Diving deep into a tiny world: effects of drought on the predatory mite Phytoseiulus persimilis

Terrestrial arthropods are particularly vulnerable to drought stress, because of their small size, and because their body has a high surface-area-to-volume ratio (SA:V). In agricultural ecosystems, where the ecological functions of terrestrial arthropods are significant (herbivores, pollinators, predators), this sensitivity to drought can have serious consequences. Biological pest control with arthropod predators, in particular, is strongly affected by relative humidity conditions. Understanding how terrestrial arthropods respond to changes in humidity in their environment is, therefore, essential to ensure the success of biological control programs. In this thesis, I investigated the effects of drought stress on the predatory mite Phytoseiulus persimilis. This mite is widely used in augmentative biological control as an effective predator of the two-spotted spider mite Tetranychus urticae. The biocontrol efficacy of P. persimilis decreases under dry conditions, and this lower efficacy has often been explained as the consequence of the drought sensitivity of P. persimilis eggs.

In CHAPTER 2, I investigated the presence of genetic variation for egg drought resistance in P. persimilis, and the potential sources (genetic or environmental) of phenotypic variation in this trait, by comparing egg hatching rates among five P. persimilis populations in different humidity conditions (constant low, constant high, and variable). I found no intraspecific genetic variation among the five tested populations in egg hatching under constant and variable humidity conditions. In all five populations, less than 20% of the eggs hatched when they were exposed to constant low humidity conditions (60% RH) at 25 °C. However, when eggs were exposed to successive cycles of low and high humidity, significantly higher hatching rates were observed. Under variable humidity conditions, more than 73% of the eggs hatched successfully, even when exposure to high humidity was limited to only 13% of the egg developmental time. These results changed my initial perspective on the drought sensitivity of P. persimilis eggs: it appears that they are capable of dealing with harsh humidity conditions more effectively than previously thought.

In CHAPTER 3, I investigated the possibilities to select for increased drought resistance in P. persimilis eggs, through artificial selection and experimental evolution. In an artificial selection trial, P. persimilis eggs from two selection lines were exposed to three selection rounds. In an experimental evolution trial, all P. persimilis life stages from two selection lines were exposed to a constant low humidity selection pressure. To evaluate the response to selection, egg hatching rate at low humidity was assessed in both trials. A significant increase in drought resistance of eggs occurred in the experimental evolution trial. Already one month after the start of the trial, egg survival at low humidity had more than doubled. However, this increase in egg drought resistance disappeared within 15 days after I had removed the selection pressure from a group of adult females. In the artificial selection trial, no response to selection was observed after three selection rounds. The results of this study indicate that drought resistance in P. persimilis eggs is a phenotypically plastic trait, regulated by their mother. This discovery raised new questions and made me change my focus from P. persimilis eggs to P. persimilis females.

In CHAPTER 4, I studied the role of transgenerational phenotypic plasticity in the adaptation of P. persimilis eggs to different relative humidity conditions. For this, I exposed P. persimilis adult females to constant and variable humidity regimes, and evaluated the hatching rate of their eggs in dry conditions, as well as the survival and oviposition rates of these females. Whereas the eggs laid by P. persimilis females exposed to constant high humidity did not survive in dry conditions, females exposed to constant low humidity started laying drought-resistant eggs after 24 hours of exposure. Around 43% of the females exposed to variable humidity conditions laid drought-resistant eggs after 102 hours of exposure. Survival and oviposition rates of the females were affected by humidity: females laid fewer eggs under constant low humidity, and had a shorter lifespan under constant high and constant low humidity. These results demonstrate that P. persimilis females are able to prepare their offspring for dry conditions through an environmental maternal effect, by laying drought-resistant eggs. Under conditions of desiccation stress combined with the production of drought-resistant eggs, P. persimilis females lay fewer eggs in constant dry conditions.

In CHAPTER 5, I investigated the mechanisms underlying drought resistance of P. persimilis eggs, by studying the physiological differences between drought-resistant and drought-sensitive eggs. I compared the volume of the eggs, their sex ratio, their chemical composition (by gas chromatography-mass spectrometry), their internal and external structure (by scanning electron microscope and transmission electron microscope images), and their developmental time. The results showed that drought-resistant and drought-sensitive eggs have a different chemical composition: drought-resistant eggs contain more free amino acids, sugar alcohols, and saturated hydrocarbons than drought-sensitive eggs. This difference may contribute to reducing water loss in drought-resistant eggs. Moreover, drought-resistant eggs are on average 8.4% larger in volume than drought-sensitive eggs. This larger volume, probably the result of a higher water content, may make drought-resistant eggs less vulnerable to water loss. I did not find difference in sex ratio, internal or external structure nor developmental time between drought-resistant and drought-sensitive eggs. These results mark the first step in the understanding of the strategies involved in the production of drought-resistant eggs in P. persimilis females.

In conclusion, I demonstrated that P. persimilis eggs can deal with harsh humidity conditions better than we previously thought. First, they are able to recover from a long exposure to drought if they are exposed to high humidity for only a few hours. Second, through a maternal effect, P. persimilis females are able to protect their offspring against desiccation stress by laying drought-resistant eggs. As a consequence, the lower efficacy of P. persimilis in dry conditions may rather be due to a lower oviposition rate and a shorter lifespan of P. persimilis females than to the drought sensitivity of their eggs. Finally, this thesis is also a first step in understanding the internal egg structure in a phytoseiid mite species.