Introduction

Tetranychus ludeni Zacher is an invasive mite pest originating from Europe and now present in Asia, Africa, America, and Australasia (Migeon & Dorkeld 2018; CABI/EPPO 2020; Zhou et al. 2021). It attacks more than 250 plant species (Gotoh et al. 2015) including economically important crops such as carrots, beans, eggplants, pumpkins and other cucurbitaceous plants in warm regions and greenhouses of temperate areas (Zhang 2002; Adango et al. 2006; Fathipour & Maleknia 2016). Because temperature is a key factor influencing physiological processes in insects and mites (Ullah et al. 2010; Gotoh et al. 2015; Zou et al. 2018) and determining their distribution and abundance (Bale et al. 2002; Roy et al. 2002), global warming may further increase the distributional range of T. ludeni (Gotoh et al. 2015) and favor the spread of other invasive mites (Ghazy et al. 2019). Therefore, investigation into the influence of temperature on life history traits provides important information for pest risk analysis and management.

Evidence shows that egg hatch rate, immature survival, developmental time, adult longevity, and life table parameters vary substantially in different mite species and even different strains of the same species in response to test temperatures in the laboratory (e.g., Zhang et al. 1999; Da Silva 2002; Roy et al. 2003; Gotoh et al. 2010, 2015; Ullah et al. 2010; Riahi et al. 2013; Bazgir et al. 2015; Li et al. 2015; Liu & Zhang 2016; Bayu et al. 2017; Zou et al. 2018; Hasanvand et al. 2019; Ristyadi et al. 2019). This may be attributed to a diverse range of physiological limits in different species (Nguyen et al. 2014) and adaptation to temperature changes in different strains (Gotoh et al. 2010). However, most studies on the effect of temperature on mite life history traits analyze their data from only one generation, making it difficult to evaluate mites' potential adaptations to variations of temperature over generations. Hence, examination of life history traits in response to different temperatures for more than one generation can provide information on how mites may adapt to dynamic thermal environment for prediction of their potential of invasions and crop damage in the world.

Temperature is also an important factor regulating sex ratio in spider mites (e.g., De Moraes & McMurtry 1987; Margolies & Wrensch 1996; Roy et al. 2003; Gotoh et al. 2015). Roy et al. (2003) suggest that females have better capacities than males to disperse and survive under harsh conditions in some spider mite species, such as T. mcdanieli McGregor, and consequently, their sex ratio should be increasingly female-biased at extremely low or high temperatures indicating deteriorating habitats. Yet, it is largely unknown whether this notion applies to other spider mites. Furthermore, body size of adults developing from immatures at different temperatures may vary substantially (Klok & Harrison 2013). For example, body size of geographic strains of a species in warmer regions should be smaller than in cooler regions (Walters & Hassall 2006; Plesnar-Bielak et al. 2013; Pequeno et al. 2018). However, it is not clear whether such temperature-dependent body size is translated into fecundity in spider mites.

In the present study, we aimed to investigate the life history strategies of T. ludeni in response to dynamic thermal conditions in two successive generations. Based on theoretic framework and empirical findings outlined above, we postulate that (1) higher temperature accelerates development and shortens adult longevity; (2) immature mortality is higher and sex ratio is more female-biased at low and high temperatures; (3) adults that develop from lower temperatures are larger and more fecund, and (4) mites can adapt to thermal changes over generations. To test these hypotheses, we carried out a series of experiments and compared various life history traits in response to dynamic temperatures within and between generations. We also created a life table using data collected.

Materials and Methods

Results

We show that proportions of eggs that hatched and immatures that survived to adults and sex ratio of resultant adults were largely similar across test temperatures in both generations (Figure 1). The only difference occurred at 30°C in the second generation where egg hatch rate was significantly lower than at 25 and 30°C in the first generation (F = 3.21; df = 7, 149; P = 0.0034) (Figure 1A), immature survival rate was significantly higher than at 15°C in the first generation (F = 2.59; df = 7, 148; P = 0.0125) (Figure 1B), and the proportion of resulting females was significantly lower than all other treatments in both generations (F = 8.68; df = 7, 141; P < 0.0001) (Figure 1C).

FIGURE 1.

Mean (± SE) percentage of egg hatch (A), immature survival (B) and resulting female adults (C) at different temperatures in the first and second generations in T. ludeni. Columns with the same letters are not significantly different (P > 0.05). For each box plot, the upper and lower box lines represent 75% and 25% of scores falling beyond the upper and lower quartiles, respectively; the ‘×' and line in a box indicate the mean and median score, respectively; the ‘' and ‘’ are the upper and lower whiskers showing scores outside the 50% middle; the circles are the outliers of scores.

FIGURE 2.

Mean (± SE) developmental time of eggs (A) and from eggs to adults (B) at different temperatures in the first and second generations in T. ludeni. Columns with the same letters are not significantly different (P > 0.05). For each box plot, the upper and lower box lines represent 75% and 25% of scores falling beyond the upper and lower quartiles, respectively; the ‘×' and line in a box indicate the mean and median score, respectively; the ‘' and ‘’ are the upper and lower whiskers showing scores outside the 50% middle; the circles are the outliers of scores.

Tetranychus ludeni significantly accelerated their development with the increase of temperature in both generations, with the second generation developing significantly faster at 15°C and 20°C than the first generation (F = 7341.52; df = 7, 4770; P < 0.0001 for eggs, and F = 9463.52; df = 7, 2443; P < 0.0001 for egg-adult) (Figure 2). Adult body size of both sexes generally decreased significantly with the increase of temperature from 20°C in both generations with it being the largest at 20°C and smallest at 30°C (F = 30.30; df = 7, 263; P < 0.0001 for females, and F = 13.34; df = 7, 219; P < 0.0001 for males) (Figure 3). Although the developmental rate and temperature were significantly positively correlated in both generations, the low temperature threshold (T₀) was lower and degree days (DD) were greater in the second generation than in the first generation (Table 1).

Table 1.

Relationship between developmental rate (1/d, y) and temperature (T, °C), and the estimated mean (± SE) low temperature threshold (T_0, °C) and degree day (DD) required to start and complete development of eggs and from egg to adult stage in T. ludeni.

FIGURE 3.

Mean (± SE) body size of female (A) and male adults (B) in T. ludeni at different temperatures. Columns with the same letters are not significantly different (P > 0.05). For each box plot, the upper and lower box lines represent 75% and 25% of scores falling beyond the upper and lower quartiles, respectively; the ‘×' and line in a box indicate the mean and median score, respectively; the ‘' and ‘’ are the upper and lower whiskers showing scores outside the 50% middle; the circles are the outliers of scores.

FIGURE 4.

Mean (± SE) number of eggs laid by females during their lifetime at different temperatures in T. ludeni. Columns with the same letters are not significantly different (P > 0.05). For each box plot, the upper and lower box lines represent 75% and 25% of scores falling beyond the upper and lower quartiles, respectively; the ‘×' and line in a box indicate the mean and median score, respectively; the ‘' and ‘’ are the upper and lower whiskers showing scores outside the 50% middle; the circles are the outliers of scores.

In the first generation, lifetime fecundity of females that developed from 15°C was significantly lower than that from other treatments (F= 4.34; df = 3, 76; P = 0.0071) where fecundity was similar (Figure 4). Adult males had similar longevity at 15 and 20°C but their longevity significantly decreased with the increase of temperature from 20 to 30°C (x² = 52.88; df = 3; P < 0.0001) (Figure 5A). Adult females survived significantly longer at 20°C than at 15 and 25°C, and their longevity was the shortest at 30°C (x² = 83.29; df = 3; P < 0.0001) (Figure 5B). As shown in Table 2, increasing temperature significantly elevated the intrinsic rate of increase (r_m) but significantly shortened the generation time (T) and the time to double the population size (Dt). The net population growth rate (R₀) was significantly higher at 20 and 25°C as compared to lower and higher temperatures.

TABLE 2.

Mean (± SE) life table parameters of T. ludeni at different temperatures.

Discussion

We show that the egg hatch rate in the New Zealand strain of T. ludeni was > 95% without significant difference between test temperatures from 15–30°C in the first generation (Figure 1A). Our finding agrees to that for the Japanese strain exposed to similar temperature range for one generation (Gotoh et al. 2015). However, the hatch rate was significantly lower at 30°C in the second generation than at 25°C and 30°C in the first generation (Figure 1A), indicating that exposure to 30°C for more than one generation would reduce egg survival in T. ludeni. Immature survival remained similar across test temperatures in the first generation but was higher at 30°C in the second generation (Figure 1B). This could be an adaptive strategy to compensate lower hatch rate at 30°C in the second generation.

FIGURE 5.

Survival of male (A) and female adults (B) at different temperatures in T. ludeni. Lines with the same letters are not significantly different (P > 0.05).

Like other haplodiploid species including spider mites (Roy et al. 2003; Macke et al. 2011; Tamura & Ito 2017), T. ludeni generally had a female-biased sex ratio across our test temperatures (Figure 1C). Based on the data from one generation, the sex ratio (proportion of female adults) is higher at 30°C than at lower temperatures in the Japanese strain of T. ludeni (Gotoh et al. 2015) and it is more female-biased in T. mcdanieli at 15°C and 34°C as compared to temperatures between 20°C and 32°C (Roy et al. 2003). Roy et al. (2003) suggest that the increased female-biased sex ratio at extreme temperatures may be an evolutionary response to deteriorating habitats because tetranychid females appear to have better abilities than males to disperse and survive under harsh conditions. However, our findings show that the sex ratio was consistent across all test temperatures in both generations except for 30°C in the second generation which was significantly lower (Figure 1C). The higher immature survival (Figure 1B) and lower sex ratio (Figure 1C) at 30°C in the second generation may be an adaptive response to higher temperature over generations in T. ludeni.

Similar to reports on T. ludeni's Japanese strain (Gotoh et al. 2015) and other mite species (Margolies & Wrensch 1996; Da Silva 2002; Bazgir et al. 2015; Li et al. 2015; Zou et al. 2018), we found that the New Zealand strain of T. ludeni developed significantly faster with the increase of temperature from 15 to 30°C in both generations (Figure 2), supporting the notion that increasing temperature elevates metabolic rate and thus shortens developmental time (Woods & Hill 2004; Potter et al. 2009; Schulte 2015). However, compared to the first generation, the second generation developed faster at 15°C and 20°C (Figure 2). These findings suggest that T. ludeni can adjust its developmental period based on its experience in the previous generation. Adaptation to thermal environment over successive generations is also reported in the predatory mite Amblydromalus limonicus Garman and McGregor (Acari: Phytoseiidae) (Walzer et al. 2020). We propose that T. ludeni accelerates its development at lower temperatures to promote an early start of reproduction after experiencing longer development and delayed reproduction in the first generation at these lower temperatures.

We demonstrate that T. ludeni adult body size in both generations (Figure 3) followed the so-called temperature-size rule where body size decreases with the increase of environmental temperature, as reported in many ectotherms (Atkinson 1994; Walters & Hassall 2006; Klok & Harrison 2013; Pequeno et al. 2018). However, the degrees and patterns of size changes in response to temperature differed between sexes as well as between generations. For example, the degree of size variation was greater in females than in males in the first generation while size changes of both sexes were smaller in the second generation (Figure 3). These findings have two implications: (1) females are more likely than males to adjust body size in response to temperatures they first experience, and (2) both sexes can adapt to temperatures they have experienced in the previous generation.

We found that temperature-dependent female body size did not translate into fecundity in T. ludeni because females that developed from 15–20°C were larger than those from higher temperatures (Figure 3A) but females from 15°C laid fewer eggs than those from higher temperatures where there was no difference (Figure 4). These findings differ from those for the Japanese strain where highest and lowest fecundity occurs at 20°C and 30°C, respectively (Gotoh et al. 2015) and for the Brazilian strain where females lay greatest number of eggs at 30°C (Da Silva 2002). In T. urticae, Riahi et al. (2013) and Zou et al. (2018) report the highest fecundity at 25°C and 28°C, respectively. Our results indicate that temperature-dependent adult body size was associated with longevity and such association was different between sexes (Figures 3 and 5). In the first generation, larger male body size at 15–20°C (Figure 3B) translated into longer longevity at the same temperature range (Figure 5A) while females had largest body size (Figure 3A) and longest longevity (Figure 5B) at 20°C. In several other mite species (Riahi et al. 2013; Sugawara et al. 2017) and the Japanese strain of T. ludeni (Gotoh et al. 2015), longevity decreases with the increase of temperature.

In this study, the lower thermal threshold (T₀) and degree days (DD) for T. ludeni development from eggs to adults (Table 1) fell within the range from 7.8 to 13.8°C and from 110 to 156 DD, respectively, reported for the genus Tetranychus for one generation (Sakunwarin et al. 2003; Gotoh et al. 2010, 2015; Ullah et al. 2010; Karami-Jamour and Shishehbor 2012; Riahi et al. 2013; Bayu et al. 2017; Hasanvand et al. 2019). The varying thermal requirements for development between species or strains of the same species probably reflect their adaptations to the local climate (Gotoh et al. 2015). Although the developmental rate and temperature were significantly positively correlated in both generations, T₀ was lower and degree day (DD) was greater in the second generation than in the first generation (Table 1). These results also suggest that T. ludeni can adapt to temperature changes by adjusting its developmental rate based on its experience in the previous generation. The life table shows that the intrinsic rate of increase (r_m) increased and doubling time (Dt) decreased with the increase of temperatures from 15 to 30°C (Table 2). These may be attributed to the shorter developmental time (Figure 2) and more daughters produced during the females' early lifespan at higher temperatures (DR unpublished data). Because population size has a significant effect on reproduction and population growth in T. ludeni (Weerawansha et al. 2020), the population size changes in response to temperatures can further facilitate its invasion success.

In conclusion, life history traits of T. ludeni are highly flexible and adaptive to dynamic thermal environment over generations. We show that higher temperature accelerates its development in both generations, but the development at the lower temperatures is faster in the second than in the first generation. This suggests that the mite shortens its developmental time at lower temperatures in the second generation to promote an early start of reproduction after experiencing longer development and delayed reproduction in the first generation at these temperatures. Adult body size in both generations decreases with the increase of temperature, with females being more likely than males to adjust body size in response to temperature changes they first experience. Larger body size results in greater longevity but not higher fecundity. Lower thermal threshold and greater degree days (DD) in the second generation than in the first generation suggest that T. ludeni can adapt to temperature changes by adjusting its developmental rate based on its experience in the previous generation.