Life Table Parameters of Tetranychus merganser Boudreaux (Acari: Tetranychidae) on Five Host Plants

Simple Summary In Mexico, the red spider mite, Tetranychus merganser, is one of the most economically important pest mites in papaya crops, causing damage to the fruits and leaves. This research aimed to assess the effect of five host plants (Carica papaya L. (papaya), Capsicum annuum var. glabriusculum (Dunal) Heiser and Pickersgill (chili piquin), Helietta parvifolia (Gray) Benth. (barreta), Phaseolus vulgaris L. (bean), and Rosa hybrida L. (rosebush)) on the biology and life table parameters of T. merganser. We hypothesized that T. merganser has a better biological performance on papaya than on other host plants. The results of this research can be used to develop management and control strategies for T. merganser. The mean immature period of red spider mite females was longer on barreta leaf disks than on chili piquin, rosebush, papaya, and bean. The oviposition of T. merganser was greater on bean disks than on the other host plants. Host plants affect the number of eggs laid by the red spider mites, which reduce their intrinsic rate of natural increase. The demographic parameters suggest the unsuitability of barreta as the host for the development of red spider mites, and the best performance of T. merganser was on P. vulgaris. Abstract The quality of the host plant affects the life history parameters of tetranychid mites. The biology and fertility life tables of Tetranychus merganser on five host plants (Carica papaya, Phaseolus vulgaris, Capsicum annuum var. glabriusculum, Helietta parvifolia, and Rosa hybrida) were assessed under laboratory conditions at 28 ± 1 °C and 70–80% relative humidity (RH) with a photoperiod of 12:12 h (L:D). The development period of immature females differed among the tested host plants and ranged from 9.32 days on P. vulgaris to 11.34 days on H. parvifolia. For immature males, it ranged from 9.25 days on P. vulgaris to 11.50 days on H. parvifolia. The female survival rate varied from 53.97% on H. parvifolia to 94.74% on P. vulgaris. The highest total fecundity rate was recorded on P. vulgaris (125.40 eggs/female) and the lowest on H. parvifolia (43.92 eggs/female). The intrinsic rate of increase (rm) varied from 0.271 (H. parvifolia) to 0.391 (P. vulgaris). The net reproductive rate (RO) was higher on P. vulgaris than on the other host plants. The longest mean generation time (GT) was calculated on C. annuum var. glabriusculum and the shortest on Rosa hybrida. The demographic parameters suggest the unsuitability of H. parvifolia as the host for the development of red spider mites, and the best performance of T. merganser was on P. vulgaris.


Introduction
The red spider mite, Tetranychus merganser Boudreaux (Acari: Tetranychidae), feeds on twenty-three host plants [1][2][3][4][5] . It is found in China, Mexico, the United States, and Thailand [5]. The red spider mite is considered an emerging pest in Mexican agriculture due to the recent increase in the range of its host plants and geographic expansion [6]. The feeding habits of T. merganser destroy the epidermal tissue, the parenchyma, and the chloroplasts of the leaves, causing the host plant to fail to grow, develop, and reproduce [7,8]. Control of T. merganser is through chemical insecticides. However, the red spider has a short life cycle and high reproductive potential, and the excessive use of acaricidal applications can cause them to develop resistance to these compounds [9,10]. Other preventive control methods for T. merganser have been reported. They cause a minimal environmental impact, including predator mites (Neoseiulius californicus Mc-Gregor and Amblyseius swirskii Athias-Henriot (Gamasida: Phytoseiidae)) [8], botanical extract (Moringa oleifera ethanol extract) [11], and entomopathogenic fungi (Metarhizium anisopliae s.l. and Beauveria bassiana) [6].
T. merganser biology needs to be better understood since it has only been studied on Phaseolus vulgaris L. (Fabaceae) [9] and C. papaya [12], at different temperatures. These authors found that the biological and demographic parameters of red spider mites, such as survival, developmental period, total fecundity, and intrinsic rate of natural increase, differ in response to different temperatures. Ullah et al. [9] reported that the optimal development for red spider mites was at 30 • C on P. vulgaris at different tested temperatures (15 to 37.5 • C and 60-70% relative humidity). Furthermore, Reyes-Pérez et al. [12] found that T. merganser had better performance at 27 • C on C. papaya, when evaluated in a range of 19 to 35 • C and 60 ± 2% relative humidity. Treviño-Barbosa et al. [13] registered the number of eggs, survival, and percentage of feeding damage daily for four days, and on the fourth day they calculated the growth rate of T. merganser on C. papaya, P. vulgaris, C. annuum var. glabriusculum, Moringa oleifera Lam. (Moringaceae), Helietta parvifolia (Gray) Benth. (Rutaceae), Pittosporum tobira (Thunb.) W.T. Aiton (Pittosporaceae), and Thevetia ahouai L. A. DC. (Apocynaceae). They found that the red spider mite has better performance on C. papaya than on other plant species. According to Treviño-Barbosa et al. [13], the population growth parameters of T. merganser, such as fecundity, survival, and food intake, may vary in response to the changes in temperature, host plant species, and nutrition quality of plants [9,12,13]. However, Treviño-Barbosa et al. [13] have already reported some demographic and biological parameters of T. merganser, such as the intrinsic (infinitesimal) rate of increase (r), the finite growth rate (λ), the doubling time (DT), and the oviposition on C. papaya, P. vulgaris, C. annuum var. glabriusculum, and H. parvifolia. These results approximate the population growth of the red spider mite when it feeds on a host plant since r is a crude rate, and they establish a foundation for examining population growth patterns over short periods [14,15], such as in the study by Treviño-Barbosa et al. [13]. They calculated r on the fourth day. To have a clear and systematic picture of the specific age at birth (mx) and survival (lx) of the red spider mite population [15,16], we analyzed in more detail the developmental time from egg to adult for both females and males; the pre-oviposition, oviposition, and post-oviposition periods; the fecundity rate; survival rates of all immature stages and differences between male and female; and several life table parameters of T. merganser.
Life table parameters have been used as an indicator to assess population growth under a given set of conditions, thus showing the effect of different host plants or varieties on the mite [17]. Furthermore, the mite fertility life table parameters are used as an endpoint to reveal the susceptibility or resistance of host plants to the mite, since host plants that support low mite population growth are important for integrated pest management [17]. The aim of this research was to assess the effect of five host plants (C. papaya, C. annuum var. glabriusculum, H. parvifolia, P. vulgaris, and Rosa hybrida) on the biology and life table parameters of T. merganser. Our hypothesis was that T. merganser has a better biological performance on C. papaya than on other host plants. The results of this research can be used to develop management and control strategies for T. merganser.

Red Spider Mite Rearing
Individuals of different stages of development (larvae, nymphs, and adults) and the sex of T. merganser were collected from piquin pepper (C. annuum var. glabriusculum) in "Cañón de la Peregrina" (23 • 46 41 N, 99 • 12 12 W, 411 m above sea level), located in the protected natural area "Altas Cumbres" in the Victoria municipality, Tamaulipas, Mexico. The mites were reared on bean plants (P. vulgaris) grown in plastic pots (15 cm diameter × 10 cm height) under greenhouse conditions (30 ± 2 • C and 70 ± 10% relative humidity (HR)) for three months (several generations) before carrying out the experiments.

Host Plants
For this study, five host plants of T. merganser were selected, i.e., C. papaya, P. vulgaris, H. parvifolia, C. annuum var. glabriusculum, and Rosa sp. (Table 1). We collected mature leaves from each species of host plants under field conditions ( Table 1). These leaves did not show any damage or any symptom of the presence of fungi or bacteria. The leaves of each host plant were transported in resealable plastic bags inside a cooler with a frozen gel pack at a temperature of 5 ± 2 • C to the Population Ecology Laboratory of the Institute of Ecology of the Autonomous University of Tamaulipas. The transfer time of the leaves to the laboratory depended on the location of the host plants, but ranged from 5 to 30 min. In the laboratory, the leaves were treated with a 2 min wash with 1.5% sodium hypochlorite solution and cut into 4 cm 2 squares [13].

Immature Development and Performance of Adults
All the experiments were carried out under laboratory conditions at 28 ± 1 • C and 70-80% relative humidity (RH) with a photoperiod of 12:12 h (light: dark). This study was conducted in the Population Ecology Laboratory of the Institute of Applied Ecology, Autonomous University of Tamaulipas, during 2020-2022.
To determine the development times, survival rate, longevity, and fecundity of T. merganser, we used the methodologies of Uddin et al. [17] and Gotoh and Gomi [18]. A pair of adult mites (one newly emerged female and one male) were randomly selected from the stock rearing of T. merganser and placed on the leaf squares of each host plant with a fine camel hairbrush. With the help of a sterile scalpel, we cut the leaf squares of each host plant to 4 cm 2 . Each leaf square was placed on water-saturated cotton in a 5 cm diameter Petri dish, with the underside of the leaf facing up. We let the female and male mate for a period of 6 h. During this period, we monitored the oviposition, and immediately a single egg was left on each leaf square (females, males, and additional eggs were removed). During all experiments, leaf squares were changed after 3-4 days to ensure freshness, and individuals were transferred to new squares. Observations were made twice daily with the help of a stereoscopic microscope (UNICO Stereo & Zoom Microscopes ZM180, Dayton, NJ, USA). The duration of the development time from egg to adult, the survival, and the sex ratio (% females) of the emerging mites were recorded for each host plant and determined after reaching adulthood.

Oviposition and Life Table Parameters
When the red mite female reached the teleiochrysalis stage, one female and one male were placed on the same leaf square for mating. We kept the male on the leaf square for as long as the female was alive. If a male died before the female or got caught in the cotton threads, he was replaced by a young one. Females that became entangled in the cotton thread or killed due to improper handling or drowned were excluded from the data analysis. The eggs laid by a female were recorded daily until her death. As the leaf square aged, the mites transferred to new leaf squares. In this way, the oviposition period, the total number of eggs laid per female, the eggs laid per female per day, the post-oviposition period, and the longevity of the female of 25 T. merganser females per host plant were determined [16,17].
We used the daily age-specific survival rate (l x ) and age-specific fecundity (m x ) to generate the life tables of T. merganser on each host plant. The intrinsic rate of natural increase (r m ) was estimated from the fertility table according to the equation given by Carey [14] and Birch [19]: ∑e −rx l x m x = 1. We calculated the gross reproductive rate (GRR = ∑mx), net reproductive rate (R O = ∑lxmx, the mean generation time (T = lnR O /rm), growth capacity rate (rc = log e R O /T), the finite rate of increase (λ = e rm ), and the doubling time (DT = ln2/rm) based on Birch [19].

Statistical Analyses
Significant differences in life table parameters (GRR, rm, rc, R O , GT, λ y DT) were tested using the Jackknife procedure to estimate the standard error of demographic parameters [20,21]. The effects of host plants on the development, oviposition period, longevity, and fecundity of T. merganser were separately analyzed by a one-way ANOVA, followed by the Tukey HSD test (p < 0.05) using R software version 4.2.1. [22].

Development and Survival of Immature Stages
Both T. merganser females and males successfully completed their development on the five tested host plants. The developmental time of the egg, larva, protochrysalis, protonymph, deutochrysalis, deutonymph, and theliochrysalis of the females differed significantly between the tested host plants (p < 0.05; Table 2). The total developmental time (from egg to adult) for females differed significantly between host plants (p < 0.0001). T. merganser females developed faster on P. vulgaris (9.32 days) and C. papaya (9.58 days) than on R. hybrida (10.30 days), C. annuum var. glabriusculum (11.30 days), and H. parvifolia (11.34 days) ( Table 2).
Regarding the T. merganser male, the mean developmental time of the egg, larva, protonymph, deutochrysalis, deutonymph, and theliochrysalis differed significantly between the tested host plants (p < 0.05; Table 3). However, the protochrysalis period was not significant (p > 0.05). The total developmental time (from egg to adult) of the males differed significantly between host plants (p < 0.0001). Red spider mite males developed faster on P. vulgaris (9.25 days) and C. papaya (9.71 days) than on Rosa sp. (10.22 days), C. annuum var. glabriusculum (11.21 days), and H. parvifolia (11.50 days) ( Table 3).  The survival of T. merganser females and males showed that the mites successfully developed on the five host plants (Tables 4 and 5). The survival rate of the immature stages (from egg to adult) of T. merganser females varied significantly from 53.97% on H. parvifolia to 94.74% on P. vulgaris (Table 4). Nevertheless, the survival rate of males did not differ significantly between the host plants (Table 5). Although the survival rates of females and males differed between host plants (Tables 4 and 5), Pearson's association test did not show a significant relationship between sex and host plants (χ 2 = 1.410; df = 4; p = 0.8424). Sex ratios (%female) ranged from 77.27 on H. parvifolia to 79.07 on P. vulgaris. However, this was statistically similar between the five host plants (χ 2 = 0.0769, df = 4, p = 0.9993).

Adult Longevity and Oviposition
Host plants had a significant effect on the period of pre-oviposition, oviposition, and postoviposition, as well as the longevity and fecundity of T. merganser adult females (p < 0.0001; Table 6). The pre-oviposition period of T. merganser was longer on C. papaya. The highest value of the oviposition period was found on C. annuum var. glabriusculum (18.24 days) and R. hybryda (17.44 days), and the shorter value on H. parvifolia (13.12 days). Nevertheless, the female longevity ranged between 15.04 (H. parvifolia) and 20.84 (C. annuum var. glabriusculum) days and was significantly influenced by the host plant (p < 0.0001). Both the total fecundity and number of eggs laid by females were significantly higher on P. vulgaris (125.40 and 7.81, respectively) (Tukey's tests, p < 0.05; Table 6).

Life Table Parameters
The gross reproduction rate (GRR), net reproductive rate (R O ), growth capacity rate (rc, day −1 ), intrinsic rate of natural increase (rm, day −1 ), mean generation time (GT, in days), finite rate of increase (λ), and doubling time (DT) of T. merganser on the five host plants are shown in Table 7. The life table parameters GRR, R O , rm, GT, λ, and DT values were significantly different between the five host plants (p < 0.0001). The GRR of T. merganser differed significantly between host plants, and it was highest on P. vulgaris (109.364) and lowest on H. parvifolia (48.039). The rm value of T. merganser was significantly higher and lower than on P. vulgaris (0.391) and H. parvifolia (0.271), respectively. Similarly, R O , rc, and λ were the highest when T. merganser fed on P. vulgaris (75.240, 0.642, and 1.478, respectively) and the lowest when it fed on H. parvifolia (22.840, 0.439, and 1.311, respectively). The mean generation time (GT) differed among the host plants and was longest on C. annuum var. glabriusculum (12.037) and shortest on R. hybrida (10.817). The mean doubling time was also found to be significantly different on the host plants (p < 0.0001). The highest and lowest DT values were observed on H. parvifolia (2.561) and P. vulgaris (1.774), respectively (Table 7).

Discussion
This study showed that T. merganser can survive successfully and complete its development on P. vulgaris, C. papaya, R. hybrida, C. annuum var. glabriusculum, and H. parvifolia, and these plants significantly affected its life history parameters. The life table parameters are reliable tools to assess the quality of host plant effects on the biology and fertility of phytophagous arthropods, since they indicate their population growth rates in the current and next generations. Therefore, understanding them is essential to develop an integrated pest management strategy [23,24].
In the literature, there are few references to the developmental time (from egg to adult) of T. merganser on different host plants [9,12]. However, other studies have researched the developmental time of Tetranychus spp., and their findings are very similar to ours. This research showed that the duration of development from egg to adult for females and males ranged from 9.32 to 11.34 and 9.25 to 11.50 days on P. vulgaris and H. parvifolia at 28 • C, respectively. The developmental times of female and male red spider mites were reported to be 8.80 days and 8.3 days on P. vulgaris at 27.5 • C, respectively [8]. Islam et al. [25] reported that the mean immature period of the T. truncatus Ehara (Acari: Tetranychidae) female was longer on Corchorus capsularis L. (Malvacea) (7.40 ± 0.07) than on Lablab purpureus (L.) Sweet (Fabaceae) (7.00 ± 0.04 days) and C. papaya (6.90 ± 0.04 days). Puspitarini et al. [26] reported that T. urticae Koch (Acari: Tetranychidae) developed faster when fed Fragaria x ananassa (Duchesne ex Weston) Duchesne ex Rozier (9.03 ± 0.40 days) than Chrysanthemum indicum L. (Asteraceae) (10.05 ± 0.90 days) and C. papaya (12.37 ± 2.40 days). Furthermore, Draz et al. [27] documented that the development times of the immature stages of T. urticae were longer on C. annuum (11.90 ± 0.41 days) and Solanum melongena L. (Solanaceae) (11.30 ± 0.40 days) and shorter on Cucumis sativus L. (Cucurbitaceae) (10.50 ± 0.27 days) and Citrullus lanatus (Thunb.) Matsum. and Nakai (Cucurbitaceae) (9.50 ± 0.22 days). De Lima et al. [28] found that development from the egg to adult female of Tetranychus bastosi Tuttle, Baker and Sales (Acari: Tetranychidae) varied significantly by the host plant (10.5 ± 0.29 days on P. vulgaris, 11.2 ± 0.18 on C. papaya, and 12.3 ± 0.24 days on Manihot esculenta Crantz (Euphorbiaceae)). Adango et al. [29] documented that the period of development from egg to adult of the T. ludeni Zacher (Acari: Tetranychidae) female at 27 • C was shorter on Amaranthus cruentus L. (Amaranthaceae) (9.6 days) than on Solanum macrocarpon L. (Solanaceae) (10.1 days). Barroncas et al. [30] found that T. mexicanus McGregor (Acari: Tetranychidae) developed faster on C. papaya (11.2 ± 0.07 days) than on Passiflora edulis Sims (Passifloraceae) (11.9 ± 0.13 days). Islam et al. [25] and Puspitarini et al. [26] mentioned that the development time from egg to adult of Tetranychus spp. was dependent on host plants. In addition, the genetic background of the tested mite population, quality of host plants used for feeding the mite, and laboratory conditions affect the development period of the mite [26].
The life table parameters, particularly the intrinsic rate of natural increase (rm), are an essential parameter to assess and compare the population growth of a pest on different host plants [25,35]. In this study, the rm value was highest for T. merganser when it fed on P. vulgaris (0.391 day −1 ) compared to when it fed on C. papaya (0.371 day −1 ), R. hybrida (0.350 day −1 ), C. annuum var. glabriusculum (0.309 day −1 ), and H. parvifolia (0.271 day −1 ). Ullah et al. [8] reported that the rm of T. merganser was 0.379 (±0.005) day −1 and 0.279 (± 0.009) day −1 on P. vulgaris at 30 • C and 25 • C and 60-70% relative humidity and 16L:8D photoperiod, respectively. Reyes-Pérez et al. [12] documented that the rm was 0.21 day −1 on C. papaya at 27 • C and a relative humidity of 60 ± 2% and 14:10 h light: dark photoperiod. Treviño-Barbosa et al. [13] found that the intrinsic (infinitesimal) rate of increase (r) of T. merganser varied significantly by the host plant. The highest r of the red spider mite was observed in C. papaya (0.8482 ± 0.00), followed by P. vulgaris (0.7133 ± 0.01), M. oleifera (0.6146 ± 0.01), C. annuum var. glabriusculum (0.5568 ± 0.02), H. parvifolia (0.4068 ± 0.01), P. tobira (0.3379 ± 0.01), and T. ahouai (0.3421 ± 0.01). There was a broad variation in the rm values of T. merganser on the five host plants. Uddin et al. [17] mentioned that these variations may be due to the nutritional quality, chemical composition, and morphology of the leaf, as well as different experimental conditions. These characteristics of the host plant affect the development period, survival, and oviposition rate of tetranychids mites and consequently affect the intrinsic rate of natural increase, so rm adequately summarizes the physiological qualities of tetranychids mites in relation to their capacity to increase [35].
In conclusion, our results indicate that the demographic and biological parameters of T. merganser depend on the host plants. Among the tested host plants, P. vulgaris is most suitable for the population growth of T. merganser due to its shorter development period from egg to adult, the higher survival rate of immature mites, higher fecundity, and the fastest intrinsic rate of increase as compared to other host plants. This differential suitability of host plants for the red spider mite is an important factor to consider when developing biological control strategies into integrated pest management programs for T. merganser. Further research is necessary, including assessing the effect of host plants' morphological, chemical, and nutritional characteristics on the biology and life table of T. merganser.