Effects of Tetranychus urticae AND Phytoseiulus persimilis (Acari: Tetranychidae: Phytoseiidae) on the chlorophyll of rosal plants (Rosa sp.)

Chacón-Hernández, Julio C.; Camacho-Aguilar, Isaac; Cerna-Chavez, Ernesto; Ordaz-Silva, Salvador; Ochoa-Fuentes, Yisa M.; Landeros-Flores, Jerónimo; Chacón-Hernández, Julio C.; Camacho-Aguilar, Isaac; Cerna-Chavez, Ernesto; Ordaz-Silva, Salvador; Ochoa-Fuentes, Yisa M.; Landeros-Flores, Jerónimo

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Agrociencia

versão On-line ISSN 2521-9766versão impressa ISSN 1405-3195

Agrociencia vol.52 no.6 Texcoco Ago./Set. 2018

Plant Protection

Effects of Tetranychus urticae AND Phytoseiulus persimilis (Acari: Tetranychidae: Phytoseiidae) on the chlorophyll of rosal plants (Rosa sp.)

Julio C. Chacón-Hernández¹

Isaac Camacho-Aguilar²

Ernesto Cerna-Chavez²

Salvador Ordaz-Silva³

Yisa M. Ochoa-Fuentes²

Jerónimo Landeros-Flores²^*

^¹Instituto de Ecología Aplicada, Universidad Autónoma de Tamaulipas, División del Golfo No. 356, 87019, Colonia Libertad, Ciudad Victoria, Tamaulipas, México.

^²Departamento de Parasitología, Universidad Autónoma Agraria Antonio Narro. Calzada Antonio Narro 1923, 25315, Buenavista, Saltillo, Coahuila; México.

^³Facultad de Ingeniería y Negocios, Universidad Autónoma de Baja California, Carretera Ensenada San Quintín, km 180.2., 22930, Ejido Padre Kino, San Quintín, Baja California, México.

Abstract

Tetranychus urticae Koch (Acari: Tetranychidae) is the main pest in rose (Rosa sp.) (Rosales: Rosaceae) by reducing the amount of chlorophyll in plants and at high densities they are overexploited and even killed. One of the most used biological controllers for this pest for its high efficiency is the mite Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae). Our hypothesis was: P. persimilis reduces the populations of T. urticae and therefore chlorophyll is not affected. The objectives were: 1) to determine the susceptibility or resistance of rose varieties to the attack of T. urticae, 2) determine the relationship between the condition of the plant and the population density of T. urticae, 3) know the predation effect of P. persimilis in the control of T. urticae and its efficiency; and 4) determine in which variety of rose P. persimilis performs best. We established the experiment in two parts; the first was one-way and the second consisted of repeated measurements to analyze the effects of T. urticae and the release of P. persimilis through the chlorophyll content variables in SPAD cm^-2 units, percentage of damage per cm² and the number of mites per cm² in rose varieties. We did three repetitions for each stratum (upper, middle and lower) by variety of rosebush per week, for which we analyzed 72 samples per variety. The varieties of rose evaluated were Virginia and Ojo de Toro. At random we released 100 T. urticae and 12 P. persimilis mites per plant. The data analysis was one-way ANOVA and repeated means, simple linear, multiple and non-linear regressions to determine the dependence between the variables. Prior to the release of P. persimilis there were significant differences between the varieties with respect to the abundance of T. urticae per cm², but not in the chlorophyll content and percentage of damage. After the release of P. persimilis, the abundance of T. urticae was different in the strata of both varieties. The Ojo de Toro variety had the lowest chlorophyll content. There was no difference in the percentage of damage and the abundance of P. persimilis between both varieties. Phytoseiulus persimilis was more efficient in the Ojo de Toro variety than in the Virginia variety. It also reduced the damage by T. urticae but did not prevent the reduction of chlorophyll content by the phytophagous.

Key words: percentage of damage; biological control; predator-prey; predation

Resumen

Tetranychus urticae Koch (Acari: Tetranychidae) es la plaga principal en rosal (Rosa sp.) (Rosales: Rosaceae), al reducir la cantidad de clorofila de la planta y en grandes densidades la sobreexplotan e incluso las matan. Uno de los controladores biológicos más utilizados para esta plaga por su alta eficacia es el ácaro Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae). La hipótesis fue: P. persimilis reduce las poblaciones de T. urticae y por ende la clorofila no es afectada. Los objetivos fueron: 1) determinar la susceptibilidad o resistencia de variedades de rosal al ataque de T. urticae, 2) determinar la relación entre la condición de la planta y la densidad poblacional de T. urticae, 3) conocer el efecto de depredación de P. persimilis en el control de T. urticae y la eficiencia, y 4) determinar en cual variedad de rosal, P. persimilis se desempeña mejor. El experimento se estableció en dos partes, la primera fue de una vía y la segunda de medidas repetidas, para analizar los efectos de T. urticae y la liberación P. persimilis mediante las variables contenido de clorofila en unidades SPAD cm^-2, porcentaje de daño por cm² y el número de ácaros por cm² en variedades de rosal. Las repeticiones fueron tres por cada estrato (superior, medio e inferior) por variedad de rosal por semana, por lo cual se analizaron 72 muestras por variedad. Las variedades de rosal evaluadas fueron Virginia y Ojo de Toro. Al azar se liberaron 100 T. urticae y 12 ácaros P. persimilis por planta. El análisis de datos fue ANDEVA de una vía y de medias repetidas, regresiones simples lineales, múltiples y no lineales para determinar la dependencia entre las variables. Previo a la liberación de P. persimilis hubo diferencias significativas entre las variedades con respecto a la abundancia de T. urticae por cm², pero no, en el contenido de clorofila y porcentaje de daño. Después de la liberación de P. persimilis, la abundancia de T. urticae fue diferente en los estratos de ambas variedades. La variedad Ojo de Toro presentó el menor contenido de clorofila. No hubo diferencia en el porcentaje de daño y la abundancia de P. persimilis entre ambas variedades. Phytoseiulus persimilis fue más eficiente en la variedad Ojo de Toro que en la variedad Virginia. Además redujo el daño por T. urticae pero no evitó la reducción del contenido de clorofila por el fitófago.

Palabras clave: porcentaje de daño; control biológico; depredador-presa; depredación

Introduction

Ornamentals of the genus Rosa L. (Rosales: Rosaceae) are produced worldwide (^{Chow et al., 2009}) and in many areas the losses in quantity and quality caused by Tetranychus urticae Koch (Acari: Tetranychidae) are significant. This has increased the production costs and reduced the possibilities of export because of the aesthetic aspect of the cut flower and therefore the capture of resources has diminished (^{Otero, 2002}). Therefore, T. urticae is one of the most important pests in greenhouse ornamentals (^{Otero, 2002}, ^{Grbic et al., 2011}), mainly in roses (Casey et al., 2007, ^{Grbic et al., 2011}). However, there are species of predatory mites used for their biological control and one of the most effective is Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae), due to its high predation capacity (^{Chacón et al., 2017}) and high rate of population increase, which allows it to rapidly decrease the population of the plague (^{Escudero and Ferragut, 2005}).

The relationship of plant quality and growth rate, and migration of T. urticae (^{Park and Lee, 2002}, ^{Nachman and Zemek, 2002a} and ^2002b, ^{Reddall et al., 2004}) was demonstrated by biological control (^{Nachman and Zemek, 2003}; ^{Eisa and Mostafa, 2013}), but some aspects that could be relevant for analysis are unknown, such as the condition of the plant. The main indicator of the condition of the plant is the content of chlorophyll in the leaf (^{Nachman and Zemek, 2002a}), and the removal of that chlorophyll will negatively affect the photosynthetic activity and therefore reduce the growth of the plant (^{Tomczyk and Kropczynska, 1985}; ^{Park and Lee, 2002}).

A non-destructive technique that allows establishing the condition of the plant by estimating the content of chlorophyll in the leaf is with a portable chlorophyll meter. Thus the study hypothesis was: P. persimilis reduces the populations of T. urticae, so chlorophyll is not affected. The objectives were: 1) to determine the susceptibility or resistance of rose varieties to the attack of T. urticae, 2) determine the relationship between the condition of the plant and the population density of T. urticae, 3) know the predation effect of P. persimilis in the control of T. urticae and its efficiency, and 4) determine the variety in which P. persimilis performs best.

Materials and Methods

The study was carried out in the facilities of the Department of Parasitology of the Antonio Narro Autonomous Agrarian University in Buenavista, Saltillo, Coahuila, Mexico. The species used were T. urticae, P. persimilis and two varieties of rose (Rosa sp.), Ojo de Toro, a new variety introduced in Mexico, and Virginia, resistant to the attack of T. urticae (^{Flores-Canales et al., 2011}). The colony of T. urticae started with nymphs and adults collected in apple orchards in the town of Huachichil, Municipality of Arteaga, Coahuila. We released these mites in bean plants grown under greenhouse conditions at 27 ± 4°C. Predatory P. persimilis mites were provided by KOPPERT Biological Systems S.A., Mexico.

We sowed 10 plants per variety at a distance of 10 cm in a sowing bed of 60 cm × 9 m and used black earth as substratum. The plants were fertilized with NPK for 75 weeks once a week, with monoammonium phosphate (12-61-0) (36.10 g), ammonium nitrate (12-00-46) (35.16 g), and urea (46 -00-00) (13.75 g) diluted in 20 L of water; in the following week we did not apply fertilizer to avoid the effect of the macroelements on T. urticae (^{Najafabadi et al., 2011}, ^{Ribeiro et al., 2012}). Twenty-five days before the infestation, we applied the insecticide Dibrol® 2.5 CE (Deltamethrin: (S) -alpha-cyano-3-phenoxybenzyl (1R, 3R)-3-(2,2-dibromovinyl)-2,2-dimethylcyclopropanecarbo- xylate), with 1 mL L^-1 of water, to prevent the presence of pests such as: Myzus persicae (Sulzer) (Hemiptera: Aphididae), Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae), and Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). The study was carried out at 27 ± 4°C and HR of 60 ± 15%.

Nineteen months after sowing (76 weeks), we conducted a randomly induced infestation with 100 freshly matched T. urticae adult females per plant; a week later we sampled the population of this mite in three leaflets per stratum (upper, middle and lower) by variety, and we immediately released 12 adult females of P. persimilis per plant (4 females per stratum: upper, middle and lower). The number of phytoseiids released was in accordance with the density of T. urticae released and the average consumption of P. persimilis (approximately eight individuals in 20 h, ^{Argüelles et al., 2013}). We adjusted the density of the predator by multiplying the density to be released, which is the predator-prey ratio determined by the maximum consumption rate of the functional response, by the mortality percentage of 7 % (^{Hilarión et al., 2008}); and 7 d later we started the population samples of T. urticae and P. persimilis by stratum/variety, respectively, and then we did them each week observing three leaflets per stratum in three random plants per sample per variety. The count was made with a 30X magnifying glass.

To determine the chlorophyll content, we used SPAD 502 (Konica Minolta, Osaka, Japan) and LI3100C (LICOR Biosciences, USA) to measure the leaf area. The damage index (IDF) was visually estimated for each leaflet using an arbitrary scale of 0 (no damage or 0 % damage) to 5 (dense mark or wilt per whole leaflet consumption (81 to 100 % damage; ^{Hussey and Parr, 1963}; ^{Nachman and Zemek, 2002a}).

Experimental design

We established the experimental design in two parts and the first one was one way. We analyzed the effects of T. urticae in the absence of the predator by using the variables chlorophyll content in SPAD cm^-2 units, percentage of damage cm^-2 and number of mites cm^-2 in rose plants. We collected three samples per stratum (upper, middle and lower) per variety of rosebush per week. The second part was a design of repeated measurements in which we analyzed the same variables plus the effect of the release of P. persimilis. We considered a rose plant as an experimental unit where we analyzed the effects of the release of T. urticae and P. persimilis. In total, we analyzed 72 samples per variety.

Statistical analysis

The statistical analysis was carried out in three stages: 1) before the release of P. persimilis, 2) after the release of P. persimilis, and 3) simple linear and multiple and non-linear regressions.

In stage 1, we performed one-way ANOVA to compare the variety and stratum of the plant with greater resistance to T. urticae, higher percentage of damage and lower chlorophyll content caused by T. urticae. Data were analyzed by using PROC GLM and to separate the means we applied the test of significant minimum differences (p ≤ 0.05).

Stage 2 comprised two parts: 1) to determine significant differences by stratum per variety, we applied the repeated measurements ANOVA (ANOVArm) for the variables T. urticae cm^-2, percentage of damage cm^-2 and the amount of chlorophyll in SPAD cm-² units, P. persimilis cm^-2; and 2) we carried out an ANOVArm to determine significant differences between varieties and strata with respect to the afore mentioned variables. Parts 1 and 2 include the eight weeks of observation of P. persimilis. The repeated measurements factor was eight weeks of sampling. Data were analyzed by using PROC MIXED and to separate the means from the variables we applied the minimum significant differences test (p ≤ 0.05), SAS version 9.0 (^{SAS, 2002}).

In stage 3, we adjusted several simple, multiple and quadratic linear regression models between the variables: number of T. urticae cm^-2, percentage of damage cm^-2, amount of chlorophyll (SPAD units) cm^-2 (y) and the exposure time of the plants to T. urticae (x). We used the Pearson method to measure the association between the variables. The GLM PROC of SAS version 9.0 (^{SAS, 2002}) was used to estimate the parameters and their standard deviations by regression; to estimate the degree of association using Pearson's method we utilized PROC CORR PEARSON; and the t-Student and F tests for the significance test of the models (p ≤ 0.05).

Results and Discussion

Prior to the release of Phytoseiulus persimilis

Per stratum

In the Virginia variety, we observed significant differences in the abundance of T. urticae (F₂, ₆ = 10.73, p ≤ 0.01), but not in the chlorophyll content or in the percentage of damage (F₂, ₆ = 1.32, p> 0.05; F₂, ₆ = 0.43, p > 0.05). Ojo de Toro presented differences in the percentage of damage (F₂, ₆ = 8.42, p ≤ 0.05), but not in the abundance of T. urticae (F₂, ₆ = 0.13, p > 0.05) and the chlorophyll content (F₂, ₆ = 0.09, p > 0.05) (Table 1). In Virginia, the chlorophyll content and the percentage of damage by stratum showed no differences, which indicates that T. urticae feeds and damages the plant with the same intensity, regardless of the position it has in the plant, but in Ojo de Toro the phytophagous damaged the lower stratum more. The highest percentage of damage was caused by a lower number of compared phytophages where we detected more of them (Table 1).

Table 1 Average of Tetranychus urticae cm^-2, chlorophyll content in SPAD cm^-2 units and percentage of damage cm^-2 in two varieties of rose.

Estrato	T. urticae cm^-2		Cantidad de clorofila cm^-2		Porcentaje de daño cm^-2
Estrato	Ojo de Toro	Virginia	Ojo de Toro	Virginia	Ojo de Toro	Virginia
Superior	0.83^a*	2.86^b	3.69^a	3.63^a	0.29^c	2.25^a
Medio	0.95^a	1.61^b	4.66^a	3.07^a	1.75^b	1.33^a
Inferior	0.65^a	4.52^a	3.85^a	3.88^a	3.18^a	3.07^a
General	0.81^B**	2.99^A	4.07^Y	3.52^Z	1.74^Q	2.22^Q

*Means with different letter in a line are statistically different (p ≤ 0.05). ** Means with different letter in a column are statistically different (p ≤ 0.05).

Per variety and between them

The differences between varieties were significant with respect to the abundance of T. urticae (F₁, ₁₆ = 17.54, p ≤ 0.01), but not with respect to chlorophyll (F₁, ₁₆ = 1.68, p > 0.05) nor in the percentage of damage (F₁, ₁₆ = 0.30, p > 0.05; Table 1), probably due to the average mite cm^-2 presented by the varieties. According to ^{Poskuta et al. (1975)}, T. urticae did not influence the content of chlorophyll a or b in the strawberries of the Talisman variety, with densities of up to 4 mites cm^-2. Besides, ^{Bounfour et al. (2002)} did not observe significant differences between the number of T. urticae and the chlorophyll content in red raspberry leaves, though the fluorescence measurements indicated an interruption in the photosynthetic apparatus.

The number of T. urticae cm^-2 on the rose varieties was statistically different, which can be attributed to the conditions that involve chemical, nutritive, physical aspects such as pubescence, tissue resistance, surface structure of the leaves, available surface for each individual and the secondary metabolites of the plants (^{Agrawal, 2000}; ^{Balkema-Boomstra et al., 2003}; ^{Biswas et al., 2004}). These factors can diminish the nutritional quality, reducing digestibility and affecting fertility, growth, population density, survival, development and the mortality of T. urticae in its juvenile stages (^{Peralta and Tello, 2011}).

After the release of the predator

Per stratum

Differences were significant between strata in both varieties with respect to the abundance of T. urticae (F₂, ₄₈ = 5.69, p ≤ 0.01, F₇, ₄₈ = 6.85, p ≤ 0.01). In Ojo de Toro the amount of chlorophyll was not different by stratum (F₂, ₄₈ = 1.63, p > 0.05); whereas in Virginia there were differences (F₂, ₄₈ = 5.80, p ≤ 0.01). In the percentage of damage by T. urticae in both varieties no differences were observed (F₂, ₄₈ = 0.77, p > 0.05, F₂, ₄₈ = 0.21, p > 0.05 (Table 2).

Table 2 Averages of Tetranychus urticae cm^-2, chlorophyll content in SPAD cm^-2 units, percentage of damage cm^-2 and Phytoseiulus persimilis cm^-2 per stratum in two varieties of rose.

Estrato	Ojo de Toro	Virginia	Ojo de Toro	Virginia	Ojo de Toro	Virginia	Ojo de Toro	Virginia
Estrato	T. urticae cm^-2		Cantidad de clorofila en unidades SPAD cm^-2		Porcentaje de daño cm^-2		P. persimilis cm^-2
A
Superior	0.45^b§	0.31^b	3.18^a	3.35^b	0.28^a	0.46^a	0.01^a	0.01^a
Medio	0.46^b	0.29^b	3.24^a	3.42^b	0.46^a	0.30^a	0.01^a	0.01^a
Inferior	1.41^a	1.03^a	3.62^a	4.57^a	0.53^a	0.27^a	0.01^a	0.01^a
General	0.77^A¥	0.54^A	3.35^Y	3.78^Z	0.42^M	0.34^M	0.001^Q	0.01^Q

^§ Means with different letters on a line are significantly different (p ≤ 0.05). ^¥ Means with different letter in a column are significantly different (p ≤ 0.05).

After the release of the predator, both varieties showed significant differences with respect to the abundance of T. urticae (F₂, ₄₈ = 2.57, p ≤ 0.05, F₇, ₄₈ = 8.28, p ≤ 0.01). In Ojo de Toro the chlorophyll content was not different (F₇, ₄₈ = 2.08, p > 0.05). While in Virginia we observed differences in the amount of chlorophyll (F₇, ₄₈ = 2.88, p ≤ 0.01). Regarding the percentage of damage, we found differences during the eight weeks in the Ojo de Toro variety (F₇, ₄₈ = 5.30, p ≤ 0.01), but not in Virginia (F₇, ₄₈ = 1.04, p > 0.05) (Table 3).

Table 3 Averages of Tetranychus urticae cm^-2, chlorophyll content in SPAD cm^-2 units, percentage of damage cm^-2 and Phytoseiulus persimilis cm^-2 per week in two varieties of rose.

Semana	Ojo de Toro	Virginia	Ojo de Toro	Virginia	Ojo de Toro	Virginia	Ojo de Toro	Virginia
Semana	T. urticae cm^-2		Cantidad de clorofila en unidades SPAD cm^-2		Porcentaje de daño cm^-2		P. persimilis cm^-2
1	1.60a^§	2.09^a	4.11^a	4.25^ab	0.38^b	0.58^a	0.01^a	0.00^a
2	1.37^ab	1.29^b	3.58^a	3.83^abc	0.13^b	1.01^a	0.00^a	0.01^a
3	1.12^ab	0.55^bc	3.55^a	3.66^bc	0.018^b	0.02^a	0.01^a	0.00^a
4	1.03^ab	0.25^c	3.38^a	4.41^ab	0.08^b	0.57^a	0.01^a	0.01^a
5	0.60^ab	0.06^c	3.37^a	5.08^a	0.17^b	0.00^a	0.01^a	0.02^a
6	0.45^ab	0.10^c	3.18^a	3.31^bc	1.49^a	0.21^a	0.02^a	0.01^a
7	0.01^b	0.00^c	2.80^a	2.85^c	1.11^a	0.35^a	0.00^a	0.00^a
8	0.00^b	0.00^c	2.78^a	2.81^c	0.00^c	0.00^a	0.00^a	0.00^a

^§ Means with different letters on a line are significantly different (p ≤ 0.05).

After the release of the phytoseiids, we observed the highest average of chlorophyll and the number of T. urticae cm^-2 in the lower stratum in both varieties, which indicates that the phytophagous seeks the best conditions such as food quality.

Among varieties

Among varieties, no significant differences were found in the abundance of T. urticae (F₁, ₉₆ = 2.00, p > 0.05), nor among strata during the eight weeks (F₂, ₉₆ = 0.21, p > 0.05). However, in the chlorophyll content we observed differences between varieties (F₁, ₉₆ = 4.78, p ≤ 0.05), but not between strata (F₂, ₉₆ = 1.75, p > 0.05); while the percentage of damage was not different between varieties (F₁, ₉₆ = 0.26, p > 0.05), and strata (F₂, ₉₆ = 0.76, p > 0.05) (Table 2).

Regarding the number of P. persimilis cm^-2 in both varieties, we observed no significant differences between strata (F₂, ₄₈ = 0.59, p > 0.05, F₂, ₄₈ = 0.10, p > 0.05); neither with respect to the abundance of P. persimilis cm^-2 (F₇, ₉₆ = 0.11, p > 0.05) (Table 2). Similarly in the phytoseiid abundance in the eight weeks (F₇, ₄₈ = 1.07, p > 0.05, F₇, ₄₈ = 0.78, p > 0.05) (Table 3). In addition, we found lower predator abundance compared to that reported by ^{Nachman and Zemeck (2003)} and ^{Eisa and Mostafa (2013)}. The plants possibly positively and negatively affect the predatory mite directly or indirectly (^{Dicke and Sabelis, 1988}). In this respect, ^{Vázquez et al. (2008)} mentioned that the host plants and the refuge also affect the predator; while ^{De Bach (1964)} reported that semiochemicals influence the predator in its establishment. These factors probably influenced the population of P. persimilis, since in both varieties the averages were similar.

Association

The Ojo de Toro variety

The chlorophyll content, percentage of damage (partial correlation r = -0.2384, p ≤ 0.05) and the number of T. urticae were negatively correlated with the exposure time of the plant to the T. urticae mite (Figure 1). This indicates that the quantified variables decrease with the passage of time (Figure 1A, 1B and 1C).

Figure 1 Relationship between the number of weeks (x) in which the plants were exposed to T. urticae and the amount of chlorophyll in SPAD cm^-2 units, damage caused and number of T. urticae cm^-2.

There was an association between the chlorophyll content in SPAD cm^-2 units, and the exposure time of the plant to the T. urticae mite and the number of mites per cm² x₂:

Amount of chlorophyll (SPAD units)/cm^-2 = 3.7614

(DE = 0.2098) -0.1290 (DE = 0.03897)x₁+0.2374

(DE = 0.0827)x₂

The value of R² (0.2747; F₂, ₇₈ = 14.77; p ≤ 0.01) indicated that 27.47 % of the variation in the amount of chlorophyll in SPAD cm^-2 units was found associated with the time of exposure of the plant to T. urticae and the number of mites per cm². The most important factor was the exposure time (x₁) (F₁, ₇₈ = 11.08; p ≤ 0.01) followed by the number of T. urticae per cm² (x₂) (F₁, ₇₈ = 8.23; p ≤ 0.01). The multiple regression model did not show any significant dependence between the percentage of damage and the time of exposure of the plant to T. urticae and the number of mites per cm² (R² = 0.0176, F₂, ₇₈ = 0.70, p > 0.05). The number of phytophages correlated positively with the amount of chlorophyll (Figure 2), which indicates that T. urticae looks for more food (Figure 2A), but not with the percentage of damage per cm² (Figure 2B).

Figure 2 Relationship between the amount of chlorophyll cm^-2, percentage of damage cm^-2 and Tetranychus urticae (Number cm^-2) in two varieties of rose.

The Virginia variety

The correlation between the content of chlorophyll SPAD cm^-2 units (r = -0.2355, p ≤ 0.05), the percentage of damage per cm², the number of phytophages cm^-2 and the exposure time of the plant to T. urticae were negative and significant (Figure 1D, 1E, and 1F). This indicates that the variables decrease over time.

The multiple regression showed a relationship between the chlorophyll content in SPAD cm^-2 units and the number of mites per cm² (x₁) and the exposure time of the plant to T. urticae (x₂).

Content of chlorophyll SPAD cm^-2 units = 2.5529

(DE = 0.6042) + 0.3272(DE = 0.1615)x₁ + 0.7876

(DE = 0.2673)x₂ - 0.0979(DE = 0.0288) x²₂ (R² = 0.1670;

F_3,77 = 5.15; p ≤ 0.01).

The most important factor was the time of exposure to the square x²₂ (F₁, ₇₇ = 11.51, p ≤ 0.01) followed by the exposure time x₂ (F₁, ₇₇ = 8.68, p ≤ 0.01) and finally the number of mites per cm² x₁ (F₁, ₇₇ = 4.10; p ≤ 0.05).

The number of phytophages correlated positively with the amount of chlorophyll and the percentage of damage (Figure 2), which indicates that the two-spotted mite seeks leaves of better nutritional quality (Figure 2A), and the greater the number of mites bigger is the damage (Figure 2D).

The association between the amount of chlorophyll and the damage index in both varieties was not significant (r = -0.637, p > 0.05 and r = -0.1076, p > 0.05). No linear association was found between the variables, number of P. persimilis cm^-2 and the number of phytophages cm^-2 in both varieties (r = -0.0331, p > 0.05, r = -0.0053, p > 0.05).

The results obtained coincide with those by ^{Tomczyk and Kropczynska (1985)}, who showed that the concentration of biochemical components (such as chlorophyll) can also be affected by the eating habits of T. urticae. Changes in the concentrations of this compound can also influence the physiology of plants. The decrease in chlorophyll content in leaves can also be attributed to changes in the chloroplast content of cells adjacent to cells damaged by mites (^{Tomczyk and Kropczynska, 1985}).

Tetranychus urticae affects rose plants, since chlorophyll has a direct association with photosynthesis and plant productivity (^{De Angelis et al., 1983}, ^{Iatrou et al., 1995}, ^{Haile and Higley, 2003}, ^{Reddall et al., 2004}). According to ^{Bounfour et al. (2002)}, longer periods of feeding by T. urticae result in a significant decrease of fluorescent chlorophyll and chlorophyll content, as happened in our study, in which we showed that the chlorophyll content cm^-2 and the percentage of damage cm^-2 decrease over time on plants exposed to T. urticae. ^{Nachman and Zemeck (2002a)} found that the main association was the time the plants were exposed to the T. urticae mite. In both varieties, a negative relationship was observed between the chlorophyll content cm^-2 and the damage index, which agrees with the results obtained by ^{Nachman and Zemek (2002a)}. The release of P. persimilis did not benefit the rose varieties, since chlorophyll content cm^-2 continued decreasing over time (Figures 1A and 1D), contrary to the results reported by ^{Eisa and Mostafa (2013)} who recorded less chlorophyll losses in vine plants by releasing two and four predatory mites Typhlodromips capsicum Mostafa per branch, in comparison with plants infested only by T. urticae. When diminishing the number of T. urticae cm^-2 by the predation of P. persimilis cm^-2 the percentage of damage cm^-2 in both varieties decreased. ^{Nachman and Zemek (2002b)} observed that the plants infested with P. persimilis were taller, had less phytophages and showed a lower level of lesions compared to plants without predators. The effect of predators on plants was greater with five phytoseiids than with three.

Results indicate that in the Ojo de Toro variety there is a positive correlation between the content of chlorophyll cm^-2 and the number of mites cm^-2, that is, the phytophagous moves to leaves of higher quality, while in Virginia no significant relationship was found (p > 0.05) although the slope was positive. In this regard, ^{Johnson (1983)} found no correlation between the number of Panonychus ulmi (Koch) and the chlorophyll content of apple leaves, which is attributed to the fact that mites move between the leaves in a way that does not determine the quality of the leaf. ^{Sances et al. (1979a)} found no relationship between the number of mites d^-1 cm^-2 in a range of 0 to 50. In the Virginia variety we observed that the higher the number of mites cm^-2, greater the percentage of damage cm^-2. ^{Sances et al. (1979b)} pointed out that the main reason for the reduction of the chlorophyll content is probably the mechanical damage of the chloroplasts during mite feeding, the loss of the amount of chlorophyll content that depends on the mite species and the variety of the host plant; as well as the duration of feeding time and the population density of the phytophagous.

In the Virginia variety, we observed that by releasing 12 females of phytoseiids per plant it is possible to control the phytophagous in six weeks, and in Ojo de Toro in eight weeks. Since the mobility of P. persimilis does not depend on the density of trichomes (^{Krips et al., 1999}) and the leaves of Rosa sp. do not present trichomes, it is likely that the functional response of the predator is favored because there is no physical barrier that limits the ability to search (^{Forero et al., 2008}). According to ^{Nachman and Zemek (2003)}, the initial number of predators also has an important function. They reported that three individuals of P. persimilis per plant might not be sufficient to guarantee control of the T. urticae mites five weeks after their release. In contrast, five predators per plant can exercise a more efficient control; in our study, it took an additional week to control the pest, since there are differences between the hosts used, such as height.

Conclusions

The Ojo de Toro variety showed greater resistance to T. urticae. Phytoseiulus persimilis helps to reduce the damage caused by T. urticae, but not to stop the decrease of the chlorophyll content because of the phytophagous feeding in both varieties of rose. Tetranychus urticae caused similar damage cm^-2 percentages in both varieties and had different chlorophyll contents. Phytoseiulus persimilis was more efficient in the Virginia variety.

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Received: February 2017; Accepted: October 2017

^*Autor para correspondencia: jlanflo@uaaan.mx

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