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International Journal of Acarology

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Some avocado mites from Michoacan, Mexico

Edith G. Estrada-Venegas a; Silvia Rodríguez-Navarro b; James A. McMurtry c a Programa de Entomologia y Acarologia, Instituto de Fitosanidad, Colegio de Postgraduados, Montecillo Edo. de México, C.P. b Departamento de Producción Agricola y Animal, UAM-Xochimilco, Col Villa Quietud, México, CP, D.F. c Department of Entomology, Oregon State University, Corvallis, OR, USA

To cite this Article Estrada-Venegas, Edith G., Rodríguez-Navarro, Silvia and McMurtry, James A.(2002) 'Some avocado

mites from Michoacan, Mexico', International Journal of Acarology, 28: 4, 387 — 393 To link to this Article: DOI: 10.1080/01647950208684315 URL: http://dx.doi.org/10.1080/01647950208684315

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SOME AVOCADO MITES FROM MICHOACAN, MEXICO

Downloaded By: [Colegio De Posgraduados] At: 03:04 27 January 2010

Edith G. Estrada-Venegas, 1 Silvia Rodriguez-Navarro 2 and James A. McMurtry 3

1. Programa de Entomologia y Acarologia, lnstituto de Fitosanidad, Colegio de Postgraduados, Km. 35.5 Cart'. M~xico-Texcoco. Montecillo Edo. de M~xico , C.P. 56230, e-mail: [email protected]; 2. Departamento de Producci6n Agrlcola y Animal, UAM-Xochimilco, Calzada del Hueso No. 1100, Col Villa Quietud, CP 04960, MOxico, D.F., e-maik [email protected]; 3. Department of Entomology, Oregon State University, Corvallis, OR, USA, e-mail: [email protected]

A B S T R A C T - The importance of the avocado crop (Persea americana var. Hass) in Mexico has increased during the last several years. Areas planted to avocado cover 124,829 ha with an average production of 8.5 ton/ha on irrigated lands. The objective of this study was to identify mite species associated with this crop. Orchards of P. americana var. Hass were sampled in seven of the most important producing counties in the State of Michoacan during 1997 and 1998. Eighteen species in nine families were found: six phytophagous, ten predatory and two species with diverse habits. Collections included representatives of the three most important phytophagous mite families - Eriophyidae, Tenuipalpidae and Tetranychidae. Key words - Acari, Eriophyidae, Tenuipalpidae, Tetranychidae, mites, avocado, Persea americana, Michoacan, Mexico. RESUblEN - La importaneia del cultivo del aguacate en M6xico ha aumentado en los flltimos tiempos. Se calcula que el hrea que se tiene plantada de aguacate es de 124,829 ha, y se estima que hay una producci6n promedio en ~eas con irrigaci6n de 8.5 ton/ha. E1 objetivo de este trabajo rue conocer las especies de ~icaros asociados a este cultivo. Huertos de Persea americana var. Hass fueron muestreados en siete de los m~s importantes municipios productores en el estado de Michoachn durantes los afios de 1997 y 1998. Se encontr6 un total de dieciocho especies pertenecientes a nueve familias: seis especies fit6fagas, diez depredadoras, y dos con h~bitos diversos. La colecta realizada incluye tres de las familias fit6fagas m~is importantes - Tetranychidae, Eriophyidae y Tenuipalpidae. Palabras clave - Persea americana, aguacate, hcaros, Eriophyidae, Tenuipalpidae, Tetranychidae, MichoacLn, Mexico.

INTRODUCTION

Mexico is the primary producer and consumer of avocado (Persea americana var. Hass) (Lauraceae) in the world, producing 45% of the world's production (Anonymous, 1994). The average production on irrigated areas is estimated to be 8.5 ton/ha, and some 1,100,000 tons are currently produced annually on 124,829 ha. Approximately 70% is sold in Mexico, 30% is exported fresh or processed. This crop is cultivated commercially in 16 states; five of the most important states are Michoacan, Puebla, Estado de Mexico, Morelos and Nayarit (S~nchez and RuN, 1994). The state of Michoacan produces

871,873 tons on 90, 000 ha, about 72% of the country's production (Bautista, 1994). The state of Michoacan has an area of 59,864 sq. km. It is bordered on the north by the States of Queretaro, Guanajuato and Jalisco; on the East by the States of Mexico and Guerrero; on the South by the State of Guerrero and the Pacific Ocean; and to the West by the States of Colima and Jalisco (Fig. 1). Many pests attack avocado crop but researchers are focusing on the most important pests. The objectives of this study were to identify the phytophagous mite species associated with the avocado crop, to determine their natural enemies, and to study their distribution patterns in the

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MU~CIPALITY OF

zn~cu~o

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-

"


"

q',(I.J1'~[CIP.4~rr Y ,

~

TACAMBARO

OE I

Ou~tum de C~ognd~ 1989)

Fig. 1. Map of the study area of mites associated with the avocado crop in the State of Michoacan State, Mexico.

State of Michoacan. Results will be utilized to develop a natural control program, part of an Integrated Pest Management (IPM) project. Knowledge of avocado mites in Mexico is limited. Previous studies were mostly from isolated and unsystematic mite collectings. These were published from the states of Morelos, Nuevo Leon, Estado de Mexico and Puebla (Estrbanes-Gonz~ilez and Rodrlguez-Navarro, 1998) but none were reported from Michoacan. In Michoacan, as in all of Mexico, Oligonychus punicae (Hirst) and (9. perseae (Tuttle, Baker and Abbatiello) were considered the two most damaging tetranychid mites on avocado (Anonymous, 1984; Gallegos, 1983; Salgado, 1993). Oligonychuspunicae (Hirst) - This species is probably native to Mexico and Guatemala. Its life cycle under laboratory conditions is 15.74 days at 22 °C (/3arbosa, 1983). The species feeds primarily on the upper leaf surface but feeds on lower leaf surface and fruit when heavy mite densities. The population develops along the midrib of the leaf. Feeding causes brownish discoloration be-

cause of the loss of chlorophyll (Aguilera and Salazar, 1991). Under severe infestations (80-100 females or 200300 immatures per leaf) the plant loses its foliage (McMurtry eta/, 1969; McMurtry, 1985a). Feeding of the mites reduces transpiration, limits photosynthesis and causes defoliation (Sances et al., 1982a). Avocado varieties show different feeding symptoms of O. punicae in the region of Coatepec Harinas, State of Mexico (Reyes et al.,1993). In that area, the population has two peaks, one in May and the other in November.

Oligonyehus perseae (Tuttle, B a k e r and A b b a tielio) - This species was described from Persea sp. foliage from Mexico, collected at E1 Paso, Texas Quarantine station (Tuttle et al., 1976). The life cycle under laboratory conditions averages 20.95 days (Salinas, 1992). The female lays an average of 10-14 eggs (Ramirez, 1992) and is confined to the underside of the leaves, where populations begin development along the midrib. The mites produce a whitish "nests" of silk, where they complete their life cycle (Aponte and

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Table 1. Mite species associated with the avocado crop and their feeding habits in the State of Michoacan, Mexico.

Suborder/ Family

Species

Distribution

Actinedida Cheyletidae Stigmaeidae


Eriophyidae

..................... Predatory. . . . . . . . . . . . . . . . . . . . Nodele philfipmensis (Baker) Mexechetes aztecorum De Leon Agistemus arcypaurus Gonzalez Agistemus terminalis (Quayle) ...................... Phytophagous . . . . . . . . . . . . . . . . . Calepitrimerus muesebecki Keifer

Tacambaro Tacambaro Tacambaro Tacambaro Uruapan, Periban, Zimcuarefiro, Taeambaro,

Tingflindin Tingambato Tenuipalpidae Telranychidae

Tarsonemidae

Brevipalpus sp. Uruapan Eotetranychus sp. Tacambaro Oligonychus perseae (Tuttle, Baker & Abbatiello) All sampled counties Oligonychus punicae (Hirst) All sampled counties ........................... Probably fungivorous ........................ Tarsonemus confusus Ewing Nuevo Parangaricutiro, Ziracuaretiro

Gamasida Ascidae Phytoseiidae

............................. Predatory............................. Melichares sp. Nuevo Parangaricutiro Ambtyseius sp. Uruapan, Nuevo Parangaricutiro Uruapan, Euseius hibisci (Chant) Tacambaro, Ziracuarefiro, Per~an,

Ting~din, Tingambato Umapan, Nuevo Parangaricutiro Ziracuaretiro Galendromus near porresi Uruapan, Metaseiulus johnsoni Mahr Nuevo Parangaricutiro Ziracuaretiro Neoseiulus sp. Typhlodromalus limonicus (Garman & McGregor) Tacambaro, Umapan

Euseius near quetzal~

Uropodidae

.......................... Various ............................... Under determination Nuevo Parangaricuth'o, Umapan,

Ziracuarofiro, Tacambaro,

Ting~dm

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McMurtry, 1997). The feeding on the sap of the plants produces necrotic spots on the leaves which grow and connect to form strips throughout. These spots may reach the upper leaf surface; perhaps this is why the species may be confused with O. punicae (Salinas, 1992). Mite clusters may be as high as 130 "nests," 2 mm in diameter, on every medium size leaf (Salgado, 1993). This species is considered one of the most important mite pests of avocado because of the high populations that develop in agricultural ecosystems and because of its resistance to organophosphates (Martinez, 1989).


MATERIALS AND METHODS

Avocado trees were sampled in seven of the most important avocado-producing counties in Michoacan: Uruapan, Periban, Nuevo Parangaricutiro, Ziracuaretiro, Tacambaro, Tingambato and TingOindin (Fig. 1). Mites were collected for two years (1997 - 1998) from trees selected at random in the study area. Foliage was sampled at different heights around each tree. Branches were beaten over a fiat black-white surface (half and half) to collect active species. This technique was used especially to recover predatory species. Avocado twigs, branches and trunks were carefully examined in order to determine the spatial distribution of mite species on the tree. Samples were collected and taken to the laboratory in plastic bags inside a cooler to prevent desiccation.Mites were collected under the microscope and preserved in 70% alcohol. Mites in all stages of development were mounted on slides in Hoyer's medium for identification and reference collection. Acarologists from the USA and Canada (J. McMurtry and E. E. Lindquist, personal communication) confirmed identifications of some species (other identitifications are still being confirmed). RESULTS AND DISCUSION

Eighteen species of mites belonging to 9 families in the suborders Prostigmata and Mesostigmata were found associated with avocado trees in the state of Michoacan (Table 1). Phytophagous and predatory species, as well as species of unknown feeding habits, were among them. With the exception of the Uropodidae, which were found only on the fruit and trunk, all families were found on foliage. Cheyletid mites were also found on the trunk and tarsonemid mites on the fruit. Species diversity was highest in Uruapan with 11, followed by Tacambaro and Nuevo Prangaricutiro with 8, Ziracuaretiro with 7, Tingambato 5, and Periban and Tingaindin with 4. Oligonychus punicae and O. perseae

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were found damaging the avocado crop in all orchards sampled. Because sampling was not done systematically in all counties, additional species may have been missed. The higher diversity found in Uruapan may be due to more samples and theTacambaro diversity may be related to the fact that several native varieties of avocado are still planted in the area, normally mixed with commercial ones (Persea americana var. Hass). Phytophagous mites - Representatives of the three important pest families were collected: Tetranychidae, Eriophyidae and Tenuipalpidae (Table 1). The last two have not been cited previously as pests of avocado in Mexico. During hot season, large number of eriophyid mites (Calepitrimerus muesbecki Keifer and an unidentified genus) were collected on foliage but not on flowers. They were collected on leaves of different ages, and with some damage from O. punicae. They lived on the underside of the leaves close to the midrib, but were distributed all over the underside of the leaf when abundant. They were usually restricted to certain regions in the study area. Crowding and direct effects of mite feeding on leaves were responsible in some cases for dispersal. Females ofO. punicae and O. perseae hung from the tree on silk threads waiting to be dispersed by wind. This was observed several different times during the study. A female Eotetranychus sp. was found. Unfortunately males were not collected to confirm identify to species level. Different species of eriophyids cause russeting, leaf distortion, and galls (Westphal and Manson, 1996). Tegolophus perseaflorae Keifer, as its name suggests, damages flowers and reduces fruit production of avocado trees (Lindquist et. aL, 1996). Calepitrimerus muesbecki Keifer has been cited as a pest on avocado, causing some russeting on leaves (Lindquist eta/., 1996). It has not been cited for avocado in Mexico. It is also not included in the recent list of insects and mites of agricultural importance (Rodriguez, 1999). Brevipalpus sp., of economic importance on different crops (Rodriguez, 1999; Rodriguez and Esttbanes, 2001), has also not been collected previously from avocado in Mexico. Some misidentifications were found in the literature. Oligonychus punicae was misidentified as Paratetranychus (=Oligonychus)yothersi (Colin, 1990; Colin, 1991; Colin and Rubi, 1992). Most information on O. punicae on avocado, is mainly from California during the last 20 years. This species causes serious problems in Mexico, USA, and other parts of the world. Oligonychus perseae has been less studied, but does not cause serious problems in Mex-


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ico. In California, it recently caused severe defoliation of avocado trees (Aponte and McMurtry, 1997). Predatory mites - We found 10 species of predatory mites as natural enemies of other mites (Table 1). The phytoseiids Typhlodromalus limonicus, Euseius hibisci and Neoseiulus sp. were important species as pest biocontrol agents on avocado. Other mites including aseid, stigmaeid and cheyletid mites were important also. Some species of these families were important biocontrol agents on different crops (De Leon, 1962; Muma, 1964; Laing and Knop, 1982). Cheyletid mites are important natural enemies of Eriophyidae (Petting and MeMurtry, 1996) but have not been previously recorded on avocado in Mexico. Euseius hibisci shows two peaks of abundance in avocado: one during the spring, correlated with the presence of pollen from avocado blossoms and another in summer or autumn correlated with increases in O. punicae (McMurtry and Johnson, 1966). Typhlodromalus limonicus Garman and McGregor arid Euseius hibisci feed readily on both adults and immatures of the spider mites including Panonychus citri (McGregor), Oligonychus punicae (Hirst) and Tetranychus cinnabarinus (Boisduval). The latter species of predatory mite became entangled in the webbing and died when introduced to a dense colony of the latter species (McMurtry and Scriven, 1965). Euseius hibisci and T. limonicus sometimes coexist in Southern California, both species are quite common in avocado orchards (McMurtry and Scriven 1965). The diet of T. limonicus includes prey, avocado pollen, or pollen. This species feeds readily and reproduces quite successfully on avocado pollen (McMurtry and Scriven, 1965). McMurtry and Scriven (1964) report that T. limonicus appears to be a more aggressive predator than E. hibisci because it can feed on adult females of Panonychus citri, whereas E. hibisci feeds only on immatures. Typhlodromalus limonicus has been mentioned as an ineffective predator of mites on cassava (Yassen and Bennet, 1977, cited by Belloti, 1985) McMurtry et aL (1985b) studied three species of Euseius distributed from Southern California to Central America. Euseius hibisci is the most common species from California to Southern Mexico; E. vivax is restricted to the hot and humid regions of Mexico and Central America; and E. quetzali was collected in high elevations of Chiapas, Mexico and Guatemala. It is not known if the three species overlap. We found specimens intermediate between E. hibisci and E. quetzali. The fact that both species occur in this region, suggest that there is some interbreding between populatons, resulting in intermediate forms (McMutry, unpubl., 1999). Congdon and

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McMurtry (1986) found partial reproductive compatibility between these species in California. Estrbanes-Gonz~iles and Rodriguez-Navarro (1998) found three species of Phytoseiidae preying on O. perseae. Metaseiulus comus was found in the states of Chiapas, Guanajuato and Jalisco; Typhlodromina johnsoni in Morelos and Euseius hibisci in Chiapas, Guanajuato, Oaxaca and Edo. de Mexico. McMurtry and Scriven (1971) found that Typhlodromalus limonicus was a more voracious and effective predator of O. punicae than E. hibisci. Natural enemies of O. punicae are known to provide good control, however agricultural management may affect the equilibrium of populations. It is possible that the same species may produce good control of O. perseae, which normally is present in low population. CONCLUSIONS

Oligonychus punicae and O. perseae are the most important pest species of avocado in Michoacan. The greatest diversity of mites was found in Uruapan with 11 species, Tacambaro with 8, followed by Ziracuaretiro with 7, Nuevo Parangaricutiro with 6, Tingambato with 5, and Periban and Tingtiindin with 4 Uruapan showed the greatest diversity of predatory mites (5) followed by Tacambaro and Ziraeuaretiro (4), and Nuevo Parangaricutiro (3). Species of Phytoseiidae, Stigrnaeidae and Cheyletidae are cited as natural enemies of pest species of the avocado crop in the state of Michoacan, and have the potential to be used in biological control programs. Species of Cheyletidae, Eriophyidae, Tenuipalpidae and Stigmaeidae are cited for the first time on avocado trees in the state of Michoacan. ACKNOWLEDGMENTS

The authors wish to thank Dr. Alison Moldenke for correcting the manuscript and Dr. Evert. E. Lindquist (Canada) for identification of the mites. The senior author also wishes to thank CONACyT (Project 9601046) for the financial support. LITERATURE CITED

Aguilera M. J. and G. Salazar. 1991. The avocado industry in Michoacan. South African Growers Association Yearbook. 14: 94-97. Aponte, O. and J. A. McMurtry. 1997. Damage on "Hass" avocado leaves, webbing and nesting behavior of Oligonychus perseae (Acari: Tetranychidae). Exp. Appl. Acarol. 21: 265-272.


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Anonymous. 1984. Manual Fitosanitario del Aguacate. Bayer de M6xico, S.A. de C.V. s/p. Anonymous. 1994. Aspectos Generales de la Fruticultura Nacional. Direcci6n de sistema de producto. S.A.R.H. s/p. Bautista, A. E. 1994. El cultivo del aguacate en M6xico. En: Reporte Final del Foro Nacional sobre Frutales (Aguacate). Gremio Agron6mico, Uruapan, Mich. s/p. Barbosa, G. A. M. 1983. Ciclo biol6gico de la arafia roja del aguacatero Oligonychus punicae (Hirst) en estudio de laboratorio. Tesis profesional. Chapingo. 52 PP. Belloti, A. C. 1985. Cassava. pp. 333-338. In: Helle W. and M.W. Sabelis (eds.). Spider Mites - Their Biology, Natural Enemies and Control. Vol. lB. Elsevier, The Netherlands. Colin, J. G. O. 1990. M6todos de control de las plagas m~is importantes en aguacate, pp. 119-125. En: Memorias CIC-Fruticola CICTAMEX. Coatepec Harinas, Mexico. Colin, J. G. O. 1991. M6todos de control de Plagas en el cultivo del aguacate, pp. 121-126. En: Memorias. Centro de Investigaciones Cientificas y Tecnol6gicas del Aguacate en el Estado de M6xico. Coatepec Harinas, M6xico. Colin, J. G. O. and M. A. Rubi. 1992. Determinaci6n de la susceptibilidad de ocho selecciones de aguacate al ataque de arafia roja y trips, pp. 149-155. En: Memorias Centro de Investigaciones Cientificas y Tecnol6gicas del Aguacate en el Estado de M6xico. De Leon, D. and E. Tennessee. 1962. Three new genera and seven new species of cheyletids (Acarina: Cheyletidae). Fla. Entomol. 45(3): 129-137. Estdbanes-Gonzfilez M. L. and S Rodriguez-Navarro. 1998. Algunas especies de ~icaros depredadores (Acari: Phytoseiidae) y sus presas (Acari-Tetranychidae. Eriophyidae) en cultivos de importancia econ6mica en M6xico. Folia Ent. Mex. 102: 77-79. Gallegos, E. R. 1983. Algunos aspectos del aguacate y su producci6n en Michoac~. Universidad Aut6noma Chapingo. M6xico. 317 pp. Laing J. E. and N. F. Knop. 1982. Potential use of predaceous mites other than Phytoseiidae for biological control of orchard pests, pp. 28-35. In: Hoy, M , G. L. Cunningham and L. 1. Knutson (eds.). Biological Control of Pest by Mites. Div. Agric. Nat. Resour. Univesity of Califomia. Lindquist, E. E. and J. W. Amrine. 1996. Systematics, diagnosis for major taxa, and keys to families and genera with species on plants of economic importance, pp. 33-87. ln: E. E. Lindquist, M. W. Sabelis and J. Bruin (eds.). Eriophyoid Mites their Biol-

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ogy, Natural Enemies and Control. Elsevier, The Netherlands. Martinez, B. R. 1989. El cultivo del aguacate en M6xico, sus problemas fitosanitarios, soluciones y perspectivas. Fruticultura de Michoac&n. 2: 7-13. McMurtry, J. A. 1985. Avocado. pp. 327-333. In: Helle W. and M. W. Sabelis (eds.). Spider Mites -Ttheir Biology, Natural Enemies and Control. Vol. lB. Elsevier, The Netherlands. McMurtry, J. A., M. H. Badii and B. D. Congdon. 1985. Studies on a Euseius species complex on avocado in M6xico and Central America, with a description of a new species. (Acari: Phytoseiidae). Acarologia. XXVI(2): 107-116. McMurtry, J. A. and G. T. Scriven. 1964. Studies on the feeding, reproduction, and development of Amblyseius hibisci (Acarina: Phytoseiidae) on various food substances. Ann. Entomol. Soc. Amer. 57: 649655. McMurtry, J. A. and G. T. Scriven. 1965. Life-History studies of Amblyseius limonicus with comparative observations onAmblyseius hibisci (Acarina: Phytoseiidae). Ann. Entomol. Soc. Amer. 58:106-111. McMurtry, J. A. and G. T. Scriven. 1971. Predation by Amblyseius limonieus on Oligonychus punicae (Acarina): Effects on initial predator-prey ratios and prey distribution. Ann. Entomol. Soc. Amer. 71: 219-224. McMurtry, J. A. and H.G. Johnson. 1966. An ecological study of the spider mite Oligonychuspunicae (Hirst) and its natural enemies. Hilgardia, 37:363-402. McMurtry, J. A., H. G. Johnson and G.T. Striven. 1969. Experiments to determine effects of mass releases of Stethorus picipes on the level of infestation of the avocado brown mite, J. Econ. Entomol. 62: 12161221. Muma, M.H. 1964. Cheyletidae (Acarina: Trombidiformes) associated with citrus in Florida. Fla. Entomol. 47(4): 239-253. Perring, M. T. and J. A. McMurtry. 1996, Other predatory arthropods, pp 471-479. In: E. E. Lindquist, M. W. Sabelis and J. Bruin (eds). Eriphyoid Mites - Their Biology, Natural Enemies and Control. Elsevier, The Netherlands. Ramirez, D. M. 1992. Constantes T6rmicas y Tablas de Vida para Oligonychus perseae Tuttle, Baker y Abbatiello (Trombidiformes: Tetranychidae). Tesis Profesional. Chapingo. 52 pp. Reyes, J. C., A. M. RuN and M. Salgado. 1993. Dinhrnica poblacional de la arafia roja (Oligonychus punicae Hirst) en 16 selecciones de aguacate. En: Memoria de Actividades. Fundaci6n Smachez Colin CICTAMEX, S.C. Coatepec Harinas, M6xico: 213-223.


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