Bioscience Journal | 2022 | vol. 38, e38028 | ISSN 1981-3163 1 Patricia Santos de Castro FERNANDEZ1 , Elen de Lima AGUIAR-MENEZES2 , Aurino Florencio de LIMA2 , Pedro Miller Rangel Mangueira FRADE3 , Alexandre Jacintho TEIXEIRA4 , Carlos Alberto BUCHER5 1 Escritório Local de Seropédica, Empresa de Assistência Técnica e Extensão Rural do Estado do Rio de Janeiro (Emater -Rio), Seropédica, Rio de Janeiro, Brazil. 2 Departamento de Entomologia e Fitopatologia, Universidade Federal Rural do Rio de Janeiro, Seropédica, Rio de Janeiro, Brazil. 3 Undergraduate Course in Agronomic Engineering, Universidade Federal Rural do Rio de Janeiro, Seropédica, Rio de Janeiro, Brazil. 4 Escritório Regional Serrano, Emater-Rio, Nova Friburgo, Rio de Janeiro, Brazil. 5 Departamento de Fitotecnia, Universidade Federal Rural do Rio de Janeiro, Seropédica, Rio de Janeiro, Brazil. Corresponding author: Elen de Lima Aguiar-Menezes Email: emenezes@ufrrj.br How to cite: FERNANDEZ, P.S.C., et al. Aleyrodid (Hemiptera) diversity in hop varieties grown in Brazil. Bioscience Journal. 2022, 38, e38028. https://doi.org/10.14393/BJ-v38n0a2022-54011 Abstract Whiteflies (Hemiptera: Aleyrodidae) are a diverse group of sap-sucking insect species that can cause severe damage in crops with global economic importance. Hops (Humulus lupulus L.) are a crop with considerable value for the brewing and pharmaceutical industries worldwide. The aim of the current study is to register whitefly species associated with this plant in Brazil. Specimens were collected from H. lupulus leaves in four different counties in Rio de Janeiro state (Cachoeiras de Macacu, Cordeiro, Nova Friburgo and Seropédica). Whiteflies belonging to nine genera and distributed in two subfamilies (Aleurodicinae and Aleyrodinae) were identified. Nine hop varieties (i.e., Brazylinsk, Cascade, Chinook, Columbus, Hallertau, Nugget, Saaz, Spalt, and Victoria) are used as host plants by these insects in Brazil. Except for Trialeurodes vaporariorum (Westwood), the other identified species were recorded in hop crops for the first time. Keywords: Humulus lupulus. Aleyrodidae. Host Plant. Plant-Insect Interaction. 1. Introduction Whiteflies (Hemiptera, Aleyrodidae) are sap-sucking insects represented by at least 1,560 species distributed in 161 genera (Martin and Mound 2007; Evans 2008; Ouvrard and Martin 2019). Some of these species are pests that are capable of affecting economically important agricultural crops in different countries; they can cause a greater than 50% yield decrease in infested crops (Kairo et al. 2001; Cassino et al. 2004; Kumar et al. 2016; Wosula et al. 2018; Rincon et al. 2019). Direct levels of economic losses are associated with nymphs and adult individuals who continuously feed on host plants by sucking their phloem sap (Borowiec et al. 2010; Carabalí et al. 2010; Murgianto and Hidayat 2017). Indirect damage can result from honeydew excretion, which functions as a substrate for the growth and proliferation of the fungus species Capnodium spp. This species causes sooty mold disease, which can reduce plants’ photosynthetic and respiratory capacity, as well as the quality or market value of the harvested product (Hilje and Morales 2008). In addition, certain whitefly species, primarily those belonging to complex Bemisia tabaci, can lead to severe economic losses due to virus transmission (Navas-Castillo et al. 2011; Gilbertson et al. 2015). ALEYRODID (HEMIPTERA) DIVERSITY IN HOP VARIETIES GROWN IN BRAZIL https://orcid.org/0000-0002-5032-7285 http://orcid.org/0000-0003-3634-0202 https://orcid.org/0000-0002-9376-9315 https://orcid.org/0000-0001-5204-4476 https://orcid.org/0000-0001-9105-2460 https://orcid.org/0000-0002-2746-816X Bioscience Journal | 2022 | vol. 38, e38028 | https://doi.org/10.14393/BJ-v38n0a2022-54011 2 Aleyrodid (Hemiptera) diversity in hop varieties grown in Brazil Humulus lupulus L. (Cannabaceae), commonly known as hops, is an herbaceous, climbing, and perennial plant that spontaneously grows in hedges and roadsides in temperate climate regions in North America, Asia, and Europe (Small 2016). However, hops are highly valued by the brewing industry, since the female inflorescences (cones) of this plant produce secondary metabolites that impart bitterness, aromas, and antiseptic properties in beer, which is the third most consumed beverage in the world with an origin dating back to 6,000 b.C. (Bocquet et al. 2018; Teixeira and Silva 2019). In addition, hops are also notable as a medicinal plant (Biendl 2009; Franco et al. 2012; Bocquet et al. 2018; Hrnčič et al. 2019). Germany, China, Ethiopia, the United States of America, and the Czech Republic are the main countries growing hops commercially to serve the beer production market, and Argentina is the only South American country presenting significant hop production (Faostat 2020). Some insect species belonging to different orders are hop crop pests in these countries, although these species do not include whiteflies (O’Neal et al. 2015; Dodds 2017; Allan-Perkins et al. 2019). However, there are two whitefly species associated with hops. Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) and the two- spotted spider mite species Tetranychus urticae Koch (Acari: Tetranychidae) are common pests that affect hop crops grown under greenhouse conditions in New Zealand, which is a reference in organic hop production (MPI 2010; Turner et al. 2011). Asterobemisia atraphaxius (Danzig) (Hemiptera: Aleyrodidae) is another whitefly species associated with hops (Evans 2008), although its incidence is only registered in Europe, Iran, Russia, Kazakhstan and Korea (Martin and Mound 2007; Evans 2008; Suh 2009). Although hops species are naturally grown in temperate regions worldwide, they are undergoing adaptation processes to be grown in other climates and present good yield under Brazil’s edaphoclimatic conditions - hop crops have gained public prominence in the country less than five years ago, mainly due to small crops grown in the Mantiqueira Mountains. Currently, there are hop producers in such states as Minas Gerais, Paraná, Rio de Janeiro, Rio Grande do Sul, Santa Catarina, São Paulo and in the Federal District, although there are no estimates regarding the total hop production in Brazil (Fagherazzi et al. 2018; Teixeira and Silva 2019). The Rio de Janeiro state government has launched the first line of credit to encourage hop production to meet the growing demand for this product by artisanal breweries (Schuabb 2019). Phytosanitary issues are expected to emerge due to the increased number of hop crop areas in Brazil. According to Teixeira and Silva (2019), such phytophagous arthropods as Diabrotica speciosa Germar (Coleoptera: Chrysomelidae) and the two-spotted spider mite species T. urticae infest hop crops grown in Cachoeiras de Macacu County, RJ. Spósito et al. (2019) have only reported leaf-cutting ants [Atta sexdens (L.), Atta laevigata (Smith) and Acromyrmex spp., Hymenoptera: Formicidae] as pests affecting commercial hop crops grown in Brazil, although these researchers did not specify regions or states. Nascimento et al. (2019) observed that phytosanitary issues associated with hop crops grown in the Horticulture Department field at UNESP (Botucatu County, SP) were caused by leaf-cutting ants and by two-spotted spider mites. However, the technical and scientific literature lacks report on other insect species associated with hop crops grown in Brazilian states. The aim of this study was to report for the first time the use of H. lupulus as a host plant by whiteflies (Aleyrodidae) in Brazil. 2. Material and Methods The study was conducted in four different counties in Rio de Janeiro state from 08/30th/2019 to 01/21st/2020: Cachoeiras de Macacu (latitude: 22°27’45” S, longitude: 42°39’11” W; altitude: 57 m), Cordeiro (latitude: 22°01’44” S, longitude: 42°21’39” W; altitude: 485 m), Nova Friburgo (latitude 22°16’55” S, longitude: 42°31’52” W; altitude: 846 m) and Seropédica (latitude 22°44’29” S, longitude: 43°42’19” W; altitude: 33 m). Sampling in the first three counties was carried out in 1-year-old commercial hop crops; one property was studied per county. Sampling in Cachoeiras de Macacu County comprised a single hop variety (Cascade). Five hop varieties (Brazylinsk, Cascade, Hallertau, Saaz and Victoria) were sampled in Cordeiro County. Plants belonging to these same varieties, in addition to Nugget and Spalt, were sampled in a property in Nova Friburgo County. Sampling in Seropédica County was performed in two different locations: in the greenhouse of the Department of Soils (DS) of the Agronomy Institute of Federal Rural University of Rio de Janeiro (UFRRJ), where Cascade, Chinook, Columbus, Nugget and Saaz hop seedlings were inspected, and in the Bioscience Journal | 2022 | vol. 38, e38028 | https://doi.org/10.14393/BJ-v38n0a2022-54011 3 FERNANDEZ, P.S.C., et al. Integrated System of Agroecological Production (SIPA - Sistema Integrado de Produção Agroecológica) (Neves et al. 2005), where 3 one-year-old Cascade hop plants were grown. Leaves were randomly inspected with a 20x pocket magnifying glass; samples were collected when leaves were infested by nymphs belonging to different whitefly instars and packed in transparent 250-ml plastic pots to be transported to the laboratory of Ângelo Moreira da Costa Lima Entomological Collection (CECL) of the Entomology and Phytopathology Department (DEnF) of the Institute of Biological and Health Sciences (ICBS) at UFRRJ (Seropédica County, RJ), where they were identified by the research group’s specialist, A.F. LIMA, based on several authors (Quaintance and Baker 1913, 1914, 1917; Baker and Moles 1921; Bondar 1923; Costa Lima 1928, 1942; Martin 1987, 1999, 2004, 2005, 2008; Hodges and Evans 2005; Dubey and Sundararaj 2015). Fourth instar aleyrodid nymphs (‘pupae’) were removed from the leaf blade with the aid of an entomological pin and mounted on Hoyer’s and/or Canada Balm medium between slides and coverslips. Slides were labeled with information regarding hop variety, location, date, and collector; next, the slides were placed in an oven to dry at 37°C for at least 48 hours. Species identification was performed under stereoscopic (Wild M 5 and Olympus SZ 40) and optical (Wild M 20 and Olympus BX 41) microscopes. Identified specimens were deposited at the CECL of DEnF/ICBS/UFRRJ. Whitefly pupae-infested leaves of Cascade and Nugget seedlings kept in the DS/UFRRJ greenhouses were also photographed, placed in transparent 500-ml plastic pots with lids and kept in the laboratory of the Integrated Pest Management Center (CIMP)/DEnF/ICBS/UFRRJ under controlled environmental conditions (25 ± 1°C, 60 ± 10% RH and 12-h photoperiod) to enable researchers to observe the likely emergence of adult individuals. 3. Results and Discussion Identified whiteflies (Hemiptera: Aleyrodidae) belonged to nine different genera: two belonged to the subfamily Aleurodicinae (Aleurodicus Douglas and Nealeurodicus Hempel), whereas seven belonged to the subfamily Aleyrodinae (Aleurothrixus Quaintance & Baker, Aleurotrachelus Quaintance & Baker, Aleurotulus Quaintance & Baker, Bemisia Quaintance & Baker, Parabemisia Takahashi, Tetraleurodes Cockerell and Trialeurodes Cockerell) (Table 1). Eight species and seven morphospecies (i.e., new species to be described in the future) were identified. Table 1. List of whitefly species (Hemiptera: Aleyrodidae) collected in hops grown in four counties in Rio de Janeiro state from 08/30th/2019 to 01/21st/2020 (x = detected; - = not detected). Whitefly Cachoeiras de Macacu Cordeiro Nova Friburgo Seropédica DS SIPA 1. Aleurodicus pulvinatus (Maskell) - - - x - 2. Aleurothrixus trachoides (Back) - - x - - 3. Aleurotrachelus sp.1 - - x - - 4. Aleurotulus mundururu Bondar - - - x - 5. Aleurotulus sp.1 - - x - - 6. Bemisia tabaci (Gennadius) x x x x - 7. Bemisia tuberculata Bondar x - - x - 8. Bemisia sp.1 - x x x - 9. Bemisia sp.2 - - x - - 10. Bemisia sp.3 - - x - - 11. Nealeurodicus moreirai (Costa Lima) - x x - - 12. Parabemisia myricae (Kuwana) - x x - - 13. Tetraleurodes sp.1 - - x - x 14. Trialeurodes vaporariorum (Westwood) - x x - - 15. Trialeurodes sp.1 - - x - - Total number of species 2 5 12 5 1 Except for T. vaporariorum, the other whitefly species identified in the present study were reported in association with hops for the first time (Evans 2008; MPI 2010). However, all of these species have already Bioscience Journal | 2022 | vol. 38, e38028 | https://doi.org/10.14393/BJ-v38n0a2022-54011 4 Aleyrodid (Hemiptera) diversity in hop varieties grown in Brazil been reported to associate with other host plants in Brazil (Martin and Mound 2007; Sottoriva et al. 2011; Alonso et al. 2012; Trindade et al. 2012; Gamarra et al. 2016; Kumar et al. 2016; Ouvrard and Martin 2019). Bemisia tabaci (Gennadius) was the only species recorded in all four investigated counties (Table 1). Therefore, this whitefly species was capable of infesting seedling leaves grown under greenhouse conditions (Seropédica County), as well as leaves of adult plants grown in the field (Cachoeiras de Macacu, Cordeiro and Nova Friburgo counties); however, this species was not found in adult plants grown at SIPA. The aforementioned species is distributed worldwide in association with more than 250 host plant species belonging to different families (Evans 2008). It is acknowledged as a species complex that is capable of causing severe damage to crops with significant global economic importance, mainly due to its ability to transmit phytoviruses (Navas-Castillo et al. 2011; Gilbertson et al. 2015). Bing et al. (2014) conducted a study in China and reported that B. tabaci infests Humulus scandens (Lour.) Merr. (Cannabaceae), which is known as Japanese or wild hops, although it is not commercially grown. Aleurothrixus trachoides (Back), Aleurotrachelus sp.1, Bemisia sp.2, Bemisia sp.3 and Trialeurodes sp.1 were only recorded in Nova Friburgo County (Table 1). Aleurothrixus trachoides, commonly known as solanaceae whitefly or pepper whitefly, is an important pest affecting pepper crops in the United States. This polyphagous species is native to the neotropical region and widely distributed in Central and South America (including the Caribbean) and in India. Although this species is associated with more than 70 host plant species distributed in 34 botanical families, it prefers plants belonging to families Solanaceae and Convolvulaceae and palm trees belonging to genus Chamaedorea Willd. (Arecaceae) (Dubey and Sundararaj 2015; Kumar et al. 2016; Wosula et al. 2018; Ouvrard and Martin 2019). The other identified species were simultaneously recorded in two or three counties. Bemisia sp.1 was recorded in three counties (Cordeiro, Nova Friburgo and Seropédica). Species simultaneously recorded in two counties comprised Bemisia tuberculata Bondar (Cachoeiras de Macacu and Seropédica), Nealeurodicus moreirai (Costa Lima), Parabemisia myricae (Kuwana) and T. vaporariorum (Cordeiro and Nova Friburgo). Nova Friburgo County has also recorded the incidence of Tetraleurodes sp.1, which was also found in Seropédica County. The largest number of Aleyrodidae species was recorded in Nova Friburgo County. Alonso et al. (2012) were the first researchers to record B. tuberculata infesting cassava leaves (Manihot esculenta Crantz, Euphorbiaceae) in Rio de Janeiro state. This whitefly species has other plant hosts belonging to the family Euphorbiaceae (Euphorbia hypericifolia L.) and it also infests plants belonging to the family Fabaceae (Erythrina sp.) and Malvaceae (Gossypium hirsutum L.) (Evans 2008). Families Annonaceae (Annona squamosa L.), Sapotaceae [Manilkara zapota (L.) P. Royen] and Arecaceae (unidentified palm species) are known in Brazil as host plants to N. moreirai (Howard 2001; Evans 2008). Parabemisia myricae, which is associated with approximately 80 host plant species distributed in 35 families, was first reported in Japan in 1924; this species caused severe damage to mulberry crops in the following year and has subsequently spread to all continents and reached approximately 20 countries, including Brazil (Franco et al. 1996; Evans 2008; Sottoriva et al. 2011; Ouvrard and Martin 2019). Trialeurodes vaporariorum is a common pest that affects hops grown under greenhouse conditions in New Zealand (MPI 2010). Based on the present study, this species was collected in the field in Cordeiro County in association with the hop varieties Saaz and Hallertau; the Hallertau hop variety was also infested by this aleyrodid insect in Nova Friburgo County (Table 2). This whitefly species is significantly distributed worldwide and is reported as a pest affecting vegetables and ornamental plants grown in more than 50 countries; however, this species has a wide list of host plants, which comprise approximately 270 species (Gamarra et al. 2016; Ouvrard and Martin 2019). Bioscience Journal | 2022 | vol. 38, e38028 | https://doi.org/10.14393/BJ-v38n0a2022-54011 5 FERNANDEZ, P.S.C., et al. Table 2. Whiteflies associated with hop varieties grown in different counties in Rio de Janeiro state from 08/30th/2019 to 01/21st/2020. Variety Whitefly Brazylinsk Bemisia tabaci, Bemisia sp.2, Parabemisia myricae, Trialeurodes sp.1 Cascade Aleurodicus pulvinatus, Aleurotrachelus sp.1, Bemisia sp.1, Bemisia sp.3, Bemisia tabaci, Bemisia tuberculata, Nealeurodicus moreirai, Parabemisia myricae, Tetraleurodes sp.1 Chinook Aleurodicus pulvinatus Columbus Bemisia tabaci, Bemisia tuberculata Hallertau Aleurothrixus trachoides, Bemisia tabaci, Parabemisia myricae, Trialeurodes vaporariorum Nugget Aleurodicus pulvinatus, Aleurotulus sp1. Saaz Aleurotulus mundururu, Bemisia sp.2, Bemisia tabaci, Parabemisia myricae, Tetraleurodes sp.1, Trialeurodes vaporariorum Spalt Bemisia sp.2 Victoria Bemisia sp.1, Nealeurodicus moreirai, Parabemisia myricae The hop variety Cascade recorded the largest number of whitefly species (n = 9) followed by Saaz (n = 6), Brazylinsk and Hallertau (n = 4, each) (Table 2). Two whitefly species were collected in the hop varieties Columbus and Nugget. Chinook and Spalt were infested with a single whitefly species. Whiteflies belonging to the genus Bemisia Quaintance & Baker infested almost all hop varieties, except for Chinook and Nugget. Aleurotulus mundururu Bondar and A. trachoides infested one of the nine hop varieties, whereas N. moreirai infested two, and P. myricae infested five. Aleurodicus pulvinatus (Maskell) and A. mundururu specimens were only collected from Cascade, Chinook, and Nugget seedlings in Seropédica County (Table 2). All the A. pulvinatus developmental stages (eggs, nymphs from different instars and adults, both male and female) were recorded in the leaves of these hop varieties (Figure 1). Fourth instar nymphs (‘pupae’) kept in Nugget and Cascade leaves were capa ble of developing into adult individuals in the laboratory. These results indicate that H. lupulus is a suitable plant species for A. pulvinatus development. However, further research is warranted to determine the potential of this whitefly species as a pest in hop plants based on its biology. Figure 1. A - abaxial face of Humulus lupulus leaf (Chinook variety) infested by Aleurodicus pulvinatus adults on 9/27th/2019; B - abaxial face of H. lupulus leaves (Nugget variety) infested by A. pulvinatus nymphs on 10/21st/2019; C - abaxial face of H. lupulus leaf (Cascade variety) infested by A. pulvinatus nymphs near the petiole on 10/21st/2019; D - approximate view of 4th instar A. pulvinatus nymphs (‘pupae’) on the abaxial face of H. lupulus leaf (Nugget variety). Bioscience Journal | 2022 | vol. 38, e38028 | https://doi.org/10.14393/BJ-v38n0a2022-54011 6 Aleyrodid (Hemiptera) diversity in hop varieties grown in Brazil Aleurotulus mundururu was first identified in Brazil in the botanical family Melastomataceae (Miconia sp.) in 1923. Subsequent records also included species Strychnos sp. (Loganiaceae) as a host, as well as its incidence in Belize, Costa Rica, Ecuador, Guyana, and Trinidad (Evans 2008; Ouvrard and Martin 2019). Aleurodicus pulvinatus, which is native to Central America, South America and several Caribbean islands, is a pest species affecting coconut trees (Cocos nucifera L., Arecaceae) and many ornamental plants, although it is associated with approximately 19 botanical families (Kairo et al. 2001; Evans 2008; Ouvrard and Martin 2019). 4. Conclusions Whiteflies (Hemiptera: Aleyrodidae) belonging to nine genera and fifteen species (Aleurodicus pulvinatus, Aleurothrixus trachoides, Aleurotrachelus sp.1, Aleurotulus mundururu, Aleurotulus sp.1, Bemisia tabaci, Bemisia tuberculata, Bemisia sp.1, Bemisia sp.2, Bemisia sp.3, Nealeurodicus moreirai, Parabemisia myricae, Tetraleurodes sp.1, Trialeurodes vaporariorum and Trialeurodes sp.1) are associated with nine hop varieties (Brazylinsk, Cascade, Chinook, Columbus, Hallertau, Nugget, Saaz, Spalt and Victoria) distributed in Cachoeiras de Macacu, Cordeiro, Nova Friburgo and Seropédica counties (RJ). This study presents the first record of aleyrodids in Humulus lupulus in Brazil. Authors' Contributions: FERNANDEZ, P.S.C.: conception and design, acquisition of data, analysis and interpretation of data, writing the original draft; AGUIAR-MENEZES, E.L.: conception and design, acquisition of data, analysis and interpretation of data, critical review of important intellectual content; LIMA, A.F.: acquisition of data, analysis and interpretation of data, identifying the insect species, critical review of important intellectual content; FRADE, P.M.R.: conception and design, acquisition of data; TEIXEIRA, A.J.: conception and design, critical review of important intellectual content; BUCHER, C.A.: conception and design, critical, review of important intellectual content. All authors have read and approved the final version of the manuscript. Conflicts of Interest: The authors declare no conflicts of interest. Ethics Approval: Not applicable. Acknowledgments: The authors are grateful to the Post-Graduation Program in Organic Agriculture (PPGAO - Programa de Pós-Graduação em Agricultura Orgânica) at Federal Rural University of Rio de Janeiro for the opportunity given to the first author to conduct this study as part of her Master’s dissertation and to producers Carlos Alberto Lopes Pereira (Sertão Farm, Cachoeiras de Macacu County, RJ), Moema Pombo Celles Cordeiro (Paulo Cordeiro Hop Nursery, Amparo, Nova Friburgo County, RJ) and Vinício Salles Monnerat (Bonsucesso Farm, Cordeiro County, RJ) for allowing leaf collections to be carried out in their hop crops. References ALLAN-PERKINS, E., MAURER, K. and LAMONDIA, J. Guidelines for integrated pest management for hops in Connecticut. New Haven: The Connecticut Agricultural Experiment Station, 2019. Available from: https://portal.ct.gov/- /media/CAES/DOCUMENTS/Publications/Bulletins/B1057.pdf?la=en ALONSO, R.S., RACCA-FILHO, F. and LIMA, A.F. 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Received: 7 December 2020 | Accepted: 21 August 2021 | Published: 24 May 2022 This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. https://doi.org/10.1146/annurev-phyto-072910-095235 https://www.gbif.org/dataset/c70d7f06-1ef8-448b-966a-498a4d697fc4 https://doi.org/10.5479/si.00963801.51-2156.335 https://ufdc.ufl.edu/AA00017576/00002/1j https://ufdc.ufl.edu/AA00017576/00001 https://doi.org/10.1016/j.cropro.2019.01.002 https://www.portalmultiplix.com/noticias/economia/cultivadores-de-lupulo-da-regiao-serrana-terao-linha-de-credito-no-banco-do-brasil https://doi.org/10.1080/14888386.2016.1199327 https://www.researchgate.net/publication/334672293_A_Cultura_do_Lupulo https://doi.org/10.1016/j.aspen.2008.11.002 https://issuu.com/redelupulo/docs/nota_tecnica_lupulo_emater_rio http://saber.ucv.ve/ojs/index.php/rev_ento/article/view/7338 https://doi.org/10.2134/agronj2011.0131