Introduction

Mexico is the main producer of blackberry (Rubus sp.) globally, with more than 13,000 ha planted, of which more than 96% of plants are grown in the state of Michoacán. This crop is cultured under a forced production system that allows growers to produce blackberries off season during the autumn, winter, and spring. Redberry disease is one of the main limiting factors affecting the production of blackberry in Mexico. This disease was observed for the first time during the 2010–2011 production season in the municipalities of Tacámbaro and Zitácuaro in the state of Michoacán. In the following years, the problem has been observed in other blackberry-producing areas in the states of Jalisco, Colima, and Baja California (Rebollar-Alviter, unpublished).

The symptoms of redberry disease consist of irregular maturity of the berries (the uneven ripening of fruit) because some drupelets remain bright red and show hard consistency, contrasting with those of black color that mature normally. These symptoms usually start in the lower part of the fruit near the peduncle of the berry but can also appear on the side of the berry in isolated groups of drupelets. These symptoms are consistent with those assumed to be caused by the redberry mite (Acalitus essigi (Hassan); Acari: Eriophyidae), which have previously been reported in different parts of the world, including New Zealand (Jeppson et al. 1975), Central and South America (Ochoa et al. 1991; Gerding 1992), Australia (Davies et al. 2001a; Scott et al. 2008), the UK (Pye and de Lillo 2010), the USA (Keifer 1941, 1952), and various European countries (Vacante 2016). An additional eriophyid mite, Acalitus orthomera (Keifer), the bud mite, has also been found in mixed populations with A. essigi, also being associated with redberry disease of blackberry (Manson 1972; Keifer et al. 1982). Acalitus orthomera has been reported in boysenberry and wild blackberry; however, this species is often confused with A. essigi because of their similar morphology. Acalitus orthomera feeds primarily within the bud scales of canes, reportedly causing warts, blisters, swelling, and tissue twisting (Jeppson et al. 1975; Shi 2000). In Mexico, Rebollar-Alviter et al. (2013) reported for the first time the presence of highly dense populations of A. orthomera associated with the lateral buds of blackberry cv. ‘Tupy’ with no clear damage to the buds of fruiting laterals and no presence of redberry disease at the time of sampling (2009–2011). Trinidad et al. (2018) reported the occurrence of A. orthomera associated with the irregular maturity of berries in Rubus sp. cv. ‘Tupy’, the same cultivar that is the basis of the blackberry industry in Mexico. Meanwhile, Ayala-Ortega et al. (2019) and Acuña-Soto et al. (2019) confirmed observations by Rebollar-Alviter et al. (2013) in the states of Michoacán and Jalisco, respectively, without relating this species to redberry disease.

In general, eriophyid mites can actively disperse among plants by walking or can passively disperse by mechanisms such as wind and rain and even phoretically through movement by insects; however, the most effective way of dispersal over long distances is considered to be through movement by wind (Michalska et al. 2010). Recently, Valenzano et al. (2019) confirmed that some eriophyid mites could survive under cold temperatures, starvation, and low oxygen concentrations, likely to occur when they disperse by vapor or fine water drops, such as those found in clouds. The main means of dispersal by A. essigi is ambulatory; however, dispersal by wind can also occur (Davies et al. 2001a). Studies of intraplant dispersion patterns in Rubus fruticosus L. indicated that this eriophyid mite is associated with the axils of leaves and buds of primocanes. These mites are concentrated in the most basal 20% of these microhabitats. Among the floricanes, 20% of mites were also found to be concentrated in the basal part, but mites were also observed in the apical part. In dormant canes, the mites colonize the basal third of the first-year canes (Davies et al. 2001b). These observations are valuable for designing integrated measures to manage redberry disease because such work relates eriophyid mites with plant development.

The management of redberry disease is primarily based on the application of miticides such as abamectin and sulfur-based products after the first appearance of symptoms, but the efficacy of these applications at this time has been low. In this regard, Szendrey et al. (2003) indicated that the application of calcium polysulfide (lime sulfur), flufenzin, fenpyroximate, and pyridaben showed better results when two applications were performed at the beginning of budbreak and during early flowering. However, the best timing of the application of different management tools and their efficacy in relation to A. orthomera densities in fruiting lateral buds are still poorly understood, as well as the relationship of these mites with redberry disease incidence.

The characteristic redberry damage, associated mainly with the presence of A. essigi and A. orthomera, significantly reduces the marketing of blackberry fruits worldwide. Therefore, given the direct impacts of these mite pests, their management demands an understanding of their habits and relationship with crop development under specific production systems considering a sustainable approach. Our hypothesis was that redberry disease is associated with the presence of eriophyid mite populations of the genus Acalitus in the buds of fruiting laterals, which are associated with the level of redberry disease at harvest. Additionally, we hypothesized that these populations can be managed by designing integrated management strategies implemented either after budbreak or at the beginning of the blooming period in IPM and organic production systems. The objectives of this work were to (a) identify the eriophyid mite species present in the buds of fruiting laterals and blackberry fruits and their relationship with redberry disease in blackberry and (b) evaluate the effects of different management strategies on the density of eriophyid mites in the buds of fruiting laterals and on the incidence of redberry disease in blackberry.

Materials and methods

Identification of the mites associated with the buds and fruits of blackberry

Twenty fruiting laterals from an equal number of plants were randomly collected from a commercial blackberry cv. ‘Tupy’ plot in the municipality of Tacámbaro in Michoacán state at 19° 14′ 0.59″ N, 101° 26′ 2.31″ W. The mites from the buds of the sampled fruiting laterals were carefully extracted from the bud scales by separating the scales with a dissecting needle under a dissecting microscope and stored in 70% ethylic alcohol. Additionally, at the beginning of the harvest period, 100 symptomatic fruits were collected from the same plot. In the laboratory, fruit drupelets were carefully detached from the berry receptacle with a dissecting needle under a dissecting microscope, and the mites were then collected from the base of the drupelets near the receptacle. The mites were preserved in 70% ethylic alcohol. Later, the mites were mounted in Hoyer´s medium (Dhooria 2016) for light microscopy observation. Additionally, scanning microscopy sample preparation was performed according to Bozzola and Russell (1992), with modifications, briefly: 70% ethanol preserved mites were dehydrated through successive passes of ethanol, 80, 90 and 100%, 1 h each; critical-point-dried (Toussimis Samdri-780A); mounted on brass stubs with carbon tape, covered with a nanometrical layer of gold (JEOL LTD JFC-1100 b Fine Coat Ion Sputter); and observed under a Jeol JSM IT300 scanning electron microscope. The mites were identified using the keys of Amrine et al. (2003) and the original description of Keifer (1951).

Evaluation of strategies to manage redberry disease

Treatments were designed based on the list of products authorized by Aneberries (National Association of Exporters of Berries) (Table 1). This list of products is based on agricultural supplies permitted by the destination countries to which blackberry is exported.

Table 1 Commercial products used in the designing of spray programs against the redberry mite in blackberry in Michoacán, Mexico, in the seasons 2014–2015 and 2015–2016
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In the 2014–2015 season, two experimental plots of blackberry cv. ‘Tupy’ were established under an integrated pest management or an organic production system. The first experiment in the IPM plot was established in the municipality of Tacámbaro (19° 32′ 33.08″ N and 102° 25′ 3.45″ W), and the second experiment was performed in a certified organic blackberry plot in Peribán municipality (19°14′ 0.59″ N and 10°26′ 2.31″ W). A third experiment was established in the 2015–2016 season in a IPM plot in the municipality of Tacámbaro (19° 21′ 19.08″ N and 101° 26′ 28.41″ W). All operations except for the treatment applications, including the fertilization and general management of the crop, were carried out by the grower.

During the 2014–2015 season in the IPM and organic blackberry plots, nine and 10 management programs (treatments) and their respective controls (untreated plots) were evaluated, with the implementation of spraying beginning at budbreak (Tables 2, 3). Additionally, based on the results obtained in the previous season, the experiment was repeated in the 2015–2016 season in a IPM blackberry plot, but during this season, treatment applications began at the floral bud stage. Seven treatments and one control (untreated plot) were evaluated at the same rates as in the previous season (Table 4).

Table 2 Strategies and application dates for the management of the redberry mite in blackberry under a conventional management system in Tacámbaro, Michoacán. Season 2014–2015
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Table 3 Strategies and application dates for the management of the redberry mite in blackberry under an organic system in Peribán, Michoacán. Season 2014–2015
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Table 4 Strategies and application dates for the management of the redberry mite in blackberry under a conventional management system in Tacámbaro, Michoacán. Season 2015–2016
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Experimental plots were established in a randomized complete block design with four replicates. An experimental unit consisted of 10 linear m of crop row. From the middle part of each experimental unit, a subsample of three fruiting laterals was randomly collected every 14 days. In the laboratory, the buds were dissected under a dissecting microscope, and the number of eriophyid mites per bud in the basal, medium, and apical parts (strata) of the fruiting lateral was determined. To determine whether a spatial aggregation of mites occurred within the fruiting lateral, the stratum factor was considered in the model during data analysis. The applications in all the experiments were carried out with a motorized sprayer (Honda Model MJR 4025, Honda Mexico) calibrated to spray 800 L ha−1. During this season, sprayings began 2 weeks after budbreak and continued every 14 days until fruit set. During the 2015–2016 season, the applications of the treatments began when approximately 5% of the plants had floral buds and continued every 14 days until harvest.

Data analysis

The number of mites per bud, stratum and fruiting lateral was determined. A repeated-measures analysis of variance (ANOVA) was performed over the different sampling dates using the PROC GLIMMIX procedure (SAS ver. 9.4) considering the treatment, time (sampling date) and stratum as fixed effects and block and fruiting lateral as random effects. To fit the GLIMMIX model, the Laplace approximation method was used. A negative binomial distribution with a log link function was assumed for the mite counts (Gbur et al. 2012). A first-order autoregressive model with an AR(1) covariance structure was selected based on the smallest adjusted Akaike’s information criterion (AICC) value. Because several zero values were obtained, the analysis was conducted with a x + 0.5 transformation. A least significant difference (LSD) test (α = 0.05) was performed for treatment mean comparisons. Estimates and standard errors on the mean scale were obtained by selecting the ilink option (inverse link scale).

Once the harvest started, all the fruits from the central 3 m of the row making up each experimental unit were harvested once a week for 6 weeks. The numbers of symptomatic and asymptomatic fruits were recorded each week. The incidence of redberry disease was estimated based on the pooled number of healthy and diseased fruits from the different harvesting times. The effect of the treatments on the incidence of redberry disease was also evaluated using the PROC GLIMMIX procedure in the SAS program. For this variable, the binomial distribution with a logit link function was assumed. A LSD test was conducted for the comparison of means, and the mean predicted probability and standard errors were obtained by selecting the ilink option in SAS.

To determine whether there was a correlation between the number of eriophyid mites in the buds of fruiting laterals and redberry disease incidence regardless of the treatment applied, a Spearman´s rank correlation analysis was conducted considering the data from the three experiments.

Results

Mites associated with fruiting lateral buds and berries

The mites associated with the fruiting lateral buds and fruits of blackberry were identified as A. orthomera. This species is very similar to A. essigi, the eriophyid mite most often associated with redberry disease. However, the morphological characteristics that mainly differentiate the two species are the pattern and distribution of the lines on the prodorsal shield of A. orthomera. Additionally, A. essigi is characterized by presenting two transverse lines curved in the shape of a half moon that are generally broken in the central part of its genital plate, whereas the genital shield of A. orthomera presents longitudinal ridges (Jeppson et al. 1975; Trinidad et al. 2018). In this study, high densities of A. orthomera were found in the fruits from the green to the red stage of development.

Effects of the treatments on eriophyid mite density

For the 2014–2015 season, the repeated-measures ANOVA of the data from the experiment conducted under the IPM production system indicated that the three-way interaction (stratum, treatment, and time factors) was not significant (F = 0.29, P = 1.0). However, the interaction between the treatment and stratum factors was significant (F = 2.70, P = 0.0003), indicating that the differential response to the treatments depended upon the stratum and was not influenced by the sampling time. As observed in Fig. 1A, the highest density of eriophyid mites was generally concentrated in the buds of the basal third of the fruiting lateral. Considering the effects of the treatments only on the basal stratum there were significant differences among the treatments (F = 18.48, P < 0.0001). The treatments that most reduced the mite density were those based only on the application of lime sulfur or programs that began with two applications of acequinocyl or abamectin, followed by lime sulfur (treatments 1, 2, 3, 9), with significant differences between these treatments and the control but not among them. The other treatments also significantly reduced the density of mites in the buds compared to that in the untreated control, although not at the same level.

Fig. 1
figure 1

Experiment on blackberry orchard under integrated pest management system in 2014–2015 season. Effects of different management strategies on the density of eriophyid mites associated with buds (A) on three strata of fruiting laterals (low, medium, apical) and (B) on the incidence of redberry disease in a IPM production system: (1) lime sulfur; (2) acequinocyl-lime sulfur; (3) lime sulfur-acequinocyl-lime sulfur; (4) Hirsutella thompsonii; (5) soybean oil; (6) acequinocyl-H. thompsonii; (7) garlic and chili pepper extract; (8) hexythiazox-lime sulfur; (9) abamectin-lime sulfur; (10) untreated control. Panel A, mean mite density per stratum and treatment comparison. Panel B, pooled mean redberry incidence across six harvests. In both charts, bars with the same letter are not significantly different (LSD test, α = 0.05). Season 2014–2015

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The results obtained from the plot under the organic production system in the same season indicated that the three-factor interaction (stratum, treatment, and time) was not significant (F = 0.74, P = 0.92), but the interaction between stratum and treatment was significant (F = 2.67, P < 0.0002). Again, the data indicated that the basal stratum of the fruiting laterals had the highest number of eriophyid mites. In this stratum, there were significant differences among the treatments (F = 19.96, P < 0.0001). Similar to the results from the IPM plot, the treatments that significantly reduced the density of mites were those based on the sequential application of lime sulfur or neem extracts or alternated applications of lime sulfur and neem extract (treatments 1, 2, and 8) (Fig. 2A). The rest of the treatments, based on the entomopathogenic fungus Hirsutella thompsonii and soybean oil, also contributed to the reduction of eriophyid mite density by more than 50% in fruiting lateral buds.

Fig. 2
figure 2

Experiment on blackberry orchard under organic production system in 2014–2015 season. Effects of different management strategies on the density of eriophyid mites associated with buds (A) in three strata of fruiting laterals (low, medium, apical) and (B) on the incidence of redberry disease: (1) lime sulfur; (2) neem extract; (3) soybean oil; (4) garlic and chili pepper extract; (5) Hirsutella thompsonii; (6) plant terpenes (Po); (7) cinnamon extract; (8) lime sulfur-neem extract; (9) soybean oil-neem extract; (10) H. thompsonii-plant terpenes; (11) untreated control. Panel A, comparison of mean mite density per stratum in each treatment. Panel B, comparison of mean redberry incidence in each treatment pooled across six harvests. In both plots, bars with the same letter are not significantly different (LSD test, α = 0.05). Season 2014–2015

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In the second production season, 2015–2016, the treatment applications began at the appearance of floral buds. As in the previous season, the analysis of the data indicated that the three-factor interaction (stratum, treatment, and time) was not significant (F = 0.73, P = 0.94), as resulted in the interaction between stratum and treatment (F = 1.02, P = 0.42), indicating that the effect of treatment was not influenced by the strata. When performing the analysis according to sections (treatments by stratum), the results indicated significant differences among treatments in each of the strata. The comparison of treatments considering only the basal stratum indicated that there were significant differences among treatments (F = 28.5, P < 0.0001). In this experiment, the data indicated that applications beginning at the appearance of the floral buds were also effective in reducing the density of mites in these buds.

Overall, all the treatment schemes significantly reduced the mite density in comparison to that in the untreated control. For example, treatments 5, 6, and 7, which generally began with a block of two applications of a miticide (acequinocyl, abamectin or hexythiazox) followed by lime sulfur applications (Table 4, Fig. 3A), had a significant effect on the reduction of eriophyid mite populations in buds of the floral shoot.

Fig. 3
figure 3

Experiment on blackberry orchard under integrated pest management system in 2015–2016 season. Effects of different management strategies on the density of eriophyid mites associated with floral buds (A) in 3 strata (low, medium, apical) and (B) on the incidence of redberry disease: (1) lime sulfur-acequinocyl-lime sulfur; (2) lime sulfur-neem extract; (3) acequinocyl-neem extract; (4) neem extract; (5) acequinocyl-lime sulfur; (6) hexythiazox-lime sulfur; (7) abamectin-lime sulfur; (8) untreated control. In panel A, mean mite density per stratum and treatment. Treatment mean comparisons are shown for the lower stratum. Panel B mean redberry incidence pooled across six harvests. In both plots, bars with the same letter are not significantly different (LSD test, α = 0.05). Season 2015–2016

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Effects of the treatments on redberry disease incidence

The analysis of the data for the 2014–2015 season indicated that there were significant differences among the treatments in terms of the incidence of redberry disease in the IPM (F = 5.45, P < 0.007) and the organic plots (F = 9.21, P < 0.0001). In general, the treatments that significantly reduced the density of eriophyid mites in the buds of fruiting laterals also had the lowest incidence of redberry disease in both production systems. In the IPM plot, treatments 1, 2, 3, 8, and 9 had the lowest incidence of redberry disease (Fig. 1B). These treatments were based on the application of only lime sulfur every 14 days from budbreak to the beginning of harvest or two applications of the miticides acequinocyl, hexythiazox or abamectin followed by lime sulfur application until the beginning of harvest (Table 2). Treatments based only on H. thompsonii application (4) or that included only two applications of acequinocyl in blocks after budbreak but were followed by H. thompsonii application (6), as well as the one based only on the application of plant extracts (7), did not give satisfactory results compared with those in the untreated control.

In the blackberry plot under organic management, the effects of the treatments on the incidence of symptomatic fruit was also similar to their effects on the density of eriophyid mites in the buds (Fig. 2A). For this variable, treatments 1 and 8 resulted in the lowest incidence of redberry disease when pooling across all the different harvests (Fig. 2B); they consisted of applications based on lime sulfur every 14 days and three applications of lime sulfur at the beginning of budbreak, followed by two additional applications of neem extract. In this experiment, treatments based on plant extracts such as cinnamon extract, neem extract, and soybean oil only slightly reduced the incidence of redberry disease.

The experiment established under the IPM production system in the following season, which considered the results of the previous season (Table 4) but with applications at the beginning of the blooming period, showed significant differences between the treatments and the control (F = 17.37, P < 0.000). However, there were no significant differences among the different management schemes (Fig. 3B). The results of the treatment applications at the beginning of the flowering period and continuing every 14 days indicated that it is feasible to significantly reduce the incidence of redberry disease regardless of whether the management program starts with blocks of two applications of the miticides acequinocyl, abamectin, or hexythiazox or with only lime sulfur or lime sulfur in alternating blocks with neem extract.

Association of eriophyid mite densities in buds and redberry disease

Spearman rank correlation analysis of the relationship between the density of eriophyid mites in each bud in the fruiting lateral or floral buds at each evaluation date and the incidence of redberry disease estimated on each harvest date (weekly) (regardless of the treatment applied) indicated the occurrence of a moderate to strong positive correlation. In the first season, the eriophyid mite population density during the first 6 weeks after budbreak in both production systems was moderate to strongly correlated with the incidence of redberry disease during the first 6 weeks of harvest (weeks 12, 13, and 14 after budbreak). Additionally, the density of eriophyid mites in the 8th week after budbreak (blooming period) was strongly and positively correlated with the incidence of redberry disease estimated until the 5th to 6 week of harvest (Table 5).

Table 5 Spearman´s rank correlation coefficients of eriophyid mite density against redberry mite incidence at harvest by evaluation time in three experimental plots of blackberry (Rubus sp.)
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Discussion

Redberry disease is one of the most critical biotic factors causing significant losses to the blackberry industry worldwide. In this study, we confirmed that A. orthomera is associated not only with buds on the fruiting laterals of blackberry cv. ‘Tupy’ but also with fruit drupelets showing symptoms of redberry disease. This study also showed that the eriophyid mite population in the buds of fruiting laterals was correlated with the incidence of redberry disease at harvest. Interestingly, although several reports have indicated that A. essigi is the main species associated with redberry disease in blackberry (Ochoa et al. 1991; Murrieta and Gaskell 2016), our study showed that A. orthomera is the species associated with this disease in subtropical blackberry production in Mexico, similar to the previous report regarding blackberries cv. ‘Tupy’ by Trinidad et al. (2018).

In Mexico, blackberry crops develop under a forced production system. This system consists of a combination of pruning practices followed by chemical defoliation and hormone applications one to 2 weeks later to stimulate budbreak and the elongation of fruiting laterals. Under subtropical conditions such as those prevailing in Mexico, it takes approximately 85–90 days from plant defoliation and budbreak to begin the harvest. Under this production system, the management strategies (sequences of applications) evaluated in this study were designed considering the previously reported dispersal mechanism of A. essigi and its association with the buds of primocanes and floricanes (Davies et al. 2001a and 2001b). Interestingly, during the 2014–2015 season, in the plots under both the IPM and organic management systems, the management strategies that began with lime sulfur application every 14 days after budbreak were effective in reducing A. orthomera densities and redberry disease incidence. Additionally, those strategies beginning with a block of two applications of chemical miticides (acequinocyl, abamectin or hexythiazox) followed by sequential applications of lime sulfur gave satisfactory results in terms of the reduction of the population density of A. orthomera and the incidence of redberry disease. Lime sulfur has been reported to be effective in controlling A. essigi on blackberry (Cross et al. 2012); however, this compound has also been regarded as disrupting integrated mite control because of its effect on phytoseiids (Marcic 2012; Venzon et al. 2013; Tuelher et al. 2013). Our results show that lime sulfur can be applied in alternation or blocks of two applications with acequinocyl, hexythiazox, and neem extract. This application strategy reduces the number of lime sulfur applications and its potentially lethal effects on predatory mites, as these ingredients have been reported to be safe or with low to moderate effects on these arthropods (Dekeyser 2005; Marcic 2012; Bernardi et al. 2013). Similarly, in the plot under organic management, excellent results were obtained with the treatments under a full program or either at least three sequential applications of lime sulfur every 14 days or followed by applications of neem extracts near the harvest period.

Additionally, programs based on soybean oil also gave satisfactory results, representing good alternatives for application either in alternation or in blocks with lime sulfur to reduce the negative impacts of this compound on the natural enemies of eriophyid mites. The results from the third plot, in which the treatments were applied at the beginning of the blooming period (with the presence of floral buds), also showed that these treatments were effective against redberry disease. These results confirm that it is also possible to significantly reduce the populations of A. orthomera with either only lime sulfur application every 14 days or starting the management strategy with a block of two applications of the evaluated miticides followed by lime sulfur or neem extracts near the harvest period. Under this approach, the mite populations were higher in floral buds compared with those when beginning the treatments after budbreak, slightly increasing the incidence of redberry disease in all the treatments. The first applications were performed in the floral bud stage because of the dispersal pattern of A. essigi; this mite is present in the receptacle of the fruit at the beginning of flowering and then moves to green fruits (Davies et al. 2001b). In addition, our previous observations showed the highest densities of mites at the base of the drupelets of green to ripening fruits near the fruit receptacle. As seen in Fig. 3A, when the treatment applications began at the appearance of the first flower buds, the density of mites in the medium and high strata was higher than that when applications began after budbreak. However, the lowest stratum of the fruiting laterals significantly concentrated the highest eriophyid density. Therefore, similar to previous reports on A. essigi (Davies et al. 2001a), under a forced production system, the eriophyid mites were mainly concentrated in the basal third of the fruiting lateral close to the main cane. As the fruiting lateral developed, the populations slightly grew in the medium third of the lateral, although a tendency towards aggregation in the buds of the basal third was evident in the three experimental plots over the two production seasons.

The effectiveness of the management strategies at the beginning of budbreak (after defoliation) may be explained by the fact that as laterals develop, mites are more exposed and more susceptible to the treatment applications (Davies et al. 2001b). These results could be observed with the effect of lime sulfur-based treatments both in organic and IPM production systems. However, the effectiveness of the strategies applied at the beginning of flowering and continuing every 14 days during the harvest period also had good efficacy among all the treatments applied, similar to previous reports on A. essigi (Szendrey et al. 2003; Cross et al. 2012). Therefore, based on our results, this timing is also feasible for treatment application. However, crop pruning management on primocane- or floricane-producing blackberry cultivars is likely to influence the populations and dispersal of eriophyids in both the buds and the berries, as has been previously reported (Murrieta and Gaskell 2016).

Interestingly, our studies evidenced a moderate to strong positive correlation between the population density of eriophyid mites in the buds and the incidence of redberry disease in fruits. Although the correlation between population density in the first 6 weeks after budbreak and the incidence of redberry disease in the first 3 weeks of harvest was strong, the mite density in week 8 after budbreak (from the floral bud to fruit set period) was most correlated with redberry disease incidence at harvest. These results suggest that this stage of crop development is a critical period for the initiation of treatment applications for the management of redberry disease.

In conclusion, the results confirm that A. orthomera is the eriophyid mite species associated with the buds of fruiting laterals and fruits in blackberry crops associated with redberry disease. This study evidenced the positive and significant correlation between the population density of A. orthomera in the buds of fruiting laterals and the incidence of redberry disease at harvest. Additionally, it was shown that in IPM blackberry growing systems, it is feasible to significantly reduce redberry disease incidence through management programs based on either sequential applications of lime sulfur alone in blocks of two applications or alternating with active ingredients such as abamectin or acequinocyl, hexythiazox or neem extracts every 14 days from the beginning of budbreak. These programs were also successful when applied at the beginning of the blooming (flowering bud) period. The results indicate that it is possible to reduce redberry disease incidence in organic systems using a complete program based on lime sulfur applications alone or in alternation with neem extracts or soybean oil.