Parental exposure to heat waves improves offspring reproductive investment in Tetranychus urticae (Acari: Tetranychidae), but not in its predator, Phytoseiulus persimilis (Acari: Phytoseiidae)

Abstract

The more frequent and intense occurrence of heat waves is a challenge for arthropods because their unpredictable incidence requires fast adaptations by the exposed individuals. Phenotypic plasticity within and across generations might be a solution to cope with the detrimental effects of heat waves, especially for fast-developing, small arthropods with limited dispersal abilities. Therefore, we studied whether severe heat may affect the reproduction of a pest species, the spider mite Tetranychus urticae, and its counterpart, the predatory mite Phytoseiulus persimilis. Single offspring females with different parental thermal origins (reared under mild or extreme heat waves) of both species were exposed to mild or extreme heat waves on bean leaves over 10 days, and the oviposition, egg sizes, survival, and escape behavior of the females were evaluated daily. The total losses of predators mainly via escapers were very high compared to prey, which makes a separation between selective and plastic effects on shifted reproductive traits impossible. Predator females laid smaller eggs, while their consumption and oviposition rates were unaffected during extreme heat waves. In comparison, larger prey females fed more and produced more, but smaller, eggs due to within- and trans-generational effects. These advantages for the prey in comparison to its predator when exposed to extreme heat waves during the reproductive phase support the trophic sensitivity hypothesis: higher trophic levels (i.e., the predator) are more sensitive to thermal stress than lower trophic levels (i.e., the prey). Furthermore, the species-specific responses may reflect their lifestyles. The proactive and mobile predator should be selected for behavioral thermoregulation under heat waves via spatiotemporal avoidance of heat-exposed locations rather than relying on physiological adaptations in contrast to the more sessile prey. Whether these findings also influence predator-prey interactions and their population dynamics under heat waves remains an open question.

Keywords: Phytoseiidae; Tetranychidae; biological control; climate change; intergenerational plasticity; predator–prey interactions.

FIGURE 1

Size measurements of the perimeter of the idiosoma of adult female P. persimilis (a) and T. urticae (b), as well as the length and width of P. persimilis eggs (c) and the diameter of T. urticae eggs (d).

FIGURE 2

Heat wave effects on the escape (cumulative residents plotted against residence time, a,b) and survival (cumulative survivors plotted against survival time, c,d) functions of predator (a,c) and prey (b,d) F1 females. F1 females, originating from parents reared under mild (M) or extreme (E) heat waves, and F1 females exposed to mild (M) or extreme (E) heat waves are labeled by the first and second upper case letters.

FIGURE 3

Daily predation rates of offspring (F1) of P. persimilis females [average ± 95% confidence limits (CL)] in function of the heat wave conditions (mild = blue, extreme = red) of F1 females and their parental (F0) origin. Triangles show F1 females derived from F0 females exposed to extreme heat waves, and dots mark F1 females derived from F0 females exposed to mild heat waves. Full lines show the predicted predation rates based on equation 2 with the 95% confidence limits (dashed lines). The estimated parameters (with the standard error in parentheses) for equation 2 are shown in the table.

FIGURE 4

Daily oviposition rates of P. persimilis females exposed to extreme (red) or mild (blue) heat wave conditions pooled over parental (F0) heat wave conditions. Dots: average oviposition ±95% confidence limits (CL) for the mean. Lines: modeled oviposition (continuous lines) ± 95% confidence limits (dashed lines). The estimated parameters (with the standard error in parentheses) for equation 2 are shown in the table.

FIGURE 5

Daily oviposition rates of T. urticae females exposed to extreme (red) or mild (blue) heat wave conditions pooled over parental (F0) heat wave conditions. Dots: average oviposition ±95% confidence limits (CL) for the mean. Lines: modeled oviposition (continuous lines) ±95% confidence limits (dashed lines). The estimated parameters (with the standard error in parentheses) for equation 2 are shown in the table.

FIGURE 6

Offspring (F1) heat wave‐ and time effects on egg sizes of P. persimilis and T. urticae, pooled over parental (F0) heat waves. (a) female eggs of P. persimilis; (b) female eggs of T. urticae; (c) male eggs of P. persimilis; and (d) male eggs of T. urticae. Dots: average size ±95% confidence limits (CL) for the mean. Lines: modeled egg sizes (continuous lines) ±95% confidence limits (dashed lines). Blue: mild heat waves; Red: extreme heat waves. The relationship between female age (t) and ln‐transformed egg volumes (ln V(t)) was modeled by equation 3. The estimated parameters (with the standard error in parentheses) are shown in the tables.

FIGURE 7

Shifts in body sizes (perimeter of the idiosoma) of the offspring (F1) females in function of their parental (F0) origin and heat wave conditions during juvenile development. F1 females, originating from parents reared under mild (M) or extreme (E) heat waves, and F1 females exposed to mild (M) or extreme (E) heat waves are labeled by the first and second upper case letters. The horizontal centerlines in each box represent the median, the box limits represent the interquartile (IQ) range from 25 to 75 percentiles, the whiskers extend the IQ range to 1.5 times, and outliers are depicted as symbols.

FIGURE A1

A schematic overview of the experimental procedure. Females and eggs of both mite species are depicted here for P. persimilis as and for T. urticae as . First, females from laboratory populations of both species were used to produce eggs (F0 generation), which were then raised to adults either under mild (M) or extreme (E) heat waves. When F0 individuals became adults, they produced F1 eggs, which were exposed to either mild (M) or extreme (E) heat waves during their juvenile development, thereby creating four groups of mites per species with different thermal histories (MM, ME, EM, and EE – first and second upper case letters indicate the parental and offspring heat wave conditions, respectively). Adult F1 individuals were transferred to experimental arenas, where they were exposed for 10 successive days to the same heat wave conditions as they experienced during juvenile development.