This laboratory study shows that A. lycopersici is an acceptable prey for both P. ubiquitus and H. anconai. The iolinids were able to attack and kill the tomato russet mites and effectively exploit them as food, allowing complete development. Both predatory mites were observed piercing and sucking the contents of all tomato russet mite stages. They were also able to successfully develop from egg to adult on fresh cattail pollen or on a mixed diet of pollen and tomato russet mites.
The durations of the different life stages of P. ubiquitus on the diets tested in the present study are considerably shorter than those reported by Abou-Awad et al. (1999) for this predator when feeding on the fig leaf mite Rhyncaphytoptus ficifoliae (Keifer) or the fig bud mite Eriophyes ficus (Cotte) at 29°C and 70–80% RH. These authors reported a mean total developmental time of P. ubiquitus females of 19 and 19.5 days on the respective prey species. Under similar climatic conditions (24–25°C), the total developmental duration of H. anconai in this study was shorter than that reported by Knop et al. (1983) who offered the iolinid cattail pollen on blackberry leaves (13.6 days). In the present study, the developmental time of H. anconai was shorter on a mixed prey-pollen diet compared to pollen alone. Hessein et al. (1988) noted a positive influence of a mixed diet of A. lycopersici and Typha latifolia L. pollen on the survival of H. anconai compared to either food alone. A beneficial effect of a mixed diet on life history parameters has been reported for other predatory mites as well (Messelink et al. 2008; Muñoz-Cárdenas et al. 2014; van Rijn et al. 2002). Whereas this beneficial effect of a mixed diet was not observed on immature survival in our experiment, survival of the immature stages exceeded 83% for both mites on all diets.
Both P. ubiquitus and H. anconai effectively suppressed the population increase of the tomato russet mite on the small scale laboratory arenas, with or without pollen as a supplementary food source (Fig. 2). These results confirm earlier reports of effective control of A. lycopersici by H. anconai (Kawai et al. 2004) and P. ubiquitus (Pijnakker et al. 2021). However, the suppressive effect of P. ubiquitus on the pest’s population growth was stronger compared to that of H. anconai, with or without pollen supplemented. Additionally, our results indicate that the presence of pollen decreases the overall predation of immature and adult tomato russet mites by both predatory mites. Without pollen, a significant reduction of the tomato russet mite population was found from the second day onwards for P. ubiquitus compared to the control treatment, while this effect was only significant from the third day for H. anconai. With pollen available, a significant reduction of the pest population was found only from the fourth day onwards for P. ubiquitus, whereas this effect was further delayed to the fifth day for H. anconai. In the absence of pollen, P. ubiquitus kills more adult tomato russet mites than H. anconai. When pollen is present, this difference between the iolinid species disappears but only few adults are killed. These findings agree with those of Hessein et al. (1988), who reported that H. anconai consumed less tomato russet mite adults in the presence of Typha latifolia L. pollen.
Although the addition of pollen to the arena lowered the tomato russet mite predation by both iolinids, it substantially increased the fecundity of the predatory mites. The average number of 3–5 eggs/female/day in P. ubiquitus observed over a five-day period in the present study is higher compared to the 1.6–1.9 eggs/female/day reported by Abou-Awad et al. (1999) on the fig leaf mite and the fig bud mite, both on fig leaf arenas, but similar to the 2.5 eggs/female/day found by Duarte et al. (2021) on T. angustifolia pollen supplied on tomato leaf arenas. Similarly, studies done by Hessein et al. (1988) showed that H. anconai laid a significantly higher number of eggs on A. lycopersici plus cattail pollen and on cattail pollen alone than on a sole diet of A. lycopersici. The numbers of eggs laid by H. anconai reported in the latter study (1–2 eggs/female on day 5) are lower than those in our study (3–5 eggs/female). This difference could be related to the plastic substrate used in the study by Hessein et al. (1988). The availability of leaf tissue is key to the fitness of H. anconai (Flaherty et al. 1971; Hessein et al. 1988; Knop et al. 1983) and P. ubiquitus (Vervaet et al., unpublished). According to Knop et al. (1983), H. anconai fails to reproduce on an artificial substrate (plastic or cork) with or without cattail pollen and survival is low. Hessein et al. (1988) reported some reproduction of H. anconai on a plastic substrate when offered A. lycopersici alone or A. lycopersici with cattail pollen, but the availability of leaf tissue clearly enhanced population development. Duarte et al. (2021) reported that P. ubiquitus females taken from the mass-rearing units and allowed to lay eggs for four days on a tomato leaf-only diet produced less than 0.5 eggs/female/day. However, this reproductive output may be the result of their food uptake during the rearing. On the other hand, attempts to rear H. anconai on grape leaf alone (Flaherty et al. 1971; Hessein et al. 1988; Knop et al. 1983) or P. ubiquitus on tomato leaf alone (Vervaet et al., unpublished) failed. Thus, whereas feeding on leaf tissue alone provides sufficient nutrients to support survival of both iolinids to some extent, it is insufficient to sustain reproduction. Whether leaf tissue provides one or more essential nutrients, moisture, specific microhabitat requirements, ovipositional cues, or a combination of these, remains unclear.
An effective biological agent against A. lycopersici should meet several requirements (Vervaet et al. 2021). First, tomato is an unsuitable host plant for many predators because of the abundant (glandular) trichomes. The results obtained in our study confirm earlier reports that both H. anconai and P. ubiquitus are not hindered by these trichomes and perform well on tomato leaf surfaces (Kawai et al. 2004; Pijnakker et al. 2021). Furthermore, a tomato russet mite infestation is difficult to detect and early symptoms are easily missed or misdiagnosed as a nutritional deficiency, plant disease or water stress (Vervaet et al. 2021). The preventive establishment of a predator to create a ’standing army’ against A. lycopersici offers a solution to this problem (Pijnakker et al. 2021). The suitability of pollen as a diet may increase the potential of biological control agents by enabling them to pre-establish well in the crop before the pest is present and to sustain their population when pest densities are low, as well as by making mass-production easier and cheaper (Duarte et al. 2021; McGregor et al. 2020). Our results corroborate earlier reports that pollen is an excellent food source for H. anconai and P. ubiquitus (Duarte et al. 2021; Flaherty et al. 1971; Hessein et al. 1988; Knop et al. 1983). Duarte et al. (2021) reported that pollen needs to be supplemented at least every other week to allow a sufficient population build-up of P. ubiquitus in tomato. Whether pollen supplementation needs to be continued even when A. lycopersici is present in the crop remains to be investigated in greenhouse conditions. Based on the findings of the present study, the positive effect of provisioning pollen on the fecundity of both iolinids is expected to compensate the associated decrease in predation on A. lycopersici in the longer run, but this also remains to be investigated under practical field conditions. Finally, compatibility with other management strategies in the greenhouse is key to the success of a biological control agent. Pesticides can negatively interfere with the performance of natural enemies in the crop. Five compounds (dicofol, abamectin, sulphur, cyhexatin and thuringiensin) tested on A. lycopersici proved toxic to H. anconai, but selective doses of abamectin showed the best potential to control A. lycopersici without reducing predator numbers (Royalty et al. 1987). Sulphur, widely used in greenhouse production as a fungicide, was also noted to be highly detrimental to P. ubiquitus (Van Houten et al. 2020). Interestingly, P. ubiquitus was recently found to simultaneously control a tomato russet mite infestation and a powdery mildew infection (Oidium neolycopersici) on potted tomato plants, suggesting that augmentative releases of this iolinid might reduce the dependence on sulphur in tomato greenhouses (Pijnakker et al. 2021). In addition, intraguild predation with other beneficials in the greenhouse ecosystem should be investigated. Given the small size of both iolinids, the direct effects of most of the currently used beneficials in tomato greenhouses are expected to be limited. However, as both iolinids feed on plant sap as well, their performance might be influenced by indirect effects associated with induced plant defenses triggered by other omnivorous natural enemies (e.g. Miridae predatory bugs (Pérez-Hedo et al. 2015)).
In conclusion, the present laboratory study indicates that the omnivorous predatory mites P. ubiquitus and H. anconai can play a crucial role in the biological control of the tomato russet mite in protected tomato cultivation. A. lycopersici, T. angustifolia pollen or a combination of both as a diet are adequate food sources to sustain development and reproduction of both iolinid mites. Overall, P. ubiquitus developed faster and suppressed the population development of A. lycopersici stronger as compared to H. anconai. Survival and fecundity on the tested diets was similar for both iolinids. Further field studies are required to determine whether augmentative releases of P. ubiquitus or H. anconai can maintain A. lycopersici under economic threshold levels as well as to optimize pollen supplementation to help establish and sustain populations of the iolinids.