Rev. Biol. Trop. 50(1): 137-144, 2002 www.ucr.ac.cr www.ots.ac.cr www.ots.duke.edu

Aphids (Hemiptera: Aphidoidea) of ornamental from São Carlos, state,

Ana Lúcia B. G. Peronti1 and Carlos Roberto Sousa-Silva2 Department of Ecology and Evolutionary Biology, Federal University of São Carlos. C. P. 676, 13565-905 São Carlos, São Paulo, Brazil. Fax: 55-16-260 83 22. 1 [email protected] 2 [email protected]

Received 10-VII-2000. Corrected 02-V-2001. Accepted 5-VI-2001.

Abstract: A total of 25 species were collected from 49 ornamental species in São Carlos - São Paulo, Brazil; 12 were monophagous, four oligophagous and nine polyphagous. A total of 58 aphid-plant asso- ciations are recorded, 43 unknown from Brazil. Eucarazzia elegans (Ferrari, 1872) (: : ) is recorded for the first time from Brazil, and Nectandra megapotamica Spreng. (Lauraceae) is recorded for the first time as host plant for Lizerius tuberculatus (E.E. Blanchard, 1939) (Drepanosiphidae: Drepanosiphinae: Lizeriini). We also describe the injuries caused by aphids to the ornamental plants.

Key words: Aphid diversity, aphid/plant associations, floricultural pests.

Floriculture, which consists of the culti- Besides the impact on the commercial value of vation of ornamental plants used for cut flow- ornamental plants, these may also ers, flowering and non-flowering potted affect urban landscapes. When infested, con- plants, and of the production of seeds, bulbs tainerized plants may easily become dissemi- and large trees, is an important part of the nators of harmful insects when they are trans- Brazilian agriculture, with annual gross sales ported by people to regions or countries far of approximately one billion Brazilian reals from their place of origin or production. (currently half a billion U.S. dollars). The state Despite the increase of ornamental plant of São Paulo holds a 70% share of this market production in Brazil, very few studies have and specialists in estimate an been made on the insects associated with annual growth of 20% in the next few years plants in gardens. Among the most recent (Arruda et al. 1996). national publications, Bergmann and The aphids (Aphidoidea) stand out as Alexandre (1995) and Imenes and Alexandre important pests among the insects that feed on (1996), refer to the occurrence of pests, dis- ornamental plants (Arruda et al. 1996). They eases and forms of control in roses and may cause damage to plants directly by suck- chrysanthemums, respectively. Favero (1996) ing their sap, and indirectly by injecting toxic describes the principal pests of flowers, orna- salivary secretions, transmitting pathogens, mental foliage and orchids and how to control attracting ants and favoring the development them and Imenes and Bergmann (2000) char- of sooty-mold (Lara 1992, Zucchi et al. 1993). acterize the principal pests of ornamental 138 REVISTA DE BIOLOGêA TROPICAL plants and forms of control, including some on plants of the same family, but not necessar- aphid-ornamental plant associations. Special ily all the plants of that family. reference is made to the occurrence of aphids The aphids were placed in the in ornamental plants in the work of Leal and Collection of the Department of Ecology and Oliveira (1983) who observed the aphid Evolutionary Biology (Coleafis/DEBE) at species most frequent in plants of the sixteen UFSCar. public squares in the municipality of Recife, Ornamental plants were identified state of Pernambuco, and Bergmann et al. according to Lorenzi (1992), Lorenzi and (1988) mentioned 16 aphid-plant associations Souza (1995) or sent to specialists. which occur in São Paulo state. The objective of this study was to survey the aphid diversity in ornamental plants in the RESULTS city of São Carlos, state of São Paulo (SP), Brazil. In addition, we also classified the A total of 137 samples of aphids were col- species of aphids according to their host speci- lected, from 49 ornamental species (9 trees, 21 ficity, and characterized some injuries caused , 18 herbaceous plants and 1 palm tree), by these aphids to their host plants. distributed among 35 botanical families. Approximately 63% of the host plants were exotics and, with the exception of Bidens MATERIALS AND METHODS bipinnata Baill (Compositae), all were peren- nials. Fifty-nine aphid-plant associations were The buds, leaves and flowers of ornamen- recorded, and 43 of them were new for Brazil. tal plants infested by aphids were collected in Twenty-five species of aphids, distributed public and private gardens in the city of São among four families, were identified. Carlos, SP, Brazil, and taken to the laboratory Aphididae members were the most common of Department of Ecology and Evolutionary (Appendix 1). This is the first recorded ocur- Biology of the Federal University of São rence of Eucarazzia elegans (Ferrari, 1872). Carlos (UFSCar). The collections were made Nectandra megapotamica (Spreng.) mainly from August 1997 to April 1999. (Lauraceae) is registered for the first time as Additional collections were conducted in host plant of Lizerius tuberculatus (E.E. September 1999 and April 2000. Blanchard, 1939). (Drepanosiphidae: In the laboratory, the aphids were collect- Drepanosiphinae: Lizeriini). ed from the plants with brushes and main- According to the host plants of aphids tained in vials filled with 95% alcohol until recorded by Patti (1984), Costa et al. (1993), they were mounted in slides according to the Eastop et al. (1993), Sousa-Silva and Ilharco technique described by Ilharco and Gomes (1995), Tavares (1996) and Foureaux and Kato (1967). The aphids were identified under opti- (1999), 12 aphid species collected were cal microscope according to Holman (1974), monophagous, 4 were oligophagous and 9 Remaudière (1994) and Eastop (1966). Some were polyphagous (Appendix 1). species were sent to specialists for final identi- An oviparous female of Tinocallis fication. Kahawaluokalani (Drepanosiphidae: The classification of the aphids according Drepanosiphinae: Phyllaphidini) was collected to their host plant specificity was based on the on Lagerstroemia indica (Lythraceae) during definitions proposed by Ilharco (1976), in the survey of August 18th 1998, indicating the which polyphagous are those species that live possibility of sexual reproduction in on plants from different families, oligophagous Neotropical region. This species was also are species that live on a reduced number of observed by Peronti (1999) in , non-related host plants, and monophagous feed RJ, Brazil in August 12th 1998. INTERNATIONAL JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION 139

DISCUSSION (Aphididae: Aphidinae: Macrosiphini), was found on Nephrolepis sp., Nephrolepis exalta Of all the aphid species collected, only L. Schott. var. florida-ruffle Hort. (Davalliaceae) tuberculatus is a South American native and Adiantum raddianum Presl. (Pteridaceae), species (Eastop et al. 1993). Most of the and has already been associated with Viola sp. Brazilian aphidfauna is exotic, as well as the (Violaceae), Phaseolus vulgaris (Fabaceae) and hosts. According to Silva et al. 1968, Rossi et Saintpaulia sp. (Gesneriaceae) (Sousa-Silva and al. 1990, Costa et al. 1993, Sousa-Silva et al. Ilharco 1995, Tavares 1996). rosae 1994, Sousa-Silva and Ilharco 1995, Tavares (Aphididae: Aphidinae: Macrosiphini) has been 1996, Lázzari et al. 1996, Carvalho 1998, found in Brazil only on species of Rosaceae, Hidalgo et al. 1998, Lazzarotto and Lázzari more commonly on Rosa spp. Its secondary hosts 1998, Foureaux and Kato 1999 and Lázzari et in the Holarctic regions are Dipsacaceae, al. 1999, only 16% of the 144 aphid species Valerianaceae and Ilex sp. (Aquifoliaceae) registered in Brazil, up to now, are native of (Sousa-Silva and Ilharco op. cit.). the Neotropical region. Most of the aphids were found on young In regard to the pattern of host specificity leaves generally causing the rolling up or with- observed among aphid species, monophagy er. More serious damages were observed in was the most common, followed by Polyscias guilfoylei (Araliaceae) infested by A. polyphagy. Oligophagy was the least-frequent- spiraecola that produced premature drying up ly observed pattern. and falling of the leaves, in A. raddianum According to Edwards and Wratten infested by I. nephrelepidis that caused dry (1981) the insect specificity to the host seems leaves, and in Hemerocallis fulva and H. flava to be an ecological advantage, that is, it allows (Liliaceae) attacked by M. hemerocallis the insect to adapt itself more exactly to its (Aphididae: Aphidinae: Macrosiphini) that medium than a species living on a variety of caused yellowing (chlorosis), dry leaves and plants. death (during periods of prolonged drought). Among the polyphagous aphids collected, A large amount of honeydew was found in Aphis gossypii, A. spiraecola and Toxoptera L. indica infested by T. kahawaluokalani. In aurantii (Aphididae: Aphidinae: ) some European countries, in the same aphid- which are also significant agricultural pests, plant relationship, intense development of were the most common, occurring in 50% of sooty-mold, limb deformation and premature the aphid-infested hosts. Aphis craccivora, A. leaf fall were observed (Patti 1984, Leclant fabae (Aphididae: Aphidinae: Aphidini), and Renoust 1986). Aulacortum solani, , The interactions listed in this study repre- persicae and M. ornatus (Aphididae: sent a great addition to the knowledge of the Aphidinae: Macrosiphini), were observed in a species of aphids that attack ornamental plants. minor number of ornamental plants (Table 1). Besides, the high host specificity observed Among the oligophagous aphids, Aphis among the major aphid species that occur on nerii (Aphididae: Aphidinae: Aphidini) was ornamental plants facilitates both the identifi- found only on Nerium oleander L. cation of these aphids when collected on their (Apocynaceae), although it also appears on hosts and, consequently, their control. species of a few other botanical families. brasiliensis (Hempel, 1901) (Hormaphididae: Cerataphidini), a common ACKNOWLEDGMENTS species of Palmae in Tropical regions, was recorded in Brazil on Cycas circinalis The authors gratefully acknowledge the (Cycadaceae) and Musa sapientum (Musaceae). help of Fernando Albano Ilharco (Estação nephrelepidis Davis, 1909 Agronómica Nacional - Oeiras, Portugal) for 140 REVISTA DE BIOLOGêA TROPICAL the identification of some aphid species, Maria Favero, S. 1996. Pragas de plantas ornamentais. Inês Salgueiro Lima (Department of Botany - Universidade Estadual do Norte Fluminense, Centro UFSCar) for the identification of some plant de Ciências Tecnológias Agropecuárias. Campos dos Goyatacazes, Rio de Janeiro. Bol. Téc. 3. 16 p. species, and the CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, Foureaux, L.V. & C.M. Kato. 1999. Primeiro registro de Brazil) for their financial support. Takecallis taiwanus (Takahashi) (Homoptera: Aphididae) no Brasil. An. Soc. Entomol. Brasil. 28: 183-184. RESUMEN Hidalgo, N.P., L.M. Bartholdy & J.M. Nieto Nafría. 1998. Two new aphid records for South America and a list Se recolectó un total de 25 especies de áfidos de 49 es- of aphids from Rio Grande do Sul State and Brazil, pecies de plantas ornamentales en São Carlos - São Paulo, p. 407-415. In J.M. Nafría & A.F.G. Dixon (eds.). Brasil; 12 áfidos eran monófagos, cuatro olífagos y nueve Aphids in natural managed ecosystems. Universidad polífagos. Se registró un total de 58 asociaciones áfido-plan- de León, Spain. ta, 43 desconocidas en Brasil. Por primera vez se registran Eucarazzia elegans (Ferrari, 1872) (Aphididae: Aphidinae: Holman, J. 1974. Los áfidos de Cuba. Instituto del Libro, Macrosiphini) en Brasil y Nectandra megapotamica La Habana, Habana. 304 p. Spreng. (Lauraceae) como planta hospedera de Lizerius tu- berculatus (E.E. Blanchard, 1939) (Drepanosiphidae: Dre- panosiphinae: Lizeriini). También describimos las heridas Ilharco, F.A. 1976. Os afídeos ou piolhos das plantas. Soc. Portuguesa de Ciências Naturais, Lisboa. 32 p. causadas por los áfidos a las plantas ornamentales. Ilharco, F.A. & A. Gomes. 1967. Montagem de afídeos para observação microscópica. Agronomia Luzit. 28: 41-45. REFERENCES Imenes, S.D. & M.A. Alexandre. 1996. Aspectos fitossan- Arruda, S.T., M.P. Olivette & C.E. Castro. 1996. itários do crisântemo. Bol. Téc. Inst. Biol. 5: 5-47. Diagnóstico da floricultura do Estado de São Paulo. Rev. Bras. 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Drepanosiphinae, Phyllaphidini) - first record in Brazil and comparison to Takecallis taiwanus Costa, C.L., V.F. Eastop & R.L. Blackman. 1993. Brazilian (Takahashi). Rev. Bras. Zool. 16: 865-870. Aphidoidea: I. Key to families, subfamilies and account of the Phylloxeridae. Pesq. Agropec. Bras. Lazzarotto, C.M. & S.M.N. Lázzari. 1998. Richness and 28: 197-215. diversity of aphids (Homoptera, Aphididae) along an altitudinal gradient in the Serra do Mar, Paraná, Eastop, V.F. 1966. Taxonomic study of Australian Brazil. Rev. Bras. Zool. 15: 977-983. Aphidoidea (Homoptera). Aust. J. Zool. 14: 399-592. Leal, M.C. & M.H. Oliveira. 1983. Estudo sistemático e Eastop V.F., C.L. Costa & R.L. Blackman. 1993. Brazilian ecológico dos afídeos de praças públicas do Recife, Aphidoidea. III Sub-family Drepanosiphinae. Pesq. PE. Brasil Florestal 56: 37-40. Agropec. Bras. 28: 1349-1355. Leclant, F. & M. Renoust. 1986. Le puceron du Edwards P.J. & S.D. Wratten. 1981. Ecologia das inter- Lagerstroemia, noveau ravageur pour notre flore. ações entre insetos e plantas. E.P.U, São Paulo. 71 p. Phytoma. 375: 49-50. INTERNATIONAL JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION 141

Lorenzi, H. 1992. Árvores Brasileiras: Manual de identifi- (Homoptera: Aphididae) na cultura de batata em cação e cultivo de plantas arbóreas nativas do Brasil. Lavras - MG. An. Soc. Entomol. Brasil, 19: 74-86. Plantarum, , São Paulo. 368 p. Silva, A.G., G.R. Gonçalves, D.M. Galvão, A.J. Gonçalves, Lorenzi, H. & H.M. de Souza. 1995. Plantas ornamentais J. Gomes, M.N. Silva & L. Simoni. 1968. Quarto no Brasil: Arbustivas, herbáceas e trepadeiras. Catálogo dos Insetos que vivem nas plantas do Brasil, Plantarum, Nova Odessa, São Paulo. 736 p. seus parasitos e predadores. Rio de Janeiro, Ministério da Agricultura. Parte II, 1o tomo. 622 p. Patti, I. 1984. Un afide nocivo alla Lagerstroemia in Italia. Informatore Fitopatologico 12: 12-14. Sousa-Silva, C.R., F.A. Ilharco & J.M. Pacheco. 1994. Primeiro registro para o Brasil de Del Peronti, A.L. 1999. Afídeos e cocóideos em plantas ornamen- Guercio, 1911 (: Aphididae). Rev. tais na região de São Carlos - SP, seus parasitóides, Agricultura 69: 256-258. predadores e suas associações com formigas. Tese de Mestrado em Ecologia e Recursos Naturais, Sousa-Silva, C.R. & F.A. Ilharco. 1995. Afídeos do Brasil e Universidade Federal de São Carlos, São Paulo, Brasil. suas plantas hospedeiras. UFSCar, São Carlos. 85 p.

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APPENDIX 1 Aphids and their host ornamental plants collected in São Carlos - SP from August 1997 to April 1999 and September 1999 to April 2000

Aphids collected Host plant species/Common names Plant Plant Plant in Portuguese shown in quotes family origin form

MONOPHAGOUS

Aphididae Aphis coreopsidis *Bidens bipinnata Baill. Compositae Exotic Herb (Thomas, 1978) “beijo-de-moça”

Aphis hederae Schefflera arboricola (Hay.) Merr. Araliaceae Exotic (Kaltenbach, 1843) “cheflera-pequena”

Eucarazzia elegans *Salvia splendens Ker-Gawl. Labiatae Native Herb (Ferrari, 1872) “alegria-dos-jardins”

Macrosiphoniella sanborni *Dendrathema grandiflora (Ram.) Tzv. Compositae Exotic Herb (Gillette, 1908) “crisântemo-da-china”

Myzus hemerocallis *Hemerocallis flava L. Liliaceae Exotic Herb Takahashi, 1921 *Hemerocallis fulva L. Exotic Herb “lírio-de-são-josé”

* New record of aphid-plant association in Brazil. Continues .... 142 REVISTA DE BIOLOGêA TROPICAL

Aphids collected Host plant species/Common names Plant Plant Plant in Portuguese shown in quotes family origin form

Pentatrichopus tetrarhodus *Rosa sp. Rosaceae Exotic Shrub (Walker, 1849) “roseira”

Rhodobium porosum Rosa sp. Rosaceae Exotic Shrub (Sanderson, 1901) “roseira”

Sitobion luteum Dendrobium phalaenopsis Fitzg. Orchidaceae Exotic Herb (Buckton, 1876) “orquídea”

Hormaphididae Cinara tujafilina Thuja sp. Cupressaceae Exotic Shrub (Del Guercio, 1909) “tuia”

Drepanosiphidae Lizerius tuberculatus *Nectandra megapotamica Spreng. Lauraceae Native Tree (E.E. Blanchard, 1939) “canelinha”

Tinocallis kahawaluokalani Lagerstroemia indica L. Lythraceae Exotic Tree Kirkaldy, 1907 “resedá”

Takecallis taiwanus Phyllostachys aurea A. and C. Riv. Poaceae Exotic Shrub (Takahashi, 1926) “bambú-de-jardim”

OLIGOPHAGOUS

Aphididae Aphis nerii Nerium oleander L. Apocynaceae Exotic Shrub (B. de Fonscolombe, 1841) “espirradeira”

Idiopterus nephrelepidis Adiantum radianum Presl. Pteridaceae Native Herb Davis, 1909 “avenca-delta” *Nephrolepis sp. Davalliaceae _____ Herb “samambaia” *N. exaltata Schott. var. florida-ruffle Hort. Davalliaceae Native Herb “samambaia-crespa”

Macrosiphum rosae Rosa sp. Rosaceae Exotic Shrub (Linné, 1758) “roseira”

Hormaphididae *Chrysalidocarpus lutescens Wendl. Palmae Exotic Palm (Hempel, 1901) “areca-bambu” tree

POLYPHAGOUS

Aphididae Aphis craccivora Portulaca grandiflora Hook. Portulacaceae Native Herb Koch, 1854 “onze-horas”

* New record of aphid-plant association in Brazil. Continues .... INTERNATIONAL JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION 143

Aphids collected Host plant species/Common names Plant Plant Plant in Portuguese shown in quotes family origin form

Aphis fabae *Anthurium x froebellii Hort. Araceae Exotic Herb Scopoli, 1763 “antúrio” *Epidendrum ellipticum R. Grah Orchidaceae Native Herb “orquídea-da-restinga”

Aphis gossypii Bauhinia variegata Linn. Fabaceae Native Tree Glover, 1877 “pata-de-vaca” *Calliandra inaequilatera Rusby Fabaceae Native Shrub “esponginha” *Catharanthus roseus G. Don Apocynaceae Exotic Shrub “boa-noite” *Cordilyne terminalis Kunth. Liliaceae Exotic Shrub “dracena-vermelha” Dieffenbachia amoena Hort. ex Gent. Araceae Exotic Herb “comigo-ninguém-pode” *Ervatamia coronaria Stapf. Apocynaceae Exotic Shrub “jasmim-café” Hibiscus rosa-sinensis L. Malvaceae Exotic Shrub “mimo-de-vênus” *Iresine herbstii Hook. Amaranthaceae Native Shrub “coração-magoado” Kalanchoe blossfeldiana v. Poelln. Crassulaceae Exotic Herb “calancoê” *Lagerstroemia indica Lythraceae Exotic Tree “resedá” *Malvaviscus arboreus Cav. Malvaceae Native Shrub “malvavisco” *Schefflera arboricola Araliaceae Exotic Shrub “cheflera-pequena” *Schinus molle L. Anacardiaceae Native Tree “aroeira-mole” *Syngonium podophyllum Schott. Araceae Exotic Herb “singônio” *Spathodea campanulata Beauv. Bignoniaceae Exotic Tree “espatódea” *Tabebuia sp. Bignoniaceae Native Tree “ipê” *Tibouchina granulosa Cogn. Melastomataceae Native Tree “quaresmeira”

Aphis spiraecola *Allamanda blanchetti DC. Apocynaceae Native Shrub Patch, 1914 “alamanda-roxa” *Bougainvillea spectabilis Willd. Nyctaginaceae Native Shrub “primavera” *Cordilyne terminalis Liliaceae Exotic Shrub “dracena-vermelha” *Gladiolus hortulanus Hort. Iridaceae Exotic Herb “palma-de-santa-rita” *Hibiscus syriacus L. Malvaceae Exotic Shrub “hibisco-colunar” * tobira (Thumb.) Ait. Exotic Shrub “pitósporo” *Polyscias guilfoylei Bailey. Araliaceae Exotic Shrub “árvore-da-felicidade”

* New record of aphid-plant association in Brazil. Continues .... 144 REVISTA DE BIOLOGêA TROPICAL

Aphids collected Host plant species/Common names Plant Plant Plant in Portuguese shown in quotes family origin form

Rosa sp. Rosaceae Exotic Shrub “roseira” *Viburnum sp. Caprifoliaceae Exotic Shrub “viburno”

Aulacorthum solani *Salvia splendens Labiatae Native Herb (Kaltenbach, 1843) “alegria-dos-jardins”

Macrosiphum euphorbiae *Turnera ulmifolia L. Turneraceae Native Herb (Thomas, 1878) “turnera”

Myzus ornatus *Duranta repens L. var. aurea Hort. Verbenaceae Native Shrub Laing, 1932 “pingo-de-ouro” *Gerbera jamesonii Bolus Compositae Exotic Herb “margarida-do-transvaal”

Myzus persicae *Duranta repens var. aurea Verbenaceae Native Shrub (Sulzer, 1776) *Gerbera jamesonii Compositae Exotic Herb

Toxoptera aurantii *Ficus benjamina L. Moraceae Exotic Tree (B. de Fonscolombe, 1841) “ficus” *Murraya exotica Jack Rutaceae Exotic Tree “falsa-murta” Moraceae *Pachystachys lutea Nees Acanthaceae Exotic Shrub “camarão-amarelo” *Schefflera arboricola Araliaceae Exotic Shrub “cheflera-pequena” Camellia japonica L. Theaceae Exotic Shrub “camélia”

* New record of aphid-plant association in Brazil.