Zergani, Ali ¹ ; Shishehbor, Parviz ² ; Nakkai, Fatemeh Naser ³ and Riahi, Elham ⁴

¹Department of Plant Protection, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran.
²Department of Plant Protection, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran.
³Department of Plant Production Engineering and Genetics, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran.
⁴✉ Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, P.O. Box 14115-336, Tehran, Iran.

2023 - Volume: 63 Issue: 3 pages: 945-954

Original research

Keywords

Abstract

Introduction

Chemical pesticides are often used to control phytophagous mites and insects on different crops worldwide. Adverse influences on the environment and natural enemies may occur through the continued application of chemical pesticides (Sumathi et al. 2019). As a result, using non-chemical methods such as biological control of mite pests is essential (Sumathi et al. 2019). Phytoseiid mites play an important role in the biological control of plant-dwelling mites, thrips, and whiteflies (McMurtry et al. 2013). While approximately 2800 species of this family are currently known, only a limited number have been investigated for their potential as biological control agents (McMurtry et al. 2013; Knapp et al. 2018).

Life styles or predation patterns of Phytoseiidae members have been categorized into four groups (from type I to IV) as a function of their dietary habits, biological traits, and morphological characteristics (McMurtry et al. 2013). Euseius scutalis (Athias-Henriot) (Acari: Phytoseiidae) is a pollen-feeding generalist predator from the category type IV (McMurty & Croft 1997; McMurtry et al. 2013). Although the reproductive capacity of this predator is highest on pollen, it can feed on a wide variety of small insects and mites, including eriophyid mites, spider mites, eggs and immature stages of whiteflies, thrips, and scale insects (El-Badry et al. 1968; El-Badry & El-Banhawy 1968; Bounfour & McMurtry 1987; Nomikou et al. 2001; Kasap & Sekeroglu 2004; Kasap 2005). The species appears suitable for a wide range of botanical families but can be found mainly on trees and bushes (Bounfour & McMurtry 1987). A close association between this species and the flat mites, spider mites, and whiteflies has been reported (El-Badry & EIBenhawy 1968; Wysoki & Cohen 1983; Meyerdirk & Coudriet 1986). In addition, a broad range of environmental tolerances have been demonstrated by this predator, but it appears to be present mostly in hot and dry climates (Bounfour & McMurtry 1987).

Some researchers determined the efficiency of immatures of E. scutalis on different kinds of food (Meyerdirk & Coudriet 1986; Romeih et al. 2004) while very few studies have shown the performance of this predator in both immature and adult stages (Bounfour & McMurtry 1987; Momen & Abdel-Khalek 2008; Abou-Elella et al. 2013; Stathakis et al. 2021; Shishehbor et al. 2022). Some researchers examined the life history of E. scutalis on the pollen of Maalephora crocea Jacq. (Bounfour & McMurtry 1987), Phoenix dactylifera L. (Al-Shammery 2011; Shishehbor et al. 2022), Ricinus communis L., (Momen & Abdel-Khalek 2008), Citrus aurandium L. (Al-Shammery 2011), and Typha latifolia (Shishehbor et al. 2022) plants.

The utilization of E. scutalis in biological control has been restricted due to inadequate information on its food spectrum and little knowledge of its biology, because of a low number of studies conducted on its full life table on different diets. Therefore, the findings of this study can be helpful in determining its food spectrum and its usefulness in biological control programs.

Material and methods

Mite culture

Phytophagous mite: Tetranychus turkestani Ugarov and Nikolskii (Acari: Tetranychidae) was collected from a Convolvulus vulgaris weed on the campus of Shahid Chamran University of Ahvaz, Ahvaz, Iran, then transferred to the laboratory and released on the leaves of seedlings of cowpea (Vigna unguiculata (L.) Walp.) grown from seeds and transplanted into compost in plastic pots (20 cm diam.). Wood-frame culture cages (120×60×60 cm) surrounded by 210 µm nylon mesh were used for keeping the infested plants under conditions of 25±1°C, 60±10% RH, and 16:8 h (L: D) photoperiod.

Predatory mite: E. scutalis was gathered on the leaves of hollyhock (Althea officinalis L.) located on the campus of Shahid Chamran University of Ahvaz, Ahvaz, Iran. Each mite-rearing unit was prepared using a Petri dish (9 cm diameter × 3 cm height), a piece of sponge (5 × 5× 2 cm), a same-size green plastic sheet, a few threads of cotton, and some strips of tissue paper. The sheets kept on the moist sponge in the Petri dish included water. The four sides of the sheet were wrapped in moist tissue papers that formed barriers preventing the mites from escaping. The unit was supplied with a small cotton thread, which made it possible to easily collect eggs laid. The adult mites were transferred and left to lay eggs on the units using a camel-hair paintbrush. They were fed with T. turkestani as the prey and kept at 25±1°C, 60±5% RH, and 16:8 h (L: D) photoperiod.

Pollen collection

Date palm tree pollen on mature spadices (Phoenix dactylifera L.) were collected from the vicinity of Ahvaz City, Khuzestan province in March. Castor bean pollen (Ricinus communis L.) was collected from the mature flower buds of the plants located in the vicinity of Karun River in Ahvaz City, Khuzestan province, between November and early February. The pollen of hopbush (Dodonaea viscosa Jacq.) was collected during the spring season from plants grown in the vicinity of Shahid Chamran University of Ahvaz, Khuzestan province, Iran. The flowers were placed on filter paper until pollen grains were released. Pollen grains were left in the laboratory for three to five days to decrease moisture content and prevent the spread of mold. Then they were poured into vials and stored in a refrigerator at 4 °C until the experiment.

Experiments

Before starting the experiments, the predator colony was divided into four primary groups by transferring the newly deposited eggs of E. scutalis from the stock culture to the rearing units. Each group was fed with one of the four following diets for one generation, T. turkestani immatures, date palm pollen, castor bean pollen, and hopbush pollen. Then, 30 newly laid eggs from each group were transferred separately to the units. After egg hatching, the larvae were provided singly by each diet. The diets were immatures of T. turkestani, hopbush pollen, castor bean, and date palm pollen, which were added to the unit ad libitum. In the natural prey treatment, a predator was supplied with 40 immatures of T. turkestani. The consumed immatures were replaced daily by new ones to maintain an adequate food supply. In other treatments, a small amount of pollen was added to the units and was replaced at 48–72 h intervals. Experimental unit examination and data recording were performed twice a day to calculate developmental time duration and pre-adult mortality.

After adult emergence, each female was paired with a male from the same food group listed before. The couples were provided with sufficient amounts of the specific food until their death. Adult survival was documented daily until all individuals died. After recording the number of eggs laid, adults were discarded from the unit daily. Euseius scutalis, which feeds on four different diets under conditions of 25±1 °C temperature, 60±5% relative humidity, and 16:8 h (L: D) photoperiod, was the subject of a life table study. Adult pre-oviposition (APOP), total pre-oviposition period (TPOP), adults' longevity, oviposition period, fecundity, and sex ratio were calculated.

Life table construction

Data analysis was performed using the method defined by Chi (Chi 1988) and the theory named the age-stage, two-sex life table (Chi & Liu 1985). The data from four diet experiments were subjected to a user-friendly software, namely TWOSEX-MSChart (Chi 2021), available at http://140.120.197.173/Ecology/prod02.htm . All parameters, including the age-stage-specific survival rate (s_xj ) (where x and j are age and stage, respectively), the age-stage specific fecundity (f_xj ) of adult females; the age-specific survival rate (l_x ); the age-specific fecundity (m_x ), APOP, TPOP, the net reproductive rate (R₀), intrinsic rate of increase (r), finite rate of increase (λ), gross reproductive rate (GRR), and mean generation time (T) were calculated using the software. The standard error of each parameter was identified by bootstrapping with 100,000 replicates. The statistical significance of the observed differences was estimated by TWOSEX-MSChart software (Chi 2021). Group differences were assessed using paired bootstrapping, P< 0.05 being considered statistically significant.

Results

The results showed that the type of food had an important effect on the length of different developmental stages of E. scutalis. Generally, the duration of the pre-adult stages attained at each diet was substantially different for both sexes, except for the larval duration. The longest protonymphal duration of females was observed when the predator fed on hopbush pollen, and the shortest duration was recorded when it fed on T. turkestani, while it was not significantly different from date palm pollen (Table 1). For males, it was the longest when E. scutalis fed on hopbush pollen (1.94 d), while it did not differ significantly between other diets (Table 1). The shortest deutonymphal duration was recorded when E. scutalis was reared on T. turkestani, and it showed no significant difference from date palm pollen for both sexes. Male and female E. scutalis reared on T. turkestani had a shorter mean pre-adult duration than those grown on date palm, castor, and hopbush pollen (Table 1).

A significant difference was found between pre-adult mortality rates of different stages of E. scutalis on different diets (Figure 1). Mortality was greatest in either the larval stage (in the populations fed on date palm and hopbush pollen) or protonymphal stage. The highest mortality rates were recorded when castor bean pollen (31.87%) was the diet followed by hopbush pollen (28.77%), whereas it was lowest on T. turkestani (2.94%) (Figure 1).

Values of the age-stage survival rate (s_xj ) presented in Figure 2 varied with developmental stages, due to different growth rates in individuals. The results reflected that it was not significantly delayed for the development of female and male E. scutalis on date palm pollen, T. turkestani, and castor bean pollen. However, the males fed hopbush pollen completed their immature development one day later than females (Figure 2).

The longest adult pre-oviposition period (APOP) was detected on hopbush pollen (2.25 d) which was not significantly different from that obtained on castor bean pollen (1.85 d) (Table 2). Similarly, the total pre-oviposition periods (TPOP) on hopbush and castor bean pollen were significantly longer than those on T. turkestani and date palm pollen (Table 2). Females laid 31.14, 17.39, 12.64, and 17.20 eggs in the duration of 11.62, 5.98, 4.79, and 7.38 days on T. turkestani, date palm, castor bean, and hopbush pollen, respectively. The highest fecundity and oviposition period were determined when T. turkestani were provided as diet (Table 2). Male E. scutalis lived for 12.70, 7.02, 8.75, and 9.70 days while females survived for 16.84, 11.03, 9.60, and 13.69 days after rearing on T. turkestani, date palm, castor bean, and hopbush pollen, respectively (Table 2). The total life span of both males and females was significantly different between treatments (Table 2). Overall, the individuals lived considerably longer when feeding the spider mites and hopbush pollen than the two other diets (Table 3).

On date palm pollen, most of the daily egg laying occurred between the 7th to 12th day, and the highest daily fecundity was 1.57 eggs per female on the 9th day (Figure 3). The individuals reared on T. turkestani showed a fertile age-range between the 7th and 16th day, with the highest daily egg production being 1.49 eggs per female per day (on the 10th day). F_x and m_x reached maximum values (1 egg) at 19 days, on castor bean pollen (Figure 3). The highest value of f_x and m_x were 0.96 and 0.71 eggs, respectively on hopbush pollen which happened on the 15th and 24th day, respectively (Figure 3).

Life-table parameters of E. scutalis on different diets are presented in Table 3. The obtained gross (GRR) and net (R₀) reproductive rates of E. scutalis on T. turkestani were greater than the values attained from other diets (Table 3). The intrinsic rate of increase (r) changed from 0.1675 (on hopbush pollen) to 0.2537 d^-1 (on spider mites), while the finite rate of increase (λ) varied from 1.1824 to 1.2888 d^-1 on the above-mentioned diets (Table 3). As it is apparent, R₀, GRR, r, and λ were almost the same with all pollen diets tested. The mean generation time (T) was 12.59 and 11.84 days on hopbush and T. turkestani, and declined to 11.09 days on castor bean pollen, and finally decreased to 10.15 days on date palm pollen (Table 3).

While the reproduction value (v_xj ) considers the entire population (except adult males), higher values are usually associated with females (Figure 4). The reproductive values of E. scutalis at age zero (v_0,1) was 1.135, 1.105, 1.088, and 1.087 after feeding on T. turkestani, date palm, castor bean, and hopbush pollen, respectively. The maximum value of this curve displayed an increasing trend as a function of age and stage of development. The highest peaks were recorded at 8 (9.90 d^-1), 7 (8.73 d^-1), 7 (6.71 d^-1), and 7 (7.73 d^-1) days on the mentioned diets, respectively (Figure 4). The highest v_xj was seen in the females reared with T. turkestani (Figure 4).

Discussion

The data demonstrated that both natural prey, T. turkestani, and pollen grains provide sufficient food for the development, longevity, and reproduction of E. scutalis. The successful development and reproduction of this predator has been demonstrated by previous studies when fed on different plants pollen including date palm, maize, castor bean, broad bean, cattail, Chloris gayana Kunth, alfalfa Medicago sativa L., and sour orange Citrus aurantium L. (Nomikou et al. 2001, 2003; Al-Shammery 2011; Maoz et al. 2011; Abou-Elella et al. 2013; Shishehbor et al. 2022), along with mites and insects (Abou-Elella et al. 2013; Nawar 2017; Shishehbor et al. 2022). In contrast, it has been reported that E. scutalis could not survive and develop to the adult stage on all life stages of the citrus flat mite, Breuipalpus lewisi McGregor (Bounfour & McMurtry 1987) and the eggs of Eutetranychus orientalis (Klein) (Momen & Abdel-Khalek 2008).

Based on the present results, the chosen diets had a direct influence on the duration of the different stages and therefore on the total pre-adult duration. In general, predators fed with T. turkestani developed more rapidly allowing E. scutalis to mature one day earlier than other diets (Table 1). The E. scutalis reared on Bemisia tabaci (Genn.) and Insulaspis pallidula (Green) showed a longer pre-adult duration (6.5 and 6.75 d, respectively) under the same experimental conditions than what we obtained on T. turkestani (Abou-Elella et al. 2013; Nawar 2017). In addition, those fed with Tetranychus urticae Koch (4.2 d), E. orientalis (4.7 d), and Phoenicococcus marlatti Cockerell (5.25 d) showed a developmental time similar to our data on T. turkestani (Abou-Elella et al. 2013; Nawar 2017). Euseius scutalis had a much longer immature development when fed on eggs of E. orientalis (8.13 d) and some artificial diets (13.9 d) (Abou-Awad et al. 1992; Momen & Abdel-Khalek 2008). This difference could be explained by the fact that the nutrient content varies between the diets, especially protein.

The findings of the present study showed that a total average number of 31.14 eggs per female and a daily rate of 2.77 eggs per female per day were laid by females E. scutalis provided with T. turkestani. However, our results on T. turkestani were similar to the values obtained on this prey (23.61 eggs per female) (Shishehbor et al. 2022), T. urticae (28.63 and 29.68 eggs per female) (Osman et al. 2013), and B. tabaci (24.30 eggs per female) (Fouly et al. 2013) on one hand; but higher than the results of El-Laithy and Fouly (1992) (on T. urticae, 13.5 eggs per female), and Momen and Abdel-Khalek (2008) (on E. orientalis nymphs and Icerya aegypticain (Douglas), 21.81 and 20.50 eggs, respectively) on the other hand. A higher total egg production of this predator was recorded by Kasap (2004) when offered Panonychus citri (McGregor). Furthermore, in our study, where pollen grains were offered as food, the total fecundity ranged from 12.64 (on castor bean) to 17.39 eggs per female (on date palm pollen). It was considerably lower than other studies investigating the effects of caster bean, corn, date, cattail, alfalfa, and bee pollen on E. scutalis efficacy (Allawi 1991; Al-Shammery 2011; Abou-Elella et al. 2013; Shishehbor et al. 2022). Differences in prey and pollen quality, experimental temperature levels, data analysis, and local populations are the main factors explaining the difference between the results of different studies. As Reuveny et al. (1996) showed, there can be variations in the life history parameters of a species collected from different geographic regions.

We found that E. scutalis developed faster, lived longer, and reproduced higher on T. turkestani than on pollen grains. Similarly, this predator showed a preference for tetranychid mites over the pollen (Abd-Elgayed & El-Khouly 2019; Shishehbor et al. 2022). By contrast to our results, better reproduction on pollen than on arthropods was documented by some authors for different Euseius species. Better demographic parameters of E. scutalis were observed on pollen than on arthropod prey, Aceria ficus (Cotte), Rhyncaphytoptus ficifoliae Keifer, E. orientalis, and I. aegyptica (Momen & Abdel-Khalek 2008). Pollen grains increased the reproductive value and population growth rate and decreased the mean generation time of E. scutalis compared to T. urticae (Fouly et al. 2013). Other species such as Euseius finlandicus (Oudemans) (Abdallah et al. 2001), Euseius tularensis (Congdon), E. hibisci (Chant), and E. stipulatus (Athias-Henriot) (Zhimo & McMurtry 1990), along with Euseius yousefi Zaher and El-Borolossy (Momen 2004) showed the same preference.

Among three pollen grains tested in this study, it was clarified that date palm pollen improved survival, accelerated development, and caused oviposition to start earlier. In addition, adult longevity and mean generation time were shorter, the oviposition period was longer, and fecundity was higher than on other pollen grains. Therefore, date palm pollen was more favorable for E. scutalis than the two other pollen grains. It was also introduced as the most suitable pollen for this predatory mite previously (Allawi 1991; Nomikou et al. 2001, 2003; Maoz et al. 2011). Furthermore, more superior life table parameters of E. scutalis were indicated when fed on date palm pollen than castor bean pollen (Momen & Abdel-Khalek 2008; Al-Shammery 2011). In another study, cattail and date palm pollen were introduced as the most appropriate alternative diet origins for straightforward and cost-effective rearing of E. scutalis (Shishehbor et al. 2022). This pollen has also been recommended as the best food source for other phytoseiid species, Typhlodromips swirskii (Athias-Henriot) (Ali & Zaher 2007; Abou-Elella et al. 2013), and Amblyseius swirskii Athias-Henriot (Rahmani Piyani et al. 2021).

In general, all diets tested in this study were adequate for development to maturity and oviposition in E. scutalis, but T. turkestani was the most favorable diet; it shortened the developmental and pre-oviposition periods, increased the growth rate and egg production, and extended adult longevity. Consequently, the role of this predator in the biocontrol of this pest is of most importance. In addition, date palm pollen was an ample useful alternative food source that accelerated the survival and reproduction of E. scutalis and it can be used for easy rearing of this predator in the laboratory as well as conservation of predator population during prey scarcity or absence. Further research is required to better understand the effectiveness of this predator on other pollen grains (from different plant species) and against various insects and mites. In addition, since pollen's nutritional composition varies from one plant species to another, more work analyzing the pollen composition is recommended.

Acknowledgement

Financial support (Grant no. SCU.AP1401.400) provided by the research deputy of Shahid Chamran University of Ahvaz, Ahvaz, Iran is gratefully acknowledged.

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