Juliano, 2001). Therefore, data were fitted to the following polynomial function that describes the relationship between Na / N0 and N0 (Equation 1):

$\frac{Na}{N_0}=\frac{\exp \left(P_0+P_1{\text{N}}_0+{\text{P}}_2\text{N}/+{\text{P}}_3{\text{N}}_0^3\right.}{1+\exp \left({\text{P}}_0+{\text{P}}_1{\text{N}}_0+{\text{P}}_2\text{N}/+{\text{P}}_3{\text{N}}_0^3\right.}$ (1)

where: P0 = Intercept; P1 = Linear coefficient; P2 = Quadratic coefficient; P3 = Cubic coefficient; Na = Prey’s number devoured; N0 = Exposed prey, count.

The method of maximum likelihood has been estimated by a coefficient. If P1> 0 and P2< 0, the proportion of prey consumed is positively density dependent, thus describing a type III functional response. If P1<0, the proportion of prey consumed declines monotonically with the initial number of preys offered, thus describing a type II functional response (Juliano, 2001). The coefficients of polynomial logistic regression were also determined. After the determination of the shape of the curve, handling times and attack coefficients of a Type II response were estimated using Holling’s disc equation modified after determination of the shape of the curve. The simplified Holling’s equation, modified by reciprocal linear transformation (Livdahl and Stiven, 1983; Pervez, 2004a) as follows (Equation 2):

$\text{Na}=\frac{a^{\prime }\text{TNo}}{1+a^{\prime }{T}_h\text{No}}$ (2)

where: Na = Prey’s number devoured; No = Exposed prey, count; a' = Rate of attack; T_h = Time taken for handling; T = Confinement time (24 hours).

4. Results

4.1. The functional response of C. carnea to aphid and thripsG. ficorum 3^rd instar nymphs

The logistic regression for the three C. carnea larval instars had a significant linear parameter P₁ < 0 (Table 1) and the proportion of prey consumed by all predators declined with increasing prey density (Figures 1 and 2). Data suggested that all three of them exhibited a Type II response. According to the Holling disk equation, the functional response depending upon different factors was estimated such as (a), (T_h) and (Na _max) for each of the three C. carnea larval instars after being released on A. craccivora and G. ficorum 3^rd instar nymphs.

Table 1
Estimation values of attack rate (a), time taken for handling (T_h) and maximum predation (Na _max) of prey (A. craccivora and G. ficorum) eaten by different instars of C. carnea.

Prey	Instar of C. carnea	Parameter	Estimate	R2	a	Th	Maximum predation rate (Na max)
A. craccivora	1st	Constant (P0)	4.6	0.995	1.29	0.063	15.87
		Linear (P1)	-0.004
		Quadratic (P2)	0.319
	2nd	Constant (P0)	4.32	0.979	1.42	0.042	23.81
		Linear (P1)	-0.007
		Quadratic (P2)	0.56
	3rd	Constant (P0)	0.106	0.995	1.23	0.02	50
		Linear (P1)	-0.014
		Quadratic (P2)	1.139
G. ficorum	1st	Constant (P0)	5.9	0.973	1.87	0.06	16.66
		Linear (P1)	-0.005
		Quadratic (P2)	0.368
	2nd	Constant (P0)	4.4	0.994	1.66	0.042	23.81
		Linear (P1)	-0.008
		Quadratic (P2)	0.626
	3rd	Constant (P0)	0.189	0.993	1.22	0.019	52.63
		Linear (P1)	-0.0137
		Quadratic (P2)	1.137

Figure 1
Functional response displayed by three larval instars of C. carnea to different prey densities (10, 20, 40, 80, 90,100 and 110 individuals) of 3^rd nymphal instar of A. craccivora.

Figure 2
Functional response displayed by three larval instars of C. carnea to different prey densities (10, 20, 40, 80, 90,100, and 110 individuals) of the 3rd nymphal instar of G. ficorum.

4.2. On A. craccivora

Regarding the data in Table 1, the time taken for handling (T_h) was recorded during one day for one larva of the three larval instars of C. carnea predator, results revealed that the T_h was (0.063, 0.042, and 0.02 day) at the 1^st, 2^nd and 3^rd larval instars, respectively. While, the attack rates were (1.29, 1.42 and 1.23) at the instar larvae 1^st, 2^nd and 3^rd respectively, which indicate the ability of predator to search and predate a prey individual of the 3^rd nymphal instar of A. craccivora. Moreover, the maximum predation rate (Na _max) during 24 h were 15.87, 23.81 and 50.00 nymphs for the 1^st, 2^nd and 3^rd instars, respectively. Data confirmed the highest predation rate (a) and maximum predation (Na _max) during one day was stated with the 3^rd larval instar of C. carnea.

4.3. On G. ficorum

The obtained results showed the handling (T_h) for each of the three larval instars of C. carnea being (0.06, 0.042 and 0.019 day) for 1^st, 2^nd and 3^rd larval instars, respectively (Table 1) to search, predate and ingest one prey of G. ficorum. During one day of exposure, the attack rates (a) were (1.87, 1.66, and 1.22) at the instar larvae 1^st, 2^nd and 3^rd, respectively. The maximum predation rate (Na _max) during 24 h was 16.66, 23.81 and 52.63 nymphs for each of the 3 larval instars, respectively. The maximum predation rate (a) during 24h occurred, also, by the 3^rd larval instar of C. carnea.

Results indicated that consumption of prey individuals (aphid or thrips nymphs) weren increased by increasing the prey density (Table 2). The highest consumption rate by C. carnea 1^st instar larva was (36.0 ± 0.89) of the 3^rd instar nymphs of G. ficorum that occurred with the offered prey density was 110 individuals. On contrary, the lowest consumption rate was (7.2 ± 0.20) of the 1^st instar nymphs of A. craccivora which counted with the lowest prey density (10 individuals). The three C. carnea larval instars manifested a type-II functional response in which consumption rate rised with prey density but gradually decelerated until a plateau is reached at which consumption rate remains constant irrespective of prey density (Figures 1 and 2).

Table 2
Effects of prey type on functional response of C. carnea to A. craccivora and G. ficorum nymphs (Mean ± SE and LSD P>0.05 0.05).

Prey type	Density of prey	Mean number larval instars of C. carnea ± SE
		1stlarval instar	2ndlarval instar	3rdlarval instar
A. craccivora	10	7.2 ± 0.20eB	8.8 ± 0.58eA	9.6 ± 0.24dA
	20	9.8 ± 0.20dC	13.6 ± 0.24dB	19.0 ± 0.32cA
	40	11.8 ± 0.86cC	16.8 ± 0.97cB	32.0 ± 1.55bA
	80	13.6 ± 1.21bcC	18.2 ± 0.58bcB	32.4 ± 0.87abA
	90	14.0 ± 0.32abC	20.0 ± 0.63abB	33.0 ± 0.95abA
	100	15.0 ± 0.95abC	21.0 ± 0.63aB	34.0 ± 2.28aA
	110	15.6 ± 1.91aC	21.2 ± 1.96aB	34.0 ± 2.28aA
LSD at 0.05 level		C*S
		1.87
G. ficorum	10	8.8 ± 0.58dA	9.8 ± 0.20fA	9.6 ± 0.24eA
	20	11.8 ± 0.97cC	13.6 ± 0.24eB	19.0 ± 0.32dA
	40	13.6 ± 1.21bC	18.2 ± 0.58dB	32.0 ± 1.55cA
	80	14.0 ± 0.32bC	19.0 ± 0.32cdB	32.4 ± 0.87cA
	90	15.0 ± 0.95abC	20.0 ± 0.63bcB	34.0 ± 2.28bA
	100	16.0 ± 0.32aC	21.2 ± 1.96abB	36.0 ± 0.45aA
	110	16.2 ± 0.20aC	22.0 ± 0.95aB	36.0 ± 0.89aA
LSD at 0.05 level		C*S
		1.55

• Means signed by the same lowercase letter was non-significant in the same column. While, means signed by the uppercase letter was non-significant in the same row at P>0.05.

This obtained results indicated that the time handling spent was prolonged as the offered prey density was increased. Thus, the amount of consumed A. craccivora or G. ficorum is limited by the time for handling the prey rather than by the availability of prey. C. carnea larval instars had similar attack rates on A. craccivora and G. ficorum nymphs, but the older predacious larvae (those of the third instar) had significantly the shortest handling time for consuming the prey than the earlier ones. It was noticed that the maximum attacking rate increased as the feeding predacious larvae grew older to subsequent instars.

5. Discussion

Regarding the obtained data, it was cleared that the functional response was the type II response, in which consumption rate increased by increasing the prey density, but the consumption rate gradually decelerated with prey density increasing until the consumption rate remains constant irrespective of prey density. The exposure time may had an effect on the predator/prey relationship, the number of A. craccivora and G. ficorum nymphs killed by C. carnea within 24 h achieved the functional response trend. In their studies, Atlýhan et al. (2004), reported that the attack rate was similar for the three C. carnea larval instars and the time taken for handling of the third instar was the shortest when the predacious larvae fed on nymphs of Hyalopterus pruni. Similarly,, previous authors found that the 3^rd instar larvae of C. carnea were the highest active to attack Hyalopterus pruni (Atlýhan et al., 2004), Myzus persicae (Scopes, 1969), Aphis gossypii (Yuksel, 1992) and Lipaphis erysimi (Liu and Chen, 2001).

The numbers of A. craccivora and G. ficorum nymphs killed by C. carnea larva was increased with increasing prey density within 24 h whereas the highest consumption rate was up to 110 individuals. In agreement with the present study, the killed numbers of H. pruni nymphs by C. carnea were high value of 160 prey per day (Atlýhan et al., 2004) and 128 prey per day for A. gossypii individuals (Montoya-Alvarez et al., 2010).

Generally, it could be stated that the relative importance of C. carnea larvae as a valuable biocontrol agent against A. craccivora and G. ficorum can be changed depending on several factors as the composition of prey community and the size of prey (Guzman and Srivastava, 2019), trophic complexity (Jonsson et al., 2018) and the relative predator’s feeding preference on prey or habitat complexity. Also, Guzman and Srivastava (2019) reported that the persistence of predators in the community was maximized when the minimum prey size was relatively intermediate, but as the prey diversity was increased, the minimum body size of prey may appear of broader value.

6. Conclusions

Obtained data in the present work showed the feeding potentiality of C. carnea larva against young prey individuals, and inversely, the ability of A. craccivora and G. ficorum nymphs as food source for this predator at the available laboratory conditions. This subsequently led to new queries about these interactions in more complex systems. Maximal values for the attack rate coefficient were obtained by the 3^rd larval instar of C. carnea, followed by 2^nd and 1^st larval instars. The shortest T_h was exhibited by 3^rd larval instar of C. carnea released on A. craccivora and G. ficorum nymphs. From the evidence of functional response curves, the coefficient of attack rates and handling time, C. carnea could be an efficient biocontrol agent. C. carnea had the potential to be successfully exploited as a biocontrol agent for the management of G. ficorum and A. craccivora infestations, however, further field-based studies are needed.

Acknowledgements

The author wishes to express her deep and sincere thanks to Dr. Fawzy Faiek Shalaby, Emeritus Professor of Economic Entomology, Plant Protection Department, Faculty of Agriculture, Benha Univeristy, for suggesting the problem, keen and close help, scientific guidance, valuable and fruitful advices and constructive criticism throughout the whole period of this study, and also for revising the manuscript.

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Publication Dates

• Publication in this collection
  19 Dec 2022
• Date of issue
  2024

History

• Received
  21 Sept 2022
• Accepted
  04 Nov 2022