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

MAURÍCIO J. FORNAZIER DAVID S. MARTINS MARIA CRISTINA G. DE WILLINK VICTOR D. PIROVANI PAULO S.F. FERREIRA JOSÉ C. ZANUNCIO About the authors

ABSTRACT

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.

Key words:
Coccidae; Coffea arabica; Diaspididae; geographical distribution; Pseudococcidae

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. 2007FORNAZIER MJ, FANTON CJ, BENASSI VLMR AND MARTINS DS. 2007. Pragas do café conilon. In: Ferrão RG, Fonseca AFA, Bragança SM, Ferrão MAG and De Muner LH (Eds), Café conilon, 1st ed., Vitória: Incaper, p. 405-449.).

Scale insects are major agricultural pests, particularly when they develop in new regions of coffee plantations free from their natural enemies (Culik et al. 2011CULIK MP, WOLF VRS, PERONTI ALBG, BEN-DOV Y AND VENTURA JA. 2011. Hemiptera, Coccoidea: Distribution extension and new records for the states of Espírito Santo, Ceará, and Pernambuco, Brazil. Check List 7: 567-570.). 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. 2005MILLER DR, MILLER GL, HODGES GS AND DAVIDSON JA. 2005. Introduced scale insects (Hemiptera: Coccoidea) of the United States and their impact on U.S. agriculture. P Entomol Soc Wash 107: 123-158., 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. 2004MARTINS DS, CULIK MP AND WOLFF VRS. 2004. New record of scale insects (Hemiptera: Coccoidea) as pests of papaya in Brazil. Neotrop Entomol 33: 655-657., 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 1997MIBEY RK. 1997. Sooty moulds. In: Ben-Dov Y and Hodgson CJ (Eds), Soft scale insects: Their biology, natural enemies and control, Amsterdam: Elsevier, p. 275-290., Vandenberg et al. 2007VANDENBERG JD, SHELTON AM AND WRAIGHT SP. 2007. Application and evaluation of entomopathogens in crucifers and cucurbits. In: Lacey L and Kaya H (Eds), Field manual of techniques in invertebrate pathology, Dordrecht: Springer, p. 361-374.). 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. 2003DAVIDSON DW, COOK SC, SNELLING R AND CHUA TH. 2003. Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300: 969-972., Hunt 2003HUNT JH. 2003. Cryptic herbivores of the rainforest canopy. Science 300: 916-917., Bluthgen et al. 2004BLUTHGEN N, STORK NE AND FIEDLER K. 2004. Bottom-up control and co-occurrence in complex communities: honeydew and nectar determine a rainforest ant mosaic. Oikos 106: 344-358., Livingston et al. 2008LIVINGSTON GF, WHITE AM AND KRATZ CJ. 2008. Indirect interactions between ant-tended hemipterans, a dominant ant Azteca instabilis (Hymenoptera: Formicidae), and shade trees in a tropical agroecosystem. Environ Entomol 37: 734-740., Shalene et al. 2009SHALENE JHA, VANDERMEER JH AND PERFECTO I. 2009. Population dynamics of Coccus viridis, a ubiquitous ant-tended agricultural pest, assessed by a new photographic method. B Insectol 62: 183-189.). 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 2000BITTENBENDER HC. 2000. Plantation profile for coffee in Hawaii. http://www.ipmcenters.org/plantationprofiles/docs/hicoffee.html/. Accessed June 20, 2015.
http://www.ipmcenters.org/plantationprof...
, Fernandes et al. 2009FERNANDES FL, PICANÇO MC, FERNANDES ME, GALDINO TV AND TOMAZ AC. 2009. Perdas causadas por Coccus viridis (Green) (Hemiptera: Coccidae) em mudas de Coffea arabica L. EntomoBrasilis 2: 49-53., Reis et al. 2010REIS PR, SOUZA JC, SANTA-CECÍLIA LVC, SILVA RA AND ZACARIAS MS. 2010. Manejo integrado de pragas do cafeeiro. In: Reis PR and Cunha RL (Eds), Café arábica: do plantio à colheita. Lavras: Epamig 1: 573-688.).

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 1992WILLIAMS DJ AND GRANARA DE WILLINK MC. 1992. Mealybugs of Central and South America. London: CAB International, 635 p., Henderson and Hodgson 2005HENDERSON RC AND HODGSON CJ. 2005. Two new species of Umbonichiton (Hemiptera: Sternorrhyncha: Coccoidea: Coccidae) from New Zealand. Zootaxa 854: 1-11.). 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.

RESULTS AND DISCUSSION

In total, eight species were found associated with Arabica coffee in Minas Gerais and Espírito Santo States. Coccus alpinus De Lotto, 1960, Cc. celatus De Lotto, 1960, Cc. lizeri (Fonseca, 1957FONSECA JP. 1957. Três novas espécies de coccídeos do Brasil, sobre cafeeiro (Homoptera: Coccidae). Arq Inst Biol 24: 123-135.), Cc. viridis (Green, 1889), and Saissetia coffeae (Walker, 1852) (Coccidae) were found associated with Arabica coffee in the two main Brazilian states coffee producers, Espírito Santo and Minas Gerais; Alecanochiton marquesiHempel, 1921HEMPEL A. 1921. Três novos coccídeos. Arch Esc Sup Agric Med Vet 5: 143-146. (Coccidae), Pseudaonidia trilobitiformis (Green, 1896) (Diaspididae), and Dysmicoccus texensis (Tinsley, 1900) (Pseudococcidae) were only found in Minas Gerais, Brazil. Alecanochiton marquesi and P. trilobitiformis are first reported occurring in Minas Gerais, and Cc. alpinus on Arabica coffee in Espírito Santo (Table I). 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).

TABLE I
Families and scale insect species (Hemiptera: Coccoidea) collected in Coffea arabica L., and respective municipalities, elevations (Elv), latitude (Lat), and longitude (Long), States of Espírito Santo (ES) and Minas Gerais (MG), Brazil, 2014.

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).

Coccus alpinus De Lotto, 1960, Cc. celatus De Lotto, 1960, Cc. lizeri (Fonseca, 1957FONSECA JP. 1957. Três novas espécies de coccídeos do Brasil, sobre cafeeiro (Homoptera: Coccidae). Arq Inst Biol 24: 123-135.), Cc. viridis (Green, 1889), and Saissetia coffeae (Walker, 1852) (Coccidae) were found associated with Arabica coffee in the two main Brazilian states coffee producers, Espírito Santo and Minas Gerais; Alecanochiton marquesiHempel, 1921HEMPEL A. 1921. Três novos coccídeos. Arch Esc Sup Agric Med Vet 5: 143-146. (Coccidae), Pseudaonidia trilobitiformis (Green, 1896) (Diaspididae), and Dysmicoccus texensis (Tinsley, 1900) (Pseudococcidae) were only found in Minas Gerais, Brazil (Table I). Coccidae showed the highest diversity (75%), and frequency (~87%). Cerococcus parahybensis Hempel, 1927, Cc. alpinus De Lotto, 1960, Cc. brasiliensis Fonseca, 1957, Cc. celatus De Lotto, 1960, Cc. lizeri (Fonseca, 1957), Eriococcus coffeae (Hempel, 1919), Nipaecoccus coffeae (Hempel, 1919) have only been reported in Brazilian coffee plantations (Table SI). Most scale insects sampled came from coffee plantations abandoned by the farmers. This fact probably has resulted in the increase of scale insects by the lack of chemical control in these abandoned crops, and the absence of efficient natural enemies.

Alecanochitonmarquesi is first reported occurring in Minas Gerais State (209 m), Brazil, and it has been recorded in the Neotropical region, including French Guiana. In Brazil, this species was first recorded in the municipality of Angatuba, São Paulo State on Coffea sp. (Hempel 1921HEMPEL A. 1921. Três novos coccídeos. Arch Esc Sup Agric Med Vet 5: 143-146., Silva et al. 1968SILVA AGA, GONÇALVES CR, GALVÃO DM, GONÇALVES AJL, GOMES J, SILVA MN AND SIMONI L. 1968. Quarto catálogo dos insetos que vivem nas plantas do Brasil seus parasitos e predadores. Parte II - 1° Tomo. Rio de Janeiro: Ministério da Agricultura, 622 p.), and it has also been reported in the States of Paraíba, Pernambuco, Rio de Janeiro, and Santa Catarina, but not associated with coffee. This species has few hosts, such as Coffea spp., Gonzalagunia spicata, Ixora spp. (Rubiaceae), Chrysophyllum caimito (Sapotaceae), Gossypium spp. (Malvaceae), Jasminum spp. (Oleaceae), Melaleuca spp. (Myrtaceae), and Lacuma caimito (Sapotaceae) (Silva et al. 1968, Hodgson 1994HODGSON CJ. 1994. The scale insect family Coccidae: an identification manual to genera. Wallingford: CAB International, 639 p., Jenkins 2015JENKINS DA. 2015. Alechanochiton marquesi: a new scale species in Puerto Rico. http://entomologylabpr.blogspot.com.br/2013/03/alechanochiton-marquesi-new-scale.html/. Accessed June 13, 2016.
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, García Morales et al. 2016).

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 1994HODGSON CJ. 1994. The scale insect family Coccidae: an identification manual to genera. Wallingford: CAB International, 639 p., Williams and Ben-Dov 2009WILLIAMS DJ AND BEN-DOV Y. 2009. A review of species names combined with the genus name Coccus Linnaeus (Hemiptera: Sternorrhyncha: Coccoidea). Zootaxa 2285: 1-64., Martin and Lau 2011MARTIN JH AND LAU CSK. 2011. The Hemiptera-Sternorrhyncha (Insecta) of Hong Kong, China-an annotated inventory citing voucher specimens and published records. Zootaxa 2847: 1-122., Wang and Feng 2012WANG F AND FENG JN. 2012. A new species of Coccus (Hemiptera, Coccoidea, Coccidae) from China. ZooKeys 244: 59-65.). 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 1991MURPHY ST. 1991. Insect natural enemies of coffee green scales (Hemiptera: Coccidae) in Kenya and their potential for biological control of Coccus celatus and C. viridis in Papua New Guinea. Entomophaga 36: 519-529.), in Papua New Guinea (Hillocks et al. 1999HILLOCKS RJ, PHIRI NA AND OVER D. 1999. Coffee pest and disease management options for smallholders in Malawi. Plantation Prot 18: 199-206.), 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 1991MURPHY ST. 1991. Insect natural enemies of coffee green scales (Hemiptera: Coccidae) in Kenya and their potential for biological control of Coccus celatus and C. viridis in Papua New Guinea. Entomophaga 36: 519-529.). 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 1957FONSECA JP. 1957. Três novas espécies de coccídeos do Brasil, sobre cafeeiro (Homoptera: Coccidae). Arq Inst Biol 24: 123-135., 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. 2013WYCKHUYS KAG, KONDO T, HERRERA BV, MILLER DR, NARANJO N AND HYMAN G. 2013. Invasion of exotic arthropods in South America’s biodiversity hotspots and agro-production systems. In: Peña JE (Ed), Potential Invasive Pests, Wallingford: CAB International, p. 373-400.); 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). Coccus viridis has a great capacity for colonization and adaptation in new areas that may be attributed to their habits of polyphagy and parthenogenetic reproduction (Malumphy and Treseder 2012MALUMPHY C AND TRESEDER K. 2012. Green coffee scale Coccus viridis (Hemiptera: Coccidae), new to Britain. Brit J Entomol Nat Hist 25: 217-225.). Their worldwide hosts include 61 families of plants, and this species has been considered as an important fruit and indoor plant pest in temperate regions (Poole 2005POOLE M. 2005. Green coffee scale Coccus viridis (Green) (Hemiptera: Coccidae). http://www.agric.wa.gov.au/objtwr/imported_assets/content/pw/gcsfactsheet041109.pdf. Accessed April 20, 2016.
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, Waite et al. 2012WAITE G, ELDER R AND CARSON C. 2012. Green coffee scale on fruit trees and ornamental plants. http://www.daff.qld.gov.au/26_17184.htm/. Accessed June 18, 2015.
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, Malumphy and Treseder 2012, García Morales et al. 2016). This coffee scale is associated with Co. arabica, Co. canephora, Co. liberica, and Co. robusta (García Morales et al. 2016), and these associations occur mostly in young host plants (Dekle and Fasulo 2009DEKLE GW AND FASULO TT. 2009. Green scale, Coccus viridis (Green) (Insecta: Hemiptera: Coccidae). Featured creatures. University of Florida’s Institute of Food and Agricultural Sciences. http://entnemdept.ufl.edu/creatures/orn/scales/green_scale.htm/. Accessed June 18, 2014.
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, Fernandes et al. 2009FERNANDES FL, PICANÇO MC, FERNANDES ME, GALDINO TV AND TOMAZ AC. 2009. Perdas causadas por Coccus viridis (Green) (Hemiptera: Coccidae) em mudas de Coffea arabica L. EntomoBrasilis 2: 49-53.). The green coffee scale was considered as the largest Arabica coffee pest in highland areas (> 1,000 m), and it may causes losses in the harvest (Murphy 1991MURPHY ST. 1991. Insect natural enemies of coffee green scales (Hemiptera: Coccidae) in Kenya and their potential for biological control of Coccus celatus and C. viridis in Papua New Guinea. Entomophaga 36: 519-529.). However, it was regarded as an ocasional pest in organic coffee (Vandermeer et al. 2010VANDERMEER J, PERFECTO I AND PHILPOTT S. 2010. Ecological complexity and pest control in organic coffee production: uncovering an autonomous ecosystem service. BioScience 60: 527-537.). Coffee plants infested by Cc. viridis have their growth delayed and may even die (Bittenbender 2000BITTENBENDER HC. 2000. Plantation profile for coffee in Hawaii. http://www.ipmcenters.org/plantationprofiles/docs/hicoffee.html/. Accessed June 20, 2015.
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, Fernandes et al. 2009).

The new finding of S. coffeae in Arabica coffee in the States of Minas Gerais and Espírito Santo (Table I) is an increase range of the species. It is considered cosmopolitan, and found in Afrotropical, Australian, Neartic, Neotropical, Oriental, and Palaearctic regions. This scale insect has been found in the Neotropics in near countries of Brazil such as Argentina, Chile, Colombia, French Guiana, Guiana, and Peru. It has been reported in the Brazilian states of Amazonas, Alagoas, Bahia, Espírito Santo, Minas Gerais, Pará, Paraíba, Paraná, Rio de Janeiro, Rio Grande do Sul, and São Paulo (Table SI). Saissetia spp. (Hemiptera: Coccidae) may cause losses of vigor, spots on the foliage, deformation of plant parts, retard plant growth, and premature death of infested parts (Valand et al. 1989VALAND VM, PATEL JI AND MEHTA DM. 1989. Biology of brown scale (Saissetia coffeae) on pointed gourd (Trichosanthes dioica). Indian J Agricult Sci 59: 610-611.). This is a polyphagous scale species and an important pest of fruit trees and ornamental plants (Peronti et al. 2001PERONTI ALBG, MILLER DR AND SOUSA-SILVA CR. 2001. Scale insects (Hemiptera: Coccoidea) of ornamental plants from São Carlos, São Paulo, Brazil. Insecta Mundi 15: 247-255., Badary 2010). Important commodity plantations in Brazil such as Co. arabica, Co. canephora (Rubiaceae), Citrus aurantium, Ci. aurantifolia, Ci. limon, Ci. reticulata, and Ci. sinensis (Rutaceae) may be damaged by S. coffeae (De Lotto 1956, Ben-Dov 1971, Nakahara 1983NAKAHARA S. 1983. List of the Coccoidea species (Homoptera) of the United States Virgin Islands. United States Department of Agriculture, Plant Protection and Quarantine. APHIS 8142: 1-21., Hamon and Williams 1984HAMON AB AND WILLIAMS ML. 1984. The soft scale insects of Florida (Homoptera: Coccoidea: Coccidae). Arthropods of Florida and Neighboring Land Areas 11: 1-194., González and Lamborot 1989GONZÁLEZ RH AND LAMBOROT L. 1989. El genero Saissetia Deplanche en Chile (Homoptera: Coccidae). Acta Entomol Chil 15: 237-242., Shafee et al. 1989SHAFEE SA, YOUSUF M AND KHAN MY. 1989. Host plants and distribution of coccid pests (Homoptera: Coccoidea) in India. Indian J Syst Entomol 6: 47-55., Williams and Watson 1990, Henderson et al. 2010HENDERSON RC, SULTAN A AND ROBERTSON AW. 2010. Scale insect fauna (Hemiptera: Sternorrhyncha: Coccoidea) of New Zealand’s pygmy mistletoes (Korthalsella: Viscaceae) with description of three new species: Leucaspis albotecta, L. trilobata (Diaspididae) and Eriococcus korthalsellae (Eriococcidae). Zootaxa 2644: 1-24., García Morales et al. 2016).

Pseudaonidia trilobitiformis (Hemiptera: Diaspididae) is first reported occurring in Arabica coffee in Minas Gerais, found in the municipalities of Campos Altos and Ervália (Table I). This species has been worldwide reported on 178 plant species of 45 families (Wolff and Corseuil 1993WOLFF VRS AND CORSEUIL E. 1993. Espécies de Diaspididae (Hom.: Coccoidea) ocorrentes em plantas cítricas no Rio Grande do Sul, Brasil: I - Aspidiotinae. Biociências 1: 25-60., Claps et al. 2001CLAPS LE, WOLFF VRS AND GONZÁLEZ RH. 2001. Catálogo de las Diaspididae (Hemiptera: Coccoidea) exóticas de la Argentina, Brasil y Chile. Rev Soc Entomol Argent 60: 9-34., Peronti et al. 2001PERONTI ALBG, MILLER DR AND SOUSA-SILVA CR. 2001. Scale insects (Hemiptera: Coccoidea) of ornamental plants from São Carlos, São Paulo, Brazil. Insecta Mundi 15: 247-255., Raga et al. 2003RAGA A, MINEIRO JLC AND WOLFF VRS. 2003. Novos registros de hospedeiros de cochonilhas (Hemiptera: Diaspididae, Coccidae) no Estado de São Paulo. Arq Inst Biol 70: 57-60., García Morales et al. 2016). In the Neotropics it has been found in Argentina, Bahamas, Bolivia, Brazil, Colombia, Costa Rica, Ecuador, El Salvador, French Guiana, Galapagos Island, Guadeloupe, Guatemala, Guyana, Haiti, Martinique, Panama, Peru, Puerto Rico & Vieques Island, Saint Martin & St. Barthelemy, Suriname, and Tobago, U.S. Virgin Islands, Uruguay, and Venezuela (Wolff and Corseuil 1993, Kondo 2001KONDO T. 2001. Las cochinillas de Colombia (Hemiptera: Coccoidea). Biota Colomb 2: 31-48., Vasquez et al. 2002VASQUEZ J, DELGADO C, COUTURIER G AND MATILE-FERRERO D. 2002. Harmful insects for the guava tree (Psidium guajava L.: Myrtaceae) in Peruvian Amazonia. Fruits 57: 323-334., Perez-Gelabert 2008, García Morales et al. 2016). It was recorded in the Brazilian states of Bahia, Ceará, Espírito Santo, Minas Gerais, Pará, Paraíba, Paraná, Pernambuco, Rio de Janeiro, Rio Grande do Norte, Rio Grande do Sul, and São Paulo (Table SI). This species may be found in Co. canephora, Ixora coccinea (Rubiaceae), Laurus nobilis (Lauraceae), Murraya paniculata (Myrtaceae), and Nerium oleander (Apocynaceae) in Espírito Santo State (Culik et al. 2008CULIK MP, MARTINS DS, VENTURA JA AND WOLFF VS. 2008. Diaspididae (Hemiptera: Coccoidea) of Espírito Santo, Brazil. J Insect Sci 8: 6. http://insectscience.org/8.17/. Accessed June 20, 2015.
http://insectscience.org/8.17/...
), but not in Arabica coffee. Diaspididae can be considered as a cosmopolitan pest of quarantine importance by the large number of host plants, particularly perennial crops (Miller et al. 2005MILLER DR, MILLER GL, HODGES GS AND DAVIDSON JA. 2005. Introduced scale insects (Hemiptera: Coccoidea) of the United States and their impact on U.S. agriculture. P Entomol Soc Wash 107: 123-158.).

Dysmicoccus texensis was found in the municipality of Manhuaçu, Minas Gerais State (Table I). This is a common species in Colombia coffee plantations (Kondo et al. 2008KONDO T, PORTILLA AAR AND NAVARRO EVV. 2008. Updated list of mealybugs and putoids from Colombia (Hemiptera: Psudococcidae and Putoidea). Bol Mus Entomol Univ Valle 9: 29-53.), and it has been reported in Mexico, and Texas in the USA (Nearctic region), Argentina, Bahamas, Belize, Brazil, Colombia, Costa Rica, Cuba, Dominican Republic, Ecuador, El Salvador, Guadeloupe, Guatemala, Haiti, Jamaica, Mexico, Peru, Puerto Rico & Vieques Island, Trinidad and Tobago, Uruguay, and U.S. Virgin Islands in the Neotropics (Table SI). García Morales et al. (2016), apud Santa-Cecília et al. (2002a) related its occurrence in the Brazilian States of São Paulo (Nakano 1972NAKANO O. 1972. Estudo da cochonilha da raiz do cafeeiro, Dysmicoccus cryptus (Hempel, 1918) comb. n. (Homoptera: Pseudococcidae), PhD. Thesis. Escola Superior de Agricultura Luiz de Queiróz, Universidade de São Paulo. São Paulo, Brasil, 130 p.), Espírito Santo, and Minas Gerais. However, these authors wrote: “Root coffee (Co. arabica) mealybugs (Hemiptera: Pseudococcidae) collected in Boa Esperança, southern Minas Gerais State, were identified as Dysmicoccus texensis (Tinsley) (=bispinosus Beardsley) and those from aerial part collected in Castelo, Espírito Santo State, as Planococcus minor (Maskell)”. The authors did not reported D. texensis occurring in Arabica coffee in Espírito Santo State; thus, the association of D. texensis with Arabica coffee must be considered restricted to the Brazilian States of São Paulo and Minas Gerais. This species was reported in Espírito Santo State infesting Ananas comosus, Cucurbita pepo, Cocos nucifera, Annona sp., and Co. canephora (Culik et al. 2011CULIK MP, WOLF VRS, PERONTI ALBG, BEN-DOV Y AND VENTURA JA. 2011. Hemiptera, Coccoidea: Distribution extension and new records for the states of Espírito Santo, Ceará, and Pernambuco, Brazil. Check List 7: 567-570.). This species occurs on Arabica coffee plantations in several municipalities of São Paulo State and southern Minas Gerais (Nakano 1972), and may infest fruits, roots, and twigs (Santa-Cecília et al. 2002a, Kondo et al. 2008). Its host plants includes 36 plant species of Anacardiaceae, Araceae, Bignoniaceae, Bromeliaceae, Calophyllaceae, Clusiaceae, Cyperaceae, Euphorbiaceae, Fabaceae, Lauraceae, Malvaceae (including Sterculiaceae), Meliaceae, Musaceae, Myrtaceae, Polygonaceae, Rubiaceae, Rutaceae, Solanaceae (Granara de Willink 2009, García Morales et al. 2016). This is a scale species that has occasionally been found on coffee plants (Souza et al. 2008SOUZA B, SANTA-CECÍLIA LVC, PRADO E AND SOUZA JC. 2008. Cochonilhas farinhentas (Hemiptera: Pseudococcidae) em cafeeiros (Coffea arabica L.) em Minas Gerais. Coffee Sci 3: 104-107.). Dactylopius texensis Tinsley, 1900, Dysmicoccus bispinosus Beardsley, 1965, and Pseudococcus texensis Fernald, 1903 are considered junior synonymous (Granara de Willink 2009, García Morales et al. 2016).

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.

ACKNOWLEDGMENTS

We thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa e Inovação do Espírito Santo (FAPES), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), Financiadora de Estudos e Projetos (FINEP) from Brazil, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and Instituto Superior de Entomología (INSUE) from Argentina.

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Publication Dates

  • Publication in this collection
    11 Dec 2017
  • Date of issue
    Oct-Dec 2017

History

  • Received
    07 Oct 2016
  • Accepted
    01 Sept 2017
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