Life history of the predatory mites Amblyseius swirskii and Neoseiulus cucumeris (Acari: Phytoseiidae), candidates for biological control of the date palm mite, Oligonychus afrasiaticus (Acari: Tetranychidae)

doi:10.21203/rs.3.rs-1983865/v1

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Life history of the predatory mites Amblyseius swirskii and Neoseiulus cucumeris (Acari: Phytoseiidae), candidates for biological control of the date palm mite, Oligonychus afrasiaticus (Acari: Tetranychidae)

https://doi.org/10.21203/rs.3.rs-1983865/v1

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The date palm mite, Oligonychus afrasiaticus (McGregor) (Acari: Tetranychidae), is a serious pest of dates in the Middle East and North Africa, inflicting severe economic damage if not controlled. As predaceous mites are known as potential biocontrol agents against several pests, predation capacity, life table, reproduction and survival of Amblyseius swirskii Athias-Henriot and Neoseiulus cucumeris (Oudemans) (Acari: Phytoseiidae), collected from date palm farms, were studied in a laboratory setting (25, 30, 35°C and 50 ± 5% RH) against all motile stages of O. afrasiaticus. For both predators, mean developmental time, oviposition period and longevity were inversely related to temperature from 25 to 35°C. The following parameters were obtained for A. swirskii and N. cucumeris at 25, 30 and 35°C, respectively: Female developmental time, 9.37, 7.29, 5.56, 10.67, 8.38, 6.45 d; oviposition period, 19.77, 16.18, 13.94, 15.90,13.84,10.64 d; longevity, 29.39, 24.79, 20.64, 25.42, 21.94, 17.39 d; fecundity, 31.91, 37.10, 42.16, 21.75, 26.84, 30.56 eggs per female. For both predators, the maximum daily predation rate was recorded at 35°C and occurred during the oviposition period. Total predation of A. swirskii and N. cucumeris female was 370.86, 387.54, 405.83, 232.14, 263.32, 248.85 prey at 25, 30 and 35°C, respectively. The maximum reproduction rate of A. swirskii and N. cucumeris (3.02, 2.87 eggs/♀/day) was recorded at 35°C while the minimum one (2.00, 1.36 eggs/♀/day,) was recorded at 25°C. Life table parameters were estimated as net reproductive rate (R_o) 21.68, 25.94, 29.52,18.95, 20.25, 22.78, Mean generation time (T) 24.92, 21.82, 18.24, 26.30, 23.60, 20.56 d, intrinsic rate of increase (r_m) 0.181, 0.232, 0.248, 0.170, 0.185, 0.196, finite rate of increase (λ) 1.365, 1.551, 1.706, 1.126, 1.324, 1.428 for A. swirskii and N. cucumeris at 25, 30 and 35°C, respectively. The results of this study suggested that the two phytoseiid species are promising biological control agents of O. afrasiaticus at a wide range of temperatures.

Phytoseiidae

biological control

Saudi Arabia

Oligonychus afrasiaticus

The date palm mite, Oligonychus afrasiaticus (McGregor) (Acari: Tetranychidae), is a serious pest of the dates in the Middle East and North Africa. It causes severe economic damage by feeding and constructing complex dense webs on the fruit bunches and causing reductions in yields of 30–100% if not controlled (Zaher et al. 1982; Palevsky et al. 2004; Arbabi et al. 2010; Ben Chaaban et al. 2011). Traditional control of O. afrasiaticus has relied heavily on chemical options (Al-Dosary 2010). Although chemical pesticides used to control phytophagous mites show effective results in a short time, over the long term they cause some significant health and environmental problems. These problems include the killing of beneficial organisms (Herron et al. 2007; Alhewairini and Al-Azzazy 2021), resistance development in mites to miticides (Whalon et al. 2008; Tang et al. 2014; İnak et al. 2019), and environmental contamination (Hernández et al. 2011; Hoai et al. 2011). Because of the aforementioned problems, a strategy that reduces the use of chemical pesticides should be considered, such as biocontrol agents for the management of phytophagous mites and other pests of date palm. Biocontrol has been one of the most environmentally safe and most economical strategies of pest management for farmers and a potential method of reducing the cost of chemical pesticides applications and preventing resistance

(Cock et al. 2010). The exploitation of indigenous natural enemies that occur in and around date palm orchards are key elements of biocontrol programs against spider mites and essential for sustainability and food security. In particular, phytoseiid mites play a major role in controlling insects and phytophagous mites in several countries around the world (McMurtry and Croft, 1997; Palevsky et al. 2009; McMurtry et al. 2013; Al-Azzazy et al. 2022). Amblyseius swirskii Athias-Henriot is an especially important species from the perspective of biocontrol and a polyphagous predator capable of preying on a broad range of food items, including tarsonemids (Onzo et al. 2012), pollen as food (Goleva and Zebitz 2013), thrips (Chow et al. 2010; Delisle et al. 2015), whiteflies (Cavalcante et al. 2015), eriophyids (Al-Azzazy and Alhewairini 2020) and T. urticae (Fathipour et al. 2021). Like A. swirskii, Neoseiulus cucumeris (Oudemans) is a generalist foliar predator and an effective biocontrol agent against broad mites (Weintraub et al. 2003), thrips (Arthurs et al. 2009), spider mites (Easterbrook et al. 2001), eriophyid mites (Al-Azzazy et al. 2018) and Tuta absoluta (Meyrick) (Al-Azzazy et al. 2022). The natural occurrence of these predators was reported at different regions of Saudi Arabia (Fouly and Rehiayani 2011; Al-Atawi 2011a). Moreover, a preliminary experiment to maintain stock culture of A. swirskii and N. cucumeris in the laboratory offering O. afrasiaticus as prey was very successful and encouraged further experiments. On the other hand, as far as we know, there is no study to date, which has examined the potential of A. swirskii or N. cucumeris on O. afrasiaticus as food source in Saudi Arabia or anywhere else. Therefore, in this paper, we evaluated the potential efficiency of A. swirskii and N. cucumeris in biological control of the date palm mite, O. afrasiaticus. The biological responses of A. swirskii and N. cucumeris have been planned to be used for getting its life-table parameters and to investigate the potential of these two phytoseiids as predators of O. afrasiaticus.

Collection and rearing of predators

Amblyseius swirskii and N. cucumeris were obtained from unsprayed date palm orchards at the Agricultural Experimental Station, Qassim University, Al-Mulida district (26.297875° N, 43.790684° E), Saudi Arabia. Amblyseius swirskii was collected from Cynodon dactylon (Poaceae) while N. cucumeris was collected from Convolvulus arvensis (Convolvulaceae) and O. afrasiaticus was obtained from severe infested date palm trees. Colonies of predatory mites were maintained separately on rearing arenas made of kidney bean (Phaseolus vulgaris L.) leaves, which were placed upside down on water-saturated cotton in plastic trays (10 × 20 cm in length, 2 cm height), in an incubator at 32°C, 55–65% RH and 16L:8D photoperiod. Predators were transferred to new rearing arenas after 4–6 d. Water was added to the plastic trays daily to keep the level of water stable and to maintain leaf freshness. The edges of bean leaves were covered with strips of wet tissue paper to prevent mites from escaping and contamination with other mites. The predatory mites were continuously fed a mixture of different stages of O. afrasiaticus according to (Negm et al. 2014). Predator eggs were collected from the stock colony and transferred individually to the new rearing units to obtain cohorts of individuals of the same age for the subsequent experiments.

Experimental Units And Conditions

The development, survival, predation rate and fecundity of A. swirskii and N. cucumeris against O. afrasiaticus were monitored at three constant temperatures (25, 30 and 35°C), Light: Dark (L:D) = 8:16 (h) photoperiod and 55 ± 5% relative humidity (RH). The predatory mites were reared individually on bean leaf disks (3 cm in diameter), which were placed upside down on moist cotton wool, inside a Pyrex® Petri dish (6 cm in diameter × 2 cm high), which was kept permanently open. In addition, distilled water was added daily to the Petri dishes to maintain moist cotton. Likewise, every 5 or 6 d, the predators were relocated to new rearing arenas. Mite eggs laid (within a 7 h period) were collected for the life table study. A total of 40 eggs of each predator were obtained randomly and transferred individually into new rearing units with a fine hair brush. After the emergence of protonymphs, mixed stages of O. afrasiaticus were supplied daily as food. Preliminary trials confirmed that immature stages of N. cucumeris and A. swirskii rarely fed on O. afrasiaticus adult females, thus this prey phase was ignored. In addition to the number of preys supplied to each predator was determined based on these experiences. Different numbers of O. afrasiaticus were supplied to different stages of A. swirskii and N. cucumeris: 10 preys of different mobile stages for protonymph, 15 for deutonymph and 40 for an adult pair (male and female), for 24 hours after which the number of preys consumed was recorded. Observations were carried out every 12 hours, and developmental times of egg, larva, nymphs and survivorship were recorded for both females and males. The survival rate to adult stage was calculated. Death of individuals was set at the mid-point between the first record of death and the last observation alive.

Observations were made using stereo microscope (Olympus Optical, Japan). After the emergence of adults, females and males were paired for mating and checked daily to record pre-, ovi- and post-oviposition periods, reproduction and longevities as well as gathering data on fecundity. To ensure successful multiple mating male and female was kept together until their death. To separate the consumption capacity of males from females, the consumption rate of 25 males was tested under same conditions. Then, the number of preys devoured of male was deducted from the average preys consumed of the couples (Moghadasi et al. 2014). To test the sex ratio, 30 eggs of each predator were obtained and transferred individually into separate rearing units with a fine camel hair brush and the hatched larvae were reared until to adulthood. Then, each individual was mounted on a slide for sex determination.

Statistical Analysis

To assess the developmental time of immature stages, generation, pre-oviposition and post-oviposition periods, total fecundity, adult longevity, predation and life span of N. cucumeris and A. swirskii and the effect of three constant temperatures on these parameters, data were compared with analysis of variance (ANOVA). using SAS computer program version 9.2 (SAS 2008). Means were separated by Duncan’s Multiple Range Test (DMRT) at P < 0.05. The means of survival rates were separated using Tukey’s Honestly Significant Difference test (Tukey’s HSD test).

Observations on the development times, survival, fecundity, and adult longevity of N. cucumeris and A. swirskii were used to construct a time-specific life table in a laboratory setting. Life table parameters for both predators were measured based on Birch (1948). Sex ratio for both predators were analysed using a Chi-square test.

Development of immatures, survival rate and adult longevity of A. swirskii and N. cucumeris

Amblyseius swirskii and N. cucumeris successfully preyed on O. afrasiaticus and reached maturity over all temperatures tested (25–35°C). The developmental time was significantly related to temperatures between 25°C and 35°C for all developmental stages. On both predators, with rising temperature, the duration of each separate life stage and the total immature phase decreased: egg to adult development of A. swirskii was slowest at 25°C (on average 9.03 days for males and 9.37 days for females) and fastest at 35°C (5.41 days for males and 5.56 days for females) while for N. cucumeris it decreased from (10.21 days for males and 10.67 days for females) at 25°C to (6.25 days for males and 6.45 days for females) at 35°C (Table 1). For both predators more than 95% of eggs hatched at 25–35°C, and there was no significant difference among temperatures, further, at all temperatures tested, survival rate of A. swirskii from larvae to adult was more than 96% while for N. cucumeris it decreased from 91.40% at 35 to 84.62% at 25 (Table 2). Increasing temperature from 25 to 35°C had a significant effect on generation period and female longevity.

At 25°C, the generation period and female longevity lasted (13.19 and 29.39 days for A. swirskii) and (14.93 and 25.42 days for N. cucumeris) (Table 2). At 35°C, the corresponding periods were (7.72 and 20.64 days for A. swirskii) and (8.35 and 17.39 days for N. cucumeris). At all temperatures between 25°C and 35°C, all emerged females lay eggs within 3.82–2.16 days for A. swirskii and 4.26–1.90 days for N. cucumeris (pre-oviposition period). Likewise, oviposition period was significantly influenced by increasing temperature. The maximum oviposition periods (19.77 and 15.90 days) were recorded at 25°C, while the minimum oviposition periods (13.94 and 10.64 days) were recorded at 35°C for A. swirskii and N. cucumeris, respectively. The post-oviposition periods of A. swirskii and N. cucumeris did not differ between the three temperatures studied. The life span period, as well, followed the same trend on the three different temperatures (F = 12.23; df = 3, 28; P = 0.0006).

Table 1

Average duration of the immature stages of *A. swirskii* and *N. cucumeris* feeding on *O. afrasiaticus* at 25, 30, 35°C and 50 ± 5% RH
Predator species	Temperature (°C)	Sex	Egg	Larva	Protochrysalis	Protonymph,	Deutochrysalis,	Deutonymph,	Teleiochrysalis,	Developmental time
Amblyseius swirskii	25 ± 1	Female Male	3.80 ± 0.16a 3.75 ± 0.14a	1.65 ± 0.10a 1.57 ± 0.12a	0.24 ± 0.04a 0.20 ± 0.03a	1.80 ± 0.16a 1.77 ± 0.12a	0.22 ± 0.06a 0.20 ± 0.04a	1.40 ± 0.12a 1.30 ± 0.14a	0.26 ± 0.03a 0.24 ± 0.02a	9.37 ± 0.82a 9.03 ± 0.74a
	30 ± 1 35 ± 1	Female Male Female Male	3.22 ± 0.15b 3.15 ± 0.10b 2.50 ± 0.18c 2.49 ± 0.12c	1.10 ± 0.07b 1.05 ± 0.08b 0.90 ± 0.02c 0.80 ± 0.04c	0.18 ± 0.03b 0.16 ± 0.03b 0.10 ± 0.03c 0.10 ± 0.02c	1.35 ± 0.10b 1.32 ± 0.12b 0.95 ± 0.04c 0.95 ± 0.03c	0.16 ± 0.04b 0.16 ± 0.03b 0.15 ± 0.03b 0.15 ± 0.02b	1.10 ± 0.06b 1.05 ± 0.04b 0.80 ± 0.02c 0.76 ± 0.02c	0.18 ± 0.02b 0.18 ± 0.03b 0.16 ± 0.02b 0.16 ± 0.03b F = 0.938;	7.29 ± 0.36b 7.07 ± 0.42b 5.56 ± 0.23c 5.41 ± 0.32c P = 0.475
Neoseiulus cucumeris	25 ± 1	Female Male	3.95 ± 0.20a 3.80 ± 0.20a	1.70 ± 0.16a 1.62 ± 018a	0.26 ± 0.04a 0.22 ± 0.03a	1.95 ± 0.18a 1.85 ± 0.16a	0.36 ± 0.08a 0.34 ± 0.06a	2.15 ± 0.12a 2.10 ± 0.11a	0.30 ± 0.08a 0.28 ± 0.04a	10.67 ± 0.74a 10.21 ± 0.68a
	30 ± 1	Female Male	3.42 ± 0.10b 3.32 ± 0.18b	1.12 ± 0.20b 1.10 ± 0.16b	0.18 ± 0.03b 0.18 ± 0.04b	1.40 ± 0.16b 1.35 ± 0.14b	0.28 ± 0.06b 0.26 ± 0.06b	1.77 ± 0.14b 1.72 ± 0.09b	0.21 ± 0.06 b 0.19 ± 0.04 b	8.38 ± 0.56b 8.12 ± 0.84b
	35 ± 1	Female Male	2.61 ± 0.20c 2.57 ± 0.16c	0.95 ± 0.08c 0.90 ± 0.08c	0.12 ± 0.04c 0.10 ± 0.04c	1.05 ± 0.08c 1.00 ± 0.04c	0.25 ± 0.08b 0.25 ± 0.06b	1.29 ± 0.08c 1.25 ± 0.06c	0.18 ± 0.03 b 0.18 ± 0.02 b F = 1.29;	6.45 ± 0.59c 6.25 ± 0.67c P = 0.391
Different letters in each column denote significant differences (ANOVA followed by Duncan’s multiple range test: P < 0.05).

Table 2

Mean duration of *A. swirskii* and *N. cucumeris* adults feeding on *O. afrasiaticus* at 25, 30, 35°C and 50 ± 5% RH.
Predator species	Temperature (°C)	Pre oviposition	Generation	Oviposition	Post oviposition	Longevity		Life span
Predator species	Temperature (°C)	Pre oviposition	Generation	Oviposition	Post oviposition	Female	Male	Female	Male
Amblyseius swirskii	25 ± 1	3.82 ± 0.20a	13.19 ± 0.62a	19.77 ± 0.1.40a	5.80 ± 0.70a	29.39 ± 1.30a	26.55 ± 1.19a	38.76 ± 1.20a	35.58 ± 2.46a
	30 ± 1	2.95 ± 0.17b	10.24 ± 0.43b	16.18 ± 0.80b	5.66 ± 0.28a	24.79 ± 0.87b	22.11 ± 1.22b	32.08 ± 1.61b	29.18 ± 1.58b
	35 ± 1	2.16 ± 0.12c	7.72 ± 0.42c	13.94 ± 0.84c	4.54 ± 0.38b	20.64 ± 0.92c	18.89 ± 0.75c	26.20 ± 1.14c F = 0.912;	24.30 ± 1.34c P = 0.467
Neoseiulus cucumeris	25 ± 1	4.26 ± 0.38a	14.93 ± 0.83a	15.90 ± 0.78a	5.26 ± 0.41a	25.42 ± 1.18a	23.74 ± 1.33a	36.09 ± 1.47a	33.95 ± 1.76a
	30 ± 1	3.15 ± 0.27b	11.53 ± 0.66b	13.84 ± 73b	4.95 ± 0.36a	21.94 ± 1.25b	20.78 ± 1.42b	30.32 ± 1.45b	28.90 ± 1.62b
	35 ± 1	1.90 ± 0.20c	8.35 ± 0.39c	10.64 ± 0.54c	4.85 ± 0.32a	17.39 ± 0.85c	15.11 ± 0.98c	23.84 ± 1.06c F = 1.18;	21.36 ± 1.18c P = 0.386

Different letters in each column denote significant differences (ANOVA followed by Duncan’s multiple range test: P < 0.05).

Table 3

Survival of immature stages of *A. swirskii* and *N. cucumeris* feeding on *O. afrasiaticus* at 25, 30, 35°C and 50 ± 5% RH
Predator species	Temperature (°C)	Stage specific survival (% ± SE)				Survival to Adulthood (% ± SE)
Predator species	Temperature (°C)	Egg	Larva	Protonymph	Deutonymph	Survival to Adulthood (% ± SE)
A. swirskii	25 ± 1	95.00 ± 4.51 a	93.51 ± 3.66 a	95.77 ± 3.60 a	97.14 ± 2.82 a	96.21 ± 3.61a
	30 ± 1	96.87 ± 3.63 a	97.21 ± 3.63 a	94.52 ± 4.08 a	100 a	97.50 ± 3.65a
	35 ± 1	98.42 ± 4.57 a	96.22 ± 4.11 a	96.00 ± 3.95 a	95.70 ± 5.36 a	98.11 ± 3.82 a
N. cucumeris	25 ± 1	95.00 ± 2.45 a	94.59 ± 2.58 a	90.64 ± 2.94 a	88.19 ± 2.45 b	84.62 ± 3.46b
	30 ± 1	95.82 ± 3.46 a	94.44 ± 3.25 a	90.10 ± 3.77 a	100 a	90.25 ± 3.98a
	35 ± 1	97.50 ± 4.77 a	95.50 ± 4.68 a	91.12 ± 4.23 a	91.46 ± 3.08 a	91.40 ± 3.12 a
Means in the same column followed by the different letters are significantly different (P < 0.05) according Tukey HSD test.

Reproduction

Temperature exerted the greatest effect on the reproductive of A. swirskii and N. cucumeris. Furthermore, increasing temperatures from 25°C to 35°C progressively increased the daily rate of reproduction. The number of total laid eggs by each female of A. swirskii and N. cucumeris at 25°C was significantly lower than that at 30°C and 35°C (Table 5). N. cucumeris laid significantly fewer eggs than A. swirskii over all temperatures tested (25–35°C). The maximum fecundity (42.16 eggs/♀) was recorded for A. swiirskii while it was (30.56 eggs/♀) for N. cucumeris at 35°C, while the minimum (31.91 and 21.75 eggs/♀) was at 25°C for A. swirskii and N. cucumeris, respectively. At all temperature studied, A. swirskii deposited more eggs than N. cucumeris (Table 4). Further, raising the temperature from 25 to 35°C increased oviposition rate. The maximum oviposition (3.02 and 2.54 eggs/♀/day) was recorded at 35°C, while the minimum (2.00 and 1.36 eggs/♀/d) was at 25°C for A. swirskii and N. cucumeris, respectively. As shown in Table 8, sex ratio at the different temperatures ranged from 60 to 80%. There were insignificant differences among 30 and 25°C, but the maximum female-biased sex ratio was 80%, which was recorded for A. swirskii at 35°C. For each predatory mite species, Female-to-male offspring ratio was about (A. swirskii, 2:1, 2:1 and 2.4:1; N. cucumeris,1.8:1, 1.9:1 and 2.2:1), at 25, 30 and 35°C, respectively (Table 4).

Table 4

Fecundity of *A. swirskii* and *N. cucumeris* feeding on *O. afrasiaticus* at 25, 30, 35°C and 50 ± 5% RH.
Temperature (°C)	Amblyseius swirskii		Neoseiulus cucumeris
Temperature (°C)	Average of eggs ± SD	Daily egg-laying rate	Average of eggs ± SD	Daily egg-laying rate
25 ± 1	31.91 ± 1.45 Aa	2.00	21.75 ± 1.62 Ab	1.36
30 ± 1	37.10 ± 1.88 Bb	2.68	26.84 ± 1.14 Bc	1.93
35 ± 1	42.16 ± 1.53 Cc	3.02	30.56 ± 1.90 Cd	2.87

The capital letter denotes the significance within the same column and small letter denotes the significance within the same row at P < 0.05.

Predation of A. swirskii and N. cucumeris

The larvae of both predators were inactive and did not feed during the experiment, and feeding activity started immediately after the predators entered the protonymphal stages. For both predators, the predation rate increased by increasing the temperatures and stage of the predator, so the adults consumed more prey compared with the nymph stages. Data analysis showed a significant effect of temperature on the total and daily predation rates of A. swirskii and N. cucumeris. The total number of O. afrasiaticus prey devoured by A. swirskii and N. cucumeris immature and adult stages under different temperatures are shown in Tables 5, 6 and 7. Immature females of A. swirskii significantly consumed a higher number of prey (21.87, 23.80 and 18.01) than N. cucumeris (17.46, 18.99 and 17.73) at 25, 30 and 35°C respectively. likewise, at 35°C, A. swirskii significantly devoured more prey (308.68) than N. cucumeris (173.43) throughout the oviposition duration (Table 3). The highest means for the daily consumption rate of females were observed throughout the oviposition period, with the female of A. swirskii devoured an average of 13.52, 16.86 and 22.14, while with the female of N. cucumeris devoured an average of 10.24, 13.11, and 16.58 at 25, 30 and 35°C, respectively. Therefore, the optimal temperature for predation of A. swirskii and N. cucumeris were about 35°C. Thereafter, daily consumption of predators fed on O. afrasiaticus decreased with age. The highest number of preys consumed during the life span was reported for A. swirskii females at 35°C (405.83 prey) while for N. cucumeris it was 248.85 prey. So, it could be concluded that A. swirskii performance was better than N. cucumeris against O. afrasiaticus.

Table 5

Predation rate by different stages of *A. swirskii* and *N. cucumeris* feeding on *O. afrasiaticus* at 25, and 50 ± 5% RH.
Predatory stage	Sex	A. swirskii
		No. of attacked mite individuals
		Total average mean ± SD	Daily rate, mean ± SD	Total average mean ± SD	Daily rate, mean ± SD
Protonymph	Female Male	9.40 ± 0.61 9.45 ± 0.52	5.20 ± 0.24 5.33 ± 0.32	6.30 ± 0.28 5.95 ± 0.30	3.23 ± 0.20 3.21 ± 0.28
Deutonymph	Female Male	12.47 ± 0.62 11.55 ± 0.76	8.90 ± 0.46 8.88 ± 0.69	11.16 ± 0.42 10.75 ± 0.45	5.19 ± 0.40 5.11 ± 0.24
Total	Female Male	21.87 ± 1.14a 21.00 ± 0.98	6.83 ± 0.62a 6.84 ± 0.57	17.46 ± 0.80b 16.70 ± 0.38	4.25 ± 0.30b 4.22 ± 0.35
Pre-oviposition	Female	40.25 ± 1.30	10.53 ± 0.78	29.96 ± 1.54	7.03 ± 0.45
Generation	Female	61.12 ± 2.14a	4.63 ± 0.20a	47.42 ± 1.56b	3.17 ± 0.20b
Oviposition	Female	267.46 ± 3.61a	13.52 ± 0.45a	162.97 ± 2.75b	10.24 ± 0.62b
Post-oviposition	Female	41.28 ± 1.22	7.11 ± 0.88	21.75 ± 1.24	4.13 ± 0.25
Longevity	Female Male	348.99 ± 3.64a 243.18 ± 2.17a	11.87 ± 0.65a9.15 ± 0.41a	214.68 ± 2.78b 148.61 ± 2.79b	8.44 ± 0.60b 6.26 ± 0.42b
Life span	Female Male	370.86 ± 4.28a 264.18 ± 2.54a	9.56 ± 0.29a 7.42 ± 1.58a	232.14 ± 3.66b 165.31 ± 2.45b	6.83 ± 0.28b 4.58 ± 0.22b

Means followed by different letters in each row for total average and daily rate separately denote significant differences (ANOVA followed by Duncan’s multiple range test: P < 0.05).

Table 6

Predation rate by different stages of *A. swirskii* and *N. cucumeris* feeding on *O. afrasiaticus* at 30, and 50 ± 5% RH
Predatory stage	Sex	A. swirskii
		No. of attacked mite individuals
		Total average mean ± SD	Daily rate, mean ± SD	Total average mean ± SD	Daily rate, mean ± SD
Protonymph	Female Male	10.05 ± 0.22 9.76 ± 0.36	7.44 ± 0.32 7.39 ± 0.25	6.32 ± 0.20 6.02 ± 0.26	4.51 ± 0.18 4.45 ± 0.24
Deutonymph	Female Male	13.75 ± 0.41 13.08 ± 0.26	12.50 ± 0.28 12.45 ± 0.36	12.67 ± 0.36 11.85 ± 0.20	7.20 ± 0.32 6.88 ± 0.28
Total	Female Male	23.80 ± 0.74a 22.84 ± 0.60	9.71 ± 0.88a 9.63 ± 0.72	18.99 ± 0.42b 17.87 ± 0.52	5.99 ± 0.22b 5.82 ± 0.31
Pre-oviposition	Female	41.65 ± 1.40	14.11 ± 0.50	32.09 ± 1.52	10.18 ± 0.60
Generation	Female	65.45 ± 1.88a	6.93 ± 0.30a	51.08 ± 1.47b	4.43 ± 0.32b
Oviposition	Female	272.89 ± 2.56a	16.86 ± 0.75a	181.56 ± 2.35b	13.11 ± 0.54b
Post-oviposition	Female	49.20 ± 1.58	8.69 ± 0.43	30.68 ± 0.72	6.19 ± 0.22
Longevity	Female Male	363.74 ± 3.50a 247.11 ± 2.42a	14.67 ± 0.55a11.17 ± 0.36a	244.33 ± 3.40b 169.35 ± 2.44b	11.13 ± 0.59b 8.14 ± 0.35b
Life span	Female Male	387.54 ± 3.49a 264.18 ± 2.28a	12.08 ± 0.26a 8.46 ± 0.22a	263.32 ± 4.15b 187.22 ± 2.30b	8.68 ± 0.36b 6.47 ± 0.28b

Means followed by different letters in each row for total average and daily rate separately denote significant differences (ANOVA followed by Duncan’s multiple range test: P < 0.05).

Table 7

Predation rate by different stages of *A. swirskii* and *N. cucumeris* feeding on *O. afrasiaticus* at 35, and 50 ± 5% RH
Predatory stage	Sex	A. swirskii
		No. of attacked mite individuals
		Total average mean ± SD	Daily rate, mean ± SD	Total average mean ± SD	Daily rate, mean ± SD
Protonymph	Female Male	8.35 ± 0.10 7.74 ± 0.18	11.13 ± 0.28 11.05 ± 0.20	5.71 ± 0.24 5.20 ± 0.18	5.43 ± 0.20 5.20 ± 0.26
Deutonymph	Female Male	9.66 ± 0.30 9.53 ± 0.26	16.10 ± 0.32 15.88 ± 0.40	12.02 ± 0.20 11.50 ± 0.18	9.31 ± 0.30 9.20 ± 0.22
Total	Female Male	18.01 ± 0.35a 17.27 ± 0.30	13.34 ± 0.64a 13.28 ± 0.60	17.73 ± 0.56a 16.70 ± 0.46	7.57 ± 0.34b 7.42 ± 0.28
Pre-oviposition	Female	39.42 ± 1.05	18.25 ± 0.75	25.59 ± 1.13	13.46 ± 0.72
Generation	Female	57.43 ± 1.22a	7.43 ± 0.44a	43.32 ± 1.08b	5.18 ± 0.41b
Oviposition	Female	308.68 ± 3.47a	22.14 ± 0.68a	173.43 ± 2.77b	16.58 ± 0.60b
Post-oviposition	Female	39.72 ± 1.18	8.74 ± 0.35	32.10 ± 0.65	6.61 ± 0.34
Longevity	Female Male	387.82 ± 4.66a 271.58 ± 2.92a	18.78 ± 0.74a14.37 ± 0.51a	231.12 ± 3.55b 158.94 ± 2.85b	13.29 ± 0.36b 10.51 ± 0.38b
Life span	Female Male	405.83 ± 4.72a 288.85 ± 3.11a	15.48 ± 0.68a 11.88 ± 0.28a	248.85 ± 3.54b 175.64 ± 2.21b	10.43 ± 0.45b 8.22 ± 0.51b

Means followed by different letters in each row for total average and daily rate separately denote significant differences (ANOVA followed by Duncan’s multiple range test: P < 0.05).

Effect of O. afrasiaticus on life table parameters of A. swirskii and N. cucumeris

The life table parameters are in harmony with the abovementioned findings. Both predators performed much preferably at relatively higher temperatures because of its rapid population growth rate therefore high oviposition (R_o) and short mean generation time (T), in contrast with low temperatures. Net reproductive rate (R_o) was 21.68, 25.94 and 29.52 females per female for A. swirskii and 18.95, 20.25 and 22.78 for N. cucumeris, at 25, 30 and 35°C, respectively (Table 8). The intrinsic rate of increase (r_m), and the finite rate of increase (λ) reached the maximal value at 35°C. The value of r_m varied from 0.181 to 0.248; 0.170 to 0.196 ♀/♀/day, and the finite rate of increase (λ) from 1.365 to 1.706; 1.126 to 1.428 at 25°C and 35° C for A. swirskii and N. cucumeris, respectively. Mean generation time (T), for A. swirskii and N. cucumeris, was longer at 25°C than at 35°C.

Table 8

Life table parameters of *A. swirskii* and *N. cucumeris* on *O. afrasiaticus* at 25, 30, 35°C and 50 ± 5% RH.
Parameters	25 ± 1°C; 50% RH		30 ± 1°C; 50% RH		35 ± 1°C; 50%RH
Parameters	A. swirskii	N. cucumeris	A. swirskii	N. cucumeris	A. swirskii	N. cucumeris
Net reproduction rate (R_o)	21.68	18.95	25.94	20.25	29.52	22.78
Mean generation time, t (days)	24.92	26.30	21.82	23.60	18.24	20.56
Intrinsic rate of increase (r_m)	0.181	0.170	0.232	0.185	0.248	0.196
Finite rate of increase (λ)	1.365	1.126	1.551	1.324	1.706	1.428
50% mortality (in day)	35	32	28	26	22	20
Sex ratio (Female/total)	24/30	18/30	20/30	19/30	20/30	22/30

Since effective agents for the biocontrol of O. afrasiaticus were not known previously, this mite had been controlled only by acaricides (Al-Doghairi, A. M. 2004; Alhewairini et al. 2021). This study is the first documentation of the life history characteristics and predation capacity of A. swirskii and N. cucumeris on the date palm mite, O. afrasiaticus as prey. However, several research papers have been carried out on both predators when fed on mites, insects, plant pollen and artificial foods. The present study showed that, both predators A. swirskii and N. cucumeris developed and reproduced successfully when fed on O. afrasiaticus with few developmental mortalities at the three temperatures tested. For both predators, larvae developed to the protonymphal stages without feeding. Non-feeding larvae behavior may be beneficial for reducing intraspecific competition or mechanism to eschew sibling cannibalism. Similar results were obtained for other predacious phytoseiid species (Zhang and Croft 1994; Metwally et al. 2005; Al-Azzazy 2021). In an evaluation of the development of A. swirskii at 30°C on Phyllocoptruta oleivora (Ashmead) and Eutetranychus orientalis (Klein), the shortest life cycle was observed when A. swirskii fed on P. oleivora (Al-Azzazy and Alhewairini 2020). The developmental time of female immatures of A. swirskii fed on Cenopalpus irani Dosse and Eotetranychus frosti (McGregor) (Bazgir et al. 2018) were very close to the present results against O. afrasiaticus. A longer life cycle (22.1 days) was recorded when A. swirskii fed on cattail (Typha latifolia L.) pollen (Lee and Gillespie 2011). This decrease in developmental rate might be attributable to variances in the nutritional value of the prey provided. Overall, faster development is essential for biocontrol agents of phytophagous mites. On the other hand, development of N. cucumeris immature females was relatively longer in our study (10.67 days at 25°C) than reported when fed on Tetranychus urticae eggs (6.4 d at 25°C) (Li and Zhang 2016), slightly longer than the 26°C (6.25 days) when N. cucumeris were fed with T. urticae eggs, too (Kolodochka 1985). On the other side, the developmental time of female immatures of this predator preying on acarid mite, Tyrophagus curvipenis Fain & Fauve eggs and eggs of T. urticae (Li and Zhang, 2016; Li et al. 2021) was close to the present findings against O. afrasiaticus. Moreover, N. cucumeris were also reported to develop faster when fed on Aculops lycopersici, shorter than on mixed stage of T. urticae in the study conducted by (Al-Azzazy et al 2018). These results indicate that A. lycopersici provides N. cucumeris with higher reproductive capability than does O. afrasiaticus. So, we assumed that it is worth studying N. cucumeris on A. lycopersici for mass rearing purposes which may give encouraging results. Temperatures ranging from 25 to 35°C were more appropriate for the survival of N. cucumeris and A. swirskii. Survival rate of A. swirskii from larvae to adult was more than 96% while for N. cucumeris it decreased from 91.40% at 35 to 84.62% at 25. This information on their life history will be useful for their rearing and release in open field. The findings of Al-Azzazy and Alhewairini (2020) support our results. They revealed that the survival rate of A. swirskii during the immature phases exceeded 90% at all temperatures between 16°C and 30°C. Further, the survival rate of N. cucumeris were similar to the findings obtained when fed on T. urticae eggs (Li and Zhang, 2016). Pre-oviposition periods of A. swirskii and N. cucumeris were very close to those stated by (Ranabhat et al 2014; Bazgir et al. 2018). The oviposition duration and adult female longevity of A. swirskii were parallel to the findings reported by (Abou-Awad et al.1999), (Bazgir et al. 2018) and (Al-Azzazy and Alhewairini 2020) for A. swirskii feedin on Rhyncaphytoptus fucifoliae and Aceria ficus, E. frosti and C. irani and E. orientalis and P. oleivora. When Cydnoseius negevi was evaluated against O. afrasiaticus (Negm et al. 2014), female longevity was longer (31.80 d) than that of A. swirskii (29.39 d). This may be due to the lower humidity level applied for C. negevi. The oviposition duration and adult female longevity of N. cucumeris (15.90, 25.42 at 25°C and 10.64, 17.39 at 35°C) against O. afrasiaticus were close to that stated against Aleuroglyphus ovatus (Troupeau) (16.40, 26.40 at 25°C) (Ji et al. 2007) and (14.02, 18.36 at 35°C) when the predatory mite, N. cucumeris fed on T. urticae (Al-Azzazy et al 2018). In this work, the highest oviposition was obtained when A. swirskii fed on O. afrasiaticus (42.16 eggs/female at 35°C). This value was higher when compared to mites that fed on A. ficus (28.20 eggs/female at 29°C) and R. ficifoliae (20.40 eggs/female at 29°C) (Abou-Awad et al. 1999), on Cattail pollen, Typha latifolia L. (23.30 eggs/female at 30°C) (Lee and Gillespie 2011), on dried fruit mite (Carpoglyphus lactis L.) (29.03 eggs/female at 23°C) (Nguyen et al. 2014), E. frosti (34.69 eggs/female at 26°C) (Bazgir et al. 2018), furthermore, the findings of Goleva and Zebitz (2013) and Al-Azzazy and Alhewairini (2020) for A. swirskii fed on Schlumbergera hybrid pollens (50.85 eggs/female at 25°C) and P. oleivora (47.99 eggs/female at 30°C) respectively, were higher than that obtained in our finding. In this study, the maximum fecundity of N. cucumeris was 30.56 eggs at 35ºC that was higher than reported by Al-Shemmary (2018) (25.06 eggs) with feeding on Anagasta kuehniella eggs at 27°C. Also, N. cucumeris has shown total fecundity of 29.4 eggs at 22°C on Tyrophagus putrescentiae (Schrank) (Ji et al. 2007). On the other hand, the findings of Zilahi-Balogh et al. (2007), Ranabhat et al. (2014) and Al-Azzazy et al. (2018) for this predator fed on Frankliniella occidentalis (83.0 eggs/ female at 24°C), tulip pollen (89.48 eggs/ female at 25°C) and A. lycopersici (60.44 eggs/ female at 35°C) respectively, were considerably higher than the value estimated in the current study. The high fecundity for both predators in the current study might be due to multiple-mated incidence. In Kampimodromus aberrans, Pappas et al. (2007) showed that the females paired with a male during the lifespan with multiple mating gave the greatest fertility (28–30 eggs/female), while females with single mating had the lowest fertility (12 eggs/female). The sex ratio of predatory phytoseiid mites is characterized by a female bias (Sabelis, 1985b). This agrees with the current results of A. swirskii and N. cucumeris in addition to other previous studies (Dyer and Swift1979; Schausberger 1991; Al-Azzazy and Alhewairini 2020). During immature stages of A. swirskii and N. cucumeris, predation rate increased with increasing temperature from 25 to 35°C. Amblyseius swirskii immature females devoured 23.80 prey of O. afrasiaticus at 30°C, while they devoured 25.27 individuals of E. frosti and 29.92 of C. irani, respectively at 25°C (Bazgir et al. 2018), and 31.54 individuals of E. orientalis nymphs and 111.13 individuals of P. oleivora, respectively at 30°C (Al-Azzazy and Alhewairini 2020). So, it could be concluded that the Optimum temperature for predation of A. swirskii was ranged from 25–35°C. Neoseiulus cucumeris immature females devoured 18.99 prey of O. afrasiaticus at 30°C in this work, while they devoured 26.54 individuals of T. urticae and 123.67 of A. lycopersici, respectively at 30°C (Al-Azzazy et al. 2018), and 15.69 individuals of Tetranychus atlanticus at 26°C (Popov and Kondryakov 2008). Data obtained from predation of N. cucumeris on T. urticae (Sarwar et al. 2009) are close to that reported in this work against O. afrasiaticus. The findings of Zaher et al. (1969) and Al-Azzazy and Alhewairini (2020) support our results. They showed that an increase in temperature leads to a positive influence on predation rate until the optimum temperature is reached. Ganjisaffar et al. (2011) also reported that more preys are devoured as the temperature increases from 15 to 35°C. Many biological studies have confirmed that the nutritional quality of food sources resulted in higher values in life table parameters (Bouras and Papadoulis 2005; Park et al. 2011; Jiale et al. 2016). The rates of population growth were promising for A. swirskii fed on O. afrasiaticus. This is proven by (r_m) which was 0.248 at 35°C. The reported intrinsic rate of natural increase for predatory mite, A. swirskii on T. urticae (0.167 at 26°C) (El-Laithy and Fouly 1992), F. occidentalis (0.138 at 25°C) and T. tabaci (0.139 at 25°C) (Wimmer et al. 2008), T. latifolia (0.133 at 34°C) (Lee and Gillespie 2011), E. frosti (0.179 at 25°C), C. irani (0.140 at 25°C). (Bazgir et al. 2018), E. orientalis (0.204 at 30°C) (Al-Azzazy and Alhewairini 2020), was lower than that obtained in the current study when A. swirskii fed on O. afrasiaticus. Atefeh et al. (2021) estimated an r_m of 0.396 and 0.291 for A. swirskii fed on date palm pollen and Tetranychus turkestani at 25°C, respectively. Also (Al-Azzazy and Alhewairini 2020) estimated an r_m of 0.280 for A. swirskii fed on P. oleivora. This is somewhat higher than our estimate. The values of (R_o), (r_m) and (λ) of A. swirskii at 25°C and 50% RH are higher than reported for Euseius scutalis against O. afrasiaticus at 25°C and 70% RH (Al-Shammery 2010). A. swirskii performed better on O. afrasiaticus than E. scutalis, and this could be due to the moderate humidity level used according to (Al-Azzazy and Alhewairini 2020). In view of this, A. swirskii could be a useful biological control agent for O. afrasiaticus. In case of N. cucumeris against T. urticae and T. putrescentiae at 25°C, the life table parameters (r_m, λ, R_o) values were 0.164, 1.179, 18.39 and 0.096, 1.100, 15.16, respectively (Yazdanpanah et al. 2022), on date palm pollen (DPP), at 25°C, the parameters were 0.152, 1.165, 14.93 (Yazdanpanah et al. 2021) and on eriophyid mite, A. lycopersici, at 25°C, 0.211, 1.321, 20.47 (Al-Azzazy et al. 2018). while in the current study they were 0.170, 1.126, 18.95 at 25°C. This indicates that N. cucumeris performs well on O. afrasiaticus, as a generalist phytoseiid predator.

In summary, these results show that both predatory mites thrived on O. afrasiaticus making them promising biocontrol agents of that pest. Both species can also feed on the date palm pollen (Atefeh et al. 2021; Yazdanpanah et al. 2021). In a biocontrol context, the existence of alternative foods on date palms like date palm pollen may help to enhance the population densities of both predatory mites and allows predatory mites to increase when O. afrasiaticus is rare or absent and thus prevent severe declines in predatory mite populations during scarcities of primary prey. This can further contribute to the control of O. afrasiaticus. Finally, the results discussed above would help to gain well understanding of the effectiveness of A. swirskii and N. cucumeris, as facultative predators, in biological control programs of O. afrasiaticus. Hence, further trials should be performed to examine the performance of these predatory mites in combination and/or singly on O. afrasiaticus under field conditions.

Funding: No funding was provided for the work.

Conflict of interest: The author declares no conflict of interest that are relevant to the content of this manuscript.

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Life history of the predatory mites Amblyseius swirskii and Neoseiulus cucumeris (Acari: Phytoseiidae), candidates for biological control of the date palm mite, Oligonychus afrasiaticus (Acari: Tetranychidae)

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Abstract

Introduction

Materials And Methods

Collection and rearing of predators

Experimental Units And Conditions

Statistical Analysis

Results

Reproduction

Discussion

Declarations

References

Additional Declarations

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