Introduction

Phytoseiid predatory mites are important natural enemies of small arthropods, such as spider mites (Escudero et al. 2005; Badrbani et al. 2015), gall mites (Castagnoli et al. 2003), thrips (Calvo et al. 2011), and whiteflies (Seiedy et al. 2016), and could also complete their life cycle on pollens (Khanamani et al. 2017; Pascua et al. 2020). McMurtry & Croft (1997) and McMurtry et al. (2013) divided phytoseiid mites into four categories based on their life styles: specialized predators of Tetranychus species (type I), selective predators of tetranychid mites (type II), generalist predators (type III), and specialized pollen feeders (type IV). Generally, the first two categories are considered as specialist predators, while the latter two as generalist predators. Phytoseiid mites have a special reproductive method that female mites will not lay eggs if they do not mate (Amano & Chant 1978; Xu & Liang 1994; Hoy 1985, 2009), and all offspring developed from a zygote. The female is diploid and the male is haploid. Haploid male mites also develop from fertilized eggs, in which half of chromosomes were lost or heterogenized and occur 24–48 hours after egg laying (Nelson-Rees et al. 1980). This special reproductive mode of phytoseiid mites is called as Pseudoarrhenotoky (Hoy 1985; Nagalkerke & Sabelis 1998; Sabelis et al. 2002).

Prey species is an important factor that affects reproductive features of phytoseiid mites, such as fecundity and offspring sex ratio, especially in specialist predators (Mesa et al. 1990). For example, Escudero & Ferragut (2005) compared the biological features of two predator mites, Phytoseiulus persimilis Athias-Henriot (type I) and Neoseiulus californicus (McGregor) (type II), with different Tetranychus species as prey. They reported that when feed on T. urticae Koch, both predator species have >85% higher cumulative fecundity and >20% higher proportion of female offspring than those feed on T. evansi Baker & Pritchard. Gotoh et al. (2006) also revealed that N. californicus adults survive 67.6% longer when preyed on T. urticae than on Panonychus ulmi Koch. Besides, Galendromus occidentalis (Nesbitt) preyed on Tetranychus pacificus (McGregor) (1.1±0.3 days) had 31.3% shorter pre-oviposition duration than those fed on Eotetranychus willamettei (McGregor) (1.6±1.0 days) (Lara 2007).

Biological control agents are always suggested to be released before pests outbreak for prevention, namely “Predator-in-First' (PIF) (Kumar et al. 2015). Phytoseiid mites in that case would easily face insufficient target pests, so forced to choose non-favorite prey. However, the pest species in the field changed dynamically (Kidd et al. 2005), when phytoseiid mites live and grow in such a dynamic environment, feeding experiences vary among individuals and life stages. It's necessary to study how different prey species consumed by both males and females, and during immature and adult stages might impact reproduction to ensure if the predatory mites still have good biocontrol efficiency in the complex field of prey.

A few studies investigated details regarding how feeding experience of both sexes affects reproduction (van den Beuken & Smallegange 2018). Yet, it is still not clear whether the prey species fed by adults have more effect on reproduction than those fed by immatures. Whether predator females can compensate the negative impact on reproduction caused by their poor prey quality immature stages? Whether prey of different quality or species fed by males will affect the reproduction of their partners? Answers to these questions will help understand the general biology and physiology and improve the mass rearing of predators.

In the present study, we used N. californicus as the target predator, and two prey species, the two-spotted spider mite T. urticae and flower thrips Frankliniella occidentalis (Pergande) as prey. N californicus is a selective predator of tetranychid species, and also can complete its life cycle on early immatures of F. occidentalis (Mizobe et al. 2005; van Baal et al. 2007). Herein we mainly focused on the reproductive performances of predator females affected by the prey species consumed by males and females during immature stages and by female adults during oviposition stage. Results of this study might provide guides to field release and population evaluations of N. californicus, and are also beginning steps in investigating male impact in reproduction regulation of phytoseiids.

Materials and Methods

Results

Impact of prey species on reproductive performances of N. californicus

The pre-oviposition, oviposition and post-oviposition duration, and longevity of N. californicus were all significantly affected by prey species of female adults (Table 2). When female adults preyed on F. occidentalis, their pre-oviposition and oviposition duration, and longevity were 126.5%, 28.6%, and 8.3% longer than that preyed on T. urticae, respectively, while post-oviposition duration was 36.0% shorter (Table 3).

TABLE 1.

Reproductive treatments depending on the prey species fed by the immature females and males and ovipositing female adults.

TABLE 2.

Impacts of female immature prey, male immature prey and female adult prey on Neoseiulus californicus reproductive performances.

Significant impacts of prey species consumed by male or female immatures on pre-oviposition stage were also observed. When both female and male immatures fed F. occidentalis, the preoviposition duration was the longest (Table 3). Marginal significant impacts of interaction between prey consumed by female adults and male immatures on post-oviposition duration and female longevity were also detected (Figure 1).

Daily and cumulative fecundity were also significantly affected by female adult prey (Table 2). When female adults preyed on T. urticae, the daily and cumulative fecundity were 54.7% and 26.1% higher than those preyed on F. occidentalis, respectively. In addition, females preyed on T. urticae during immature stages also had higher fecundity than those preyed on F. occidentalis. No significant impact of prey on egg hatch rate and sex ratio was observed (Table 2).

FIGURE 1.

Mean (±SEM) post-oviposition duration and female longevity of Neoseiulus californicus as affected by prey of female adults (F-A) and male immatures (M-I).

FIGURE 2.

Mean (±SEM) egg size of Neoseiulus californicus as affected by prey of female adults (F-A) and male immatures (M-I).

TABLE 3.

Neoseiulus californicus reproduction and offspring development in different feeding experience.

Impact of prey species on N. californicus progeny development and sex allocation

Eggs that developed to females were ca. 7.5% larger than those developed to males. In addition, egg size was significantly affected by prey species of female adults, male immatures, and the interaction between sex and prey of female immatures (Table 4). When female adults preyed on T. urticae, their eggs were ca. 12.6% larger than those preyed on F. occidentalis (Figure 2, Table 3). In addition, eggs laid by females that mated with males preyed on F. occidentalis were ca. 5.5% larger than eggs with fathers preyed on T. urticae (Figure 2, Table 3). No significant impact of prey species on offspring developmental duration was observed. However, larger eggs tended to develop faster than small ones (Figure 3).

TABLE 4.

Impact of parent prey and sex on egg size and developmental duration of Neoseiulus californicus.

TABLE 5.

The sex probability of the first egg of Neoseiulus californicus in different feeding experiences.

There was no significant difference in proportion of female offspring detected treatments, with an overall mean of 68.2%. Eighty-eight percentage of the first-laid eggs and at least one of first two eggs developed to males. The proportions of males among the first-laid eggs do not differ significantly across the treatments (χ²=5.965, P =0.544) (Table 5). Four sex sequence patterns were observed for the first three eggs: MFF, MFM, MFF and FMF (M: male, F: female). The overall sex sequences do not differ significantly across the treatments (χ²=23.543, P =0.316) (Table 6). Among the four sex sequence patterns, MFF was mostly observed (45%), followed by MFM (34%), FMF (12%), and the MMF (9%).

TABLE 6.

The sex sequence of the first three egg of Neoseiulus californicus in different feeding experiences.

FIGURE 3.

Correlation between Neoseiulus californicus egg size and developmental duration A, eggs develop to females. B, eggs develop to females.

FIGURE 4.

Assumed accumulated nutrition pattern for oviposition in Neoseiulus californicus.

Discussion

In this experiment, we found that females preyed on F. occidentalis or T. urticae have similar cumulative fecundity, but differed in daily fecundity. The average daily fecundity of females fed on F. occidentalis was 1.5 eggs/female/day, while that of those fed on T. urticae was 2.5 eggs/female/day (Table 3). In other words, N. californicus fed on T. urticae had shorter oviposition duration than those fed on F. occidentalis (Table 3). Based on these results, we assume that there might be a nutritional threshold for each egg formation (Jaumann & Snell-Rood 2019). Females might still be able to lay eggs when fed on prey of poor nutritional quality, but required longer time to accumulate nutrient. When N. californicus preyed on F. occidentalis, the process of egg maturation in was slower when preyed on T. urticae (Figure 4).

Poor nutrient of prey fed by N. californicus males or females in immature stages have negative impact on female reproduction, leading to the reduced fecundity and postponed oviposition duration. However, these negative impacts are relatively minor and reversible. If mated female had sufficient food of good quality, such negative impact was limited. These results are similar to some previous studies. Greco et al. (2006) reported that if N. californicus females starve for 2–4 days, their daily fecundity will be recovered in 2–3 days when sufficient preys are provided. Ogawa & Osakabe (2008) also reported that N. californicus females could recover fecundity when their food is switched from artificial diet to natural prey, T. urticae.

In this study, no significant impact of the prey species on offspring sex ratio was observed. In contrast, Abdel-Khalek & Momen (2009) reported that the proportion of N. californicus female offspring is 18.2% lower when fed on T. evansi than fed on T. urticae, but the lower proportion of female offspring is accompanied by 90% decrease in fecundity. Similarly, Toyoshima & Amano (1998) found that starvation may led to 90% decrease of fecundity and 50% decrease of proportion of female offspring in two phytoseiid mites, P. persimilis and Amblyseius womersleyi Schicha. In most phytoseiid species, eggs are dimorphism, with those develop to females are larger than those develop to males. It is assumed that female embryos have higher nutritional requirement, so they may suffer more from environmental pressure of limited or low quality of prey. When the mother is under poor nutritional conditions, more female embryos deceased during early development, especially before eggs were laid, which led to decreased proportion of female offspring. In contrast, limited changes in proportion of female offspring were expected when no significant decrease in cumulative fecundity was observed.

For selective and generalist phytoseiid species, field releases are usually performed when pest density is low or before pests reach the economic injury level, so-called Predator-In-First (Kutuk & Yigit 2011; Kumar et al. 2015). Thus the pest population are expected to be controlled as early as possible, with fewer predators released and lower economic costs. Therefore, predatory mites are expected to experience low prey density or hard hunting conditions after released. Both T. urticae and F. occidentalis are important greenhouse pests worldwide, while F. occidentalis has lower temperature threshold and optimal temperature for development (Hart et al. 2002; Kasap 2004; Chaisuekul & Riley 2005). Thus, F. occidentalis population often occur earlier in greenhouses than T. urticae. If N. californicus are released early in the season when there is only F. occidentalis in field, the fecundity would be 0.6–1.6 eggs per female per day (Van Baal et al. 2007), its population could still catch up the increase of T. urticae population when their fecundity compensated when better prey species available.

Momen (1994) showed that 17% Neoseiulus barkeri (Hughes) females mate with starved males fail to oviposit, others have shorter mating duration and lower daily fecundity compared to those mated with normal males. In the present study, female had longer pre-oviposition duration when they mated with males developed under poor nutritional conditions. In some insects, males transfer some nutritional contents (nuptial gift) to females during mating (Vahed 1998). For example, Immonena et al. (2009) reported that female Drosophila subobscura Collin under poor nutritional conditions prefer to mate with males grow under good nutritional conditions, so that they could increase their fecundity. Similar situations have also been observed in a few Acari species. van den Beuken & Smallegange (2018) reported that starved female bulb mite Rhizoglyphus robini Claparède mate with satiated males lay more eggs, and had higher proportions of female offspring. Phytoseiid males deliver spermatophores to females during mating. Investigating the contents in spermatophores, such as seminal fluid proteins as well as sperm, may provide evidences about functions of nuptial gifts in phytoseiids.

In this study, we investigated how feeding experiences of both males and females affect the reproduction of phytoseiid mites. Although females play dominant roles in reproduction regulation, nutritional stress of males may also affect their partners reproduction. Further studies are expected to investigate the mechanisms how males impact female reproduction, and to evaluate field release strategies under complicated prey species and density conditions.