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SEMIAPHIS DAUCI (FABRICIUS) (INSECTA, HEMIPTERA, APHIDIDAE) – FORMAL RECORD OF OCCURRENCE ON ARRACACHA (ARRACACIA XANTHORRHIZA BANCR.) (APIACEAE) IN BRAZIL, MORPHOLOGICAL CHARACTERIZATION, DESCRIPTION OF DAMAGES AND ARTHROPODS ASSOCIATED TO THE CULTURE

SEMIAPHIS DAUCI (FABRICIUS) (INSECTA, HEMIPTERA, APHIDIDAE) – REGISTRO FORMAL DE OCORRÊNCIA EM MANDIOQUINHA–SALSA (ARRACACIA XANTHORRHIZA BANCR.) (APIACEAE) NO BRASIL, CARACTERIZAÇÃO MORFOLÓGICA, DESCRIÇÃO DOS DANOS E ARTRÓPODES RELACIONADOS À CULTURA

ABSTRACT

This paper reports formally the occurrence and describes the damages by Semiaphis dauci (Fabricius, 1775) (Insecta, Hemiptera, Aphididae, Aphidinae, Macrosiphini) on arracacha (Arracacia xanthorrhiza Bancr.) (Apiaceae) in Brazil. The infestation was initially noted on April/2002 at Núcleo de Produção de Mudas, Departamento de Sementes Mudas e Matrizes, Coordenadoria de Assistência Técnica Integral, Secretaria de Agricultura e Abastecimento, São Bento do Sapucaí, State of São Paulo. Posteriorly the occurrence was detected in other parts of the municipality of São Bento do Sapucaí such as Serrano, Paiol Grande and Cantagalo, being the incidence higher in localities at lower altitudes. The colonies, with large number of individuals, were settled on both sides of the leaves and also hidden under petiole, but with lower number of specimens. The adult plants were underdeveloped and the growing of aphid colonies induced the blossoming. In the seedlings the symptoms were severer with reduction in the development and death of plants. When the colonies were placed in the dorsal side of the leaves, there was a tendency to wrinkling and rolling to upper side that was used as shelter by the aphids. Morphological characterization, illustrations and notes on biology of .. dauci and a survey of the Arthropoda related with .. xanthorrhiza are also presented.

KEY WORDS
Aphidinae; Apiaceae; arracacha; Arracacia xanthorrhiza ; Macrosiphini; Semiaphis dauci

RESUMO

Este trabalho efetua o registro formal de ocorrência e descreve os danos de Semiaphis dauci (Fabricius, 1775) (Insecta, Hemiptera, Aphididae, Aphidinae, Macrosiphini) em cultura de mandioquinha-salsa (Arracacia xanthorrhiza Bancr.) (Apiaceae) no Brasil. A infestação foi observada, inicialmente, em abril/2002, no Núcleo de Produção de Mudas, Departamento de Sementes Mudas e Matrizes, Coordenadoria de Assistência Técnica Integral, Secretaria de Agricultura e Abastecimento, São Bento do Sapucaí, SP. Posteriormente, a ocorrência foi detectada em outras localidades do município como Serrano, Paiol Grande e Cantagalo sendo que a incidência foi maior nas áreas de menor altitude. As colônias estavam localizadas em ambas as faces das folhas, e em menor número no pecíolo escondidas na bainha da folha. As plantas adultas apresentavam subdesenvolvimento e o aumento das colônias induzia o florescimento. Nas mudas os sintomas foram mais severos com redução no desenvolvimento e posterior morte das plantas. Quando havia formação de colônias na superfície superior das fo-lhas, havia tendência de encarquilhamento e enrolamento para cima, servindo de abrigo para os pulgões. Caracterização morfológica, ilustrações, notas sobre a biologia de .. dauci e levantamento dos Arthropoda relacionados com .. xanthorrhiza também são apresentados.

PALAVRAS-CHAVE
Aphidinae; Apiaceae; mandioquinha-salsa; Arracacia xanthorrhiza ; Macrosiphini; Semiaphis dauci

INTRODUCTION

In Brazil due geography, history, and social and cultural reasons, exotic plant species are frequently introduced without adequate phytosanitary control. As many of them have horticultural, forestry, medical and ornamental importance they are quickly spread through many areas. The human factor associated with propitious whether favor the introduction and establishment of many pests, especially the aphids (Insecta, Hemiptera, Sternorrhyncha, Aphidoidea), previously absent and that are associated with these plants.

The present geographical distribution of aphid species is result of a long historical process in which natural causes and man action are the most important actors. Their occurrence in certain places is closely related to presence of genera and/or species of plants that serve as hosts along with prevalence of adequate climatic conditions (Mier Durante; Nieto Nafría, 1994MIER DURANTE, M.P.; NIETO NAFRÍA, J.M. Species of the Spanish aphidfauna with discontinuous geographical distribution. Journal of Aphidology, v.8, n.1/2, p.72-78, 1994.; Dixon, 1998DIXON, A.F.G. Aphid ecology. 2ed. London: Chapman and Hall, 1998. 300p.; Holman, 1974HOLMAN, J. Los áfidos de Cuba. La Habana: Instituto Cubano del Libro, 1974. 304p.).

Aphids or plantlices (Aphididae) constitute a large group of small, soft–bodied insects that are frequently found in large numbers on leaves or steams of plants (Triplehorn; Johnson, 2005TRIPLEHORN, C.A.; JOHNSON, N.F. Order Hemiptera, true bugs, cicadas, hoppers, psyllids, whiteflies, aphids, and scale insects. In: TRIPLEHORN, C.A.; JOHNSON, N.F. (Ed.). Borror and DeLong’. Introduction to the study of insects. 7.ed. Belmont: Thomson Learning, 2005. chap.22. p.268-332.). The family is widely distributed and includes about 350 genera and 3,500 species (Kosztarab, 1982KOSZTARAB, M. Homoptera. In: PARKER, S.P. (Ed.). Synopsis and classification of living organisms. New York: McGraw-Hill, 1982. v.2., p.447-470, pls. 117, 118.).

Due to their biological characteristics they are one of the most important groups of insects on agronomic point of view and when present in the cultures they are able to cause severe economic losses (Delfino, 2005DELFINO, M.A. Inventario de las asociaciones áfido–planta en el Perú. Ecología Aplicada, v.4, n.1/2, p.143-158, 2005.). Therefore, any information concerning their relationships with host plants and geographical distribution of each species are considered of great importance.

A large number of species damages cultivated plants, including vegetables, forestry and ornamentals. The main troubles caused by their action over the plants are: (i) the sucking activity removes sap and injects saliva that can cause stunting of the shoots, galls or deformation and discoloration of leaves, twigs, flowers and fruits; (ii) may serve as vectors of phytovirus; and (iii) excrete honeydew on which sooty mold grows, interfering in the photosynthesis (Kosztarab, 1982KOSZTARAB, M. Homoptera. In: PARKER, S.P. (Ed.). Synopsis and classification of living organisms. New York: McGraw-Hill, 1982. v.2., p.447-470, pls. 117, 118.; Blackman; Eastop, 2000BLACKMAN, R.L.; EASTOP, V.F. Aphids on the world’. crops. an identification and information guide. Chichester: John Wiley & Sons., 2000. 466p.).

The genus Semiaphis van der Goot, 1913GOOT, P. VAN DER. Zur Systematik der Aphiden. Tijdschrift voor Entomologie, v.56, n.1/2, p.69-155, 1913. is included in subfamily Aphidinae, tribe Macrosiphini (Blackman; Eastop, 2000BLACKMAN, R.L.; EASTOP, V.F. Aphids on the world’. crops. an identification and information guide. Chichester: John Wiley & Sons., 2000. 466p.). Semiaphis dauci (Fabricius, 1775FABRICIUS, J.C. Systema Entomologiae. sistens insectorum classes. ordines. genera. species. adiectis synonymis. locis. descriptionibus. observationibus. Flensburgi & Lipsiae: Officina Libraria Kortii, 1775. xxvii + 832p.) is originally a Eurosiberian species and nowadays is widely distributed in Europe, Turkey, Israel, Siberia and Central Asia (Heie, l992HEIE, O.E. The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. IV. Family Aphididae: part 1 of tribe Macrosiphini of subfamily Aphidinae. Fauna Entomologica Scandinavica, v.25, p.1-189, 1992.). In South America, previous notes on occurrence of this species were made by Delfino et al. (2005)DELFINO, M.; DAPOTO, G.; GIGANTE, H.; BERNAT, M. Primera cita para Argentina de Semiaphis dauci (Fabricius) y para la Patagonia de Dysaphis foeniculus (Theobald) (Hem.: Aphididae) en zanahoria. In: CONGRESO LATINOAMERICANO DE HORTICULTURA, 12. & CONGRESO ARGENTINO DE HORTICULTURA, 28., 2005, General Roca, Río Negro. Resúmenes. General Roca: 2005. p. 312. on carrot (Daucus carota L. - Apiaceae) in Argentina and by Yuki et al. (2006)YUKI, V.A.; DELFINO, M.A.; TAKADA, H.M.; HOJO, H.; IDE, S.; PERONTI, A.L.B.G.; BROMBAL, J.C.; SOUSA-SILVA, C.R.; BUENO, S.C.S. Primeiro registro de Semiaphis dauci (Fabricius) (Hemiptera, Aphididae) em cultura de mandioquinha-salsa (Arracacia xanthorrhiza Bancr. var. Senador Amaral - Apiaceae) no Brasil. O Biológico, São Paulo, v.68, abstract 059/452. Suplemento 2. Presented in REUNIÃO ANUAL DO INSTITUTO BIOLÓGICO, 19., 2006, São Paulo, SP. São Paulo: 2006. Available in: <http://www.biologico.sp.gov.br/biologico/v68_supl_raib/059.PDF>. Access in: 28 Jun. 2007.
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on arracacha (Arracacia xanthorrhiza Bancr. - Apiaceae) in Brazil.

Arracacia xanthorrhiza has, as most commonly used vernacular name, arracacha, which is derived from Quechua word racacha. Arracacha has also been accepted as the standard term in the English literature and names such as Peruvian carrot or Peruvian parsnip are confusing and their use in the literature should be discontinued (Hermann, 1997HERMANN, M. Arracacha. Arracacia xanthorrhiza Bancroft. In: HERMANN, M.; HELLER, J. (Ed.). Andean roots and tubers: ahipa, arracacha, maca and yacon. Promoting the conservation and use of underutilized and neglected crops. Rome: International Plant Genetic Resources Institute, 1997. v.1. p.75-172.). In Brazil, it is popularly known as batata-aipo, batata-baroa, batata-cenoura, batata-fiúza, batata-jujuba, batata-salsa, batata-suíça, batata-tupinambá, cenoura-amarela, mandioca-salsa, mandioquinha, mandioquinha-salsa and pastinaca (Hermann, 1997HERMANN, M. Arracacha. Arracacia xanthorrhiza Bancroft. In: HERMANN, M.; HELLER, J. (Ed.). Andean roots and tubers: ahipa, arracacha, maca and yacon. Promoting the conservation and use of underutilized and neglected crops. Rome: International Plant Genetic Resources Institute, 1997. v.1. p.75-172.; Pistrick, 2001; United..., 2007). In other Latin American countries, it is known as arracacha, huia sampilla, lacache, oqqe and racacham in Bolivia; lacache in Chile; arocueche, arracacha, guaud, huahué, pacucarrá, sacarracacha, yengó and zanahoria in Colombia; afió in Cuba; zanahoria in Ecuador; arracacha, huisampilla, lacache, racacha, ricacha, virraca, zanahoria blanca and zanahoria in Peru; apio in Puerto Rico; apio, apio criollo, arecate or arrecate, aricachi, arracacha, kui–titsí and racacha in Venezuela (Hermann, 1997HERMANN, M. Arracacha. Arracacia xanthorrhiza Bancroft. In: HERMANN, M.; HELLER, J. (Ed.). Andean roots and tubers: ahipa, arracacha, maca and yacon. Promoting the conservation and use of underutilized and neglected crops. Rome: International Plant Genetic Resources Institute, 1997. v.1. p.75-172.; Pistrick, 2001PISTRICK, K. Arracacia xanthorrhiza Bancroft (1825). In: HANELT, P.; LEIBNIZ–INSTITUT FÜR PFLANZENGENETIK UND KULTURPFLANZENFORSCHUNG (Ed.). Mansfeld’. encyclopedia of agricultural and horticultural crops [online]. Gatersleben: Leibniz–Institut für Pflanzengenetik und Kulturpflanzenforschung, 2001. Available in: <http://mansfeld.ipk–gatersleben.de/Mansfeld/Taxonomy/datenvoll.afp?module=mf&source=botnam&taxid=1147&akzanz=0&rehm=0>. Access in: 13 Jun. 2007.
http://mansfeld.ipk–gatersleben.de/Mansf...
; United..., 2007UNITED STATES. Agricultural Research Service. Germplasm Resources Information Network. Arracacia xanthorrhiza Bancr. Available in: <http://www.ars–grin.gov/cgi–bin/npgs/html/taxon.pl?4256>. Access in: 13 Jun. 2007.
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).

Zanin; Casali (1984)ZANIN, A.C.W.; CASALI, V.W.D. Origem, distribuição geográfica e botânica da mandioquinha-salsa. Informe Agropecuário, v.10, n.120, p.9-11, 1984. presented circumstantial evidence for the introduction of arracacha to Brazil early in last century. The culture must have been spread quickly since it was widely consumed as early as in the 1920s in rural areas of Minas Gerais, São Paulo and Rio de Janeiro. Today, arracacha is mostly grown in the uplands of southern and southeastern Brazil, particularly in the Serra do Mar (Paraná, São Paulo, ca. 26° S), in the Serra da Mantiqueira (São Paulo, Minas Gerais, 22° - 23° S, 1,000 - 1,800 m), in the Serra do Espinhaço (Minas Gerais, 16° S, under 1,000 m), and the Planalto Central (Minas Gerais, Goiás, Tocantins, 15° - 18° S, 800 - 1,000 m). According to an extensive survey the four foremost arracacha-producing states in 1993 were Minas Gerais (3,500 ha), Paraná (2,800 ha), Santa Catarina (850 ha) and Espírito Santo (660 ha). The area is expanding in Espírito Santo and Minas Gerais and total national area in 1996 is estimated to exceed 12,000 ha. Moreover, the area under arracacha shows high growth rates in Goiás and Tocantins, states to which arracacha culture was introduced a few years ago. In São Paulo, where arracacha was in the 1960s a source of “great wealth” (Normanha; Silva, 1963NORMANHA, E.S.; SILVA, J.R. Mandioquinha-salsa tem vários problemas. Coopercotia, v.20, n.16, p.36-38, 1963.) and grown to a larger extent than in any other federal state, arracacha production has been reduced to some 200 ha in the 1992/1993 growing season (Monteiro et al., 1993MONTEIRO, D.A.; TREMOCOLDI, W.A.; LORENZI, J.O.; PERESSIN, V.A. A realidade da mandioquinha-salsa no estado de São Paulo. . Agronômico, v.45, n.2/3, p.20-25, 1993.). Booming service industries have forced out arracacha culture around metropolitan area of São Paulo. For example, the former arracacha–growing municipality of Piedade near São Paulo nowadays acts as a transshipment point for arracacha from all over Brazil. Piedade no longer produces arracacha, but washes, classifies and packs arracacha from other states for sale on the wholesale market Companhia de Entrepostos e Armazéns Gerais de São Paulo, São Paulo (Hermann, 1997HERMANN, M. Arracacha. Arracacia xanthorrhiza Bancroft. In: HERMANN, M.; HELLER, J. (Ed.). Andean roots and tubers: ahipa, arracacha, maca and yacon. Promoting the conservation and use of underutilized and neglected crops. Rome: International Plant Genetic Resources Institute, 1997. v.1. p.75-172.).

Arracacha is typically grown by small farmers with less than 1 ha of arracacha per holding. Yields average 6 - 14 t/ha in Paraná and Minas Gerais (Hamerschmidt, 1984HAMERSCHMIDT, I. A cultura da mandioquinha-salsa no Estado do Paraná. In: ENCONTRO DE TÉCNICOS DE ENSINO, PESQUISA E EXTENSÃO RURAL SOBRE A CULTURA DA MANDIOQUINHA-SALSA, 1984, Barbacena, MG. Relatório. Belo Horizonte: 1984. p.28-30.; Santos, 1984SANTOS, J. A. Cultura da mandioquinha-salsa na região de Muriaé-MG. In: ENCONTRO DE TÉCNICOS DE ENSINO, PESQUISA E EXTENSÃO RURAL SOBRE A CULTURA DA MANDIOQUINHA-SALSA, 1984, Barbacena, MG. Relatório. Belo Horizonte: 1984. p.21-24.), 15 - 30 t/ha in São Paulo, with irrigation (Monteiro et al., 1993MONTEIRO, D.A.; TREMOCOLDI, W.A.; LORENZI, J.O.; PERESSIN, V.A. A realidade da mandioquinha-salsa no estado de São Paulo. . Agronômico, v.45, n.2/3, p.20-25, 1993.) and a nation–wide mean of 8 t/ha has been reported. Plantings are year-round, with marketed volumes reaching a maximum between July and September when prices are lowest.

Arracacha is generally regarded as a robust culture with few disease or pest problems if it is appropriately rotated. But insects, bacteria and fungi can cause significant damage.

This paper records formally the occurrence of S. dauci on A. xanthorrhiza in Brazil based on previous note by Yuki et al. (2006)YUKI, V.A.; DELFINO, M.A.; TAKADA, H.M.; HOJO, H.; IDE, S.; PERONTI, A.L.B.G.; BROMBAL, J.C.; SOUSA-SILVA, C.R.; BUENO, S.C.S. Primeiro registro de Semiaphis dauci (Fabricius) (Hemiptera, Aphididae) em cultura de mandioquinha-salsa (Arracacia xanthorrhiza Bancr. var. Senador Amaral - Apiaceae) no Brasil. O Biológico, São Paulo, v.68, abstract 059/452. Suplemento 2. Presented in REUNIÃO ANUAL DO INSTITUTO BIOLÓGICO, 19., 2006, São Paulo, SP. São Paulo: 2006. Available in: <http://www.biologico.sp.gov.br/biologico/v68_supl_raib/059.PDF>. Access in: 28 Jun. 2007.
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. Morphological characterization, illustrations, notes on biology of the aphid and description of the damages and a survey of the Arthropoda related with A. xanthorrhiza are also presented.

MATERIAL AND METHODS

The survey was carried out on April/2002 at Núcleo de Produção de Mudas (NPM), Departamento de Sementes Mudas e Matrizes, Coordenadoria de Assistência Técnica Integral, Secretaria de Agricultura e Abastecimento, São Bento do Sapucaí/SP. The municipality of São Bento do Sapucaí (22º 40’ 53.6” S, 45º 44’ 37.6” W) in the east side of Serra da Mantiqueira at 864 m a. s. l., about 200 km east of city of São Paulo. On March/2003 with the increase in the damages and losses, specimens were collected in arracacha seedlings production area at NPM and send to one of the authors (MAD) for identification. In the same year, infestations were reported by small farmers mainly from Serrano, Paiol Grande and Cantagalo, districts of São Bento do Sapucaí. The infestation levels were inversely proportional to the altitude of the place where the farm was located.

Plants highly infested with aphids were collected in field cultures of arracacha in São Bento do Sapucaí, SP, put in plastic bags and taken to Laboratório de Vetores, Centro de Pesquisa e Desenvolvimento de Fitossanidade, Instituto Agronômico de Campinas, Campinas, São Paulo. The aphids were removed with aid of thin and soft brush and preserved in 20 mL of ethanol 70% in eppendorf tubes until identification. Apterous adults and alates were collected.

For identification permanent slides were prepared and observed under optical microscope. The specimens (aptera and alates) were mounted in Canada balsam according to Remaudière (1992)REMAUDIÈRE, G. Une méthode simplifiée de montage des aphides et autres petits insectes dans le baume du Canada. Revue Française .’Entomologie (N. S.), v.14, n.4, p.185–186, 1992. technique slightly modified. It was employed 10% KOH solution instead of 40% as originally recommended. The specimens are deposited in Facultad de Ciencias Exactas Físicas y Naturales, Universidad Nacional de Córdoba, Córdoba.

RESULTS

Formal record of occurrence. The aphid was identified as S. dauci and before 2002, it was not recorded in Brazil. The first report of occurrence in this country was published by Yuki et al. (2006)YUKI, V.A.; DELFINO, M.A.; TAKADA, H.M.; HOJO, H.; IDE, S.; PERONTI, A.L.B.G.; BROMBAL, J.C.; SOUSA-SILVA, C.R.; BUENO, S.C.S. Primeiro registro de Semiaphis dauci (Fabricius) (Hemiptera, Aphididae) em cultura de mandioquinha-salsa (Arracacia xanthorrhiza Bancr. var. Senador Amaral - Apiaceae) no Brasil. O Biológico, São Paulo, v.68, abstract 059/452. Suplemento 2. Presented in REUNIÃO ANUAL DO INSTITUTO BIOLÓGICO, 19., 2006, São Paulo, SP. São Paulo: 2006. Available in: <http://www.biologico.sp.gov.br/biologico/v68_supl_raib/059.PDF>. Access in: 28 Jun. 2007.
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in a previous note and probably was the first world record of this species of aphid on arracacha.

On April/2002, it was verified severe infestation by an aggressive aphid species in A. xanthorrhiza culture at Núcleo de Produção de Mudas (NPM), Departamento de Sementes Mudas e Matrizes, Coordenadoria de Assistência Técnica Integral, Secretaria de Agricultura e Abastecimento, São Bento do Sapucaí/SP. The municipality of São Bento do Sapucaí (22º 40’ 53.6” S, 45º 44’ 37.6” W) is placed in the east side of Serra da Mantiqueira at 864 m a. s. l., about 200 km east of city of São Paulo. On March/2003 with the increase in the damages and losses, specimens were collected in arracacha seedlings production area at NPM and send to one of the authors (MAD) for identification. In the same year, infestations were reported by small farmers mainly from Serrano, Paiol Grande and Cantagalo, districts of São Bento do Sapucaí. The infestation levels were inversely proportional to the altitude of the place where the farm was located.

Taxonomy and morphological characterization. The originally Palaearctic genus Semiaphis van der Goot, 1913GOOT, P. VAN DER. Zur Systematik der Aphiden. Tijdschrift voor Entomologie, v.56, n.1/2, p.69-155, 1913. contains 14 described species, is included in subfamily Aphidinae, tribe Macrosiphini and is very similar to Hyadaphis Kirkaldy, 1904 but with very short siphunculi (Blackman; Eastop, 2000BLACKMAN, R.L.; EASTOP, V.F. Aphids on the world’. crops. an identification and information guide. Chichester: John Wiley & Sons., 2000. 466p.).

According to Prior (1971)PRIOR, R.N.B. Some notes on new or uncommon aphids recently found in Britain. Zoological Journal of Linnaean Society, v.50, n.4, p.397-430, 1971., Semiaphis dauci was described by Fabricius (1775)FABRICIUS, J.C. Systema Entomologiae. sistens insectorum classes. ordines. genera. species. adiectis synonymis. locis. descriptionibus. observationibus. Flensburgi & Lipsiae: Officina Libraria Kortii, 1775. xxvii + 832p. in the genus Aphis Linnaeus, 1758 based on specimens from umbels of D. carota. Koch (1854)KOCH, C.L. Die Pflanzenläuse. Aphiden. getreu nach dem leben abgebildet und beschrieben, Hefts I–IV. Nurnberg: J. L. Lotzbeck, 1854. viii + 134p. described and illustrated Aphis carotae from carrot. van der Goot (1913)GOOT, P. VAN DER. Zur Systematik der Aphiden. Tijdschrift voor Entomologie, v.56, n.1/2, p.69-155, 1913. erected Semiaphis and considered Koch’s (1854)KOCH, C.L. Die Pflanzenläuse. Aphiden. getreu nach dem leben abgebildet und beschrieben, Hefts I–IV. Nurnberg: J. L. Lotzbeck, 1854. viii + 134p. Aphis carotae the type species. Theobald (1927)THEOBALD, F.V. The plant lice or Aphididae of Great Britain. London: Headley Brothers, 1927. v.2. iv + 411p. transferred Aphis dauci to Anuraphis Del Guercio, 1907, and made Aphis carotae a synonym thus also making Semiaphis junior synonym of Anuraphis. Theobald’s (1927)THEOBALD, F.V. The plant lice or Aphididae of Great Britain. London: Headley Brothers, 1927. v.2. iv + 411p. synonymy was correct, but Anuraphis carotae is, in fact, Dysaphis crataegi (Kaltenbach, 1843) (Hille Ris Lambers, 1934HILLE RIS LAMBERS, D. Notes on Theobald’s “The plant lice or Aphidiidae of Great Britain”, II and III. Stylops, v.3, p.25-33, 1934.). Börner; Schilder (1932)BÖRNER, C.; SCHILDER, F.A. Aphidoidea, blattläuse. In: SORAUER, P. (Ed.). Handbuch der pflanzenkrankheiten. für landwirthe. gärtner und forstleute, v.5, n.2. Berlin: Verlagsbuchhandlung Paul Parey, 1932. v.5, pt2. p.551-673. agreed with Theobald’s (1927)THEOBALD, F.V. The plant lice or Aphididae of Great Britain. London: Headley Brothers, 1927. v.2. iv + 411p. synonymy of Aphis carotae with Aphis dauci, but correctly ascribed both species to Semiaphis. Börner (1952)BÖRNER, C. Europae Centralis Aphides. Die Blattläuse Mittleuropas. Namen, Synonyme, Wirtspflanzen, Generationszyklen. Mitteilungen der Thüringischen Botanischen Gesellschaft, v.3, n.1/2, 1952. reaffirmed the synonymy and described the biology of S. dauci. Heinze (1960)HEINZE, K. Systematik der mitteleuropäischen Myzinae (Homoptera: Aphidoidea-Aphididae) mit besonderen Berücksichtigung der im Deustschen Entomologischen Institut befindlichen Sammlung Carl Börner. Beitrage zur Entomologie, v.10, n.7/8, p.744-842, 1960. and Shaposhnikov (1964)SHAPOSHNIKOV, G.K. Suborder Aphidinae - aphids. In: BEI–BIENKO, G.Y. (Ed.). Taxonomic keys for insects of the European part of the USSR. v.1: Apterygota, Palaeoptera, Hemimetabola. Moscow & Leningrad: Nauka, 1964. p.489-616. included the species in identification keys.

Morphological characterization of apterous viviparous, alate viviparous, alate male and illustration of apterous viviparous of S. dauci were presented by Prior (1971)PRIOR, R.N.B. Some notes on new or uncommon aphids recently found in Britain. Zoological Journal of Linnaean Society, v.50, n.4, p.397-430, 1971.. In that paper, he also included biometric data for apterous and alate viviparae and alate males of the species.

Apterous (Figs. 1, 2). Small, length 1.3 - 2.1 mm. Blue greenish recovered by white waxy secretion, head, legs, siphunculi and cauda dark green to brownish. Antennae extending to about half of body length, without secondary sensoria, terminal process about 2 or 3x longer than antennomere VI base. Siphunculi (Fig. 3) very short, about 0.04 to 0.05x body length, almost conical, slightly curved inwardly. Cauda pointed and long, tongue like, at least 2x longer than siphunculi.

Fig. 1
Semiaphis dauci (Fabricius, 1775FABRICIUS, J.C. Systema Entomologiae. sistens insectorum classes. ordines. genera. species. adiectis synonymis. locis. descriptionibus. observationibus. Flensburgi & Lipsiae: Officina Libraria Kortii, 1775. xxvii + 832p.) (Insecta, Hemiptera, Aphididae), aptera and nymph on Arracacia xanthorrhiza Bancr. (Apiaceae) (scale in μm).
Fig. 2
Semiaphis dauci (Fabricius, 1775FABRICIUS, J.C. Systema Entomologiae. sistens insectorum classes. ordines. genera. species. adiectis synonymis. locis. descriptionibus. observationibus. Flensburgi & Lipsiae: Officina Libraria Kortii, 1775. xxvii + 832p.) (Insecta, Hemiptera, Aphididae), apterous viviparous (slide mounted).
Fig. 3
Semiaphis dauci (Fabricius, 1775FABRICIUS, J.C. Systema Entomologiae. sistens insectorum classes. ordines. genera. species. adiectis synonymis. locis. descriptionibus. observationibus. Flensburgi & Lipsiae: Officina Libraria Kortii, 1775. xxvii + 832p.) (Insecta, Hemiptera, Aphididae), siphunculus (slide mounted).
Fig. 4
Colonies of Semiaphis dauci (Fabricius, 1775FABRICIUS, J.C. Systema Entomologiae. sistens insectorum classes. ordines. genera. species. adiectis synonymis. locis. descriptionibus. observationibus. Flensburgi & Lipsiae: Officina Libraria Kortii, 1775. xxvii + 832p.) (Insecta, Hemiptera, Aphididae) under leaves of Arracacia xanthorrhiza Bancr. (Apiaceae).
Fig. 5
Wrinkled and curled leaves of Arracacia xanthorrhiza Bancr. (Apiaceae) resulting of infestation by Semiaphis dauci (Fabricius, 1775FABRICIUS, J.C. Systema Entomologiae. sistens insectorum classes. ordines. genera. species. adiectis synonymis. locis. descriptionibus. observationibus. Flensburgi & Lipsiae: Officina Libraria Kortii, 1775. xxvii + 832p.) (Insecta, Hemiptera, Aphididae).
Fig. 6
Bed of Arracacia xanthorrhiza Bancr. (Apiaceae) in São Bento do Sapucaí/SP showing dead and underdeveloped plants after heavy infestation of Semiaphis dauci (Fabricius, 1775FABRICIUS, J.C. Systema Entomologiae. sistens insectorum classes. ordines. genera. species. adiectis synonymis. locis. descriptionibus. observationibus. Flensburgi & Lipsiae: Officina Libraria Kortii, 1775. xxvii + 832p.) (Insecta, Hemiptera, Aphididae).
Fig. 7
Precocious blossoming of Arracacia xanthorrhiza Bancr. (Apiaceae) plant after attack by Semiaphis dauci (Fabricius, 1775FABRICIUS, J.C. Systema Entomologiae. sistens insectorum classes. ordines. genera. species. adiectis synonymis. locis. descriptionibus. observationibus. Flensburgi & Lipsiae: Officina Libraria Kortii, 1775. xxvii + 832p.) (Insecta, Hemiptera, Aphididae).

Alate. Color similar to that apterous females, head and thorax black. Antennomere III with 17 to 22 secondary sensoria, IV with 3 to 6. Abdomen light, dark marginal plates and transverse bands on tergite VII and VIII. Siphunculi and cauda similar to those apterous.

Remarks. No species of aphids infesting arracacha was cited by Blackman; Eastop (2000)BLACKMAN, R.L.; EASTOP, V.F. Aphids on the world’. crops. an identification and information guide. Chichester: John Wiley & Sons., 2000. 466p., but they mentioned that 18 species are able to colonize carrot. Among them, two species are of genus Semiaphis: S. dauci and S. heraclei (Takahashi, 1921). Both species have very small siphunculi, which attain, at maximum, half of tail length, and did not have apical crown. The distinctive characters of species are: S. dauci presents siphunculi longer than 1.5 times of width of base, setae very short, the longest in the posterior femur rarely exceeding 20 µm; in S. heraclei the siphunculi are shorter than 1.5 times of base width, the longest setae in the metafemur exceeding 60 µm, longer than half of diameter of femoral base.

Notes on biology. The species of Semiaphis are heteroecious between Lonicera L. (Caprifoliaceae) and Apiaceae, or live without host alternation on one or other of this host-plant groups. A few species occur on other plants, including two on species of genus Impatiens L. (Balsaminaceae) (Blackman; Eastop, 2000BLACKMAN, R.L.; EASTOP, V.F. Aphids on the world’. crops. an identification and information guide. Chichester: John Wiley & Sons., 2000. 466p.).

Semiaphis dauci in the Eurosiberian region, from where it is native, is holocyclic and monoecious on plants of wild and cultivated carrots. In other parts of its distribution area, like southern England, the populations are maintained during the whole year by parthenogenesis (Blackman; Eastop, 2000BLACKMAN, R.L.; EASTOP, V.F. Aphids on the world’. crops. an identification and information guide. Chichester: John Wiley & Sons., 2000. 466p.). Anholocyclic populations also certainly occur in Brazil taking in account the geographical position and weather conditions of São Bento do Sapucaí region.

Kavallieratos et al. (2004)kavallieratos, N.G.; tomanoviĆ, Z.; starÝ, P.; atHanassiou, C.G.; sarlis, G.P.; PetroviĆ, O.; niketiĆ, M.; veroniki, M.A. A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of southeastern Europe and their aphid-plant associations. Applied Entomology and Zoology, v.39, n.3, p.527-563, 2004. mentioned as parasitoids of this aphid, species of genera Lysiphlebus Förster, 1862 (Insecta, Hymenoptera, Braconidae) andBinodoxys Mackauer, 1960 (Braconidae).

Besides the direct damages by feeding activity, S. dauci is vector of many viruses such as Celery mosaic virus (Potyviridae), and several other non–persistent ones (Blackman; Eastop, 2000BLACKMAN, R.L.; EASTOP, V.F. Aphids on the world’. crops. an identification and information guide. Chichester: John Wiley & Sons., 2000. 466p.). Katis et al. (2006)KATIS, N.I.; TSITSIPIS, J.A.; LYKOURESSIS, D.P.; PAPAPANAYOTOU, A.; MARGARITOPOULOS, J.T.; KOKINIS, G.M.; PERDIKIS, D.C.; MANOUSSOPOULOS, I.N. Transmission of Zucchini yellow mosaic virus by colonizing and non–colonizing aphids in Greece and new aphid species vectors of the virus. Journal of Phytopathology, v.154, n.5, p.293-302, 2006. tested 19 species of aphids and verified that S. dauci is able to transmit, experimentally, the Zucchini Yellow Mosaic Virus – ZYMV (Potyviridae).

Description of damages. The damages by S. dauci are known only in carrot (Daucus carota L. - Apiaceae) plants. The leaves present, near the area were the colonies were settled, strong curling and rolling up and the sprouts present a certain degree of paralysis. No previous record on damage in arracacha exists before the note by Yuki et al. (2006)YUKI, V.A.; DELFINO, M.A.; TAKADA, H.M.; HOJO, H.; IDE, S.; PERONTI, A.L.B.G.; BROMBAL, J.C.; SOUSA-SILVA, C.R.; BUENO, S.C.S. Primeiro registro de Semiaphis dauci (Fabricius) (Hemiptera, Aphididae) em cultura de mandioquinha-salsa (Arracacia xanthorrhiza Bancr. var. Senador Amaral - Apiaceae) no Brasil. O Biológico, São Paulo, v.68, abstract 059/452. Suplemento 2. Presented in REUNIÃO ANUAL DO INSTITUTO BIOLÓGICO, 19., 2006, São Paulo, SP. São Paulo: 2006. Available in: <http://www.biologico.sp.gov.br/biologico/v68_supl_raib/059.PDF>. Access in: 28 Jun. 2007.
http://www.biologico.sp.gov.br/biologico...
. On arracacha the damages by S. dauci are proportional to the insect population. The colonies generally are composed by a large number of individuals (Fig. 4) and were settled in both sides of leaves. The colonization usually starts by the superior surface of the leaves and there was a tendency to wrinkling and curling (Fig. 5). As the colonies grow the leaves roll up hiding aphids, the plants had their development retarded and the blossoming is induced. When the control is not adequately done the population increases so much in size, spreads to petioles and sprouts, killing the plant (Fig. 6). The plants that survive infestation blossom precociously (Fig. 7). In the seedlings, the symptoms were severer with reduction in the development and death of plants. These symptoms are similar to those observed in carrot.

Arthropoda related to arracacha. Bibliographical research was done to verify what are the main mites (Arachnida, Acari) and other insects (Insecta) that can be limiting to cultivation of this tuber. Information on damages by the species of Acari, Hemiptera, Coleoptera and Lepidoptera is added and the results of survey are summarized in Table 1.

Table 1
Mites (Arthropoda, Arachnida, Acari) and insects (Arthropoda, Insecta) related with culture of arracacha (Arracacia xanthorrhiza Bancr. - Apiaceae).

Tetranychus urticae Koch, 1836 (Arachnida, Acari, Tetranychidae). The two spotted spider mite can became an important pest in the arracacha culture regions. In certain parts of states of Minas Gerais and Espírito Santo it is considered the main pest of A. xanthorrhiza (Fornazier et al., 1988FORNAZIER, M.J.; BALBINO, J.M. de S.; MENEGHITTE, G.L. Controle do ácaro rajado, Tetranychus urticae, em batata-baroa, na região serrana, do Espírito Santo. Horticultura Brasileira, v.6, n.13, p.54, 1998.; Correia, 1984CORREIA, L.G. A cultura da mandioquinha–salsa. In: ENCONTRO DE TÉCNICOS DE ENSINO, PESQUISA E EXTENSÃO RURAL SOBRE A CULTURA DA MANDIOQUINHA-SALSA, 1984, Barbacena, MG. Relatório. Belo Horizonte: 1984. p.8-11.).

The specimens live in colonies on the inferior surface of the leaves. They feed on sap causing general yellowing of the culture, leaf lost, strong reduction in the production of new leaves, lateness in the plant development and consequently diminishing in the production (Bôas et al., 1997BÔAS, G.L.V.; SANTOS, F.F. dos; FRANÇA, F.H.; BRANCO, M.C. Pragas da mandioquinha–salsa. Informe Agropecuário, v.19, n.190, p.49-51, 1997.).

Tetranychus sp. According to Fonseca (1984)FONSECA, P.C. Cultura da mandioquinha–salsa na região de Juiz de Fora-MG. In: ENCONTRO DE TÉCNICOS DE ENSINO, PESQUISA E EXTENSÃO RURAL SOBRE A CULTURA DA MANDIOQUINHA-SALSA, 1984, Barbacena, MG. Relatório. Belo Horizonte: 1984. p.16-20. a red mite of genus Tetranychus Dufour, 1832 also can infest arracacha culture especially when associated with bean (Phaseolus vulgaris L.) (Fabaceae). The colonies develop on inferior side of the leaves that are recovered by silk web. The infestation can attain high level, in dry season, in not irrigated cultures (Santos et al., 1991SANTOS, F.F. dos; VIEIRA, J.V.; PEREIRA, A.S.; LOPES, C.A.; CHARCHAR, J.M. Cultivo da mandioquinha-salsa (Arracacia xanthorrhiza Bancroft). Brasília: EMBRAPA-CNPH, 1991.).

Aphis fabae Scopoli, 1763 (Insecta, Hemiptera, Aphididae). This black aphid species infests only inflorescences and does not diminish the productionof tubercles. However for research purposes and seeds production A. fabae can be very harmful due high populational level that it can attain (Bôas et al., 1997).

Aphis spiraecola Patch, 1914. Menezes (1970)MENEZES, M. de Reprodução sexuada de Aphis spiraecola Patch, 1914 no Estado de São Paulo (Homoptera: Aphididae). . Biológico, São Paulo, v.36, n.2, p.53-57, 1970. cited the arracacha as host of A. spiraecola but did not mention the damage due the species. It was also listed in arracacha in the catalogue by Souza-Silva; Ilharco (1995)SOUZA-SILVA, C.R.; ILHARCO, F.A. Afídeos do Brasil e suas plantas hospedeiras (lista preliminar). São Carlos: Editora da Universidade Federal de São Carlos, 1995. 85p..

Aphis sp. An unidentified species of Aphis Linnaeus, 1758 was considered by Bôas et al. (1997)BÔAS, G.L.V.; SANTOS, F.F. dos; FRANÇA, F.H.; BRANCO, M.C. Pragas da mandioquinha–salsa. Informe Agropecuário, v.19, n.190, p.49-51, 1997. the most important aphid that infests arracacha culture. They observed pink or grey colonies. The species attacks the petiolar base in the insertion of the leaves with stems just underground surface. Its detection depends on removal of the leaves nearest the soil. The aphid lives in symbiosis with Solenopsis saevissima (Hymenoptera, Formicidae) and the presence of the ant is indicative of infestation. Aphis sp. sucks sap causing decaying of plants and are able to transmit viruses; the infestation results in reduction in the productivity (Santos et al., 1991SANTOS, F.F. dos; VIEIRA, J.V.; PEREIRA, A.S.; LOPES, C.A.; CHARCHAR, J.M. Cultivo da mandioquinha-salsa (Arracacia xanthorrhiza Bancroft). Brasília: EMBRAPA-CNPH, 1991.).

Dysaphis apiifolia (Theobald, 1922THEOBALD, F.V. The plant lice or Aphididae of Great Britain. London: Headley Brothers, 1927. v.2. iv + 411p.) (Aphididae). This species was collected by Costa et al. (1972)COSTA, C.L.; EASTOP, V.F.; COSTA, A.S. A list of the aphid (Homoptera: Aphidoidea), collected in São Paulo, Brazil. Revista Peruana de Entomología, v.15, n.1, p.131-134, 1972. with water traps in culture of A. xanthorrhiza in Piedade, SP in V-VI.1968. No information on damage was mentioned by them. It was catalogued by Souza-Silva; Ilharco (1995)SOUZA-SILVA, C.R.; ILHARCO, F.A. Afídeos do Brasil e suas plantas hospedeiras (lista preliminar). São Carlos: Editora da Universidade Federal de São Carlos, 1995. 85p. as one of the aphid species hosted by arracacha.

Hyadaphis foeniculi (Passerini, 1860) (Aphididae). This species presents green coloration and does not occur often. The losses caused by this aphid are still not significant. It infests the leaves that facilitate the visualization and control (Santos et al., 1991SANTOS, F.F. dos; VIEIRA, J.V.; PEREIRA, A.S.; LOPES, C.A.; CHARCHAR, J.M. Cultivo da mandioquinha-salsa (Arracacia xanthorrhiza Bancroft). Brasília: EMBRAPA-CNPH, 1991.). This specie was present on arracacha in mix with S. dauci.

Conotrachelus cristatus Fahraeus, 1837 (Coleoptera, Curculionidae). Nowadays this is the most important pest of arracacha culture in Brazil. In the state of São Paulo, in 1984, it was verified an intense attack by this borer in 100% of the seedlings, and this event was considered one of the main reasons for decreasing of arracacha cultivated area in the state (Zanin, 1984ZANIN, A. C.W. Cultura da mandioquinha-salsa no estado de São Paulo. In: ENCONTRO DE TÉCNICOS DE ENSINO, PESQUISA E EXTENSÃO RURAL SOBRE A CULTURA DA MANDIOQUINHA-SALSA, 1984, Barbacena, MG. Relatório. Belo Horizonte: 1984. p.24-27.). In the southern part of state of Minas Gerais it was detected in 1993 in the largest and most important production areas. According to farmers C. cristatus did not occur in São Bento do Sapucaí, but with improvement in the culture income in 1994/1995 there was an increase in the culture in the year of 1996. The seedlings necessary to attend the expansion were brought from Senador Amaral and Gonçalves, southern Minas Gerais, and were infested. The introduction of the pest in São Bento do Sapucaí led to reduction of about three times in the productivity.

The weevil has as hosts, species of Inga Mill. (Fabaceae) which are widely distributed in Brazil, making easy the beetle spreading. The biology of the species was not studied yet. It attacks propagules making them unviable to vegetative propagation. The larvae penetrate the petiole by the internal side which is softer and causes, initially, yellowing in the leaf bases. They open galleries inside of petiolar bases and posteriorly bore the vegetative bud which presents high starch concentration. The larvae make an extensive damage in this part of plant opening many galleries and becoming the material improper for cultivation (Bôas et al., 1997BÔAS, G.L.V.; SANTOS, F.F. dos; FRANÇA, F.H.; BRANCO, M.C. Pragas da mandioquinha–salsa. Informe Agropecuário, v.19, n.190, p.49-51, 1997.).

Agrotis ipsilon (Hufnagel, 1767) (Insecta, Lepidoptera, Noctuidae). This is a polyphagous species. The caterpillar cut the new leaves very close to ground level and eliminate the apical shoot, the plants die and the beds is not uniformly formed (Salgado, 1984SALGADO, L. O. Praga das umbelíferas. Informe Agrope-cuário, v.10, n.120, p.49-50, 1984.). During heavy infestations even the tuberous roots are damaged and posteriorly rotten by invasion of microorganisms. The attack occurs up to 30 days after planting (Santos et al., 1991SANTOS, F.F. dos; VIEIRA, J.V.; PEREIRA, A.S.; LOPES, C.A.; CHARCHAR, J.M. Cultivo da mandioquinha-salsa (Arracacia xanthorrhiza Bancroft). Brasília: EMBRAPA-CNPH, 1991.).

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Publication Dates

  • Publication in this collection
    31 Aug 2020
  • Date of issue
    Jan-Mar 2011

History

  • Received
    26 June 2008
  • Accepted
    17 Jan 2011
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