Population growth of Tetranychus urticae Koch (Acari: Tetranychidae) and predation rate of the pest mite by Neoseiulus idaeus Denmark & Muma (Acari: Phytoseiidae) in two grape cultivars* * This paper is part of the dissertation thesis of the first author.

Andréia Alex Sandra da Silva Pantaleão José Osmã Teles Moreira Mário Eidi Sato José Anchieta de Assunção Pionório About the authors

ABSTRACT

The two-spotted spider mite, Tetranychus urticae Koch, has caused significant damage to vineyards in the valley of the São Francisco River in Brazil. Neoseiulus idaeus Denmark & Muma is one of the most abundant species of predatory mites on vines in this region. This study evaluated the population growth rates of T. urticae on leaves of two grape (Vitis vinifera L.) cultivars (‘Italia’ and ‘Superior Seedless’) and jack bean [Canavalia ensiformis (L.) DC.] and, also, to estimate the predation rates of the pest mite by N. idaeus on leaves of both grape cultivars and jack bean. A higher oviposition rate of T. urticae was observed on ‘Superior Seedless’ than on ‘Italia’ grape leaves; however, there was no significant difference in the instantaneous growth rates of T. urticae for these grape cultivars. For ‘Superior Seedless’, the spider mite egg viability was significantly lower than on ‘Italia’ grape, indicating a resistance factor in this grape cultivar. The phytoseiid N. idaeus preyed higher number of T. urticae females on ‘Superior Seedless’ leaves than on ‘Italia’ grape and jack bean leaves for the densities of 10 and 20 pest mites per leaf arena (9 cm2). Evaluations of leaf trichomes in both grape cultivars indicated the occurrence of longer trichomes on the basal portion of the main veins of ‘Superior Seedless’ leaves. The presence of these longer trichomes may be associated with the better performance of N. idaeus on ‘Superior Seedless’ leaves.

Keywords
two-spotted spider mite; plant resistance; biological control

INTRODUCTION

The grapevine, Vitis vinifera L., is a crop of great importance for Brazilian agriculture, mainly in the Northeast region of the country (ACADEMIA DO VINHO, 2014ACADEMIA DO VINHO. Brasil - Vale do São Francisco. 2014. Available from: http://www.academiadovinho.com.br/_regiao_mostra.php?reg_num=BR04. Access on: 25 Oct. 2017.
http://www.academiadovinho.com.br/_regia...
). The edaphoclimatic conditions of the São Francisco River Valley (SILVA et al., 2009SILVA, P.C.G.; CORREIA, R.C.; SOARES, J.M. Histórico e importância socioeconômica. In: SOARES, J.M.; LEÃO, P.C.S. (ed.) A vitivinicultura no semiárido brasileiro. Petrolina: Embrapa, 2009. p.21-34.) are favorable for the occurrence of several pests, including some phytophagous mites that cause losses in production and quality of fruits (BERTOLO et al., 2011BERTOLO, F.O.A.; OTT, A.P.; FERLA, N.J. Ácaros em videira no Rio Grande do Sul (Boletim Técnico 21). Porto Alegre: Fepagro, 2011. 24p. Available from: http://www.fepagro.rs.gov.br/upload/20111227185231boletim_a%C2%81caros___versao_online.pdf. Access on: 20 Jun. 2019.
http://www.fepagro.rs.gov.br/upload/2011...
). The two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), is responsible for significant damages to several crops, such as cotton, kidney beans, papaya, strawberries and roses, in Brazil (MORAES; FLECHTMANN, 2008MORAES, G.J.; FLECHTMANN, C.H.W. Manual de Acarologia: Acarologia básica e ácaros de plantas cultivadas no Brasil. Ribeirão Preto: Holos, 2008. 288p.).

The two-spotted spider mite is highly polyphagous, colonizing especially the under surface of the leaves, hindering the productivity and vigor of the plants (MORAES; FLECHTMANN, 2008MORAES, G.J.; FLECHTMANN, C.H.W. Manual de Acarologia: Acarologia básica e ácaros de plantas cultivadas no Brasil. Ribeirão Preto: Holos, 2008. 288p.). Symptoms of attack on vineyards start with small chlorotic areas on the leaves, between the main veins, and subsequently the damaged area becomes necrosed (CARMONA et al., 1996CARMONA, M.M.; DIAS, J.C.S.; GANHÃO, J.F.P. Fundamentos de Acarologia Agrícola. Lisboa: Fundação Calouste Gulbenkian, 1996. 423p.). In high infestations, the spider mite can cause plant defoliation and tanning of the berries (BERTOLO et al., 2011BERTOLO, F.O.A.; OTT, A.P.; FERLA, N.J. Ácaros em videira no Rio Grande do Sul (Boletim Técnico 21). Porto Alegre: Fepagro, 2011. 24p. Available from: http://www.fepagro.rs.gov.br/upload/20111227185231boletim_a%C2%81caros___versao_online.pdf. Access on: 20 Jun. 2019.
http://www.fepagro.rs.gov.br/upload/2011...
).

Chemical control is still the primary method used against the pest mites, causing quite a significant environmental impact (MORAES; FLECHTMANN, 2008MORAES, G.J.; FLECHTMANN, C.H.W. Manual de Acarologia: Acarologia básica e ácaros de plantas cultivadas no Brasil. Ribeirão Preto: Holos, 2008. 288p.). An alternative method is the biological control with the use of predatory mites of the family Phytoseiidae, which are considered the most important agents for the biological control of phytophagous mites in agricultural systems (MORAES; FLECHTMANN, 2008MORAES, G.J.; FLECHTMANN, C.H.W. Manual de Acarologia: Acarologia básica e ácaros de plantas cultivadas no Brasil. Ribeirão Preto: Holos, 2008. 288p.). In Brazil, several studies on the use of phytoseiid mites for the control of T. urticae were carried out in the South and Southeast regions of Brazil, with emphasis on strawberries and ornamental plants (FERLA et al. 2007FERLA, N.J.; MARCHETTI, M.M.; GONÇALVES, D. Ácaros predadores (Acari) associados à cultura do morango (Fragaria sp., Rosaceae) e plantas próximas no Estado do Rio Grande do Sul. Biota Neotropica, Campinas, v.7, n.2, p.bn01807022007, 2007. https://doi.org/10.1590/S1676-06032007000200012
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; SATO et al., 2007SATO, M.E.; SILVA, M.Z.; SOUZA FILHO, M.F.; MATIOLI, A.L.; RAGA, A. Management of Tetranychus urticae (Acari: Tetranychidae) in strawberry fields with Neoseiulus californicus (Acari: Phytoseiidae) and acaricides. Experimental and Applied Acarology, Amsterdam, v.42, n.2, p.107-120, 2007. https://doi.org/10.1007/s10493-007-9081-2
https://doi.org/10.1007/s10493-007-9081-...
; BERNARDI et al., 2010BERNARDI, D.; BOTTON, M.; CUNHA, U.S.; NAVA, D.E.; GARCIA, M.S. Bioecologia, monitoramento e controle do ácaro-rajado com o emprego da azadiractina e ácaros predadores na cultura do morangueiro (Circular Técnica 83). Bento Gonçalves: Embrapa Uva e Vinho, 2010. 8p. Available from: https://www.infoteca.cnptia.embrapa.br/infoteca/bitstream/doc/879820/1/cir083.pdf. Access on: 10 Jun. 2019.
https://www.infoteca.cnptia.embrapa.br/i...
; IWASSAKI et al., 2015IWASSAKI, L.A.; SATO, M.E.; CALEGARIO, F.F.; POLETTI, M.; MAIA, A.H.N. Comparison of conventional and integrated programs for control of Tetranychus urticae (Acari: Tetranychidae). Experimental and Applied Acarology, Amsterdam, v.65, n.2, p.205-217, 2015. https://doi.org/10.1007/s10493-014-9853-4
https://doi.org/10.1007/s10493-014-9853-...
); however, studies on predaceous mites in vineyards cultivated in the Northeast region of the country are still scarce (DOMINGOS et al., 2014DOMINGOS, C.A.; MELO, J.W.S.; OLIVEIRA, J.E.M.; GONDIM JÚNIOR, M.G.C. Mites on grapevines in northeast Brazil: occurrence, population dynamics and within-plant distribution. International Journal of Acarology, Arkansas, v.40, n.2, p.145-151, 2014. https://doi.org/10.1080/01647954.2014.891651
https://doi.org/10.1080/01647954.2014.89...
).

The presence of the phytoseiid mites Euseius citrifolius Denmark & Muma and Neoseiulus idaeus Denmark & Muma associated with T. urticae infestations in Brazilian vineyards (MOREIRA et al., 2010MOREIRA, A.N.; OLIVEIRA, J.V.; OLIVEIRA, J.E.M.; SANTOS, A.C.; GONDIM JÚNIOR, M.G.C. Acarofauna of vineyards associated with three production systems in the São Francisco River Valley, northeast Brazil. In: XXI INTERNATIONAL CONGRESS OF ACAROLOGY. Anais... Recife: Sociedade Entomológica do Brasil, 2010. Available from: https://www.alice.cnptia.embrapa.br/bitstream/doc/862359/1/AcarofaunaofvineyardsassociatedwiththreeproductionsystemsintheRioSaoFranciscoRiverValleyNortheastBrazil.pdf. Access on: 20 Jun. 2019.
https://www.alice.cnptia.embrapa.br/bits...
; DOMINGOS et al., 2014DOMINGOS, C.A.; MELO, J.W.S.; OLIVEIRA, J.E.M.; GONDIM JÚNIOR, M.G.C. Mites on grapevines in northeast Brazil: occurrence, population dynamics and within-plant distribution. International Journal of Acarology, Arkansas, v.40, n.2, p.145-151, 2014. https://doi.org/10.1080/01647954.2014.891651
https://doi.org/10.1080/01647954.2014.89...
) have been recorded. The occurrence of N. idaeus was reported in commercial vineyards of the cultivars Sugraone and Italia Muscat, with high infestations of T. urticae in the São Francisco Valley (DOMINGOS et al., 2014DOMINGOS, C.A.; MELO, J.W.S.; OLIVEIRA, J.E.M.; GONDIM JÚNIOR, M.G.C. Mites on grapevines in northeast Brazil: occurrence, population dynamics and within-plant distribution. International Journal of Acarology, Arkansas, v.40, n.2, p.145-151, 2014. https://doi.org/10.1080/01647954.2014.891651
https://doi.org/10.1080/01647954.2014.89...
).

The species N. idaeus is widely distributed in South America and is frequently found in manioc plantations in the northeast and southeast regions of Brazil (MORAES et al. 1994MORAES, G.J.; SILVA, C.A.D.; MOREIRA, A.N. Biology of a strain of Neoseiulus idaeus (Acari: Phytoseiidae) from Southwest Brazil. Experimental and Applied Acarology, Amsterdam, v.18, n.4, p.213-220, 1994. https://doi.org/10.1007/BF00114168
https://doi.org/10.1007/BF00114168...
; MORAES, 2002MORAES, G.J. Controle biológico de ácaros fitófagos com ácaros predadores. In: PARRA, J.R.P.; BOTELHO, P.S.M.; CORRÊA-FERREIRA, B.S.; BENTO, J.M.S. (Orgs.). Controle biológico no Brasil: parasitoides e predadores. São Paulo: Manole, 2002. p.225-237.). Although there is little information on its importance to vineyards, N. idaeus has potential use for spider mite biological control programs in this crop. Neoseiulus idaeus is a type II selective predator (HOLLING, 1959HOLLING, C.S. Some Characteristics of Simple Types of Predation and Parasitism. The Canadian Entomologist, Cambridge, v.91, n.7, p.385-398, 1959. https://doi.org/10.4039/Ent91385-7
https://doi.org/10.4039/Ent91385-7...
) with preference for feeding on tetranychid mites (WATANABE et al., 1994WATANABE, M.A.; MORAES, G.J.; GASTALDO JÚNIOR, I.; NICOLELLA, G. Controle biológico do ácaro rajado com ácaros predadores fitoseídeos (Acari: Tetranychidae, Phytoseiidae) em culturas de pepino e morango. Scientia Agricola, Piracicaba, v.51, n.1, p.75-81, 1994. https://doi.org/10.1590/S0103-90161994000100012
https://doi.org/10.1590/S0103-9016199400...
; CROFT et al., 2004CROFT, B.A.; BLACKWOOD, J.S.; MCMURTRY, J.A. Classifying Life-Style Types of Phytoseiid Mites: Diagnostic Traits. Experimental and Applied Acarology, Amsterdam, v.33, n.4, p.247-260, 2004. https://doi.org/10.1023/B:APPA.0000038622.26584.82
https://doi.org/10.1023/B:APPA.000003862...
; MCMURTRY et al., 2013MCMURTRY, J.A.; MORAES, G.J.; SOURASSOU, N.F. Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Systematic and Applied Acarology, Auckland, v.18, n.4, p.297-320, 2013. https://doi.org/10.11158/saa.18.4.1
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). This phytoseiid mite presented a good performance in controlling T. urticae in commercial papaya fields in the states of Rio de Janeiro and Espírito Santo in Brazil (COLLIER et al., 2004COLLIER, K.F.S.; LIMA, J.O.G.; ALBUQUERQUE, G.S. Predacious mites in papaya (Carica papaya L.) orchards: in search of a biological control agent of phytophagous mite pests. Neotropical Entomology, Londrina, v.33, n.6, p.799-803, 2004. https://doi.org/10.1590/S1519-566X2004000600020
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; 2007COLLIER, K.F.S.; ALBUQUERQUE, G.S.; LIMA, J.O.G.; PALLINI, A.; MOLINA-RUGAMA, A.J. Neoseiulus idaeus (Acari: Phytoseiidae) as a potential biocontrol agent of the two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae) in papaya: performance on different prey stage-host plant combinations. Experimental and Applied Acarology, Amsterdam, v.41, n.1-2, p.27-36, 2007. https://doi.org/10.1007/s10493-006-9041-2
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; MORAES; FLECHTMANN, 2008MORAES, G.J.; FLECHTMANN, C.H.W. Manual de Acarologia: Acarologia básica e ácaros de plantas cultivadas no Brasil. Ribeirão Preto: Holos, 2008. 288p.).

Phytophagous and predaceous mites might be directly affected by the host plants via some structures or chemical compounds present on leaves and other plant parts, which may influence their movement, feeding and reproduction behaviors. In this aspect, structures like trichome and domatium may affect the searching and prey-capture efficiency for predaceous mites, influencing on the survival and oviposition rates of the mites (WALTER, 1996WALTER, D.E. Living on Leaves: Mites, Tomenta, and Leaf Domatia. Annual Review of Entomology, Palo Alto, v.41, p.101-114, 1996. https://doi.org/10.1146/annurev.en.41.010196.000533
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; KRIPS et al., 1998KRIPS, O.E.; WITUL, A.; WILLEMS, P.E.L.; DICKE, M. Intrinsic rate of population increase of the spider mite Tetranychus urticae on the ornamental crop gerbera: intraspecific variation in host plant and herbivore. Entomologia Experimentalis et Applicata, Wageningen, v.89, n.2, p.159-168, 1998.; AFZAL; BASHIR, 2007AFZAL, M.; BASHIR, M.H. Influence of certain leaf characters of some summer vegetables with incidence of predatory mites of the family Cunaxidae. Pakistan Journal of Botany, Karachi, v.39, n.1, p.205-209, 2007. Available from: http://www.pakbs.org/pjbot/PDFs/39(1)/PJB39(1)205.pdf. Access on: 10 Jun. 2019.
http://www.pakbs.org/pjbot/PDFs/39(1)/PJ...
; ROMERO et al., 2011ROMERO, G.Q.; DAUD, R.D.; SALOMÃO, A.T.; MARTINS, L.F.; FERES, R.J.F.; BENSON, W.W. Mites and leaf domatia: no evidence of mutualism in Coffea arabica plants. Biota Neotropica, Campinas, v.11, n.1, p.27-34, 2011. https://doi.org/10.1590/S1676-06032011000100002
https://doi.org/10.1590/S1676-0603201100...
; RAMALHO et al., 2014RAMALHO, T.K.A.; MATOS, C.H.C.; MELO, A.L.; OLIVEIRA, C.R.F.; MENEZES, T.G.C.; SILVA, J.K.L. Leaf domatia in montane forest and caatinga in the semiarid of Pernambuco State: Morphology and ecological implications. Acta Scientiarum. Biological Sciences, Maringá, v.36, n.3, p.327-332, 2014. https://doi.org/10.4025/actascibiolsci.v36i3.20275
https://doi.org/10.4025/actascibiolsci.v...
).

Considering the limited knowledge on the phytophagous and predaceous mites on vineyards of the São Francisco Valley, this study aimed at evaluating the population growth rates of the two-spotted spider mite and the predation rates of N. idaeus on T. urticae mites on leaves of two grape cultivars (‘Italia’ and ‘Superior Seedless’) for establishing a management program for this pest mite in Brazilian vineyards.

MATERIALS AND METHODS

Mite populations

Samples of T. urticae and predatory mites were collected from commercial vineyards located in São Francisco Valley [Casa Nova municipality (9°10’S; 40°58’W), state of Bahia (BA), and Petrolina city (9°20’S; 40°30’W), state of Pernambuco (PE)] in the period from November 2011 to November 2012. Collected mites were reared in jack bean [Canavalia ensiformis (L.) DC.] leaf arenas, constituted of a bean leaf placed on a layer of polyurethane foam saturated with water in a Petri dish. Arenas were replaced when they showed initial deterioration, generally every 5 days. The rearing room was kept at 25 ± 2 °C, relative humidity of 70 ± 10% and a photoperiod of 12:12 h (L:D).

Preliminary surveys for phytoseiid mites in vineyards of São Francisco Valley (Casa Nova, BA; Petrolina, PE) indicated that N. idaeus was the most abundant species in this region. The predaceous mites were collected from the vineyards at the same cultivation areas where T. urticae were collected. After collection, N. idaeus mites were maintained in jack bean leaf arenas, as described for the spider mite.

All life stages (eggs, larvae, protonymphs, deutonymphs, and adults) of T. urticae mites were provided as food source for the predatory mites.

Samples of adults of the predatory and phytophagous mites were mounted in Hoyer’s medium on microscope slides for identification.

Instantaneous growth and oviposition rates of Tetranychus urticae

The experiment was conducted under laboratory conditions from January to February 2013. Mature leaves were collected from vineyards of the grape cultivars Italia and Superior Seedless. Jack bean leaves were obtained from the plants cultivated under laboratory conditions. The leaves of both plant species were washed with running water prior to the arena preparation. Each leaf disc (9 cm2) was placed on water-soaked cotton in a Petri dish. The edge of the leaf disc was surrounded by a wet cotton wool to prevent the mites from escaping.

The treatment with jack bean leaves was used as a comparison standard. The experiment of T. urticae population growth was based on the method described by MATIOLI; OLIVEIRA (2007)MATIOLI, A.L.; OLIVEIRA, C.A.L. Biologia de Agistemus brasiliensis Matioli, Ueckermann & Oliveira (Acari: Stigmaeidae) e sua potencialidade de predação sobre Brevipalpus phoenicis (Geijskes) (Acari: Tenuipalpidae). Neotropical Entomology, Londrina, v.36, n.4, p.557-582, 2007. https://doi.org/10.1590/S1519-566X2007000400016
https://doi.org/10.1590/S1519-566X200700...
.

A four-day old previously mated female of T. urticae was placed into each leaf arena. The evaluations were carried out daily until the tenth day, assessing the mite survival and oviposition rates. Arenas were kept at the temperature of 25 ± 2 °C, relative humidity of 70 ± 5% and a 12-hour photophase. The total number of eggs and active forms of T. urticae were recorded on the tenth day after the mite introduction into each arena. Eq. 1 was used to calculate the instantaneous growth rate (ri) of T. urticae:

r i = Ln ( N f / N 0 ) / Δ t (1)

where Nf is the total number of T. urticae mites on the tenth day after the arena infestation, N0 is the initial number of mites placed into each arena and Δt is the period in which the mites were in contact with the substrates (grape or jack-bean leaves) (STARK; BANKS, 2003STARK, J.D.; BANKS, J.E. Population-Level Effects of Pesticides and Other Toxicants on Arthropods. Annual Review of Entomology, Palo Alto, v.48, p.505-519, 2003. https://doi.org/10.1146/annurev.ento.48.091801.112621
https://doi.org/10.1146/annurev.ento.48....
).

For statistical analysis, groups of four arenas were considered as one replicate per treatment. The experiment was completely randomized with 20 replicates.

Data were submitted to the analysis of variance (one-way ANOVA) and the comparisons of means were done using LSD Post-Hoc test (p < 0.05).

Another aspect observed was the number of T. urticae trapped in the cotton barrier, which would be considered an indicative of a repellent effect of each substrate. Chi-square (X2) test was used to compare the results for jack bean and grape cultivars.

Pest predation by Neoseiulus idaeus

The predation rate of T. urticae by the predatory mite N. idaeus was evaluated in leaf disc arenas of the grape cultivars Italia and Superior Seedless and of jack bean, using different prey densities. Leaf arenas were prepared as described before, infesting each arena with adult females of T. urticae at the densities of 5, 10, 20, and 30 mites per arena. One adult female of N. idaeus was placed into each leaf disc arena. Arenas were kept at the temperature of 25 ± 2 °C, relative humidity of 70 ± 5% and a 12-hour photophase. The number of females killed by the predator was evaluated every 24 h during 5 days. All preyed females were replaced by live females at each evaluation time. Only adult females of T. urticae were kept on the arenas, removing all other stages of mites.

For statistical analysis, groups of five arenas were considered as one replicate per treatment (leaves of the two grape cultivars and of jack bean). The experiment was completely randomized with 12 treatments and five replicates.

Data on the number of preyed females were analyzed using two-way ANOVA (3 leaf types × 4 prey densities). Comparisons of mean number of preyed mites for each treatment were conducted using LSD test (p < 0.05).

In addition, to observe the relationship between the number of T. urticae adult females offered to and preyed by N. idaeus in the leaf disc arenas, a correlation analysis was performed using the Pearson correlation coefficient.

Grape leaf trichomes

Leaves of both grape cultivars and jack bean were morphologically characterized based on the number and size of leaf trichomes. The leaves of grape cultivars (‘Italia’ and ‘Superior Seedless’) practically do not have trichomes on the surface, however, there are a large number of these structures on the lateral sides of the leaf veins, especially on the basal portion of the main veins (Fig. 1).

Figure 1
Number of T. urticae adult females offered and preyed per day by N. idaeus in leaf disc arenas of two grape cultivars (‘Italia’ and ‘Superior Seedless’) and jack bean. Columns with the same letter are not significantly different at 5% significance.

The number and size of trichomes were evaluated in five replicates of 1 mm, distributed in the first centimeter of the basal region of the leaf veins of both grape cultivars, totaling 21 veins observed per cultivar. The size of trichomes was estimated based on the measurement of at least 10 trichomes per mm of leaf vein. Images of a stereoscopic microscope with image overlapping and analyzing resources (Leica Microsystems) were used for counting and measurement of the leaf trichomes.

Trichomes were not counted or measured for jack bean leaves due to the lack of these structures on the leaves.

Data of the number and length of trichomes were submitted to the analysis of variance, using the t test to compare means.

RESULTS

Instantaneous growth and oviposition rates of Tetranychus urticae

Results indicated a higher oviposition rate (F = 37.41; d.f. = 57; p < 0.0001) of T. urticae on the leaves of ‘Superior Seedless’ than those of ‘Italia’; however, the egg viability was significantly lower (F = 17.95; d.f. = 57, p < 0.0001) in ‘Superior Seedless’ (57.5%) than in ‘Italia’ grape (96.7%). The population growth rates (0.211 ≤ ri ≤ 0.225) of the spider mite were similar in both grape cultivars (Table 1).

Table 1
Number of Tetranychus urticae eggs per female per day (mean values ± SD) (n = 20); percentage of egg viability (mean values ± SD), and instantaneous growth (ri) per day (mean values ± SD) in leaf disc arenas of two grape cultivars (‘Italia’ and ‘Superior Seedless’) and jack bean.

The oviposition (4.4 eggs/female/day) and population growth rates (ri= 0.35) of T. urticae were significantly higher (F = 41.61; d.f. = 54; p < 0.0001) on the leaves of jack bean than those of ‘Italia’ and ‘Superior Seedless’ grapes.

The viability of T. urticae eggs was high (94.9%) in ‘Italia’ grape and did not differ from jack bean (97.5%). Lower egg viability (57.5%) was observed for ‘Superior Seedless’ grape, differing significantly (F = 43.93; d.f. = 54; p < 0.0001) from the other two treatments.

A higher and significant (X2 = 5.556; p = 0.00184) percentage of mites trapped and killed in the wet cotton barrier around the leaves was observed for ‘Superior Seedless’ grape (17.5%) in comparison with ‘Italia’ grape (10%) and jack bean leaves (5%). No significant difference was detected between ‘Italia’ grape and jack bean leaves.

Pest predation by Neoseiulus idaeus

Considering the three evaluated substrates (leaves of two grape cultivars and jack bean) and the four prey densities, the number of preyed mites was affected significantly by the substrates [F(2, 44) = 60.84, p < 0.001] and prey densities [F(3, 44) = 72.77, p < 0.001], with interactions of both parameters [F(6, 44) = 11.07, p < 0.001].

Positive and significant correlations (p ≤ 0.0012) were observed between the prey densities and the number of mites consumed by N. idaeus for the leaves of both grape cultivars and jack bean (Table 2).

Table 2
Relationship between the number of T. urticae adult females offered and preyed by N. idaeus in leaf disc arenas of two grape cultivars (‘Italia’ and ‘Superior Seedless’) and jack bean.

Significant differences among the substrates for the predation rates of N. idaeus on T. urticae adult females were observed only for the densities of 10 and 20 prey mites per leaf arena (9 cm2), without significant differences for the lowest (5 mites/arena) and the highest prey (30 mites/arena) densities (Fig. 1).

At the intermediate densities (10 and 20 prey mites/arena), the number of T. urticae females consumed by N. idaeus on ‘Superior Seedless’ leaves varied from 1.5 to 1.7 mite a day, which was up to 14 times higher than the mite consumption values observed for ‘Italia’ grape and jack bean.

No significant differences were observed between ‘Italia’ grape and jack bean leaves for the preying behavior of N. idaeus for the different prey densities.

Grape leaf trichomes

Evaluations of the leaves of both grape cultivars indicated significant differences in the number (t = 4.99; d.f. = 20; p < 0.0001) and size (t = 6.21; d.f. = 20; p < 0.0001) of trichomes located on the basal portion of the main leaf veins (Figs. 2 and 3). No trichomes were observed on the surface of leaves (between the veins) of these grape cultivars.

Figure 2
Aspects of leaf trichomes for ‘Superior Seedless’ (2a) and ‘Italia’ (2b) grape cultivars.
Figure 3
Number (a) and size (b) of leaf trichomes for ‘Superior Seedless’ and ‘Italia’ grape cultivars.

DISCUSSION

The spider mite egg viability in grape cultivar Italia was high and similar to that observed for jack bean (~ 98%), which is considered an excellent host plant for T. urticae (SATO et al., 2011aSATO, M.E.; SILVA, M.Z.; RAGA, A.; CANGANI, K.G.; VERONEZ, B.; NICASTRO, R.L. Spiromesifen toxicity to the spider mite Tetranychus urticae and selectivity to the predator Neoseiulus californicus. Phytoparasitica, Bet Dagan, v.39, n.5, p.437-445, 2011a. https://doi.org/10.1007/s12600-011-0189-x
https://doi.org/10.1007/s12600-011-0189-...
). VALADÃO et al. (2012)VALADÃO, G.S.; VIEIRA, M.R.; PIGARI, S.A.A.; TABET, V.G.; SILVA, A.C. Resistência de cultivares de videira ao ácaro-rajado Tetranychus urticae na região de Jales, estado de São Paulo. Revista Brasileira de Fruticultura, Jaboticabal, v.34, n.4, p.1051-1058, 2012. https://doi.org/10.1590/S0100-29452012000400011
https://doi.org/10.1590/S0100-2945201200...
also reported high egg viabilities (> 85%) for the spider mite in the grape cultivars Italia, Benitaka and Redimeire, evaluating T. urticae populations from the Jales municipality, in the state of São Paulo.

High values (0.40 to 0.49/female/day) of instantaneous growth rate (ri) of T. urticae in jack bean leaves were also reported by SATO et al. (2011a)SATO, M.E.; SILVA, M.Z.; RAGA, A.; CANGANI, K.G.; VERONEZ, B.; NICASTRO, R.L. Spiromesifen toxicity to the spider mite Tetranychus urticae and selectivity to the predator Neoseiulus californicus. Phytoparasitica, Bet Dagan, v.39, n.5, p.437-445, 2011a. https://doi.org/10.1007/s12600-011-0189-x
https://doi.org/10.1007/s12600-011-0189-...
, mentioning values similar to or slightly higher than that (0.35/female/day) observed in the present study.

The number of eggs laid by T. urticae females on grape leaves (1.2 to 1.9 eggs/females/day) was similar to the values (between 1.5 and 2.0 eggs/female/day) reported by VALADÃO et al. (2012)VALADÃO, G.S.; VIEIRA, M.R.; PIGARI, S.A.A.; TABET, V.G.; SILVA, A.C. Resistência de cultivares de videira ao ácaro-rajado Tetranychus urticae na região de Jales, estado de São Paulo. Revista Brasileira de Fruticultura, Jaboticabal, v.34, n.4, p.1051-1058, 2012. https://doi.org/10.1590/S0100-29452012000400011
https://doi.org/10.1590/S0100-2945201200...
for leaves of some grape cultivars (‘Italia’, ‘Redimeire’, ‘Benitaka’, ‘Niagara’).

Oviposition and population growth rates of T. urticae on the leaves of ‘Italia’ and ‘Superior Seedless’ grapes were lower than on jack bean leaves, possibly due to the lower nutritional quality of the grape leaves (AWMACK; LEATHER, 2002AWMACK, C.S.; LEATHER, S.R. Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology, Palo Alto, v.47, p.817-844, 2002. https://doi.org/10.1146/annurev.ento.47.091201.145300
https://doi.org/10.1146/annurev.ento.47....
; MORO et al. 2012MORO, L.B.; POLANCZY, R.A.; CARVALHO, J.R.; PRATISSOLI, D.; FRANCO, C.R. Parâmetros biológicos e tabela de vida de Tetranychus urticae (Acari: Tetranychidae) em cultivares de mamão. Ciência Rural, Santa Maria, v.42, n.3, p.487-493, 2012. https://doi.org/10.1590/S0103-84782012000300016
https://doi.org/10.1590/S0103-8478201200...
). Another possibility is the presence of one or more defense mechanism (MITCHELL et al., 2016MITCHELL, C.; BRENNAN, R.M.; GRAHAM, J.; KARLEY, A.J. Plant Defense Against Herbivorous Pests: Exploiting Resistance and Tolerance Traits for Sustainable Crop Protection. Frontiers in Plant Science, Lausanne, v.7, p.1132, 2016. https://doi.org/10.3389/fpls.2016.01132
https://doi.org/10.3389/fpls.2016.01132...
) in grapes that limit the T. urticae population growth on their leaves.

Comparing the number of eggs of T. urticae on the leaves of the evaluated grape cultivars, it was observed a higher oviposition rate in ‘Superior Seedless’; however, the value of the instantaneous growth rate of the spider mite was similar to that verified for ‘Italia’, indicating that leaves of ‘Superior Seedless’ may have an unfavorable factor for the pest population increase (MITCHELL et al. 2016MITCHELL, C.; BRENNAN, R.M.; GRAHAM, J.; KARLEY, A.J. Plant Defense Against Herbivorous Pests: Exploiting Resistance and Tolerance Traits for Sustainable Crop Protection. Frontiers in Plant Science, Lausanne, v.7, p.1132, 2016. https://doi.org/10.3389/fpls.2016.01132
https://doi.org/10.3389/fpls.2016.01132...
).

The lower egg viability for the spider mite in ‘Superior Seedless’ is an indicative of the presence of toxic compounds (allelochemicals) in the leaves. Allelochemicals, such as alkaloids, ketones and organic acids, present in plants might be toxic to arthropods (GERHOLD et al., 1984GERHOLD, D.L.; CRAIG, R.; MUMMA, R.O. Analysis of trichome exudates from mite-resistant geraniums. Journal of Chemical Ecology, Penn, v.10, n.5, p.713-722, 1984. https://doi.org/10.1007/BF00988538
https://doi.org/10.1007/BF00988538...
; MITCHELL et al., 2016MITCHELL, C.; BRENNAN, R.M.; GRAHAM, J.; KARLEY, A.J. Plant Defense Against Herbivorous Pests: Exploiting Resistance and Tolerance Traits for Sustainable Crop Protection. Frontiers in Plant Science, Lausanne, v.7, p.1132, 2016. https://doi.org/10.3389/fpls.2016.01132
https://doi.org/10.3389/fpls.2016.01132...
). Antibiosis resistance in vineyards was also reported by VALADÃO et al. (2012)VALADÃO, G.S.; VIEIRA, M.R.; PIGARI, S.A.A.; TABET, V.G.; SILVA, A.C. Resistência de cultivares de videira ao ácaro-rajado Tetranychus urticae na região de Jales, estado de São Paulo. Revista Brasileira de Fruticultura, Jaboticabal, v.34, n.4, p.1051-1058, 2012. https://doi.org/10.1590/S0100-29452012000400011
https://doi.org/10.1590/S0100-2945201200...
, who observed lower fertility and survival of T. urticae in the cultivar Niagara Rosada.

In the grape cultivar Superior Seedless, a higher percentage (≥ 75%) of mites trapped in the wet cotton barrier (around the leaf) was observed. This escaping behavior of T. urticae on the leaves of ‘Superior Seedless’ may be associated with the presence of allelochemicals unfavorable to the settlement of this species, with repellent and/or phagodeterrent effect (VENDRAMIM; GUZZO, 2009VENDRAMIM, J.D.; GUZZO, E.C. Resistência de plantas e a bioecologia e nutrição dos insetos. In: PANIZZI, A.R.; PARRA, J.R.P. (ed). Bioecologia e nutrição de insetos: base para o manejo integrado de pragas. Brasília: Embrapa, 2009. p.1055-1058.; VALADÃO et al., 2012VALADÃO, G.S.; VIEIRA, M.R.; PIGARI, S.A.A.; TABET, V.G.; SILVA, A.C. Resistência de cultivares de videira ao ácaro-rajado Tetranychus urticae na região de Jales, estado de São Paulo. Revista Brasileira de Fruticultura, Jaboticabal, v.34, n.4, p.1051-1058, 2012. https://doi.org/10.1590/S0100-29452012000400011
https://doi.org/10.1590/S0100-2945201200...
). This repellent effect of the leaves may also have affected the walking behavior of the mites, leading them to spend more time walking on the leaves in attempt to escape the arenas, wasting more energy and resulting in a lower oviposition rate.

However, to elucidate the possible mechanism involved in the resistance of ‘Superior Seedless’ grape to the spider mite, further biochemical studies for this grape cultivar are required.

In the case of N. idaeus, other authors (WATANABE et al., 1994WATANABE, M.A.; MORAES, G.J.; GASTALDO JÚNIOR, I.; NICOLELLA, G. Controle biológico do ácaro rajado com ácaros predadores fitoseídeos (Acari: Tetranychidae, Phytoseiidae) em culturas de pepino e morango. Scientia Agricola, Piracicaba, v.51, n.1, p.75-81, 1994. https://doi.org/10.1590/S0103-90161994000100012
https://doi.org/10.1590/S0103-9016199400...
; COLLIER et al., 2004COLLIER, K.F.S.; LIMA, J.O.G.; ALBUQUERQUE, G.S. Predacious mites in papaya (Carica papaya L.) orchards: in search of a biological control agent of phytophagous mite pests. Neotropical Entomology, Londrina, v.33, n.6, p.799-803, 2004. https://doi.org/10.1590/S1519-566X2004000600020
https://doi.org/10.1590/S1519-566X200400...
; DOMINGOS et al., 2014DOMINGOS, C.A.; MELO, J.W.S.; OLIVEIRA, J.E.M.; GONDIM JÚNIOR, M.G.C. Mites on grapevines in northeast Brazil: occurrence, population dynamics and within-plant distribution. International Journal of Acarology, Arkansas, v.40, n.2, p.145-151, 2014. https://doi.org/10.1080/01647954.2014.891651
https://doi.org/10.1080/01647954.2014.89...
) also reported the association of this phytoseiid mite with the biological control of the two-spotted spider mite in crops like strawberry, cucumber and papaya in Brazil.

Very low predation rates of T. urticae by N. idaeus were observed for the lowest prey density (5 spider mites per arena); however, a trend towards increasing the predation rate was observed as the number of offered prey increased. The influence of prey density on the predation performance of phytoseiid mites was also reported by other authors. REIS et al. (2003)REIS, P.R.; SOUSA, E.O.; TEODORO, A.V.; PEDRO NETO, M. Effect of prey density on the functional and numerical responses of two species of predaceous mites (Acari: Phytoseiidae). Neotropical Entomology, Londrina, v.32, n.3, p.461-467, 2003. https://doi.org/10.1590/S1519-566X2003000300013
https://doi.org/10.1590/S1519-566X200300...
observed an increase in the predation rate of Brevipalpus sp. (Acari: Tenuipalpidae) by Iphiseiodes zuluagai Denmark & Muma (Acari: Phytoseiidae) as the available prey densities increased. These authors attributed to the lower consumption rate at low pest densities to the difficulty of the predators in finding their preys in these conditions.

Relative low predation rates of Tetranychus adult females by phytoseiid mites, as observed for N. idaeus (1.4 to 2.6 adult spider mites/phytoseiid female/day), were also reported by FURUICHI et al. (2005)FURUICHI, H.; OKU, K.; YANO, S.; TAKAFUJI, A.; OSAKABE, M. Why does the predatory mite Neoseiulus womersleyi Schicha (Acari: Phytoseiidae) prefer spider mite eggs to adults? Applied Entomology and Zoology, Tokyo, v.40, n.4, p.675-678, 2005. https://doi.org/10.1303/aez.2005.675
https://doi.org/10.1303/aez.2005.675...
, evaluating the performance of Neoseiulus womersleyi Schicha (Acari: Phytoseiidae) fed on eggs or adults of Tetranychus kanzawai Kishida. The authors observed a rate of approximately 1.7 adult spider mites preyed by each phytoseiid female per day, which was similar to that verified for N. idaeus in the present study. The number of T. kanzawai eggs (14.6) preyed by N. womersleyi was 8.6 times higher than that for adults, indicating a clear preference of the predatory mites in preying eggs rather than adults.

A greater predation of T. urticae adult females by N. idaeus was observed for ‘Superior Seedless’ leaves rather than ‘Italia’ grape and jack bean leaves, only at the prey densities of 10 and 20 adult tetranychid mites per leaf arena. This higher consumption of T. urticae by N. idaeus on ‘Superior Seedless’ leaves compared with other substrates is probably associated with the chemical and morphological characteristics of the leaves of this grape cultivar (KRIPS et al., 1999KRIPS, O.E.; KLEIJN, P.W.; WILLEMS, P.E.L.; GOLS, G.J.Z.; DICKE, M. Leaf hairs influence searching efficiency and predation rate of the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae). Experimental and Applied Acarology, Amsterdam, v.23, n.2, p.119-131, 1999. https://doi.org/10.1023/A:1006098410165
https://doi.org/10.1023/A:1006098410165...
; LOUGHNER et al., 2008LOUGHNER, R.; GOLDMAN, K.; LOEB, G.; NYROP, J. Influence of leaf trichomes on predatory mite (Typhlodromus pyri) abundance in grape varieties. Experimental and Applied Acarology, Amsterdam, v.45, n.3-4, p.111-122, 2008. https://doi.org/10.1007/s10493-008-9183-5
https://doi.org/10.1007/s10493-008-9183-...
; MITCHELL et al., 2016MITCHELL, C.; BRENNAN, R.M.; GRAHAM, J.; KARLEY, A.J. Plant Defense Against Herbivorous Pests: Exploiting Resistance and Tolerance Traits for Sustainable Crop Protection. Frontiers in Plant Science, Lausanne, v.7, p.1132, 2016. https://doi.org/10.3389/fpls.2016.01132
https://doi.org/10.3389/fpls.2016.01132...
).

In this aspect, it is possible that some compounds (allelochemicals) present in the leaves of ‘Superior Seedless’ may have affected the vigor and behavior of T. urticae mites, making them more susceptible to the attack by the predatory mite (BAIER et al., 2015BAIER, J.E.; RESENDE, J.T.V.; FARIA, M.V.; SCHWARZ, K.; MEERT, L. Indirect selection of industrial tomato genotypes that are resistant to spider mites (Tetranychus urticae). Genetics and Molecular Research, Ribeirão Preto, v.14, n.1, p.244-252, 2015. https://doi.org/10.4238/2015.January.16.8
https://doi.org/10.4238/2015.January.16....
). The higher movement of the spider mites on the leaves of this grape cultivar (escaping behavior) may have favored their encounter with the predatory mites, resulting in increased predation rates.

The allelochemicals present on ‘Superior Seedless’ grape leaves may also have affected the nutritional quality and taste of the preys (T. urticae females), leading the predator to abandon the prey mites before their complete consume. This possible behavior change may induce higher rates of spider mite killing by N. idaeus to compensate the lower nutritional gain resulting from each attack (ELBROCH; WITTMER, 2013ELBROCH, L.M.; WITTMER, H.U. Nuisance Ecology: Do Scavenging Condors Exact Foraging Costs on Pumas in Patagonia? PLoS ONE, San Francisco, v.8, n.1, p.e53595, 2013. https://doi.org/10.1371/journal.pone.0053595
https://doi.org/10.1371/journal.pone.005...
; ELBROCH et al., 2014ELBROCH, L.M.; ALLEN, M.L.; LOWREY, B.H.; WITTMER, H.U. The difference between killing and eating: ecological shortcomings of puma energetic models. Ecosphere, v.5, n.5, p.1-16, 2014. https://doi.org/10.1890/ES13-00373.1
https://doi.org/10.1890/ES13-00373.1...
). In this aspect, according to SUNDERLAND (1999)SUNDERLAND, K. Mechanisms underlying the effects of spiders on pest populations. The Journal of Arachnology, Portland, v.27, n.1, p.308-316, 1999., for some spider species, if the pest is distasteful spiders may kill more than they consume, which increases the rate of pest kill per unit of the predator food demand.

Other factors that may be associated with the differential predation rates on spider mites in different grape cultivars are the abundance and characteristic of the leaf trichomes. The presence of longer trichomes on the basal portion of main leaf veins of ‘Superior Seedless’ grape, forming a structure similar to the domatia described in vineyards by LOUGHNER et al. (2008)LOUGHNER, R.; GOLDMAN, K.; LOEB, G.; NYROP, J. Influence of leaf trichomes on predatory mite (Typhlodromus pyri) abundance in grape varieties. Experimental and Applied Acarology, Amsterdam, v.45, n.3-4, p.111-122, 2008. https://doi.org/10.1007/s10493-008-9183-5
https://doi.org/10.1007/s10493-008-9183-...
, may serve as shelter for predaceous mites, increasing the oviposition rate and improving their predation performance (WALTER; DENMARK, 1991WALTER, D.E.; DENMARK, H.A. Use of leaf domatia on wild grape (Vitis munsoniana) by arthropods in Central Florida. The Florida Entomologist, Lutz, v.74, n.3, p.440-446, 1991. https://doi.org/10.2307/3494838
https://doi.org/10.2307/3494838...
; MATOS et al., 2006MATOS, C.H.C.; PALLINI, A.; BELLINI, L.L.; FREITAS, R.C.P. Domácias e seu papel na defesa das plantas. Ciência Rural, Santa Maria, v.36, n.3, p.1021-1026, 2006. https://doi.org/10.1590/S0103-84782006000300050
https://doi.org/10.1590/S0103-8478200600...
; LOUGHNER et al., 2008LOUGHNER, R.; GOLDMAN, K.; LOEB, G.; NYROP, J. Influence of leaf trichomes on predatory mite (Typhlodromus pyri) abundance in grape varieties. Experimental and Applied Acarology, Amsterdam, v.45, n.3-4, p.111-122, 2008. https://doi.org/10.1007/s10493-008-9183-5
https://doi.org/10.1007/s10493-008-9183-...
).

In vines, domatia are comprised of groups of trichomes on main leaf axils (LOUGHNER et al., 2008LOUGHNER, R.; GOLDMAN, K.; LOEB, G.; NYROP, J. Influence of leaf trichomes on predatory mite (Typhlodromus pyri) abundance in grape varieties. Experimental and Applied Acarology, Amsterdam, v.45, n.3-4, p.111-122, 2008. https://doi.org/10.1007/s10493-008-9183-5
https://doi.org/10.1007/s10493-008-9183-...
). The presence of leaf trichomes forming domatia was also associated with a higher performance in the biological control of the red mite Panonychus ulmi (Koch) (Acari: Tetranychidae) by the predaceous mite Typhlodromus pyri Scheuten (Acari: Phytoseiidae) in different grape cultivars in Europe. GROSTAL; O’DOWD (1994)GROSTAL, R.; O’DOWD, D.J. Plants, mites and mutualism: leaf domatia and the abundance and reproduction of mites on Viburnum tinus (Caprifoliacea). Oecologia, Buenos Aires, v.97, n.3, p.308-315, 1994. https://doi.org/10.1007/BF00317319
https://doi.org/10.1007/BF00317319...
also showed that leaf domatia in the ornamental plant Viburnum tinus L. (Adoxaceae) favored the predation of T. urticae by Galendromus occidentalis (Nesbitt) (Acari: Phytoseiidae).

Although the longer leaf trichomes, present in the leaf veins of ‘Superior Seedless’, have been associated with a better performance of N. idaeus, negative effects of different types of trichomes on predatory mites were also reported by some authors, for instance, by limiting the movement of these predators on the leaves and affecting their predatory capacity (DRUKKER et al., 1997DRUKKER, B.; JANSSEN, A.; RAVENSBERG, W.; SABELIS, M.W. Improved control capacity of the mite predator Phytoseiulus persimilis (Acari: Phytoseiidae) on tomato. Experimental and Applied Acaralogy, Amsterdam, v.21, n.6-7, p.507-518, 1997. https://doi.org/10.1023/B:APPA.0000018885.35044.c6
https://doi.org/10.1023/B:APPA.000001888...
; SATO et al., 2011bSATO, M.M.; MORAES, G.J.; HADDAD, M.L.; WEKESA, V.W. Effect of trichomes on the predation of Tetranychus urticae (Acari: Tetranychidae) by Phytoseiulus macropilis (Acari: Phytoseiidae) on tomato, and the interference of webbing. Experimental and Applied Acarology, Amsterdam, v.54, n.1, p.21-32, 2011b. https://doi.org/10.1007/s10493-011-9426-8). However, due to the absence of trichomes on the leaf surface of both grape cultivars (trichomes only on the main veins), the possible negative effect of trichomes on the movement and predation performance of N. idaeus on T. urticae is probably very low or absent.

In the case of the highest evaluated prey density (30 mites/arena), it was not observed any difference among the substrates for the predation rates of T. urticae by N. idaeus. This result is probably associated with the greater availability of preys on the leaf arenas, increasing the consumption of T. urticae by the predaceous mites on ‘Italia’ grape and jack bean leaves, due to the lower necessity of searching for preys (REIS et al., 2003REIS, P.R.; SOUSA, E.O.; TEODORO, A.V.; PEDRO NETO, M. Effect of prey density on the functional and numerical responses of two species of predaceous mites (Acari: Phytoseiidae). Neotropical Entomology, Londrina, v.32, n.3, p.461-467, 2003. https://doi.org/10.1590/S1519-566X2003000300013
https://doi.org/10.1590/S1519-566X200300...
; HIGGINSON; RUXTON, 2015HIGGINSON, A.D.; RUXTON, G.D. Foraging mode switching: the importance of prey distribution and foraging currency. Animal Behaviour, Saunt Aundraes, v.105, p.121-137, 2015. https://doi.org/10.1016/j.anbehav.2015.04.014
https://doi.org/10.1016/j.anbehav.2015.0...
).

Further field studies are still necessary to evaluate the actual influence of the different grape cultivars on the establishment and reproduction of two-spotted spider mites, as well as the importance of N. idaeus as a biological control agent against the pest mite in the vineyards of the São Francisco Valley in Brazil.

CONCLUSION

The oviposition rate of T. urticae was higher on ‘Superior Seedless’ than on ‘Italia’ grape leaves; however, the instantaneous growth rates of T. urticae were similar for these grape cultivars. For ‘Superior Seedless’, the spider mite egg viability was significantly lower than on ‘Italia’ grape. The phytoseiid N. idaeus preyed higher number of T. urticae mites on the leaves of ‘Superior Seedless’ than of ‘Italia’ grape, for the densities of 10 and 20 pest mites per leaf arena. Longer leaf trichomes were found on the basal portion of the main veins of ‘Superior Seedless’ leaves. The present study indicates that the use of N. idaeus in combination with grape cultivars, like ‘Superior Seedless’, with possible resistance to T. urticae and favorable characteristic for the establishment of the predaceous mite, can be an interesting strategy for the management of the spider mite in the northeast region of Brazil.

ACKNOWLEDGEMENTS

We would like to thank Dr. Jeferson Luiz de Carvalho Mineiro (Instituto Biológico, São Paulo) for the identification of the predaceous mites and Dr. Valmir Antonio Costa (Instituto Biológico, São Paulo) for the assistance to get the images of the leaf trichomes.

  • AVAILABILITY OF DATA AND MATERIAL

    The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
  • FUNDING

    Conselho Nacional de Desenvolvimento Científico e Tecnológico
    Grant No: 306852/2019-5
    Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
    Finance Code 001
  • ETHICAL APPROVAL

    Not applicable.
  • Peer Review History: Double-blind Peer Review.
  • *
    This paper is part of the dissertation thesis of the first author.

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Publication Dates

  • Publication in this collection
    25 Oct 2021
  • Date of issue
    2021

History

  • Received
    23 Oct 2019
  • Accepted
    30 Oct 2020
Instituto Biológico Av. Conselheiro Rodrigues Alves, 1252 - Vila Mariana - São Paulo - SP, 04014-002 - São Paulo - SP - Brazil
E-mail: arquivos@biologico.sp.gov.br