Scale insects ( Hemiptera : Coccoidea ) associated with arabica coffee and geographical distribution in the neotropical region

Coffee is one of the most important Brazilian agricultural commodities exported, and Minas Gerais and Espírito Santo States are the main coffee producers. Scale insects are important coffee pests, and 73 species of Cerococcidae (3), Coccidae (18), Diaspididae (6), Eriococcidae (1), Ortheziidae (3), Pseudococcidae (21), Putoidae (2) and Rhizoecidae (19) have been associated with roots, branches, leaves, flowers and fruits of Arabica coffee in the Neotropics. Eight species were found associated with Arabica coffee in Minas Gerais and Espírito Santo States in this study, and Coccidae was the most frequent family. Coccus alpinus, Cc. celatus, Cc. lizeri, Cc. viridis, and Saissetia coffeae (Coccidae) were found in both states; Alecanochiton marquesi, Pseudaonidia trilobitiformis (Diaspididae), and Dysmicoccus texensis (Pseudococcidae) were only found in Minas Gerais. Alecanochiton marquesi and P. trilobitiformis are first reported in Minas Gerais, and Cc. alpinus in Espírito Santo, on Arabica coffee. All scale insect species were associated with coffee leaves and branches, except D. texensis, associated with coffee roots. Fourty seven scale insect species have been found occurring in Brazilian Arabica coffee, and in Espírito Santo (28) and Minas Gerais (23). Widespread and geographical distribution of each species found are discussed.


INTRODUCTION
Coffee is one of the most important Brazilian agricultural commodities exported, and 80% of this coffee is produced in Minas Gerais and Espírito Santo States.Both coffee species, Coffea arabica L. (Arabica coffee) and Co. canephora Pierre ex A. Froehner (Robusta coffee) have been cultivated in Brazil, and first former accounts for ~75% of the total production (IBGE 2015).Insects may reduce coffee yield, and scale insects (Hemiptera: Coccoidea) play an important role as pest associated with roots, branches, leaves, flowers and fruits of Arabica coffee in the Neotropics.The economic level of damage depends on climatic conditions, costs of production and prices in the international market (Fornazier et al. 2007).
Scale insects are major agricultural pests, particularly when they develop in new regions of coffee plantations free from their natural enemies (Culik et al. 2011).They have the habit of sucking the sap on leaves, stems, and roots, are polyphagous and attack a large number of agricultural and ornamental plantations (Miller et al. 2005, García Morales et al. 2016).These are insects of quarantine importance affecting the domestic and export market, causing damage to plants mainly by injecting toxins and transmitting pathogens such as viruses (Martins et al. 2004, Culik et al. 2006).The feeding behavior of scale insects affect negatively plant healthy or weakens plants, and may reduce plant vigor, causes premature defoliation, impact formation of new shoots, can lead to branch dieback, and eventually plant death.In addition, the honeydew excreted by scales allows the development of sooty mold that inhibits photosynthesis and causes cosmetic damage to fruits (Mibey 1997, Vandenberg et al. 2007).Also, it attracts ants and creats a mutual interaction between ants and scale insects as protective benefit to the scale insect against predators (Davidson et al. 2003, Hunt 2003, Bluthgen et al. 2004, Livingston et al. 2008, Shalene et al. 2009).Particularly young plants of coffee may be affected under field conditions, and depending on the scale insect species, age of the plantation, and infestation level, the replanting or total replacement of seedlings in the area may be required.They can also infest sprouts of seedlings in nurseries, and be disseminated to new plantations (Bittenbender 2000, Fernandes et al. 2009, Reis et al. 2010).
Worldwide 114 species of scale insects (Hemiptera: Coccoidea) have been cited in Arabica coffee, and 73 species Cerococcidae (3), Coccidae (18), Diaspididae (6), Eriococcidae (1), Ortheziidae (3), Pseudococcidae (21), Putoidae (2) and Rhizoecidae ( 19) have been associated with roots, branches, leaves, flowers and fruits of Arabica coffee in the Neotropics.Fourty seven scale insect species have been found occurring in Brazilian Arabica coffee (García Morales et al. 2016).Coccidae (soft scales), Diaspididae (armored scales) and Pseudococcidae (mealybugs) are widespread throughout the world as pests on agricultural plantations and ornamental plants (Williams and Granara de Willink 1992, Henderson andHodgson 2005).This research aimed to verify the geographical distribution of scale species (Hemiptera: Coccoidea) associated with Arabica coffee in the two main Brazilian states coffee producers, Espírito Santo and Minas Gerais, report those species associated with this coffee species, and their range expansion in the Neotropics.

MATERIALS AND METHODS
Scale insects were sampled from Arabica coffee commercial producing plantations with no chemical spraying at altitudes between 209 to 1,050 m in Minas Gerais and Espírito Santo States.Samplings were carried out in the municipalities of Cachoeirinha, Campos Altos, Ervália, Florestal, Itabira, Manhuaçu, Muriaé and Viçosa, Minas Gerais State, and in the municipalities of Domingos Martins, Ibatiba, Ibitirama, Iúna and Venda Nova do Imigrante, Espírito Santo State.Scale insects were collected manually from the leaves, branches, trunk, roots, and fruits.The canopies and roots of ten coffee plants were examined in each coffee orchard sampled for the presence of scale insects.Branch and trunk bark, and leaves infested with scale insects were collected, cut into 2 x 2 cm pieces; infested rosettes and fruits were collected; the main and secondary roots of the coffee tree were sampled by digging a 20 cm diameter hole by 20 cm deep.The specimens collected were prepared and assembled on slides for microscopy (Granara de Willink 1990).This method consists on clarification using Essig solution composed of 20 parts of lactic acid (85%), two parts of saturated phenol, four parts of glacial acetic acid and one part of distilled water; coloration was performed with fuchsin acid, dehydration with different concentrations of alcohol, and they were assembled in Canada balsam.Scale insects were identified in the Facultad de Ciencias Naturales e Instituto Miguel Lillo, Universidad Nacional de Tucumán, Argentina.Voucher specimens were deposited in the Regional Museum of Entomology, Department of Entomology, Universidade Federal de Viçosa (UFV) in Viçosa, Minas Gerais State, Brazil.
In the Neotropics, 73 scale species have been found associated with Arabica coffee.The largest number of species associated with coffee in the Neotropics, and found in Brazil belongs to Pseudococcidae (21), Coccidae (18) and Rhizoecidae ( 19).Cerococcidae has only three species occurring in the Neotropics, and two of them occur in Brazil; Putoidea was not recorded occurring in Brazilian Arabica coffee, but two scale species of this family have been associated with this crop in the Neotropics.From those 19 species of Rhizoecidae, four of them have been related in Brazilian Arabica coffee.The genera with the larger number of species associated with Arabica coffee in the Neotropics are Rhizoecus (11 species), Coccus (7), Dysmicoccus (6), and Pseudococcus (6); in Brazil, they are Coccus (7), Pseudococcus (6) and Dysmicoccus (5) (Table SI -Supplementary Material).
The genus Coccus has about 90 widely distributed species in all zoogeographical regions.Some species of this genus are pests in horticultural and ornamental plants (Hodgson 1994, Williams and Ben-Dov 2009, Martin and Lau 2011, Wang and Feng 2012).It is the second most common genus of this scale insect family, and all species of this genus associated with Arabica coffee have been found in Brazil (Table SI).
The new finding of Cc. alpinus represents the range expansion of its geographical distribution in Minas Gerais State, and its first report in Arabica coffee in Espírito Santo State (Table I).This scale species was related to the Afrotropical and Neotropical regions, and its host plants include species of Apocynaceae, Celastraceae, Ehretiaceae, Myrtaceae, Rubiaceae, Rutaceae, and Theaceae (García Morales et al. 2016).This coccid was found in Malawi in Arabica coffee above 1,220 m (Murphy 1991), in Papua New Guinea (Hillocks et al. 1999), and on coffee plants in the Brazilian States of Bahia, and Minas Gerais (Granara de Willink et al. 2010, García Morales et al. 2016).This species remains restrict to Brazilian Arabica coffee in the Neotropics (Table SI).
Coccus celatus was found in Arabica coffee in Espírito Santo and Minas Gerais States which represents its range expansion at different elevations from 209 m to 1,050 m (Table I).This soft scale is distributed in the Afrotropical, Australasian, Neotropical, and Oriental regions.Its host plants belong to Annonaceae, Apocynaceae, Calophyllaceae, Casuarinaceae, Clusiaceae, Costaceae, Euphorbiaceae, Fabaceae, Myrtaceae, Rubiaceae, and Rutaceae (García Morales et al. 2016).This species had been one of the main pests of Arabica coffee in highland above 1,000 m in Papua New Guinea for several decades (Murphy 1991).This species was first reported associated with Arabica coffee in Brazil by Granara de Willink et al. ( 2010) (Table SI).
A range expansion of the geographical distribution of Cc. lizeri in Arabica coffee was observed to the municipality of Campos Altos (1,200m ), Minas Gerais State (Table I).This species had been reported on Coffea spp. in São Paulo State, Brazil (Fonseca 1957, García Morales et al. 2016), and altitude seems not bring any influence on this species distribution.It has been associated with Arabica coffee in the Brazilian states of Bahia, Espírito Santo, Minas Gerais, and São Paulo (Table SI), and hitherto it remains restrict to these Brazilian states (Granara de Willink et al. 2010).
Coccus viridis associated with Arabica coffee was found in the municipalities of Campos Altos, Minas Gerais, and Iuna, Espírito Santo (Table I) representing a range expansion of the geographical distribution of this green coffee scale in Brazil.The species was found only at high altitudes above 1,000 m.This is a generalist and invasive pest species spread on tropical and subtropical regions under anthropogenic activities (Wyckhuys et al. 2013); it is reported in many countries in the Neotropics, including Brazil (Granara de Willink et al. 2010, García Morales et al. 2016) where it has been related occurring in several hosts in the States of Bahia, Espírito Santo, Minas Gerais, Pará, Paraná, Rio de Janeiro, Rio Grande do Norte, Rio Grande do Sul, Santa Catarina and São Paulo (Table SI).Diaspididae can be considered as a cosmopolitan pest of quarantine importance by the large number of host plants, particularly perennial crops (Miller et al. 2005).
Scale insects associated with Arabica coffee showed the diversity of this group in Brazil and the wide range expansion of several of these species.Most Rhizoecidae scale species associated with Arabica coffee in the Neotropical region are not reported occurring in Brazilian Arabica coffee, and it is important because if introduced they may be established in Brazil.Alecanochiton marquesi and P. trilobitiformis are first reported associated with Arabica coffee in Minas Gerais, and Cc.alpinus in Espírito Santo.Dismycoccus texensis remains restricted to Minas Gerais and São Paulo in Arabic coffee.The periods of low coffee prices in international market may influence the spread of scale insect species due to the reduced pest control by Brazilian coffee producers.Elevations, in general, did not seem to influence the spread of scale insect species found on samples.Information obtained in this study are of interest to Brazilian coffee producers, and to other regions.It will help to improve the knowledge of geographical distribution, and spread of scale insects associated with Arabica coffee in the Neotropics, particularly in Brazil.