Comparative demography, population projection, functional response and host age preference behavior of the parasitoid Goniozus legneri on two lepidopterous insect hosts
Egyptian Journal of Biological Pest Control volume 33, Article number: 2 (2023)
This study was conducted to investigate life table characteristics of the parasitoid species, Goniozus legneri Gordh (Hymenoptera: Bethylidae), a major gregarious larval ecto-parasitoids of the carob moth, Ectomyelois ceratoniae Zeller (Lep.: Pyralidae). Demographic parameters of G. legneri reared on two hosts, the carob moth and the flour moth, Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae), were studied under laboratory conditions using age-stage, two-sex life table. Host stage preference and the functional response of this parasitoid were also determined.
The duration of the immature period, adult pre-ovipositional period and total pre-ovipositional period of G. legneri reared on E. kuehniella was significantly longer than that of those reared on E. ceratoniae, while fecundity and ovipositional days of the wasp were greater/longer in females reared on E. ceratoniae. There were also significant differences in intrinsic and finite rates of increase and mean generation time between wasp parasitoid reared on two hosts. Moreover, population projection indicated that the G. legneri population can grow swifter when reared on E. ceratoniae than on E. kuehniella. Based on the experiments conducted to determine the larval stage preferences of G. legneri, for both hosts, larger larvae were more preferred stages compared to smaller ones, thereby fulfilling the optimal oviposition theory. The functional responses of G. legneri to different population densities of E. kuehniella two last instar larvae were determined as type III at 25 °C and 60% RH.
The results offer valuable information on some life history attributes of G. legneri. Although G. legneri performed better on E. ceratoniae larvae than on E. kuehniella, as the use of E. ceratoniae larvae as the main host in rearing of G. legneri might be a laborious process and can increase the production costs, E. kuehniella can be used as an alternative host. Further studies are required under greenhouse and field conditions for effective use of this biocontrol agent against the carob moth.
Behavior of individual parasitoids in response to an increasing host density or the functional response is undeniably a salient feature, which is influential in parasitoid success (Tomasetto et al. 2018). Host stage might be another factor, which can affect the development and reproduction of a parasitoid at the time of parasitization and hence influence the parasitoid efficiency (Pandey and Singh 1999).
The carob moth, Ectomyelois ceratoniae (Zeller) (Lepidoptera: Pyralidae), is a polyphagous devastating pest throughout the world which invades various fruits both before and after harvest. Pomegranate, Punica granatum L. (Lythraceae), is one of the preferred hosts of this pest in nearly all pomegranate producing areas of the Middle East and its yield may be significantly reduced due to the attack of this species (Sobhani et al. 2015). Not only feeding of larvae from internal parts of fruits, but also contamination of fruits with saprophytic fungi cause the fruits become inedible and unsuitable for consumption in food processing industries (Shakeri 2004). Because larval feeding takes place inside the fruits, commercial insecticides are inefficacious and hence not applicable against this pest (Hosseini et al. 2017). Hence, development of integrated pest management programs aiming to decrease the damage caused by the pest below the economic injury level is of great priority and importance (Del Pino et al. 2015).
The genus Goniozus is one of the most important genera of bethylid parasitic wasps (Polaszek 1998). Goniozus legneri Gordh (Hymenoptera: Bethylidae) is a gregarious primary ecto-larval parasitoid of some lepidopterans, particularly members of the Pyralidae (Basha and Mandour 2006). This species firstly reported from pomegranate orchards of Iran in 2010, parasitizing larvae of carob moth (Ehteshami et al. 2013). The parasitoid is a high potential biological control agent in integrated management programs for the carob moth (Sarhan et al. 2004).
The Mediterranean flour moth, Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae), is an easily reared species, which hitherto has been widely utilized for mass rearing of various natural enemies including larval ecto-parasitoids (Nakano et al. 2018). As rearing of the carob moth is tedious, E. kuehniella may be a suitable alternative host candidate for rearing of G. legneri (Shoeb et al. 2005).
Life tables, as the best way to project population growth and reveal the details of life history parameters such as survival, stage development and also reproduction, lubricate a full comprehension of insect population dynamics (Huang et al. 2018). They are considered as crucial instruments for prophesying anticipated damage from a pest population, implementing pest management programs and determining best timing of pest control practices (Huang et al. 2018). Comprehensive knowledge of life table and some behavioral responses (such as functional response) of a natural enemy lead to unerring description of growth, stage differentiation, and reproduction of the biocontrol agent in order to expound an efficacious mass-rearing procedure, which is an important factor for the success of biological control programs (Eliopoulos 2019).
In the present study, raw data on the life history of G. legneri and its functional response on two hosts, E. ceratoniae and E. kuehniella (as an alternative host) were collected and analyzed. The results from this study are expected to be beneficial in providing basic information on the utilization of G. legneri to control the population of E. ceratoniae.
Infested fruits were collected from underneath and on the trees of pomegranate orchards of Shiraz and vicinity, Iran, and were transferred to the laboratory for dissection and removal of the carob moth larvae. The parasitized larvae were individually placed in plastic containers (10 cm height 20 cm width) until emergence of the adult parasitoids. Parasitoids were reared separately on two hosts, E. kuehniella and E. ceratoniae larvae, in the laboratory (26 ± 1 °C, 50 ± 5% RH and 14 L: 10 D) for three generations before using in the experiments. Honey solution (10%) was placed in the containers as adult food.
Original carob moth colonies were obtained from adults emerged from infested pomegranate fruits collected from orchards in Shiraz vicinity, Iran. Emerged adults were transferred into mating cages (50 × 50 × 100 cm) and after 24 h. of exposure, each mated female was removed from the cage and placed separately in a plastic container (1 L volume). The container was inverted on a piece of rough filter paper. A 3-cm-diameter opening was cut on bottom of the plastic container and covered with a fine mesh for ventilation. During oviposition adult females were provided with cotton wool pieces which were soaked in 10% honey water solution for feeding. The hatched larvae were transferred on the artificial diet (wheat bran 300 g, sugar 80 g, yeast 9 g, multivitamin 1.4 g, tetracycline antibiotics 0.6 g, sterile distilled water 120 ml, and glycerin 130 ml) using a fine brush.
Life table analysis
The age-stage, two-sex life table approach was utilized to analyze the raw life-history data for G. legneri (Chi 1988) via the computer program TWOSEX-MSChart (Chi 2020a). The population parameters including age-stage-specific survival rate (sxj), age-stage-specific fecundity (fxj), age-specific fecundity of total population (mx), age-specific survival rate (lx), age-specific maternity (lxmx), intrinsic rate of increase (r), finite rate of increase (λ), net reproductive rate (R0), mean generation time (T), age-stage life expectancy (exj) and reproductive value (vxj) were calculated. In order to estimate the variances and standard errors of population parameters, the bootstrap technique with 100,000 resampling was applied (Wei et al. 2020). Quick paired bootstrapping (paired 1 by 1) function was used for estimating the significant differences between means. Sigma plot v. 12.5 was used to create graphs.
where G, D and F are growth, development and fecundity matrices produced via using TWOSEX-MSChart.
Host stage preference
To determine the host larval stage preferences of G. legneri, a non- and a choice experiment were designed based on the size of larvae of each host, i.e., small (L1 and L2) and large (L4 and L5). Experiments were conducted separately for each host species. In the non-choice experiment, a female and male of G. legneri were confined in a Petri dish (8 cm) and provided with 10% honey solution for food. The insects were 2–3 days old, and the females were naïve. A total of 60 larvae, in batches of 30 for each group (L1 + L2 and L4 + L5), were placed separately in Petri dishes. The larvae were exposed to the parasitoids for 24 h in an incubator at 25° C and a 14:10 (L:D) photoperiod. After exposure, the parasitoids were removed from the Petri dishes, and the parasitized larvae were counted. In choice experiment, the procedures were the same as above, except that in each Petri dish, a mixture of larvae belonging to two groups, i.e., 15 small larvae (L1 + L2) and 15 large larvae (L4 + L5), were provided. Each experiment was replicated 10 times.
Comparisons of host larval stage preferences in non- and a choice experiment were done by independent t test (P < 0.05). Data were normalized using arcsine transformation. All analyses were done with SPSS software version 19 (SPSS Inc., Chicago, USA).
Parasitoid’s preference for the host stage was evaluated by calculating a preference index according to Manly (1974). This index is as follows:
where βi is the preference for prey group i, ei are the numbers of hosts remaining after the experiment; Ai and As are the number of prey groups i and s offered, respectively. This index provides a value between 0 and 1. With two-prey choices, as in our experiment, the value 0.5 for βi shows that the predator has no preference for any of prey groups, whereas values greater and lower than 0.5 indicate a preference for prey group i and prey groups, respectively (Meyling et al. 2004). To assess if the estimates deviated from 0.5, a two-tailed t test (P < 0.05) SPSS 19 software was utilized.
Parasitoid’s preference for the host stage was also assessed by calculating a preference index according to Jervis and Kidd (1996) using the following equation:
where the N1 and N2 are the number of small and large larvae, and E1 and E2 are the number of small and large parasitized larvae, respectively. The value c < 1 indicates preference for prey 2 (group 2), whereas c > 1 depicts preference for prey 1.
Since in nature, only one larva in each pomegranate fruit is exposed to G. legneri females for being parasitized, so the functional response with E. ceratonia larvae seemed to be meaningless. Therefore, only the flour moth larvae were included in the experiment. The 4th and 5th instar larvae of E. kuehniella were placed within the Petri dishes in different densities of 4, 6, 10, 20, 30, 50 and 60. One mated 10-day-old female parasitoid (fed on drop of 20% honey/water) was introduced into each Petri dish. Ten replicates for each host density were utilized. The parasitoids were removed after 24 h, and the parasitized larvae were counted. In order to determine the shape (type) of functional response, the logistic regression of the proportion of parasitized hosts (Na/N0) as a function of host density (N0) is used. For doing this, a polynomial function (Eq. 1) is fitted:
where Na/Nt is the proportion of parasitized hosts, Nt is the initial host density, P0, P1, P2 and P3 are the intercept, linear, quadratic, and cubic coefficients estimated through the CATMOD procedure in SAS, respectively. If the signs of the linear parameter (P1) and the quadratic parameter (P2) are both negative, the proportion of parasitized host decreases monotonically with host density (De Clercq et al. 2000) implying type II functional response. If P1 and P2 are positive and negative, respectively, the proportion of parasitized host is positively density-dependent depicting type III functional response (Juliano 2001).
After determination of the type of functional response, to estimate the parameters associated with functional response models, a nonlinear least square regression (SAS Institute 2014) was utilized. As our data fit a type III functional response, the type III equation for parasitoids was utilized as follows (Eq. 2):
where Na is the number of parasitized hosts, Nt is the initial number of hosts, Pt is the number of the parasitoid, T is the total time of the experiment (24 h in our study), Th is the handling time, b and c are constants, (24 h). The coefficient of determination (R2) was calculated using the following equation: R2 = 1 − (residual sum of squares/corrected total sum of squares).
Developmental time, survival, longevity and fecundity
The mean developmental durations of each pre-adult stage and the adult longevities of females and males as well as reproductive features of females are given in (Table 1). The total immature stages of G. legneri reared on E. ceratoniae were significantly shorter than the equivalent durations on E. kuehniella. Female wasps lived an average of 76.33 and 53.79 d on flour moth and carob moth, respectively. The adult pre-ovipositional period (APOP) of Goniozus wasps was significantly shorter on the carob moth. In other words, the mated females of G. legneri began oviposition, on average, 0.62 and 0.77 d after emergence when reared on E. ceratoniae and E. kuehniella, respectively. There were also significant differences between total pre-ovipositional periods (TPOP) of parasitoid wasps on two hosts (Table 1). The mean fecundity per Goniozus female was (101.17) on flour moth which was remarkably lesser compared to (118.04) eggs on carob moth (Table 1). The number of ovipositional days of parasitoids reared on E. kuehniella (13.53 d) was significantly lesser than those reared on E. ceratoniae (14.74 d).
The age-stage survival rates (sxj) of G. legneri on two hosts are depicted in (Fig. 1). These curves show the likelihood that a newly deposited egg will survive to age x and stage j. The overlap of stages in the survival curves is due to variable developmental rates among individuals (Yu et al. 2013).
The age-stage specific survival rate (lx), age-specific fecundity (mx) and age-specific maternity (lxmx) of parasitoid wasps on two lepidopteran hosts are plotted in Fig. 2. Because only female wasps reproduce, there was just a single curve, fx4, representing the number of hatched eggs produced by each female (fourth life stage) at age x. Age-specific fecundity (mx) depicts the mean number of hatched eggs produced by each individual (regardless of sex or stages) on age x. As shown in Fig. 2, on both hosts, the cure fx4 is higher than the representative mx curve. The cohorts began the production of offspring on days 11 and 14, reached a peak for 16 d and 19 d and ended on days 55 and 78, on carob moth and flour moth, respectively.
The age-stage life expectancy (exj), as one of the major outputs of life table analysis, defines the number of days that an individual at age x and stage j is anticipated to survive after age x (Chi and Su 2006). The life expectancy of each age-stage of G. legneri is depicted in Fig. 3. With increasing time intervals, the expectancy of different life stages of G. legneri decreased (Fig. 3). A newly deposited egg (e01) was anticipated to live and develop through succeeding stages until an age of (71.5 and 50 d) on flour moth and carob moth larvae, respectively, which was quite equal to the mean longevity in Table 1. As shown in Fig. 3, the exj curves showed a gentle linear decreasing trend due to the lack of notable high mortality throughout life history of the wasp.
The age-stage reproductive value (vxj) of G. legneri expounds the contribution of an individual wasp of age x and stage j to the upcoming offspring. In other words, the vxj curves distinctly depicted the impact of age on the reproductive value. The results of the current study displayed that the reproductive value sharply raised when females started egg laying. The highest reproductive values were recorded at the age of 17 and 13 days on flour moth and carob moth hosts, respectively (Fig. 4). After emergence of all female wasps and when all of them began depositing eggs (after TPOP), the greatest contribution value of female parasitoids was 17 at age (35.08 d) when reared on E. kuehniella, while the highest vxj of wasps, which were reared on E. ceratoniae was 14 at age (34.12 d) (Fig. 4). As the contribution of males to the subsequent populations was not described by Fisher (1930), there was not any curve for males.
Life table parameters including intrinsic rate of increase (r), net reproductive rate (R0), mean generation time (T) and finite rate of increase (λ) calculated using the age-stage, two-sex life table method are shown in (Table 2). Except for net reproductive rate, all other population parameters were significantly different on E. kuehniella from those gained on E. ceratoniae. According to the results, if the population reaches the stable age-stage distribution and if the physiological factors are the only mortality factors, the population of G. legneri reared on E. kuehniella can increase 1.2270-fold per day or at an exponential rate of 0.2046 per day, and it can multiply 91.06 times every 22.05 d. By comparison, when reared on E. ceratonia, the wasp population had the capability to grow 1.2767-fold per day or at an exponential rate of 0.2442 per day, and it was capable to increase 101.52 times every 18.91 d.
The population growth projections of G. legneri utilizing the life table data are shown in Fig. 5. The parasitoid population grew much faster on E. ceratoniae than on E. kuehniella (Fig. 5). After 100 days, there were 227,553,267 individuals in various pre-adult stages, 81,422,480 female and 9,457,624 male adult wasps (reared on E. kuehniella), while on E. ceratoniae, there were 111,142,980,734 individuals in pre-adult stages, and 4,476,203,151 female and 731,806,109 male adults (Fig. 5). With an increase in time, the growth rate of all stages of Goniozus wasps on both hosts in natural logarithmic scale approaches the intrinsic rate of increase (Fig. 5 c, d).
Host stage preference
When different stages (L1 + L2 as small larvae and L4 + L5 as large larvae) of the Mediterranean flour moth and carob moth larvae were offered to the parasitoids under no-choice conditions, there were non-significant differences among the larval stages in the number of hosts parasitized (P = 0.26, df = 18) (Table 3). Nonetheless, Goniozus wasps significantly preferred larger larvae of E. ceratoniae for egg laying (P < 0.01, df = 18) (Table 3). When the Mediterranean flour moth larvae of various developmental stages were offered together to G. legneri, there were significant differences among the larval stages in the number of hosts parasitized (P < 0.0001, df = 18). Smaller larval stages (L1 and L2) were less preferred by G. legneri than larger ones (L4 and L5) (Table 3). Similar results were obtained for Goniozus wasps on carob moth larvae (P < 0.0001, df = 18) and the parasitoid wasps preferred larger larvae over smaller ones (Table 3). The values of Manly’s preference index for two groups of larvae of each host (E. kuehniella and E. ceratoniae) are presented in (Table 4). This index was higher than 0.5 for larger larvae for both the flour moth (0.64) and the carob moth (0.70) meaning that the parasitoid wasp showed a distinct preference for laying eggs on larger larvae.
The value of Jervis and Kidd preference index between zero and one indicated a preference for smaller larvae and the value between 1 and infinity indicated a preference for larger larvae. These parameters were 1.37 and 1.44 for the flour moth and the carob moth, respectively, which indicated preference for larger larvae (Table 4).
Functional responses of G. legneri determined as type III by a logistic regression (Table 5). The results of logistic regression analysis (Table 5) indicating the linear and cubic coefficients were positive for parasitism which is an indication of a type III functional response. The parasitization rate first rose at lower host density and then decreased at a higher host density resulting a sigmoid curve. The attack coefficients b and the handling time Th for E. kuehniella larvae were (0.0176 ± 0.0058) and (0.8950 ± 0.0342), respectively (Table 6).
Adequate information about a biocontrol agent is prerequisite for implementing any decision to use it in any pest management program. The intrinsic rate of increase, survival rate, developmental rate and fecundity, as basic elements representing the life history and stage differentiation, can be utilized in population ecology research, forecasting population growth and the stage structure of a population in both short- and long-term intervals. The life table data should be taken into account as the foundation of any release program of a biocontrol agent, including G. legneri, to achieve accurate timing and coincident with susceptible stages of the host (Getu et al. 2004). Moreover, information on the biological parameters of a parasitoid contributes mightily to prognosticating the generation time and preparing a reference for mass-rearing of it (Chen et al. 2021).
Based on obtained results, total pre-adult developmental period of Goniozus wasps reared on E. kuehniella was significantly lengthier than those reared on E. ceratoniae. Nonetheless, the larval development of wasps was fairly shorter when reared on E. kuehniella. The present findings showed that adult females began egg laying nearly immediately or in less than 1 day after emergence on both hosts, a pattern which has been observed in many parasitoids (Ebrahimi et al. 2013). The total pre-ovipositional period (TPOP) was 15.87 d and 13.26 d on E. kuehniella and E. ceratoniae, which were both close to the age of peak reproductive value at age 17 and 13 D on these two hosts, respectively (Fig. 4). Similar results have been reported in some other studies based on the two-sex life table (Amir-Maafi and Chi 2006). Although female wasps lived remarkably longer when reared on E. kuehniella, the mean fecundities and number of oviposition days of them were significantly greater/longer when reared on E. ceratoniae (Table 1). There were non-significant differences on male longevities between the wasps reared on two hosts. There were also non-significant differences in immature survival rates (sxj) between the two hosts.
In the present study, the sex ratio was in favor of females, which was in line with some previous studies (Khidr et al. 2012). The sex ratios of most bethylid species, including G. legneri, were female biased with low variances (Khidr et al. 2012). The reproductive biology of G. legneri conformed closely to the assumptions of the model of sex ratio evolution under local mate competition theory (LMC). In this species, each host was stung and paralyzed by an adult female, which protects it against utilization by other females (Lize et al. 2012). Because of brood guarding and conspecific infanticide, all offspring developing on the same host are the offspring of a mother (Khidr et al. 2012). Moreover, in G. legneri, sibling mating was greatly prevalent before dispersal and brood sex ratios are mainly female biased (9–19% of offspring are male) and had a low variance (Hardy and Mayhew 1998) qualitatively conforming to expectation under single founders LMC (Krackow et al. 2002).
If a parasitoid has an equal or greater population growth rate compared to that of its host, it will probably capable of regulating its host population. The intrinsic rate of increase of G. legneri on E. kuehniella and E. ceratoniae were 0.2046 and 0.2442, respectively, whereas it ranged from 0.107 to 0.018 in case of (the carob moth) (Norouzi et al. 2008); the intrinsic rate of increase in G. legneri was much higher than those of its host. Hence, G. legneri had the potential to be used in integration with other compatible control methods to achieve an efficacious control of carob moth.
The population growth rates (r and λ) of G. legneri wasps were significantly higher on E. ceratoniae than those on E. kuehniella. It should be noted that both r and λ are efficacious parameters for evaluating population fitness (Chi et al. 2020). Overall, all these results demonstrated that varying hosts may result in considerable changes in various population traits of a parasitoid species which is in line with some the results of previous studies (Saadat et al. 2014).
Although parasitoids may have the ability to develop successfully in various larval instars of the same host, either the costs of parasitism or the suitability may vary among different instars (Fellowes et al. 2005). According to the results of the present study, the parasitoid parasitized all larval stages of both E. kuehniella and E. ceratoniae; nevertheless, there were significant differences in the parasitism rates on the different larval instars. A preference for the last two stages (L4 + L5) compared to two first instars (L1 + L2) was observed for both hosts. Based on the optimal foraging theory (Charnov 1976), which our results agreed with it, when given a choice, female parasitoids prefer larger host larvae than smaller ones for oviposition.
According to the various conducted studies on functional response of insect parasitoids, more than three-quarters of functional responses were type II and less than one-fifth were type III (Fernández-Arhex and Corley 2003). Nonetheless, our study depicted that the functional response of G. legneri followed Type III model. For G. legneri, we do not know on which behavioral mechanism the type III functional response was based. Nonetheless, this response resulted in an increasing percentage of host parasitized at a certain range of host densities, and that over this range the response may act as a stabilizing factor. It is noteworthy to mention that each species of natural enemy can show different types of functional responses depending on various elements such as the age of the natural enemy and its hunger status, the species of a host, host size and distribution, availability of alternative hosts, the temperature and also conditions of the experiment (Van Lenteren et al. 2016). As type III functional response represents a density-dependent relationship between the proportion of parasitism and host density (Holling 1959), it seems that G. legneri probably was efficient at high density of its host. However, it should be noted that interpretation of functional response results is mostly strenuous and their meaning for evaluating the control capability of a biocontrol agent is restricted (Van Lenteren et al. 2016).
Overall, obtained results offered valuable information on some life history attributes of G. legneri which can be useful for using it as a biological control agent. The findings theoretically verified that G. legneri is a promising biocontrol agent against E. ceratoniae by showing that the parasitoid is intrinsically has the capability to suppress its host as revealed by the intrinsic rate of increase (r) comparisons. From present results it can also be concluded that different hosts had a significant effect on life history traits and also performance of G. legneri. Although G. legneri could be reared on both E. ceratoniae and E. kuehniella larvae, this parasitoid wasp performed better on carob moth. Nonetheless, as rearing of the flour moth is more cost-efficient and less strenuous compared to carob moth, this species could be a suitable alternative candidate host for mass-rearing of this parasitoid. It is noteworthy to mention that if hosts other than those studied here are considered for rearing, it is required to evaluate the performance of the parasitoid wasp on those hosts.
Availability of data and materials
Ehteshami F, Aleosfoor M, Allahyari H, Kavousi A, Fekrat L (2022) Comparative demography, population projection, functional response and host age preference behavior of the parasitoid Goniozus legneri on two lepidopterous insect hosts. https://doi.org/10.5281/zenodo.5941599.
- s xj :
Age-stage-specific survival rate
- v xj :
Age-stage reproductive value
- e xj :
Age-stage life expectancy
- l x :
Age-specific survival rate
- f xj :
- m x :
- l x m x :
- R 0 :
Net reproductive rate
- r :
Intrinsic rate of increase
- λ :
Finite rate of increase
- T :
Mean generation time
Adult preoviposition period
Total preoviposition periods
- β i :
Preference for prey group i
- e i :
The numbers of hosts remaining after the experiment
- A i :
The number of prey groups i offered
- A s :
The number of prey groups s offered
- N 1 :
The number of small larvae
- N 2 :
The number of large larvae
- E 1 :
The number of small parasitized larvae
- E 2 :
The number of large parasitized larvae
- N a/N t :
The proportion of parasitized hosts
- N t :
The initial host density
- N a :
The number of parasitized hosts
- N t :
The initial number of hosts
- P 0 :
- P 1 :
- P 2 :
- P 3 :
- P t :
Number of the parasitoid
- T h :
- T :
Total time of the experiment (24 h)
- α :
The attack rate
- R 2 :
Coefficient of determination
Amir-Maafi M, Chi H (2006) Demography of Habrobracon hebetor (Hymenoptera: Braconidae) on two pyralid hosts (Lepidoptera: Pyralidae). Ann Entomol Soc Am 99(1):84–90. https://doi.org/10.1603/0013-8746(2006)099[0084:DOHHHB]2.0.CO;2
Basha E, Mandour N (2006) Effect of Goniozus legneri Gordh (Hymenoptera: Bethylidae) on the life table of Palpita unionalis Hb. (Lepidoptera: Pyralidae). Egypt J Biol Pest Co 16(1):5–11
Charnov EL (1976) Optimal foraging, the marginal value theorem. Theor Popul Biol 9(2):129–136
Chen W, Li Y, Wang M, Mao J, Zhang L (2021) Evaluating the potential of using Spodoptera litura eggs for mass-rearing Telenomus remus, a Promising Egg Parasitoid of Spodoptera frugiperda. InSects 12(5):384. https://doi.org/10.3390/insects12050384
Chi H (1988) Life-table analysis incorporating both sexes and variable development rates among individuals. Environ Entomol 17(1):26–34. https://doi.org/10.1093/ee/17.1.26
Chi H (1990) Timing of control based on the stage structure of pest populations: a simulation approach. J Econ Entomol 83(4):1143–1150. https://doi.org/10.1093/jee/83.4.1143
Chi H (2020a) TWOSEX-MSCart: a computer program for the age-stage two-sex life table analysis. . National Chung Hsing University, Taichung, Taiwan (https://188.8.131.52/Ecology/)
Chi H (2020b) TIMING-MSChart: computer program for population projection based on age-stage, two-sex life table. . National Chung Hsing University, Taichung, Taiwan. (https://184.108.40.206/Ecology)
Chi H, Su H-Y (2006) Age-Stage, Two-Sex Life Tables of “Aphidius gifuensis” (Ashmead) (Hymenoptera: Braconidae) and its host “Myzus persicae” (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate. Environ Entomol 35(1):10–21. https://doi.org/10.1603/0046-225X-35.1.10
Chi H, You M, Atlıhan R, Smith C, Kavousi A, Özgökçe M et al (2020) Age-stage, two-sex life table: an introduction to theory, data analysis, and application. Entomol Gen 40:103–124. https://doi.org/10.1127/entomologia/2020/093
De Clercq P, Mohaghegh J, Tirry L (2000) Effect of host plant on the functional response of the predator Podisus nigrispinus (Heteroptera: Pentatomidae). Biol Control 18(1):65–70. https://doi.org/10.1006/bcon.1999.0808
Del Pino M, Carnero A, Suárez EH, García TC (2015) Bases para la gestión integrada de Chrysodeisis chalcites (Lep. Noctuidae) en cultivos de platanera de Canarias. Phytoma España: La Revista Profesional De Sanidad Vegetal 271:40–47
Ebrahimi M, Sahragard A, Talaei-Hassanloui R, Kavousi A, Chi H (2013) The life table and parasitism rate of Diadegma insulare (Hymenoptera: Ichneumonidae) reared on larvae of Plutella xylostella (Lepidoptera: Plutellidae), with special reference to the variable sex ratio of the offspring and comparison of jackknife and bootstrap techniques. Ann Entomol Soc Am 106(3):279–287. https://doi.org/10.1603/AN12015
Ehteshami F, Aleosfoor M, Allahyari H, Alichi M (2013) First record of Goniozus legneri (Hym.: Bethylidae), the larval ectoparasitoid of carob moth, in Iran. J Entomol Soc Iran 33(1): 89
Eliopoulos PA (2019) Life table parameters of the parasitoid Cephalonomia tarsalis (Hymenoptera: Bethylidae) and its host the saw-toothed grain beetle Oryzaephilus surinamensis (Coleoptera: Silvanidae). J Plant Prot Res 59(4):544–551
Fellowes MDE, Van Alphen JJM, Jervis MA (2005) Foraging Behaviour. In: Jervis MA (ed) Insects as natural enemies: a practical perspective. Springer, Dordrecht, pp 1–71. https://doi.org/10.1007/978-1-4020-2625-6_1
Fernández-arhex V, Corley JC (2003) The functional response of parasitoids and its implications for biological control. Biocontrol Sci Technol 13(4):403–413. https://doi.org/10.1080/0958315031000104523
Fisher RA (1930) The genetical theory of natural selection. Clarendon Press. https://doi.org/10.5962/bhl.title.27468
Getu E, Overholt WA, Kairu E (2004) Comparative studies on the influence of relative humidity and temperature on life table parameters of two populations of Cotesia flavipes (Hymenoptera: Braconidae). Biocontrol Sci Technol 14(6):595–605. https://doi.org/10.1080/09583150410001682322
Hardy IC, Mayhew PJ (1998) Sex ratio, sexual dimorphism and mating structure in bethylid wasps. Behav Ecol Sociobiol 42(6):383–395
Holling CS (1959) Some characteristics of simple types of predation and parasitism1. Can Entomol 91(7):385–398. https://doi.org/10.4039/Ent91385-7
Hosseini SA, Goldansaz SH, Fotoukkiaii SM, Menken SB, Groot A (2017) Seasonal pattern of infestation by the carob moth Ectomyelois ceratoniae in pomegranate cultivars. Crop Prot 102:19–24
Huang H-W, Chi H, Smith CL (2018) Linking demography and consumption of Henosepilachna vigintioctopunctata (Coleoptera: Coccinellidae) fed on Solanum photeinocarpum (Solanales: Solanaceae): with a new method to project the uncertainty of population growth and consumption. J Econ Entomol 111(1):1–9. https://doi.org/10.1093/jee/tox330
Jervis M, Kidd N (1996) Phytophagy: insect natural enemies, practical approaches to their study and evaluation. In: Jervis M, Kidd N (eds) Insect natural enemies. Practical approaches to their study and evaluation. Chapman and Hall, London, pp 375–394
Juliano SA (2001) Nonlinear curve fitting: predation and functional response curves. In: Cheiner SM, Gurven J (eds) Design and analysis of ecological experiments, 2nd edn. Chapman and Hall, London, pp 178–196
Khidr SK, Mayes S, Hardy ICW (2012) Primary and secondary sex ratios in a gregarious parasitoid with local mate competition. Behav Ecol 24(2):435–443
Krackow S, Meelis E, Hardy ICW (2002) Analysis of sex ratio variances and sequences of sex allocation. In: Hardy ICW (ed) Sex ratios: concepts and research methods. Cambridge University Press, Cambridge, pp 112–131
Lizé A, Khidr SK, Hardy IC (2012) Two components of kin recognition influence parasitoid aggression in resource competition. Anim Behav 83(3):793–799. https://doi.org/10.1016/j.anbehav.2012.01.001
Manly B (1974) A model for certain types of selection experiments. Biometrics 30(2):281–294. https://doi.org/10.2307/2529649
Meyling NV, Enkegaard A, Brødsgaard H (2004) Intraguild predation by Anthocoris nemorum (Heteroptera: Anthocoridae) on the aphid parasitoid Aphidius colemani (Hhymenoptera: Braconidae). Biocontrol Sci Technol 14(6):627–630. https://doi.org/10.1080/09583150410001683583
Nakano S, Gau J-J, Maeto K (2018) Host suitability of the Mediterranean flour moth for rearing Meteorus pulchricornis (Hymenoptera: Braconidae), a polyphagous endoparasitoid of pest lepidopteran larvae. Appl Entomol Zool 53:291–296. https://doi.org/10.1007/s13355-018-0555-y
Norouzi A, Talebi AA, Fathipour Y (2008) Development and demographic parameters of the carob moth Apomyelois ceratoniae on four diet regimes. Bull Insectol 61:291–297
Pandey S, Singh R (1999) Host size induced variation in progeny sex ratio of an aphid parasitoid Lysiphlebia mirzai. Entomol Exp Appl 90(1):61–67. https://doi.org/10.1046/j.1570-7458.1999.00423.x
Polaszek A (1998) Bethylidae. In: Polaszek A (ed) African cereal stem borers: economic importance, taxonomy, natural enemies and control. CAB International, Wallingford, pp 133–136
Saadat D, Bandani RA, Dastranj M (2014) Comparison of the developmental time of Bracon hebetor (Hymenoptera: Braconidae) reared on five different lepidopteran host species and its relationship with digestive enzymes. Eur J Entomol 111(4):495–500. https://doi.org/10.14411/eje.2014.069
Sarhan AA, Hassanein FA, Shoukry AA, El-Basha NA (2004) Biology of the bethylid parasitoid Goniozus legneri Gordh. Agric Res J Suez Canal Univ 4:93–99
SAS Institute (2014) SAS system for Windows, versions 9.2. SAS Institute, Cary, USA
Shakeri M (2004) A review on investigations on pomegranate neck worm in Iran. In: A proceeding on evaluation of finding and current problems associated with Spectrobates ceratoniae management in pomegranate. Ministry of Jahad-e-Keshavarzi, organization of research and education, Yazd Agriculture and Natural Resources Research Center, Iran, pp 18–30 (in Persian)
Shoeb M, AbulFadl H, El-Heneidy A (2005) Biological aspects of the ectolarval parasitoid species, Goniozus legneri Gordh (Hymenoptera: Bethylidae) on different insect hosts under laboratory conditions. Egypt J Biol Pest Co 15(1):5–9
Sobhani M, Goldansaz SH, Hatami B, Hosseini SA (2015) A field screening of pomegranate cultivars for resistance to the carob moth, Ectomyelois ceratoniae, and compatibility with its larval parasitoids. Int J Pest Manag 6(4):346–352. https://doi.org/10.1080/09670874.2015.1069418
Tomasetto F, Casanovas P, Brandt SN, Goldson SL (2018) Biological control success of a pasture pest: has its parasitoid lost its functional mojo? Front Ecol Evol 6:215. https://doi.org/10.3389/fevo.2018.00215
Van Lenteren JC, Hemerik L, Lins JC, Bueno Vanda HP (2016) Functional responses of three Neotropical Mirid predators to eggs of Tuta absoluta on tomato. Insects 7(3):34. https://doi.org/10.3390/insects7030034
Wei L, Jing B, Li H (2020) Bootstrapping promotes the RSFC-behavior associations: an application of individual cognitive traits prediction. Hum Brain Mapp 41(9):2302–2316
Yu J-Z, Chi H, Chen B-H (2013) Comparison of the life tables and predation rates of Harmonia dimidiata (F.) (Coleoptera: Coccinellidae) fed on Aphis gossypii Glover (Hemiptera: Aphididae) at different temperatures. Biol Control 64:1–9. https://doi.org/10.1016/j.biocontrol.2012.10.002
The authors are thankful to the Department of Plant Protection, Shiraz University, for providing facilities for the experiments.
We would like to express great appreciation to the Shiraz University for providing generous support for this study.
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Ehteshami, F., Aleosfoor, M., Allahyari, H. et al. Comparative demography, population projection, functional response and host age preference behavior of the parasitoid Goniozus legneri on two lepidopterous insect hosts. Egypt J Biol Pest Control 33, 2 (2023). https://doi.org/10.1186/s41938-022-00645-0
- Goniozus legneri
- Ectomyelois ceratoniae
- Functional response
- Biological parameters