Herbivory-associated degradation of tomato trichomes and its impact on biological control of Aculops lycopersici

Abstract

Tomato plants have their leaves, petioles and stems covered with glandular trichomes that protect the plant against two-spotted spider mites and many other herbivorous arthropods, but also hinder searching by phytoseiid mites and other natural enemies of these herbivores. This trichome cover creates competitor-free and enemy-free space for the tomato russet mite (TRM) Aculops lycopersici (Acari: Eriophyidae), being so minute that it can seek refuge and feed inbetween the glandular trichomes on tomato cultivars currently used in practice. Indeed, several species of predatory mites tested for biological control of TRM have been reported to feed and reproduce when offered TRM as prey in laboratory experiments, yet in practice these predator species appeared to be unable to prevent TRM outbreaks. Using the phytoseiid mite, Amblydromalus limonicus, we found exactly the same, but also obtained evidence for successful establishment of a population of this predatory mite on whole plants that had been previously infested with TRM. This successful establishment may be explained by our observation that the defensive barrier of glandular plant trichomes is literally dropped some time after TRM infestation of the tomato plants: the glandular trichome heads first rapidly develop a brownish discoloration after which they dry out and fall over onto the plant surface. Wherever TRM triggered this response, predatory mites were able to successfully establish a population. Nevertheless, biological control was still unsuccessful because trichome deterioration in TRM-infested areas takes a couple of days to take effect and because it is not a systemic response in the plant, thereby enabling TRM to seek temporary refuge from predation in pest-free trichome-dense areas which continue to be formed while the plant grows. We formulate a hypothesis unifying these observations into one framework with an explicit set of assumptions and predictions to be tested in future experiments.Electronic supplementary materialThe online version of this article (doi:10.1007/s10493-012-9638-6) contains supplementary material, which is available to authorized users.

Size of predatory mites and refuge entrance determine success of biological control of the coconut mite

“…However, some herbivores can also benefit from plant structures to hide from predators (Magalhães et al 2007). For example, herbivores are known to live in between the scales of flower bulbs (Lesna et al 2004(Lesna et al , 2014, inside dense forests of leaf trichomes (van Houten et al 2013;Glas et al 2012Glas et al , 2014, and in shafts of grasses (Oldfield 1996;Lindquist and Oldfield 1996;Sabelis and Bruin 1996), which reduces the risk of predation.…”

Drought-stressed tomato plants trigger bottom-up effects on key mite pests

“…When feeding, they introduce the stylet between epidermal pavement cells or through a stomatal opening, without damaging the epidermis, and inject saliva on a single parenchyma A. lycopersici is an oligophagous mite that has tomato as its primary host but it can feed on other solanaceous crops including potato, tobacco, eggplant and pepper, and some , 1992). It is a species that is difficult to control, since it´s small size allows it to hide in the forest of tomato trichomes that protects them from predators and pesticides (Van Houten et al, 2013). The lack of tomato varieties resistant to russet mites and the difficulties in timely identification of damage symptoms, since the damage is similar to that caused by broad mite and thrips, make it seriously noxious to the tomato (Duso et al, 2010).…”

“…On tomato, A. lycopersici feeds on foliage, stems, inflorescences and young fruits, causing shriveling and necrosis of leaves (Figure 1.4D), dropping of flowers, russeting of fruit and, if uncontrolled, death of the plant (CABI, http://www.cabi.org/isc/datasheet/56111) (Duso et al, 2010, Van Houten et al, 2013. As consequence, russet mite infestation can cause up to 50 % of yield losses on tomato (Duso et al, 2010), the loss being mainly due to the dead of flower buds (Kamau et al, 1992).…”

“…As consequence, russet mite infestation can cause up to 50 % of yield losses on tomato (Duso et al, 2010), the loss being mainly due to the dead of flower buds (Kamau et al, 1992). It is a species that is difficult to control, since it´s small size allows it to hide in the forest of tomato trichomes that protects them from predators and pesticides (Van Houten et al, 2013). The lack of tomato varieties resistant to russet mites and the difficulties in timely identification of damage symptoms, since the damage is similar to that caused by broad mite and thrips, make it seriously noxious to the tomato (Duso et al, 2010).…”

“…They confer resistance to small arthropods, including T. urticae and T. evansi (Simmons and Gurr, 2005), and have been used in plant breeding to increase herbivore resistance (Glas et al, 2012). However, a tiny mite like A. lycopersici is too small to be hindered General Introduction │CHAPTER 1 11 by tomato trichomes, which confer shelter to this mite by creating a competitor-free and natural enemy-free space (Van Houten et al, 2013). The defensive role of trichomes in varieties with low trichome density, such as Moneymaker (Glas et al, 2012), is likely to be negligible.…”