Patrones de distribución de Tetranychus urticae Koch y Phytoseiulus persimilis Athias-Henriot (Acari: Tetranychidae, Phytoseiidae) en tres variedades de rosas

J C Chacón-Hernandez; E Cerna-Chavez; S G Mora-Ravelo; Y M Ochoa-Fuentes; M Rocandio-Rodríguez; J Landeros Flores

Distribution patterns of Tetranychus urticae Koch and Phytoseiulus persimilis Athias-Henriot (Acari: Tetranychidae, Phytoseiidae) in three roses varieties

J. C. Chacón-Hernández¹; E. Cerna-Chave²; S. G. Mora-Ravelo¹; Y. Ochoa-Fuentes²; M. Rocandio-Rodríguez¹; J. Landeros-Flores²^*

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

<postal-code>87019</postal-code>

<city>Ciudad Victoria</city>

<state>Tamaulipas</state>

, Mexico , 2. Departamento de Parasitología Agrícola. Universidad Autónoma Agraria Antonio Narro. Calzada Antonio Narro 1923. C.P. 25315 Buenavista, Saltillo, Coahuila; México., Universidad Autónoma Agraria Antonio Narro, Departamento de Parasitología Agrícola, Universidad Autónoma Agraria Antonio Narro,

<postal-code>25315</postal-code>

<city>Saltillo</city>

<state>Coahuila</state>

, Mexico

Correspondence: *. Corresponding Author: Landeros-Flores, J. Universidad Autónoma Agraria Antonio Narro, Departamento de Parasitología Agrícola. Calzada Antonio Narro 1923. C.P. 25315 Buenavista, Saltillo, Coahuila; México. E-mail: E-mail:

Abstract

Tetranychus urticae (T. urticae), is an important plague in crops reared under greenhouse and field conditions. One of its biological controls is the predatory mite Phytoseiulus persimilis (P. persimilis) for its efficiency. Knowledge on preys and predators spatial distribution is important for assessing the persistence in a crop and the potential of a natural enemy to reduce its prey. The aims of this study were to determine: 1) T. urticae preference for the upper or back sides of leaflet, 2) T. urticae and P. persimilis spatial and vertical distribution pattern in the four stages of development, on three rose bush varieties under greenhouse conditions. T. urticae and P. persimilis spatial distribution was determined by four methods: variance-mean ratio, dispersion index, Taylor’s power law and Iwao’s patchiness regression. Significant differences were found in population density in the four developmental stages of T. urticae before and after release of P. persimilis. T. urticae prefers to colonize the underside of leaflets in the three rose bush varieties. Results showed a different vertical distribution among the four developmental stages of T. urticae in the three varieties. The four methods used showed that T. urticae and P. persimilis have an aggregated distribution. P. persimilis does not modify T. urticae spatial distribution but if its vertical distribution. The aggregation presented by the predator favors a more effective control over the phytophagous.

Received: 2017 December 19; Accepted: 2018 June 13

revbio. 2020 Mar 23; 5(spe1): e423

doi: 10.15741/revbio.05.nesp.e423

Keywords: Key words: Predator-prey, vertical distribution, spatial distribution, biological control.

Introduction

Tetranychus urticae (Acari: Tetranychidae) is one of the most polyphagous herbivore arthropods, it feeds on more than 1,100 species of plants belonging to more than 140 different families, including species known for producing toxic compounds. Moreover, it is an important plague in cultivations under greenhouse and field conditions (Grbic et al., 2011). Tetranychus urticare (T. urticae), is economically one of the most important plagues in roses (Khajehali et al., 2011).

Phytoseiulus persimilis, Athias-Henriot (Acari: Phytoseiidae) is a predator mite specialized on phytophagous mites Tetranychus spp. (Tello et al., 2009). It has been studied for its efficiency in the biological control of T. urticae on discus of rose Rosa sp. Royal variety under laboratoty conditions (Chacón et al., 2017) and by means of releases in greenhouses (Alatawi et al., 2011). Phytoseiulus persimilis (P. persimilis), is the most commercialized mite and widely released in greenhouses (Naher & Haque, 2007; Tello et al., 2009).

Knowledge on preys and predators spatial distribution is important for evaluating the persistence of a crop and the potential of a natural enemy to reduce its prey (Slone & Croft, 1998). The measurement of species aggregation is a central topic in ecology and applied biology, especially for studies of sampling and density (Gutiérrez, 1996). With the purpose of developing sustainable strategies for biological control, understanding the effects of the habitat structure on the capacity of natural enemies is necessary (Stavrinides & Skirvin, 2003). Understanding the seasonal development and the vertical dispersion of the pest and its predators in plants is crucial for the development of an optimal release strategy for P. persimilis (Lilley et al., 1999). Many factors affect spatial patterns and the aggregation among mites that commonly occur in plant foliage, such as walking, searching, dispersing, fecundity, development, territoriality, search for sexual partners or responses to plants or preys quality and quantity (Slone & Croft, 1998), changes in plant height and the density of natural enemies populations (Strong, et al., 1997). The hypothesis of this study was: P. persimilis modifies the distribution patterns of the four developmental stages of T. urticae. Therefore, the purposes of this study were to determine: 1) T. urticae preference for the upper or back sides of leaflet and, 2) T. urticae and P. persimilis spatial and vertical distribution pattern in the four developmental stages on three varieties of rose bush varieties under greenhouse conditions.

Materials and Methods

Experimental protocol

T. urticae colony was obtained in de the Acarology Area of the Universidad Autónoma Agraria Antonio Narro. Buenavista, Saltillo, Coahuila, Mexico. Three varieties of roses (Rosa sp.) were used Selena, Vision and Anastasia. Ten plants per variety were planted at a distance of 10 cm in a 60 cm x 9 m bed planting. Plants were fertilized with ammonium phosphate monobasic (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, once a week. The varieties were left to fertilize a week before releasing T. urticae, to avoid any effect of the macro elements on the plague (Najafabadi et al., 2011). Dibrol® 2.5 CE (Deltametrin: (S)-alfa-cyano-3-phenoxybenzyl (1R,3R)-3-(2,2-dibromo vinyl)-2,2- dimethyl cyclopropane carbo -xylate). Fertilization was applied 25 days before infestation of T. urticae, with a dose of 1 mL L^-1 of water to prevent pests such as: Myzus persicae (Sulzer) (Hemiptera: Aphididae), Trialeurodes vaporariorum (Westwood) (Hemiptera:Aleyrodidae) and Frankliniella occidentalis (Pergande) (Thysanoptera: Thirpidae). The study was developed under greenhouse conditions at a temperature of 28 ± 4 ºC, with a H.R. of 60 ± 15 %.

Population density

A non-conventional method was used to infest rose bush plants; one hundred adult female mites were released in each variety, by pinto bean leaf discs (Phaseolus vulgaris L.) of 2.5 cm of diameter (Chacón et al., 2016). One week after, the four developmental stages of T. urticae (egg, larva, nymph and adult) were counted and 24 hours later, 12 females of the phytoseiid P. persimilis were released per plant (predator was obtained from Koppert Mexico, S.A. de C.V. company, subsidiary of the Dutch Koppert Biological Systems company). P. persimilis releases were performed according to the average density of T. urticae of the three rose bush varieties and to the average consumption of P. persimilis of the four developmental stages of the phytophagous (approximately 14 individuals in 24 hours) (Argüelles et al., 2013). Predator density was adjusted by multiplying the density when releasing, which is the predator-prey relationship, determined by the maximum consumption rate of the functional response multiplied by mortality rate 7 % (Hilarión et al., 2008). Weekly records were performed for the four developmental stages of T. urticae and P. persimilis, by counting on the three leaflets per stratum per variety with a 30X portable microscope, the plant being the experimental unit. Densities of prey and predator egg, larva, nymph, and adults were statistically analyzed, by means of an analysis of variance (ANOVA). Data were compared among the three rose bush varieties on each sampling date and in general by means of Fisher’s minimum significant differences (MSD) test (p≤0.05).

Distribution of mites on leaflets and plants

Whole data were considered in order to determine the preference for the upper and back sides of leaflets, as well as the vertical distribution, inferior (0-40 cm), medium (41-80 cm) and superior (81-160 cm) of the four developmental stages of the two species of mites (prey and predator) on plants.

Spatial distribution pattern

T. urticae and P. persimilis spatial distribution was determined using four methods: the variance/mean ratio, dispersion index, Taylor’s power law and Iwao’s patchiness regression.

The dispersion of a population can be classified by calculating the -variance-mean ratio S² /m = 1 random, <1 uniform y >1 aggregate. The result of a random distribution can be proven by calculating the dispersion index (DI) when n is the number of samples: DI = (n-1) S ² /m.

In the next stage, the Z coefficient was calculated to prove the goodness of fit: where v is the degree of freedom (n-1);

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If 1.96 ≥Z≥-1.96, spatial distribution is random; but if Z<-1.96 or Z>1.96, distribution is uniform or aggregated, respectively (Pedigo & Buntin, 1994).

Taylor’s power law: S² =am^b or log(S²)=log(a)+blog(m), where S² is the variance; m is the sample mean; a is a scale factor related to sample size; and b measures the aggregation of the species. If b =1, <1 and >1, distribution is random, uniform and aggregated, respectively (Taylor, 1961).

Iwao’s patchiness regression method was used to quantify the relationship between the mean overcrowding index (m^*) and the mean (m). m^* =a+βm, where α indicates the attraction (positive) and repellence «competition» (negative) among organisms, while β reflects the spatial distribution of the population (Iwao, 1968). It is interpreted in the same way as b constant in Taylor’s power law. Student’s t-test was used to determine whether mites populations are randomly dispersed.

Results and Discussion

Table 1 shows the estimated mean population density per leaflet of T. urticae and P. persimilis in their four developmental stages, in three rose bush varieties , for nine dates of sampling for the prey and eight for the predator. Before releasing the predator, results indicate significant differences in the three rose bush varieties (p<0.05) in egg densities, but not in larva, nymph and adults (p>0.05). After releasing the predator, the population density of eggs and nymphs of the phytophagous was different among the three varieties (p<0.05). In relation to predator density, significant differences were detected on the last three dates of sampling only at larval stage (Table 1).

Table 1.

Population mean (± SD) of eggs, larvae, nymphs and adults of Tetranychus urticae and Phytoseiulus persimilis in three roses varieties

	Tetranychus urticae
Eggs			Larvae			Nymphs			Adults
	Selena	Visión	Anastasia	Selena	Visión	Anastasia	Selena	Visión	Anastasia	Selena	Visión	Anastasia
	Before release of Phytoseiulus persimilis
0	69.00^a	24.89^ab	10.00^b	9.00^a	5.44^a	5.78^a	9.56^a	3.56^a	7.44^a	20.56^a	9.89^a	14.67^a
After release of Phytoseiulus persimilis
1	16.44^a	12.44^a	4.78^a	2.67^a	3.33^a	3.89^a	7.89^a	12.11^a	3.22^a	3.11^a	4.33^a	4.22^a
2	28.22^a	28.78^a	6.00^a	2.67^a	7.22^a	3.11^a	12.00^a	8.78a^b	3.67^b	10.44^a	2.56^a	7.56^a
3	43.67a	2.11^a	1.56^a	3.89^a	1.44^a	1.00^a	19.44^a	6.78^b	6.11^b	7.56^a	6.89^a	4.33^a
4	3.11^b	0.56^b	0.00^b	1.33^a	0.11^a	0.11^a	16.11^a	1.89^b	1.11^b	1.22^a	0.44^a	2.22^a
5	13.89a	0.22^b	0.22^b	2.11^a	0.00^b	0.00^b	14.78^a	0.89^a	0.33^b	4.56^a	0.44^b	0.78^b
6	0.25a	0.00^b	0.00^b	--	--	--	2.00^a	0.11^a	0.22^a	0.11^a	0.22^a	0.333^a
7	--	--	--	0.22^a	0.00^a	0.00^a	0.56^a	0.00^a	--	--	--	--
8	--	--	--	--	--	--	0.11^a	0.00^a	--	--	--	--
Gen. Ave.	13.26a	5.44^b	1.63^c	1.61^a	1.51a	1.01^a	9.11^a	3.70^b	1.90^b	5.29^a	2.74^a	3.79a
Phytoseiulus persimilis
1	0.00^a	0.00^a	0.22^a	0.11^a	0.00^a	0.00^a	0.11^a	0.00^a	0.00^a	0.11^a	0.00^a	0.11^a
2	0.00^a	0.00^a	0.44^a	--	--	--	--	--	--	0.00^a	0.00^a	0.33^a
3	1.22^a	0.67^a	0.33^a	--	--	--	0.33^a	0.33^a	0.00^a	0.11^a	1.33^a	0.22^a
4	0.44^a	0.44^a	0.33^a	0.22^a	0.11^a	0.33^a	0.44^a	0.11^a	0.11^a	0.33^a	0.00^a	0.44^a
5	3.00^a	0.00^a	0.22^a	0.67^a	0.00^b	0.00^b	0.22^a	0.11^a	0.11^a	1.11^a	0.56^a	2.00^a
6	0.33^a	0.00^a	0.00^a	0.11^a	0.00^b	0.00^b	0.33^a	0.00^a	0.11^a	0.33^a	0.00^a	0.11^a
7	--	--	--	--	--	--	0.22^a	0.00^a	0.00^a	0.22^a	0.00^a	0.11^a
8	--	--	--	--	--	--	--	--	--	0.22^a	0.11^a	0.00^a

^TFN1Mean with the same letter between columns are not significantly different (p<0.05).

P. persimilis controlled eggs of T. urticae in five weeks in Vision and Anastasia varieties, and in six weeks in the Selena variety. While controlling T. urticae larvae only took four weeks in Vision and Anastasia varieties and seven weeks in Selena variety. Regarding phytophagous nymphs, the phytoseiid controlled them in six weeks in Vision and Anastasia varieteies and in eight in Selena variety. T. urticae adults were predated in six weeks by P. persimilis in the three varieties. Therefore, P. persimilis preferred consuming T. urticae larvae in Vision and Anastasia varieties, followed by the eggs in the same varieties (Table 1). Contrary to what observed by Parvin et al., (2010), who found that on the seventh day, the different stages (nymph, female and male adults) of P. persimilis, preferred eggs as food rather than other stages of T. urticae.

Preference for upper or back sides

T. urticae prefers colonizing the back side of the leaflets in the three rose bush varieties (Table 2A). Similar results were observed by Soler-Salcedo et al., (2006) in leaflets of the common bean (Phaseolus vulgaris), they found that between 70 and 80 % of mobile stages of T. urticae prefers occupying the back side, while in a study performed in raspberry (Rubus idaeus), they established that 70.9 % of phytophagous population is found on the back of the leaves (Salazar et al., 1998). After releasing P. persimilis, an increase in the percentage of occupation in the upper side was observed, but the back side presented the highest proportionality. Consequently, T. urticae developed its colonies in the back side of the leaflets of rosebush varieties with or without presence of P. persimilis.

Table 2.

Preference for the underside and beam of leaves (A), vertical distribution of Tetranychus urticae (B) and Phytoseiulus persimilis (C) in three roses varieties

	Selena				Visión				Anastasia
Preference	Development stage
Preference	Eggs	Larvae	Nymphs	Adults	Eggs	Larvae	Nymphs	Adults	Eggs	Larvae	Nymphs	Adults
A. Preference of T. urticae
Before release of Phytoseiulus persimilis
Underside	96	91	83	87	100	88	84	92	100	100	100	96
Beam	4	9	17	13	0	12	16	8	0	0	0	4
After release of Phytoseiulus persimilis
Underside	94	79	77	65	72	87	79	77	99	92	94	95
Beam	6	21	23	35	28	13	21	23	1	8	6	5
B. Vertical distribution T. urticae
Estratum	Before release of Phytoseiulus persimilis
Upper	66	32	36	78	96	63	69	93	18	31	22	17
Middle	4	26	31	14	4	37	31	7	42	17	24	45
Low	30	42	33	8	0	0	0	0	40	52	54	38
After release of Phytoseiulus persimilis
Upper	81	66	37	55	22	37	51	41	37	34	19	13
Middle	10	18	39	26	16	22	28	21	37	48	64	61
Low	9	16	24	20	62	41	21	38	25	18	18	26
C. Vertical distribution of P. persimilis
Upper	71	40	27	64	0	0	0	6	36	0	33	63
Middle	20	30	47	14	90	100	60	67	36	33	67	30
Low	9	30	27	23	10	0	40	28	29	67	0	7

Vertical distribution

Results showed an unequal vertical distribution in the four developmental stages of T urticae in the three rose bush varieties (Table 2B). Before releasing P. persimilis, the two-spotted spider mite preferred depositing its eggs on superior stratum in Selena and Visión varieties, and in the medium stratum in Anastasia variety. The highest percentage of larvae was observed in the inferior stratum in Selena and Anastasia varieties, and in the superior stratum in Vision variety. The nymphal state was observed in the upper stratum in Selena and Visión, while in the lower stratum in Anastasia variety. The highest percentage of adult was showed to be in the superior stratum in Selena and Vision varieties, and in the medium stratum in Anastasia variety (Table 2B).

After releasing the phytoseiid in Selena variety, the phytophagous maintained its preference for depositing eggs on the superior stratum, while in Visión variety, it changed its preference from superior to inferior and in Anastasia variety, it presented the same percentage of eggs in the medium and superior stratums. Preference of T. urticae larvae was modified in all of the varieties. In Selena variety, from inferior to superior, in Vision variety, from superior to inferior, and in Anastasia variety, from inferior to medium. As well, nymphs changed its preference in Selena and Anastasia varieties, from superior to medium and from inferior to medium, respectively, while in Vision variety, preference was maintained in the superior stratum. Regarding adults, they were found in the same stratum (inferior) in Selena and Vision varieties, while in the medium stratum in Anastasia variety.

The four developmental stages of the phytophagous were affected by the presence of P. persimilis, but it was more remarkable in Vision variety, since individuals were not observed in the inferior stratum before releasing them, then the two-spotted spider mite was distributed in the three stratums of the plant, having more eggs and larvae in the inferior stratum. Regarding P. persimilis, the highest percentage of eggs was observed in the superior stratum in the variety Selena, in the medium stratum in Visión variety and, in the superior and medium stratum in Anastasia variety. In Selena variety, phytoseiid larvae were observed in a higher proportion in the superior stratum, in the medium stratum in Visión variety and in the inferior stratum in Anastasia variety. While for nymphs, in medium stratum in Selena, Visión, and Anastasia varieties. Adults in the superior stratum in Selena and Anastasia varieties, and in the medium stratum in Visión variety. Walzer et al., (2009) found similar behaviors in adults of P. persimilis on bean under greenhouse conditions; they observed that phytoseiid was located in higher abundance in the medium stratum. In our research, prey and predator were observed to present the highest percentage of eggs, larva, and nymphs in the same stratums in Selena and Anastasia varieties, indicating that the predator is located where the highest abundance of its prey is present; and deposits its eggs where there is food for its next generations and it possibly increases its survival rate (Table 2C). Contrary to what was reported by Walzer et al., (2007), who observed that T. urticae avoided the occupied stratums for P. persimilis and Neoseiulus californicus, and prematurely migrated to the superior stratum in bean plants. As well, Grostal & Dicke (1999) reported that in the short term (in leaves) T. urticae females avoided depositing eggs in patches where P. persimilis females were present.

Spatial distribution

An aggregated distribution pattern of T. urticae was registered under greenhouse conditions (Bidarnamani et al., 2015) and together with P. persimilis (Zhang & Sanderson, 1995; Nachman, 2006). Results of the variance-mean- ratio, dispersion coefficient (DI) and the Z test are presented in Table 3. The obtained results indicate that the spatial distribution for the four developmental stages of T. urticae was aggregated. Before releasing the predator, in Taylor’s model, the regression between log S² and log m was not significant (p>0.05), while in presence of P. persimilis, T. urticae presents an aggregated distribution in egg, larva, nymph, and adult, because calculated t (t_c) is higher than the t table (t_t) (Table 4). Similar to Taylor’s power law, Iwao’s model showed that the four developmental stages of T. urticae present an aggregated distribution (Table 5), indicating that P. persimilis does not modify the spatial distribution of the four developmental stages of growth of T. urticae.Zhang & Sanderson (1995) found similar results in rose plants (Goldrush) under greenhouse conditions.

Table 3.

Spatial distribution parameters of Tetranychus urticae on three roses varieties using the variance-average ratio, dispersion index, and Z coefficient to test the goodness of fit.

		m	S²	S²/m		Z
Selena
Eggs	Before	69.00	4,925.00	71.38	571.01	29.92
Eggs	After	1,652.67	65,681,242.03	39,742.58	2,821,723.39	2,363.72
Larvae	Before	9.00	110.25	12.25	98.00	10.13
Larvae	After	16.22	4,312.85	265.86	18,876.11	182.42
Nymphs	Before	9.56	33.28	3.48	27.86	3.59
Nymphs	After	318.39	1,419,116.24	4,457.18	316,459.70	783.69
Adults	Before	20.56	501.28	24.39	195.09	15.88
Adults	After	60.19	122,599.12	2,036.72	144,606.99	525.91
Visión
Eggs	Before	24.89	1,534.11	61.64	493.11	27.53
Eggs	After	370.22	6,259,212.12	16,906.64	1,200,371.11	1,537.56
Larvae	Before	5.44	58.53	10.75	86.00	9.24
Larvae	After	11.47	1,552.90	135.36	9,610.69	126.77
Nymphs	Before	3.56	33.53	9.43	75.44	8.41
Nymphs	After	73.83	128,375.97	1,738.73	123,449.58	485.02
Adults	Before	9.89	213.61	21.60	172.81	14.72
Adults	After	16.00	2,458.14	153.63	10,908.00	135.83
Anastasia
Eggs	Before	10.00	84.50	8.45	67.60	7.75
Eggs	After	17.28	3,351.92	194.00	13,774.14	154.10
Larvae	Before	5.78	30.44	5.27	42.15	5.31
Larvae	After	8.42	1,496.11	177.76	12,620.61	147.00
Nymphs	Before	7.44	78.78	10.58	84.66	9.14
Nymphs	After	20.33	9,146.25	449.82	31,936.92	240.86
Adults	Before	14.67	287.50	19.60	156.82	13.84
Adults	After	34.22	24,951.84	729.11	51,766.96	309.89

Table 4.

Spatial distribution of four stages of development of Tetranychus urticae on different roses varieties using the Taylor´s power law.

Variety	a	±Se_a	B	±Se_b	R²	P_reg	P_a	P_b	t_c	t_t
Before release of Phytoseiulus persimilis
Eggs
Selena	0.736	1.156	1.639	0.295	0.969	0.113	0.639	0.113	2.164	6.314
Visión	0.492	0.655	1.561	0.259	0.973	0.105	0.590	0.105	2.170	6.314
Anastasia	1.320	2.200	1.356	0.970	0.661	0.395	0.656	0.395	0.367	6.314
Larvae
Selena	-3.311	5.508	3.614	2.519	0.673	0.388	0.655	0.388	1.038	6.314
Visión	-0.546	2.959	1.615	1.741	0.463	0.524	0.884	0.524	0.353	6.314
Anastasia	1.945	3.383	0.688	1.971	0.109	0.786	0.668	0.786	-0.158	6.314
Nymphs
Selena	-19.21	26.577	10.056	11.780	0.422	0.550	0.602	0.550	0.769	6.314
Visión	0.061	0.179	2.192	0.133	0.996	0.039	0.792	0.039	8.953	6.314
Anastasia	-3.164	5.499	3.463	2.801	0.605	0.433	0.668	0.433	0.880	6.314
Adults
Selena	1.353	1.274	0.997	0.469	0.819	0.280	0.481	0.280	-0.006	6.314
Visión	0.034	0.043	1.475	0.022	1.000	0.010	0.580	0.010	21.421	6.314
Anastasia	-9.510	1.655	5.359	0.626	0.987	0.074	0.110	0.074	6.959	6.314
After release of Phytoseiulus persimilis
Eggs
Selena	-0.451	0.400	2.115	0.173	0.903	<0.0001	0.276	<0.0001	6.433	1.746
Visión	0.362	0.331	1.681	0.181	0.869	<0.0001	0.294	<0.0001	3.755	1.771
Anastasia	0.339	0.341	1.982	0.234	0.911	<0.0001	0.353	<0.0001	3.772	1.895
Larvae
Selena	0.411	0.139	1.914	0.145	0.916	<0.0001	0.009	<0.0001	6.300	1.746
Visión	0.388	0.214	1.510	0.175	0.882	<0.0001	0.099	<0.0001	2.917	1.895
Anastasia	0.225	0.185	1.657	0.229	0.767	<0.0001	0.243	<0.0001	2.873	1.746
Nymphs
Selena	0.153	0.200	1.766	0.101	0.933	<0.0001	0.453	<0.0001	7.608	1.717
Visión	0.272	0.287	1.557	0.183	0.818	<0.0001	0.358	<0.0001	3.034	1.746
Anastasia	0.498	0.211	1.571	0.183	0.821	<0.0001	0.031	<0.0001	3.111	1.746
Adults
Selena	0.160	0.344	1.462	0.233	0.711	<0.0001	0.647	<0.0001	1.985	1.746
Visión	0.221	0.317	1.734	0.242	0.837	<0.0001	0.501	<0.0001	3.027	1.812
Anastasia	0.463	0.223	1.741	0.184	0.848	<0.0001	0.054	<0.0001	4.027	1.746

Table 5.

Spatial distribution of Tetranychus urticae on different roses varieties using Iwao’s patchiness regression analysis.

Variety	α	±Se_α	β	±Se_β	R²	P_reg	P_α	P_β	t_c	t_t
Before release of Phytoseiulus persimilis
Eggs
Selena	15.223	21.599	1.192	0.250	0.958	0.132	0.609	0.132	0.367	6.314
Visión	1.914	1.989	1.177	0.048	0.998	0.026	0.512	0.026	3.705	6.314
Anastasia	2.783	11.232	1.526	1.066	0.672	0.388	0.845	0.388	0.400	6.314
Larvae
Selena	-31.228	26.791	5.921	2.920	0.804	0.292	0.451	0.292	1.651	6.314
Visión	-2.443	6.735	2.239	0.976	0.840	0.262	0.779	0.262	1.269	6.314
Anastasia	5.820	8.266	0.798	1.316	0.269	0.653	0.609	0.653	-0.153	6.314
Nymphs
Selena	-17.371	38.217	3.186	3.992	0.389	0.571	0.728	0.571	0.523	6.314
Visión	-0.028	0.056	2.284	0.012	1.000	0.003	0.707	0.003	106.363	6.314
Anastasia	-4.521	9.834	2.757	1.212	0.838	0.264	0.726	0.264	1.450	6.314
Adults
Selena	3.221	2.438	1.000	0.086	0.993	0.054	0.412	0.054	0.002	6.314
Visión	0.106	0.115	1.140	0.007	1.000	0.004	0.525	0.004	19.511	6.314
Anastasia	-26.537	29.080	3.981	1.873	0.819	0.280	0.529	0.280	1.592	6.314
After release of Phytoseiulus persimilis
Eggs
Selena	-2.568	4.491	2.539	0.135	0.957	<0.0001	0.575	<0.0001	10.652	1.746
Visión	-1.310	2.984	2.312	0.166	0.937	<0.0001	0.668	<0.0001	7.885	1.771
Anastasia	0.904	2.069	2.063	0.404	0.788	0.001	0.675	0.001	2.631	1.895
Larvae
Selena	-0.040	1.032	2.323	0.300	0.790	<0.0001	0.970	<0.0001	4.083	1.746
Visión	0.507	0.912	1.446	0.217	0.816	<0.0001	0.590	<0.0001	2.056	1.812
Anastasia	0.342	0.700	1.811	0.258	0.755	<0.0001	0.632	<0.0001	3.145	1.746
Nymphs
Selena	-3.304	3.117	2.192	0.226	0.811	<0.0001	0.301	<0.0001	4.833	1.717
Visión	-0.833	1.139	1.892	0.142	0.918	<0.0001	0.475	<0.0001	6.293	1.746
Anastasia	0.374	0.634	1.775	0.149	0.898	<0.0001	0.564	<0.0001	5.186	1.746
Adults
Selena	-2.367	1.301	2.189	0.185	0.898	<0.0001	0.087	<0.0001	6.440	1.746
Visión	0.128	1.093	1.750	0.234	0.849	<0.0001	0.909	<0.0001	3.208	1.812
Anastasia	0.455	0.484	1.842	0.089	0.964	<0.0001	0.361	<0.0001	9.411	1.746

Iwao’s model showed that most of the developmental stages of P. persimilis presents an aggregated spatial distribution; however, in Anastasia variety, eggs distribution was uniform (β<1), while it was random (β=1) and uniform in nymphs in Selena and Visión varieties (Table 6). Predators aggregation in high densities of preys has been considered as a key attribute of effective biological control agents (Beddington et al., 1978). In this research, P. persimilis was found to present an aggregated spatial distribution in the highest density of preys in the varieties where the models (Taylor’s & Iwao’s) were significant. Regarding the previous statement, Zhang & Sanderson (1995) mention that the force of aggregation increases with predator density and it is positively associated with the suppression of prey density. The same authors mention that the intensity of the aggregated response by P. persimilis is positively correlated with the effectiveness of the biological control of T. urticae in rose plants under greenhouse conditions.

Table 6.

Spatial distribution of Phytoseiulus persimilis on different of roses varieties using Taylor´s power law and Iwao’s patchiness regression analysis.

	Variety	a	±Se_a	b	±Se_b	R²	P_reg	P_a	P_b	t_c	t_t
	Eggs
Taylor	Selena	0.247	0.089	1.709	0.152	0.852	<0.0001	0.011	<0.0001	4.664	1.717
	Visión	0.087	0.063	1.757	0.239	0.711	<0.0001	0.182	<0.0001	3.166	1.717
	Anastasia	1.077	0.175	0.161	0.083	0.633	<0.0001	0.064	<0.0001	0.439	1.717
	Larvae
	Selena	0.019	0.031	0.910	0.094	0.812	<0.0001	0.538	<0.0001	-0.959	1.717
	Visión	--	--	--	--	--	--	--	--	--	1.717
	Anastasia	-0.015	0.050	0.308	0.207	0.096	0.150	0.768	0.150	-3.350	1.717
	Nymphs
	Selena	0.032	0.040	1.007	0.055	0.938	<0.0001	0.424	<0.0001	0.127	1.717
	Visión	0.021	0.032	0.946	0.080	0.864	<0.0001	0.524	<0.0001	-0.678	1.717
	Anastasia	-0.147	0.080	-0.162	0.334	0.011	0.633	0.078	0.633	-3.478	1.717
	Adults
	Selena	-0.215	0.144	0.293	0.202	0.087	0.162	0.150	0.162	-3.497	1.717
	Visión	0.054	0.051	1.451	0.133	0.844	<0.0001	0.304	<0.0001	3.387	1.717
	Anastasia	0.099	0.204	0.757	0.526	0.086	0.164	0.633	0.164	-0.463	1.717
		α	±Se_α	β	±Se_β	R²	P_reg	P_α	P_β	t_c	t_t
Iwao	Eggs
	Selena	0.247	0.089	1.709	0.152	0.956	<0.0001	0.453	<0.0001	12.459	1.717
	Visión	-0.086	0.144	2.817	0.313	0.787	<0.0001	0.559	<0.0001	5.812	1.717
	Anastasia	-0.105	0.065	2.825	0.170	0.926	<0.0001	0.123	<0.0001	10.753	1.717
	Larvae
	Selena	0.008	0.044	1.239	0.131	0.812	<0.0001	0.849	<0.0001	1.828	1.717
	Visión	--	--	--	--	--	--	--	--	--	1.717
	Anastasia	-0.009	0.020	2.216	0.132	0.927	<0.0001	0.659	<0.0001	9.186	1.717
	Nymphs
	Selena	-0.021	0.051	1.303	0.157	0.758	<0.0001	0.680	<0.0001	1.930	1.717
	Visión	-0.007	0.006	1.219	0.020	0.994	<0.0001	0.224	<0.0001	11.001	1.717
	Anastasia	0.045	0.024	-0.081	0.160	0.012	0.617	0.077	0.617	-6.770	1.717
	Adults
	Selena	0.240	0.152	0.183	0.465	0.007	0.697	0.129	0.697	-1.755	1.717
	Visión	-0.093	0.071	1.705	0.110	0.915	<0.0001	0.202	<0.0001	6.379	1.717
	Anastasia	0.935	0.567	-1.306	4.810	0.003	0.788	0.113	0.788	-0.479	1.717

The sign (negative) of the parameter of Iwao’s model indicates that larvae and adults of T. urticae present competition for food in Selena variety, while nymphs present this competition in Selena and Visión varieties. As well, nymphs of P. persimilis compete for food in Selena and Visión varieties, while adults compete for food in Selena variety. This reflects that meanwhile the phytophagous competes for its food, its predator competes for depredating them.

Conclusions

P. persimilis does not modify spatial distribution of T. urticae, but it does for its vertical distribution. Moreover, the phytoseiid ovopisite where there is a higher population density of T. urticae, favoring the survival of the next generations on rose bush plants, nevertheless, the phytoseiid depends on the abundance of its prey. The aggregation presented by the predator favors a more effective control on the phytophagous.

^fn1Cite this paper: Chacón-Hernández, J. C., Cerna-Chave, E., Mora-Ravelo, S. G., Ochoa-Fuentes, Y., Rocandio-Rodríguez, M., Landeros-Flores J. (2018). Distribution patterns of Tetranychus urticae Koch and Phytoseiulus persimilis Athias-Henriot (Acari: Tetranychidae, Phytoseiidae) in three roses varieties. Revista Bio Ciencias 5(nesp), e423. doi: https://doi.org/10.15741/revbio.05.nesp.e423

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Revista Bio Ciencias, Año 12, vol. 8, Enero 2021. Sistema de Publicación Continua editada por la Universidad Autónoma de Nayarit. Ciudad de la Cultura “Amado Nervo”, Col. Centro, C.P.: 63000, Tepic, Nayarit, México. Teléfono: (01) 311 211 8800, ext. 8922. E-mail: revistabiociencias@gmail.com, revistabiociencias@yahoo.com.mx, http://revistabiociencias.uan.mx. Editor responsable: Dr. Manuel Iván Girón Pérez. No. de Reserva de derechos al uso exclusivo 04-2010-101509412600-203, ISSN 2007-3380, ambos otorgados por el Instituto Nacional de Derechos de Autor. Responsable de la última actualización de este número Dr. Manuel Iván Girón Pérez. Secretaria de Investigación y Posgrado, edificio Centro Multidisciplinario de Investigación Científica (CEMIC) 03 de la Universidad Autónoma de Nayarit. La opinión expresada en los artículos firmados es responsabilidad del autor. Se autoriza la reproducción total o parcial de los contenidos e imágenes, siempre y cuando se cite la fuente y no sea con fines de lucro.

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