Typhlodromus (Typhlodromus) setubali (Dosse) (Acari: Phytoseiidae) is an indigenous predatory mite, previously reported on various crops in the surrounding Mediterranean countries. In this study, the effects of temperature and food diet on its development and reproduction were evaluated when fed with the immature stages of Panonychus ulmi (Koch) and Tetranychus urticae (Koch) (Acari: Tetranychidae), as well as with the pollen of Typha latifolia L. (Typhaceae), at five constant temperatures. Data set was analysed using the age-stage two-sex life table method and the development-temperature relationship was established by the linear model of each life stage of predator. Overall, the optimal development and reproduction of T. (T.) setubali were observed at 30 °C, when fed on P. ulmi, as indicating the shortest developmental times for both sexes (6.02 d for female and 5.13 d for male) and the lowest degree-days (148.28 ± 3.57 and 132.04 ± 3.1, respectively). The estimated values of the developmental thresholds (tmin) and the thermal constant (K) from egg to adult stage were higher on T. latifolia than on prey. Subsequently, the oviposition period decreased significantly as the temperature increased from 15 to 35 °C. Also, the predator population can increase 1.22 ± 0.008 per single day at 30 °C, when fed on immature stages of P. ulmi, with higher values of the intrinsic rate of increase rm = 0.205 d-1, net reproduction rate R0 = 14.49 offspring/individual and the total fecundity (25.89 eggs /female), simultaneously. The age-stage survival rate Sxj, age-specific survival rate Ix, age-stage specific fecundity f(x,5), and age-specific life expectancy (Exj), were given in illustrations. Considering these results, T. (T.) setubali can develop and reproduce on various food diets, suggesting a character generalist of Type III of this species. Among the food diets tested, P. ulmi is more preferred as support food at temperatures neighbor 30 °C. Therefore, it can be released as a biological control agent against Tetranychid mite populations in the agricultural Mediterranean areas. Further laboratory-based experiments are needed to draw biological conclusions.
Keywords: Phytoseiidae; Development; Temperature; Life table; Food diet.
Typhlodromus (Typhlodromus) setubali is a predatory mite belonging to the family Phytoseiidae. It was reported on Olea europea, Cupressus sp, and Cynodon dactylon, in many countries of the Mediterranean basin (McMurtry and Bounfour 1989), later after on the vine by Tixier et al., (2003). In Morocco, the investigations conducted during two years (2002 /2003), succeeded to describe five new species and improved the old description of two species, T. (T.) setubali and T. (A.) clairathiasae (Tixier et al., 2016).
Typhlodromus (T.) setubali has been morphologically confused with T. (T.) moroccoensis (Denmark, 1992). Both species present a taxonomic similarity among the genus Typhlodromus (Typhlodromus), by the presence of six setae on the Genu II (Chant and Yoshida-Shaul 1987). For both sexes of T. (T.) setubali, identification keys are now given and the new measurements are now available.
Lacking bibliographic information on the development and reproduction of T. (T.) setubali is a real limit to assess our result with the necessary confidence. In this study, some biological features of this species were established on three food diets at different temperatures, which were chosen in correspondence to the local climatic conditions. However, the temperatures of 15 and 20 °C represent the averages recorded between February and March at the beginning of the growing season, 25 °C is approximately the average of temperatures reigning during April and May, whereas levels of 30 °C and 35 °C occur between July and November when females prepare to hibernation.
Through a series of experiments, three food diets were tested at each temperature. The immature stages of Panonychus ulmi (Koch) and Tetranychus urticae (Koch) (Acari: Tetranychidae) were massively reared, then provided as prey. The third food diet was the cattail pollen of Typha latifolia L., imported from the biological center for population management, SupAgro Montpellier, France. The pollen of T. latifolia is a standard natural food mostly used in the life table studies of the predatory mites (Park et al., 2011).
MATERIALS AND METHODS
Rearing of mites
Panonychus ulmi and T. urticae were collected from the apple tree, Malus domestica Borkh, cv. Jeromine (Rosaceae), at Oulmes region, Morocco (33 ° 26 ' 19.6 " N, 5 ° 58 '35.7 " W). Mites were reared separately on the green bean plants Phaseolus vulgaris L. (Leguminosae), in a growth chamber under the ambient conditions of summer for four generations before the beginning of experiments.
The initial population of T. (T.) setubali was obtained from Riyad-Fruit orchard, located in the region of Tiddas, Morocco (33 ° 33' 37.0 " N, 6 ° 15' 40.8 " W). The specimens were collected on the apple tree, Malus pumila Mill. cv. Anna (Rosaceae) and kept in the culture chamber of the Faculty of Sciences, Moulay Ismail University, Meknes, Morocco. The predator was reared separately on the food diets mentioned above in growing containers under conditions of 25 ± 1 °C, 65 ± 5 % RH, and 16: 8 (L: D) as a photoperiod for four successive generations before the starting of experiments. Each rearing unit hosts the predator on a black plastic mat, which is deposited on floating sponges surrounded with wet cotton strips. Each strip extremity was kept in contact with water to prevent the escape of mites
To produce original T. (T.) setubali colonies for tests, predators in each rearing unit were fed with a single type of food. Immature forms of P. ulmi and T. urticae were daily added through infested green bean leaflets and an amount of 0.5 mg of the cattail pollen of T. latifolia L. was supplied every day. Therefore, three predator colonies were obtained for four generations before starting the experiments.
Two-sex life table study
To determine the life table parameters of T. (T.) setubali, 30 matted females were isolated from the rearing units and left to lay eggs for 24 hours. 60 eggs were collected and individually transferred using a fine brush onto a bean leaf disc (3 cm in diameter), which was placed on wet cotton in a Petri dish (9 cm in diameter). After hatching, the first instars received 10 separate immature forms of P. ulmi, T. urticae as prey, and 0.5 mg of pollen every 24 hours. The survival and development of T. (T.) setubali were recorded daily.
Newly emerged males and females were paired onto new bean leaf discs for copulation, each pair received daily 20 immature stages as prey and adult males were subsequently removed as soon as observed. Survival, longevity, and fecundity were recorded daily until the death of the cohort of females. Overall, 12 replicates were tested for each food diet at 15, 20, 25, 30, and 35 ° C, the relative humidity of 65 ± 5%, and 16: 8 (L: D)h as a photoperiod, respectively.
The intrinsic rate of increase (rm) according to the two-sex life table is calculated as:
The net reproduction rate (R0) is an indicative parameter of the growth of a population after a generation. The calculation of R0 gives the number of emerging females that can produce the initial cohort of T. (T.) setubali during the lifespan of its individuals, this parameter is calculated as:
Where m is the number of predator's life stage. The finite growth rate (λ) describes the growth potential as the multiplication rate of a stable population per time unit. When the time approaches infinity, the stable age-stage distribution is reached and the proportions of individuals in age x and stage j are provided as a matrix a(x,j) in comparison with a(0,1).
Data set were analysed according to the two-sex life table procedure (Chi and Liu 1985) and the method described by (Chi 1988). The mean values of life table parameters were calculated using the TWOSEX program (Chi, 2012), whereas the associated standard errors were estimated using the bootstrap method (Efron and Tibshirani 1993).
The survival rates recorded of predator feeding with the three food diets were compared by the Chi-square test χ2. The effects of the food diet as variables with temperature as a covariate on two-sex life table parameters were assessed using the analysis of covariance (ANCOVA). Data normality was examined using the Shapiro-Wilk test. When it indicates that the data is normally distributed, pairwise comparison between groups was done using the Levene (F) test. When the data is not normally distributed, the nonparametric Kruskal-Wallis (K) test was used. Means were compared using the Tukey-Kramer Honestly Significant Difference Test (HSD). For all tests, the P-values less than or equal to 0.05 are considered significant (Sokal and Rohlf 1994).
A temperature-development relationship was established for each life stage of the predator, according to the temperature summation model. Both parameters, the low developmental threshold (tmin) and thermal constant (K) were estimated plotting the inverse of development time (1 /d) on the temperature (T) (Campbell et al., 1974).
All statistical treatments were performed using R Commander, a graphical user interface in conjunction with R program ver. 3.5.3. (R Core Team 2019).
The age-specific survival rate of T. (T.) setubali at age x and stage j are given as a matrix (Sxj). The probabilities that a newborn will survive to age x and stage j when T. (T.) setubali fed on three food diets are given at each temperature in Figure 1. The probabilities that a newly laid egg survives to adulthood vary with diet and temperature changes. The graphs showed the differentiation of stages and the survival rate peaks of predator individuals. For example, for the tests carried out at 15 °C, the probability that an egg, survives to the larval stage is 0.9 on P. ulmi, in the protonymphal and deutonymphal stages are respectively 0.88 and 0.8, while those at the adult stage are 0.42 for female and 0.26 for male (Figure 1). Overall, when T. (T.) setubali fed on the immature forms of P. ulmi and T. urticae, the probabilities are higher than those recorded on T. latifolia pollen, whatever the temperature tested. The highest probabilities were recorded at 30 ° C on P. ulmi (0.72 for females and 0.31 for males), occurring at 12 and 9 days of age, respectively. Those observed when the predator has been reared on immatures of T. urticae are 0.60 for the adult female after 8 days and 0.30 for the male, which it reached at the age x = 9 days.
For both sexes, the results showed that the probability of a newborn surviving to adulthood increased significantly with increasing temperature from 15 to 30 °C on prey than pollen. At 35 °C, the probabilities were similar on all food diets (0.60 for female and 0.30 for male), recorded similarly at the same age (around the 8th and 6th day, respectively).
Regardless of the food diet and temperature tested, T. (T.) setubali immature survival rates obtained over the entire cohort studied were higher. The results showed that T. (T.) setubali survived on T. latifolia with high proportions ranged from 71.83 % at 15 °C to 85.75 % at 30 °C, then decreased at 35 °C to 75.92 %. Similar trends were also observed when the cohort of predators fed on both immature prey (Table 1). The χ2 test statistic did not reject the null hypothesis of equality of survivals among the different temperatures at each food source, at a 5 % level of significance, yielding a P-value from 15 to 35 °C equal to 0.987 (χ2 = 9.978) and 0.997 (χ2 = 8.005), respectively. Moreover, no significant differences were found between the mean proportions among the food sources tested, as indicated by the P-value on each one (Table 1).
The mean developmental time of each stage of the predator is given in Table 2. The time required for eggs to hatch (incubation period) ranged from 7.05, 6.71, and 6.75 days at 15 °C to 1.36, 1.38, and 1.40 days at 35 °C when T. (T.) setubali fed on T. latifolia pollen, P. ulmi, and T. urticae, respectively. The developmental times of larvae, protonymphs, and deutonymphs were slightly longer on pollen than on T. urticae and P. ulmi at 15 °C and 20 °C (Table 2). For both sexes, total immature developmental time of T. (T.) setubali decreased as temperature increased from 15 to 30 °C whatever the food diet, the longest time was significantly observed on cattail pollen at 15 °C (25.33 days for females and 24.25 days for males), whereas the shortest developmental period was recorded at 30 °C when predator fed on P. ulmi (6.02 days for female and 5.13 days for male.
Analysis of covariance ANCOVA revealed a significant effect of temperature on the developmental times whatever the life stage, while that of the food diet varies with temperature changes. The total development time for predators at the second stage, third and fourth stage, which fed on T. latifolia pollen, was not influenced by temperature, as long as results showed similar periods at the temperatures from 15 to 35 °C (F = 8.096, R2 = 0.73, P = 0.065) (Table 2).
Development time of eggs was similar on both prey and pollen items at 35 °C (K = 0.808, P = 0.668). For larvae and protonymphs, no difference between the average periods was observed at 15 °C (F = 3.215, P = 0.053 and F = 0.820, P = 0.449, respectively) and 30 °C (F = 2.600, P = 0.089 and F = 1.101, P = 0.344, respectively), the same trend occurs at 25 °C for deutonymphs (F = 1.662, P = 0.205), whereas the developmental time for females was similar on prey and pollen at 30 °C and 35 °C (F = 0.054, P = 0.947 and F = 0.962, P = 0.392, respectively). For both sexes, no effect of the food diet was observed on the development of adult males, below 25 °C (K = 4.388, P = 0.111 and K = 2.277, P = 0.320, respectively), while adult females can develop as the same time on all foods tested at high temperatures (Table 2).
The relationship between the development of predator and temperature can be fitted using linear and nonlinear model items (Ikemoto, Lactin...). The values estimated of the low developmental threshold (tmin) and the constant thermal (K) at each stage of predator are displayed in Table 3. The results showed that tmin changes from one stage to another depending on the food considered. However, the lowest values of tmin of females and males were obtained when predator fed on P. ulmi immatures than on T. latifolia or T. urticae. The development of protonymphs and deutonymphs needs more degree days on T. latifolia, therefore, an inversed result was obtained for larval forms fed with the same foods.
The results revealed also that more degree-days are needed for completing the development of predator immatures, fed with T. latifolia than on prey. However, from egg to adult, T. (T.) setubali required a thermal budget of approximately the same day-degrees above the low developmental threshold estimated for both sexes (154.65 and 156.12 degree-days for females, as well as 143.70 and 147.27 degree-days, on T. latifolia and T. urticae, respectively.
Life expectancy and longevity
The age-specific life expectancy of T. (T.) setubali obtained on the food diets is illustrated in Figure 2 as a matrix (Exj). Life expectancy describes the expected lifespan that an individual of age x and stage j expects to live. The two-sex life table analysis leads to a satisfactory result, which showed that life expectancy gradually decreased with aging. The life expectancy of a new individual (egg) is defined as the average longevity of the entire cohort studied. For example, at 15 °C, the life expectancy (E01) at age x = 0 (birth) and j = 1 (egg) is 63 days when females fed with P. ulmi, 64 days with T. urticae and 67 days on T. latifolia (Figure 2).
The lowest values of longevity were recorded at 30 °C among the temperatures tested,. Indeed, the life expectancy of a new egg laid by fed females with P. ulmi is 19.30 days, a similar value to that obtained on T. urticae (19.60 days). The relative life expectancy on T. latifolia is 22.50 days. The low values observed at high temperatures represent the average longevity of individuals, due to the rapid development of predator, as reported in the previous section
The mean values of the reproduction parameters with error types associated are presented in Table 4. Overall, both temperature and food diet influenced significantly the reproduction parameters, especially, the oviposition period, longevity, and daily fecundity, but not the total fecundity and sex ration (P > 0.05). However, no significant difference among the food diets tested, which lead to similar values of preoviposition and postoviposition at all temperatures, except for 25 °C (K = 25.616, P < 0.0001 and K = 14.945, P = 0.001, respectively). In the same way, the oviposition period of predator females feeding on prey and pollen items was similar at temperature ranged from 15 to 30 °C with the alone except when the temperature rises to 35 °C (K = 8.270, P = 0.016). On another side, predator females had a different oviposition activity, females tend only to lay a similar total number of eggs at 20 °C (F = 0.411, P = 0.666) with similar daily number at 15 and 20 °C (K = 2.910, P = 0.233 and K = 0.001, P = 0.999) (Table 4).
The longevity of predator females decreased from 67.10, 63.31 and 64.79 days, at 15 °C to 18.01, 15.80 and 16.10 days at 35 °C, when feeding on cattail pollen, P. ulmi and T. urticae immatures, respectively (Table 4). The highest fecundity of T. (T.) setubali females was recorded at 30 °C when the predator fed on P. ulmi (25.89 egg/ female), with an average daily fecundity of 2.05 eggs/female/day, whereas, the lowest was observed on pollen (12.17 eggs/ female), with an average of 1.02 eggs/ female/day.
Subsequently, both the food diet and temperature did not significantly influence the sexual dimorphism of predator progeny. Whether on prey or pollen, the sex ratio takes similar values at temperatures from 15 to 30 °C, but a significant difference among food diets was observed at 35 °C (K = 17.663, P = 0.0001). However, the offspring was strongly male at low temperatures from 15 to 20 °C, whatever the food diet, whereas, the progeny had the highest female-biased sex ratio when T. (T.) setubali fed on P. ulmi and T. urticae immatures than the progeny of predators consuming T. latifolia pollen (78, 73 and 63 %, respectively) (Table 4).
The numerical response of T. (T.) setubali, including the daily and total female fecundity, are displayed in Table 4. The food diet influenced significantly the daily fecundity of female at temperatures below 25 °C, the highest fecundity was recorded at 30 °C on P. ulmi immatures (25.89 eggs /female), with an average daily fecundity of 2.05 eggs /female /day, while the lowest was obtained on T. latifolia (12.17 eggs/female), with an average of 1.02 eggs /female /day).
The number of offspring reproduced by individual T. (T.) setubali of age x and stage 5 per day f(x,5), age-specific survival rate (lx), and age-specific fecundity (mx) of T. (T.) setubali are plotted in Figure 3. The age-specific maternity of T. (T.) setubali females brings both the age-specific survival rate (Ix) and age-specific fecundity at x age mx and can be calculated as Ixmx. The two-sex life table analysis gives the age-specific fecundity taking into account the preadult development results and includes the development of male individuals.
If the same data set were analyzed using classical life table analysis, it would be impossible to view the changes in the stage structure because traditional life tables ignore the variable developmental rate among individuals, with a hard stage differentiation.
No significant effect of both factors on the sexual dimorphism of the offspring, except for results obtained at 35 °C, which, showed a high proportion of females on P. ulmi (60 %) (K = 17.663, P = 0.0001). The offspring were strongly male at temperatures of 15-20 °C, regardless of food provided, while the highest sex ratios were recorded at 30 °C on immature P. ulmi, followed by those obtained on T. urticae and T. latifolia (78, 73 and 63 %, respectively).
The means and associated standard errors of the demographic parameters of the predator's population are given in Table 5. Two fundamental parameters explain the growth of T. (T.) setubali: the intrinsic rate (rm) and the finite rate of increase (λ). The rm represents the innate potential of an increase of T. (T.) setubali per unit time (1 day). No significant effect of the food diet on the growth of the predator was observed. The growth of T. (T.) setubali was positively correlated with temperature, the highest values of rm and λ were recorded at 30 °C (0.13, 0.20, 0.20 and 1.14, 1.22, 1.22 d-1, on T. latifolia, T. urticae, and P. ulmi, respectively), while the lowest values were obtained at 15 °C, whatever the food diet (Table 5).
Although the type of food does not have a significant effect on the growth of predator, its effect on reproduction, expressed as the net reproduction rate (R0), is significant (P > 0.05). The lowest rates of R0 were obtained on pollen than on prey, whatever the temperature tested, except at 25 °C (F = 1.132, P = 0.305) (Table 5). The mean generation time (T) decreased significantly as the temperature increased on prey and pollen items, the longest value of T was recorded at 15 °C for predators fed with T. latifolia, while the shortest was obtained on immature forms of P. ulmi at 35 °C (11.24 days) (Table 5).
This is the first study on the biology of the predatory mite, T. (T.) setubali. The two-sex life table analysis suggests a character generalist of Type III this species (McMurtry and Croft, 1997; McMurtry et al., 2013). Several similar results have been reported on predators of the family Phytoseiidae, mainly used as a biological control agent (Eveleigh and Chant, 1981; Croft and Croft, 1993; Davidson et al., 2016; Liu and Zhang, 2017). The development of T. (T.) setubali seems to be more influenced by temperature rather than the food diet, whereas the female fecundity was higher on prey than pollen. The low developmental threshold tmin was lower for both sexes of T. (T.) setubali fed with both prey than on pollen, suggesting an ability of females to overwinter in reproductive diapause coincided therefore to their enhancement to withstand lower temperatures (Veerman 1992; Coleman et al., 2014), with a need to more degree-days feeding on T. urticae immatures (Table 2).
The food diet did not influence the development of T. (T.) setubali from larval to the deutonymphal stage. Both sexes of adult stages were not sensible to food change at high temperatures (Table 2). Considering these results, we can conclude that T. (T.) setubali immatures are not affected by the qualitative characteristics of food as the nutritious and energetic value of each one may be more important for reaching adulthood. Similar results have been reported for several phytoseiid species, such as Typhlodromus phialatus Athias-Henriot and Euseius stipulatus Athias-Henriot (Ferragut et al., 1987), Typhlodromus athenas Swirski and Ragusa (Kolokytha et al., 2011) and Typhlodromus talbii Athias-Henriot (Camporese and Duso 1995).
The model presented by Chi and Liu (1985) and Chi (1988) overcomes the problem related to the traditional life table analysis. However, neglecting the variation in the development between individuals and the male population can lead to errors in the calculation of the age-specific survival rate and reproductive value of predator at age x and stage j. This method has been using to describe the characteristics of many insects and mite pest populations at different experimental conditions (Huang and Chi 2012; Yin et al. 2013; Yu et al. 2013; Arcaya et al. 2017). The two-sex life table procedure takes into account the stage differentiation and developmental variation between individuals at age x, leading to evident overlaps as illustrated graphically in Figure 1.
Age stage survival rate of predator gives the probability that a newborn survived to age x and stage j. The peaks of survival rate at both adult stages were recorded at 30 °C on P. ulmi, coinciding with a higher female oviposition activity (Table 4). The development of adult males was faster completed than females, whatever the temperature and food diet. Therefore, this developmental behavior can be considered as an advantage for successful mating and increasing the population (Gotoh et al., 2004).
In the classical life table analysis, only the survival rate of females by age (lx) is calculated and such variation is not observed. An in-depth discussion of the problem of two-sex life tables for females can be found in the studies of Chi (1988); Yu et al., (2005); Chi and Su (2006) and Huang and Chi (2012). On the other hand, the life expectancy (Exj) of T. (T.) setubali gradually decreased with aging. The value attributed to a newborn at age 0 and j = 1 (Egg), gives the expected longevity of the cohort (Figure 2). The calculation takes into consideration the stable age stage distribution of T. (T.) setubali under the laboratory conditions, without the adverse effects encountered in the field as exposure to natural enemies or parasitoids, and also exposure to chemical treatments (Van Rijn and Tanigoshi 1999).
Two-sex life table analysis of T. (T.) setubali provides complementary knowledge for implementing the management strategies including this specie, as a biological control agent against mites and insect pests. Inversely to the traditional life tables, which ignore the variation between individuals.
The development of T. (T.) setubali from egg to the adult stage was significantly influenced by temperature rather than the food diet, which showed a significant effect on the oviposition activity of females. The results presented here showed that the pollen of T. latifolia is an alternative food for this species, when the suitable foods are absent.
The highest values of the female fecundity and dynamic parameters were recorded on prey than pollen, especially on P. ulmi immatures, at temperatures ranged from 25 to 35 °C, suggesting that, the predatory mite, T. (T.) setubali can be released as an effective biocontrol control agent in the agricultural Mediterranean areas.
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