Population dynamics and infestation of Holopothrips fulvus Morgan (Thysanoptera: Phlaeothripidae) in dwarf cashew genotypes

: The objective of this study was to evaluate the Holopothrips fulvus Morgan (Thysanoptera: Phlaeothripidae) population dynamics and to identify dwarf cashew genotypes less infested by the pest in 2015 and 2016, under field conditions. H. fulvus population evaluations were carried out by monthly observations in the plants and using a score scale varying from 0 to 4. H. fulvus infestation occurred from October to December, and in the cashew genotypes CAP 112/8, CAP 121/1, CAP 131/2, CAP 145/2, CAP 145/7, CAP 128/2, CAP 120/4, CAP 123/6, CAP 130/1, and CAP 157/2 was dependent on the flowering period of the crop in 2015. In 2016, there was dependence in all evaluated genotypes between H. fulvus infestation and the cashew flowering period. In 2015, no significant differences were observed between the evaluated genotypes regarding H. fulvus infestation. In 2016, genotypes CAP 105/5, CAP 143/7, CAP 150/3, CAP 155/2, CAP 158/8, CAP 161/7, CAP 163/8, CAP 31, CAP 71, CAP 92, CAP 113, CAP 120, CAP 155, CAP 165, CAP 106/1, CAP 111/2, CAP 127/3, CAP 157/2, and BRS 226 were less infested. H. fulvus occurs from October to December and we could identify the dwarf cashew genotypes less infested by the pest.


INTRODUCTION
Cashew cultivation in Brazil has high socioeconomic importance, especially in the states that are located in the semi-arid regions of the northeast (Serrano & Oliveira 2013). In the 2017 harvest, the production of cashew nuts, the main product of the crop, reached 134,000 tonnes, and the States of Ceará, Piauí, and Rio Grande do Norte accounted for 89.5% of this production (IBGE 2018). However, this production has been affected by several insect pests, which interfere with the yield and the quality of the fruits, resulting in low economic return (Serrano & Oliveira 2013).
In Brazil, Holopothrips fulvus Morgan (Thysanoptera: Phlaeothripidae) was recently reported damaging dwarf cashews in the municipality of Pacajus, Ceará (Lima et al. 2017). This species of thrips feeds on cashew leaves and fruits, which can damage the reproductive organs (flowers), producing necrotic spots in the feeding site, around the insertion point of the nut, in the accessory fruit, and in the abaxial surface of the leaf, which become yellow and wilted, causing the senescence and fall of leaves and inflorescences (Lima et al. 2017). Thrips can cause direct damages from the sucking of the sap and consequent reduction in the photosynthetic rate of plants. They also cause abortion of flowers and reduction of fruiting from the consumption of pollen grain (Riley et al. 2011b). Indirect damages can occur with the transmission of phytopathogens, especially tospovirus (Rotenberg et al. 2015).
In Brazil, cashew producers do not have certified formulated products or active ingredients to control H. fulvus, probably because of their recent introduction to the country, however, studies aimed at the management of this pest are necessary since thrip population outbreaks in other agricultural crops may cause significant losses in production (Pereira et al. 2017, Kaur et al. 2018. In fact, chemical control appears to be the most widely used method for thrip management. However, the indiscriminate use of synthetic chemical molecules has increased the selection pressure, favoring the emergence of resistant populations, as well as the death of natural enemies and contamination of the environment and animals (Wang et al. 2016, Conte et al. 2014, Ferreira et al. 2017.
In this way, the knowledge and use of other control tactics within Integrated Pest Management (IPM) are of the utmost importance. Plant resistance to insects is an effective alternative, within the IPM context, as it offers a long-lasting solution with minimal financial investment for the maintenance of phytophagous insect populations. In addition, the knowledge about the dynamics of thrips in agricultural crops seems to be a key point in their management, since their populations may occur at different times of the year from the influence of abiotic factors (Lin et al. 2015, Ahmed et al. 2017. In Brazil, studies on the H. fulvus resistance of cashew genotypes and the knowledge about their population dynamics in this crop have been neglected. Therefore, the objective of this work was to (1) (Kottek et al. 2006), the local climate is the equatorial savanna with dry winter, which is a climatically arid region with rainy season concentrated between February and March. Environmental data (rainfall and temperature) were registered at a weather station located 3.4 km from the experimental area. During the experiment, no phytosanitary practices were carried out.

H. fulvus population dynamics in cashew plants
We considered all genotypes to evaluate the H. fulvus population dynamics in cashew plants. The H. fulvus population dynamics was evaluated indirectly through leaf damage, estimated by a diagrammatic scale ( Figure 1). According to the scale, 0 corresponds to a healthy leaf, 1 corresponds to 1-25% of leaf area damaged, 2 corresponds to 26-50% of leaf area damaged, 3 corresponds to 51-75% of leaf area damaged, and 4 corresponds to >75% of leaf area damaged and change in color (yellowing).
For two years (2015)(2016), at monthly intervals, ten leaves were randomly collected from eight plants of each genotype (2800 leaves per month). The mean level of damage was obtained from the mean scores of the leaves and plotted as a function of time. Since the damage of H. fulvus was not observed throughout the year, we performed an association test between the occurrence of damage and the flowering period using a presence-absence matrix (contingency table, according to Ludwig & Reynolds 1988).
The association was quantified by Pearson's chisquared test: In this equation, a corresponds to the time intervals when both damage and the flowering period occurred in the field, b corresponds to only when damage occurred, c corresponds to only when the flowering period occurred, d corresponds to when neither damage nor the flowering period occurred, and N corresponds to all time intervals (96 = eight plants x 12 months). According to the association test, the variables are dependent when χ² is significant (P < 0.05), while they are independent when it is not significant (P > 0.05).

H. fulvus infestation in different cashew genotypes
To evaluate the susceptibility of the different cashew genotypes, mean damage levels were subjected to the generalized linear model (SAS Institute 2001), in which genotype, year, and month were the independent variables. Subsequently, the means were compared by Fisher's exact test or Tukey's HSD test.

Holopothrips fulvus infestations occurred from
October to December, corresponding to the flowering months of the cashew crop, in the crop years 2015 and 2016. In the months of occurrence, a peak was observed in November in the mean damage score, decreasing in December ( Figure  2). In 2015, H. fulvus infestation in genotypes CAP 112/8, CAP 121/1, CAP 131/2, CAP 145/2, CAP 145/7, CAP 128/2, CAP 120/4, CAP 123/6, CAP 130/1, and CAP 157/2 was dependent on the flowering period of the crop (Table II). In 2016, there was dependence in all evaluated genotypes between H. fulvus infestation and the cashew flowering period (Table II).

DISCUSSION
The occurrence  It is also believed that the occurrence of H. fulvus from October to December, in the cashew crop, is also related to the low rainfall in this period, considered the dry season with high temperatures, being thus the most favorable period for the biological development of the pest (Morsello et al. 2008, Reitz 2009. Similarly, significant negative correlations have been found between rainfall and the populations of Scirtothripes dorsalis and Azaleothrips sp. in cashew panicles (Navik et al. 2016).
The behavior of increased H. fulvus populations in October, in the flowering and fruiting period of the cashew crop, and decreased populations in December, when the fruit is harvested, corroborates the studies of Palomo et al. (2015), who have found higher Frankliniella occidentalis population densities during tomatillo flowering, and a decrease in this density during its fruiting stage. H. fulvus infestation during this period gives the pest a great potential to damage the crop, since it can damage an important stage, that is the production.
Holopothrips fulvus abundance was highly seasonal, occurring at the same time in the two years of study, with an increase in infestation from one year to the next, this increase may be related to the establishment of the insect in the field, as the cashew crop is perennial. In contrast, in annual short cycle crops, such as onion and cabbage, the seasonality of the Thrips tabaci Lindeman species may vary (Nault et al. 2014 In fact, in thrips, the attraction of adult insects may vary according to genotype ( Therefore, given the lack of more information in the literature on H. fulvus in the cashew crop, our results provide unprecedented evidence for the occurrence of H. fulvus associations between the different dwarf cashew genetic materials, as well as their seasonal variation. However, it would be interesting to investigate the causes of resistance of the less infested clones, so that the materials could be considered as candidates for further investigation within our genetic improvement program, whose main objective is to increase the cashew resistance to biotic stress.