2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA)

CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ1

Gladys González Dufau2; Julio Santamaría Guerra3

RESUMEN El control biológico es considerado un componente esencial y viable en el manejo integrado de plagas (MIP) y con el movimiento actual hacia la agricultura sostenible, se espera que juegue una función relevante en el MIP. El objetivo del trabajo fue revisar los esfuerzos de investigación realizados para el manejo integrado de la mosca blanca de los invernaderos T. vaporariorum, que afecta la producción de tomates bajo el sistema de cultivo protegido en tierras altas en Panamá. Se revisó la identidad y atributos biológicos de la plaga y sus enemigos naturales, se resumió los estudios llevados a cabo en ellos, así como se documentó los esfuerzos actuales en el control biológico del complejo mosca blanca tanto en cultivos protegidos como en campo abierto. Esta revisión permitió recomendar temas de investigación para el desarrollo de estrategias sostenibles, seguras y eficaces para el control de la mosca blanca que ataca los tomates bajo cultivo protegido en Panamá. La realización exitosa de estas recomendaciones podría proporcionar una alternativa eficaz al control químico, especialmente bajo cultivo protegido, y reducir drásticamente el uso intensivo de insecticidas químicos costosos y tóxicos. También, puede tener aplicación en una amplia gama de cultivos y ofrece insumos para una estrategia de manejo integrado de cultivos con énfasis en Control Biológico bajo el enfoque de Gestión Integrada del Conocimiento y la Innovación, con la participación activa de los principales interesados locales.

PALABRAS CLAVES: Manejo integrado de plagas, control biológico de conservación, parasitoides, artrópodos depredadores, entomopatógenos.

1Recepción: 13 de junio de 2014. Aceptación: 6 de marzo de 2015. 2M.Sc. en Entomología. IDIAP. Centro de Investigación Agropecuaria Occidental (CIAOc). e-mail: [email protected] 3Ph.D. en Innovación Institucional. IDIAP. CIAOc. e-mail: [email protected]

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BIOLOGICAL CONTROL: AN INTEGRATED MANAGEMENT ALTERNATIVE FOR Trialeurodes vaporariorum IN GREENHOUSES

ABSTRACT Biological control is considered an essential and viable component for integrated pest management (IPM), and with the current movement towards sustainable agriculture, biological control can be expected to play an even more extensive role in IPM. The objective of this review is to go through the current efforts on biological control of the greenhouse whitefly (Trialeurodes vaporariorum), and finally suggest research topics to develop sustainable safe and effective control strategies for whitefly damaging tomatoes under protected cultivation in Panama. The identity and biological attributes of the pest and its natural enemies is reviewed, related studies are summarized and current efforts to biological control of whitefly complex, both protected and open field crops are documented. This review allows recommending research topics to develop sustainable, safe and effective control strategies for whitefly attacking tomatoes in Panama under protected cultivation. Successful completion of these recommendations could provide an effective alternative for chemical control to Panamanian producers, especially under protected cultivation, and sharply reduce the current heavy use of expensive and toxic chemical insecticides. The result may have application in a range of cropping system and offers inputs for a strategy on integrated crop management, emphasizing on Biological Control under Integrated Knowledge and Innovation Management with active participation of the local main stake holders.

KEY WORDS: Integrated pest management, conservation biological control, parasiotids, artropod predators, pathogens.

INTRODUCCTION this objective could provide an effective The objective of this review is to alternative to chemical control for go through what have been done on this Panamanian growers and sharply reduce matter and finally suggest research topics the current heavy use of expensive and to develop sustainable safe and effective toxic chemical insecticides. Moreover, the control strategies for whitefly damaging results will be broadly applicable in view of tomatoes under protected cultivation in the importance and wide distribution of this Panama. The general approach is to insect pest throughout Central America study and achieve the potential biological Region. The result may have application control of the naturally present parasitoids in a range of cropping system. It may in Panama. Successful completion of help also to establish biological control

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 87 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA) as a reliable alternative in devising pest field crops and their associated hazards management strategies in Panamanian in the environment. Whitefly parasitoids agriculture. are an addition to the natural enemy’s pool and any control management should The extensive use of chemical be integrated, mainly for those where pesticides with the consequent results individual strategies alone are inadequate. in development of insect resistance, adverse effects on beneficial insects Our understanding of the role of and wildlife, residues in food crops and naturally present whiteflies parasitoids associated danger to human health, in Panama is clearly deficient and efforts has increased the demand for the to integrate specimens identification development of environmental and human with pathogenic efficacy criteria should friendly alternative control measures. be encouraged, as such studies One alternative method is the use of provide fundamental knowledge useful biological control agents. Biological in increasing our ability to use them control is considered an essential and effectively for biological control. Moreover viable component for integrated pest biological control with Encarsia formosa, management (IPM), and with the current which has been successfully used in movement toward sustainable agriculture greenhouse on greenhouse whitefly, biological control can be expected to play Trialeurodes vaporariorum turned out to an even more substantial role for IPM. As be less effective (Hoddle and Driesche an applied science, biological control often 1996). Selecting more efficient parasitoids involves releases of exotic natural enemies for B. tabaci B biotype is urgently needed. in an attempt to suppress introduced pest species in agriculture, forestry, and Polaszek et al. (1992), stated human health, but it is also implemented that “A trough taxonomic study of all B. trough the augmentation or conservation tabaci parasitoids is necessary, given the of native natural enemies (Gaugler 2002). urgent necessity of identifying at least the Biological control is operationally defined known species which could be used, in as the action of natural enemies which biological control programmes“. Hanson maintains a host population at levels lower (1995) pointed out that our knowledge than would occur in the absence of the of parasitoids is limited and there are enemies (Ehler 1990). The development several current research need such as: of techniques for biological control can 1) to confirm identification of whitefly effectively reduce the use of chemicals on parasitoids, 2) to determine the efficacy

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 88 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA) of whitefly parasitoids already existing in particularly organophosphates and their natural agroecosystem. synthetic pyrethroids (Prabhaker et al. 1985, Horiwitz et al. 1988, Dittrich and Information about this will allow us Ernt 1990, Horiwitz et al. 2007). Another to improve the potential control of naturally problem is the decrease or extermination present parasitoids against whiteflies in of naturally occurring enemies as a result Panama. of excessive use of chemical control (Eveleens 1983), the cultivation of virus- Whitefly and its control susceptible plant varieties, the movement The whitefly species, Trialeurodes of infected plant material and the recent vaporariorum, and B. tabaci B biotype emergence of new highly virulent races or (Homoptera: Aleyrodidae) have enormous biotypes of whiteflies (Brown et al. 1995). economic impacts in temperate and B. tabaci is known to transmit at least 19 tropical regions of the world, damaging plant viruses, including tobacco leaf curl, many different crops in both outdoor and mosaic and cucumber yellows greenhouse crops (Mound and Halsey (Brunt 1986). Today, the prevention of 1978, Lenteren and Woet 1988, Perring et these virus-caused losses by whiteflies is al. 1993, Brown et al. 1995, Menn 1996). a matter of worldwide high priority (FAO Apart from the direct feeding damage, 1994). This worldwide importance of virus transmission and fungal growth on whiteflies as pests is well illustrated by honeydew also cause mayor yield losses. the compilated work by Gerling (1990), Several sources indicate crop value losses Gerling and Mayer (1996), Naranjo et al. exceeding $500 million annually since (1999), listing some 323 references. 1991 for the United States (Naranjo et al. 1998, Perring et al. 1993). In addition Whitefly Biology, Pest Status and to its economic cost, reliance on periodic Taxonomy application of insecticides for whitefly Biology management causes others problems. Whiteflies are small sucking insects Several factors within agricultural (Martin 1987). They are often present in production systems have contributed to great numbers on the underside of leaves increasing cost of whitefly control (Castle and may be abundant on greenhouse 1999). One problem is the development and house plants as well as on wild of widespread of resistance (including plants. Whitefly adults lay eggs and cross-resistance) of whiteflies to many immature stages of whitefly develop on commonly used conventional insecticides the undersides of leaves on most crops

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(Byrne and Bellows 1991, Costa et al. Whiteflies also excrete honeydew, which 1991). Adults congregate, feed, mate, promotes sooty mold that interferes with and oviposit on the undersurfaces of the photosynthesis and may lower harvest leaves of the host plant. This can occur in quality. In some hosts, damage can such numbers as to create clouds when result from whitefly feeding toxins, which disturbed, oviposition is heaviest on these cause plant disorders such as silver leaves. The location on the plant of the leaf of squash and irregular ripening of various stages of the whitefly follows the tomato. Whiteflies, also transmits viruses, development of the plant. Eggs and early such as the geminiviruses in tomatoes, instar nymphs are found on the young peppers and cabbage (Polston and leaves and larger nymphs are usually Anderson 1999). Plant disorders and virus more numerous on older leaves (Butler transmissions are of particular concern et al. 1983, Berlinger et al. 1985, Cock because they can occur even when a 1986). Adult appear to be more active whitefly population is small. In general, the during sunny daylight periods, and do older the plant when infected with virus or not fly as readily during early morning, the later the onset of plant disorders, the late evening, or night hours. The nymphal less damage to the crop, so prevention of stages are sedentary, with the exception early development of whitefly populations of the crawler, which after hatching moves is critical. Prevention is also crucial in over a short distance. Once a feeding managing whiteflies in crops with high site is selected the nymphs do not move cosmetic value such as ornamental plants, anymore. They suck juices from the where even low numbers of whiteflies plant phloem with their piercing-sucking can affect marketability (Hoelmer et al. mouthparts. The nymphs are located on the 1991). Excessive B. tabaci induced losses undersides of the leaves and can become worldwide occur in field, vegetable and so numerous that they almost cover the ornamental crop production. Losses entire undersurface area (Coudriet et occur from plant diseases caused by B. al. 1985, Horiwitz and Gerling 1992, Gill tabaci transmitted viruses, direct feeding 1990, Powell and Bellows 1992a, 1992b). damage, plant physiological disorders, and honeydew contamination and associated Injury caused by whiteflies fungal growth. The number of B. tabaci Direct crop damage occurs when transmitted plant viruses has increased, whiteflies feed on plant phloem, remove and total yield losses of important food plant sap and reduce plant vigour. With and industrial crops has occurred (Oliveira high whitefly populations plants may die. et al. 2001).

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Taxonomy hosts not yet formally documented. The recent outbreaks of Bemisia Biotypes have been identified in different sp. (Gennadius) morphotypes has areas of the world suggesting that stimulated a renewed interest in whitefly B. tabaci may be a species-complex systematics (Perring et al. 1993), which undergoing evolutionary change. These was limited until then (Campbell et al. biotypes may exhibit differences in viruses 1996). Further, increased international transmitted and transmission efficiency, trade and travel are providing additional rates of development, endosymbionts, routes for introduction of exotic species host utilization, and physiological host and/or biotypes of whitefly, as well as damage (Oliveira et al. 2001). Accurate their parasitoids, on a worldwide scale. species identification for both, pest The ability to identify closely related but species as well as their parasitoids, is morphological indistinguishable species an increasingly important component or atypical morphological strains is for the recommendation of appropriate critical for determining the geographic management practices (Neal and Bentz origin of a newly introduced whitefly 1999), particularly in biological control. pest and consequently their parasitoids. Knowing the geographic origin is vital One approach towards a better to the search for natural enemies used understanding of whitefly parasitoids in biological control programs (Gerling taxonomy is through molecular techniques. 1990). Moreover, early morphological Whitefly parasitoids are worthy candidates identification of structures of pupal exuviae for molecular phylogenetic analyses is important, because the identification to aid in establishing sound higher of whitefly species is often based on the level taxonomic groups and species pupal stage (Gill and Mayer 1996). Mound identifications because their morphological and Halsey (1978) also noted that pupal distinctions are still unclear (Campbell et case morphology varied on different host al. 1996). Moreover, a thorough taxonomic leaves and that this has resulted in name study of parasitoids of important whitefly synonymy. According to this, Rosell et pest species is therefore necessary given al. (1996) state that polymorphism and the urgent necessity for identifying at least plasticity within the global population of the known species of parasitoids used, in whitefly exists to a greater degree than has biological control programs or those, which been documented until now. B. tabaci has could be, used in the future (Polaszek et been recorded from more than 600 plant al. 1992). Ribosomal (rDNA) is present species and there may be many additional in all organisms, and is composed of

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 91 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA) several regions (genes and spacers) that members of the squash family (squash, evolve at different rates. Ribosomal DNA melons, cucumbers, pumpkins), tomato sequences are suitable for phylogenetic family (tomato, eggplant, ), cotton studies at many taxonomic levels: from family (cotton, okra, hibiscus), bean family major lineages of life to intraspecific levels (beans, , peanuts), Gerbera (Hillis and Dixon 1991). At the species and daisies, salvia, poinsettia, and many other intraspecific levels, the internal transcribed weeds and ornamental plants (Mound spacer regions (ITS-1 and ITS-2) are often and Halsey 1978, Arnal et al. 1993). used as a taxonomic tool in many groups In Panama, Valderrama et al. (1994) such as fungi (e.g. Campbell et al. 1993, reported transmission of a geminivirus Hoy 1994; Kuperus and Chapco 1994). associated with B. tabaci in tomato. The sequencing and restriction analysis Regarding the field of hosts, the virus of ITS rDNA have been described as infected plants of the Solanacea (Solanum promising and/or effective in distinguishing esculentum, Nicotiana tabacum y Sansum Trichograma individuals from different annum, Capsicum annum), Leguminosae populations (Orrego and Agudelo-Silva (Phaseolus vulgaris) and Malvaceae 1993, Pinto et al. 1997, Sappal et al. 1995, (Hibiscus esculentum, Sida sp. and Schilthuizen and Stouhamer 1997). Most Malachra alcetifolia) families. Aditionally, analyses of relationship have been based Osorio (1998) informed 23 species of on internal and external morphological weeds as host plants of B. tabaci in Los traits, but molecular techniques are Santos province belonging to the family now being applied to understanding the Asteraceae, Euphorbiaceae, Malvaceae, higher phylogeny of the Chalcidoidea and Solanaceae, Tiliaceae and Fabaceae. the relationships among species of the genus Encarsia between others (Babcock The whitefly problem in Panama and Heraty 2000, De Barro et al. 2000, Agriculture in Panama is largely Campbell et al. 2000). centered in Chiriquí Province, sometimes referred to as the breadbasket of Panama. Host Plants of Whitefly Although agriculture is diverse, tomatoes Trialeurodes vaporariorum and and onions are the most important Bemisia tabaci are highly polyphagous horticultural commodities and the basic species, currently known from more than staples in Chiriquí, as they are in Central 500 species of host plants (Greathead America (González 1998). However 1986) representing 74 plant families. tomato yields in Panama are much lower They have been a particular problem on than the potential yield of the varieties

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 92 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA) that are used. One seriously limiting import of insecticides by the order of 3%, yields factor is the damage caused by resulting on one hand, capital flight and in whitefly, which is considered as one of the the other an increase in production costs most important insect pest of this crop in (González et al. 2009). Moreover, there are Panama (Gonzalez et al. 1994, Sánchez potentially more risk of an indiscriminate and Serrano 1994). Valderrama et al. use of pesticides which might cause (1994) reported that since 1991, tomato environmental problems and represent in Azuero Region is affected by a viruse a global concern. There are, however, disease transmitted Bemisia tabaci. In few alternative technologies available for addition, in Azuero region, Ferguson farmers for whitefly control. Historically (1994) found from population dynamic very little has been done in Panama to studies that there are three populations develop or improve technical knowledge peaks: 1) January/March (weeks 13-21); 2) about the ecological interrelationships and April/May (weeks 25-30); 3) June/August its effect on agricultural productivity, since (weeks 36-45). Biologically based control its economy has been based mainly on efforts to date have been very limited the service sector. The National Institute due to a lack of effective control agents for Agricultural Research has increased available for farmers. Chemical control, information on environmental effects of when used, is usually by application of agriculture and pest control during the the acephate, which is a very expensive last 10 years i.e. compared research and dangerous chemical in view of its done in 1984 and 2010, there has been high mammalian toxicity. The hazard an increased on the priority of friendly potential is particularly acute in Chiriqui alternative research in crop protection from because growers are not trained in the 20 percent to 90 percent. Nevertheless proper application of toxic chemicals. It is more effort needs to be done, in order common to see farmers wash out a tank to get growers aware of alternatives for of pesticide in a stream also used it for chemical control. drinking water, washing and recreation. Panama imported approximately 241 Information from Central America million of agrochemicals in 2009 (MIDA). and Panama species of whiteflies Of these imported agrochemicals, 83% parasitoids is sparse (King y Saunders were defensive products, some of them 1984). Mound and Halsey (1978) highly toxic insecticides. Regarding wrote and excellent but short report insecticidal importation during the last on Panamanian species, it discusses five years, there was an increase in the only four species (out of 1156 species

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 93 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA) worldwide) that inhabit in Panama, within Trialeurodes variabilis, Aleurothrixus four genera and two families. Nonetheless, floccosus, Aleuroplatus sp., Trialeurodes the worldwide distributed genus Bemisia acaciae. and species of Trialeurodes vaporariorum are not indicated to be present in Panama Natural Enemies of Whitefly by these authors. It is known from The main groups of whiteflie natural the literature that Bemisia B biotype is enemies are predators, pathogens and actually present in Panama (Brown et al. parasitoids. 1995), and more recently, Name (2000) indicate as a result of a survey in Chiriqui Predators. About 75 species province, a preliminary distribution of prey upon whiteflies, especially general the species Trialeurodes vaporariorum predators such as spiders, beetles, and Bemisia tabaci of which, Bemisia etc. Individual predator species in the tabaci was the predominant whitefly families Anthocoridae, Coccinellidae, species in the lowlands, and Trialeurodes Chrysopidae, Hemerobiidae and most vaporariorum is more abundant at higher of the Miridae are unable to maintain altitudes (above 1200 m). Bemisia greenhouse whitefly numbers below tabaci biotype B in the lowlands was damaging levels, although inundative also found by Fernandez 20014. Bemisia releases of a complex of predators may do tabaci biotype B is polyphagous, attacks so (Heinz 1996). Some predatory bugs in a range of glasshouse and field crops, the genera Macrolophus or Dicyphus can and often causes phythotoxic damage sufficiently reduce whitefly populations (CABI 1999a, 1999b). In Central America, (Onillon 1990), although some also 14 species within 10 genera in two sub- damage plants. In warm climates, where families (Aleurodicinae and Aleyrodinae) greenhouses often have large ventilation of whiteflies have been reported: openings, generalist predators move in Paraleyrodes sp., Ceraleurodicus naturally and may cause considerable altissimus, Aleurodicus cocois, mortality of whiteflies. Aleurocanthus woglumi, Dialeurodes citrifolii, Tetraleurodes mori, Tretraleurodes Pathogens. In general, pathogens abutiloneus, Trialeurodes vaporariorum, of insects belong to very different taxonomic Trialeurodes floridensis, Bemisia tabaci, groups like viruses, bacteria, protozoa,

4Fernández, O. 2001. Department of Virology (interview). IDIAP (National Institute of Agricultural Research). Panama. Panama.

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 94 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA) rickettsiae, fungi and entomophagous Two categories of fungi that nematodes. The spectrum of whitefly attack whitefly can be distinguished: pathogens is narrow. There are no records fungi specialized on Aleyrodidae like of nematodes parasitizing whiteflies. While Aschersonia spp. and Conidiobolus it is possible that viruses or bacteria kill spp. (Fransen 1990, Gidin and Ben whiteflies, this is mainly due to secondary Ze’ev 1994). And broad-spectrum fungi, infections by entrance through existing containing various genera like Beauveria, wounds. So far, the pathogens reported Lecanicillium and Isaria, which can infect from Aleyrodidae have been exclusively insects belonging to different orders. fungi, because only they are able to infect these plant-sucking insects by penetrating Aschersonia fungi have an the cuticle. Four genera of fungi attacking essentially tropical and sub-tropical whitefly are regularly mentioned in the distribution. They have been successfully literature: Beauveria, Aschersonia, applied and established to control whiteflies Lecanicillium a genus formerly known on citrus and additionally, they have been as Verticillium and Isaria also formerly tested against the greenhouse whitefly known as Paecilomyces (Vega et al. in glasshouses of Central and Eastern 2009). Entomopathogenic fungi infest Europe and some Oriental countries their aleyrodid hosts by penetrating the (Fransen 1990). Aschersonia isolates cuticle after the conidiospores germinates. may kill up to 90% of T. vaporariorum and Subsequently, various fungal structures B. tabaci B biotype Bellows and Perring are produced, which circulate in the at greenhouse experimental conditions haemolymph, invading the insect’s organs (Meekes 2001). Aschersonia spp. equally and probably producing lethal toxins attacked T. vaporariorum and B. argentifolii (Fransen 1990). One major limitation of Bellows and Perring and caused the same entomopathogenic fungi as biological mortality levels for both whitefly species control agent is their needs for high (Meekes et al. 1996). In fact, each fungus humidity to germinated and infect the host that is introduced to control Bemisia, will (Lacey et al. 1995). Another limitation almost certainly affect T. vaporariorum. comprises the restrictions placed on the use of so-called exotic strains that could Most research has been done harm non-target organisms (Lacey et al. on Beauveria, Lecanicillium and Isaria 1995). because they are broad-spectrum

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 95 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA) fungi, and therefore, more attractive for injecting uninfected hosts. Lecanicillium commercial production. Lecanicillium lecanii did not directly infect the parasitoid lecanii (Zimm) Viegas seems promising for Amitus fuscipennis when they were controlling greenhouse whitefly, although tested together on T. vaporariorum, but an effective infection requires high relative the fungus seemed to decrease the humidity but moderate temperatures parasitoid’s parasitic activity (Pachón and (Ekbom 1979). Isaria fumorososeus Cotes 1997). var. beijingesis attacks T. vaporariorum on glasshouse cucumbers at moderate Parasitoids. About 100 species of whitefly temperatures and high relative humidity parasitoids are known and more species (Fransen 1990). are expected to be found. Most of the parasitoids are very host specific, but some So far Aschersonia is more difficult species are hyperparasitoids and their to produce commercially than the other importation might reduce the efficiency of fungi. It takes 14 days to mass-produce primary parasitoids, e.g. E. pergandiella Aschersonia spp. spores, whereas it only Howard in New Zealand. Many important takes five days to produce millions of whitefly parasitoids belongs to the genus Beauveria spores. Using fungi to control Encarsia, family Aphelinidae (Lenteren et insects is not only a question or using the al. 1997). They show a wide variety of best fungus species, but also a question reproductive behaviour (Gerlings 1990). of using the best commercial formulation Some species, like E. formosa are primary (Meekes 20015 ). thelytokus parasitoids, i.e. females are produced on a phytophagous host insect When reporting these fungi’s parthenogenetically. Other Encarsia interactions with other natural enemies, species are also primary parasitoids, but Fransen (1990) observed that populations produce haploid males from unfertilized of the parasitoid E. formosa Gahan eggs and diploid femeles from fertilized survived treatments with Aschersonia eggs, i.e. they are arrhenotokus. Still aleyrodis Webber and adult parasitoids did other species are arrhenotokous not become infected. E. formosa females hyperparasitoids and they produced may even help with fungal transmission males and femeles by laying eggs in by probing infested hosts, carrying other, inmmature parasitoids of a different fungal structures on their oviposition and species. Further, species are known where

5Meeke, E. 2001. Laboratory of Entomology (interview). Wageningen University. The Netherlands.

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 96 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA) one sex, usually the female, develops as Eretmocerus the most abundant for tomato a primary parasitoid, and the other sex, grown under field conditions in the southern the male, develops hyperparasitically on region known as Azuero (Ferguson 1994, their own or another species of parasitoid, Bernal 2001). More recently, Gonzalez et i.e. heteronomous hyperparasitoids or al. 2009 reported the genus: Encarsia (E. facultative autoparasitoids. bimaculata, E. hispida, E. pergandiella/ tabacivora, E. porteri, E. nigricephala, It has been extensively E. citrella, Encarsia sp.), Eretmocerus demonstrated in inoculative and (E. eremicus, Eretmocerus sp.), Amitus seasonal inoculative biological control (Amitus sp.), and a hyperparotoid that introductions with individuals of one Signiphora (S. aleyrodis). Other than this, parasitoids species and particularly with little is known regarding local data about E. formosa - are sufficient for economically biology of these parasitoids and their feasible whitefly control (Gerling 1990). efficiency in controlling whiteflies (Hanson In warm climates, like the Mediterranean 1995). area, parasitoids of whitefly may immigrate into greenhouses and provide natural pest Whitefly management methods control. During the past years others The management of insect pests parasitoids have been tested and used rarely relies on a single control practice; to control whiteflies, like species from usually varieties of tactics are integrated the genera Eretmocerus (Hymenoptera: to maintain pests at acceptable levels. The Aphelinidae) and Amitus (Hymenoptera: goal of integrated pest management is Plastygasteridae). not to eliminate all pests; some pests are tolerable and essential so that their natural Whitefly Natural Enemies in Panama enemies remain in the crop. Rather, the aim Russell (1962) describes natural is to reduce pest populations to less than enemies of whiteflies found in Panama damaging numbers. The control tactics of the genera Encarsia, Eretmocerus used in integrated pest management (Chalcidoidea: Aphelinidae) and Amitus include pest resistant or tolerant plants, hesperidius Silvestri; Amitus sp.; and cultural, physical, mechanical, Amitus hesperidius var variipes Silvestri biological, and chemical control. Applying (Proctotrupoidea: Plastygastenidae). multiple control tactics minimizes the Carreiro (1994) reported Eretmocerus, chance that insects will adapt to any one Encarsia and Aleurodiphilus (Aphelinidae) tactic. The definition for integrated pest as Bemisia tabaci parasitoids; being management most relevant comes from

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Flint and Bosch (1981): “An ecologically the risks to man and environment and based pest control strategy that relies the problem of development of resistance heavily on natural mortality factors and against insecticides by insects (Dittrich seeks out control tactics that disrupt these and Ernt 1990) are recognized and factors as little as possible”. alternatives are being considered. Years ago, development of resistance to certain Integrated pest management pesticides is reported of T. vaporariorum requires an understanding of the ecology and B. tabaci, as well as acceleration of the cropping system, including that of or resurgence of whitefly populations the pests, their natural enemies, and the through chemicals (Wardlow et al. 1976; surrounding environment. Knowledge Dittrich and Ernt 1990). Therefore, non- about the ecological interrelationships chemical control methods of whiteflies between insects and their environment is pests are being looked for. Monitoring critical to effective pest management. of whiteflies is used to trace the insects in a crop and to keep a record of their In natural ecosystems and presence. Alternative control methods agroecosystems where pesticides are are, for example, integrated pest not used, an array of natural enemies management and breeding for host plant usually keeps whiteflies at low numbers: resistance to insect. Biological control of predators, parasitoids and pathogens are whitefly (T. vaporariorum), an element of all influenced. Studies in two cropping integrated pest management, may offer systems, tomatoes in the 1960s in a possibility and several methods can be California and cotton during the period followed (Lenteren et al. 1996): 1925-1992 in Sudan, has shown that whiteflies can be kept under perfect natural (1) Conservation biological control gives control (Lenteren et al. 1996). However, emphasis to the preservation and when pesticides are applied, natural enhancement of natural enemies enemies are exterminated resulting in and is the basis of all approaches to whitefly pest outbreaks, in the above biological control. Conservation of mentioned cases T. vaporariorum and B. natural enemies is often credited with tabaci, respectively. being the oldest form of biological control. However, compared In protected crops, the low tolerance with classical and augmentation of pest insect is reflected by widespread and biological control it has received frequent use of insecticides. Nowadays, relatively little attention as a method

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of arthropod pest suppression (Ehler (4) The seasonal inoculative release 1998). It can be broadly categorized method. This method differs into three overlapping components essencially from the above which encompass survey and mentioned inundative releases in potential of extant natural enemies, the fact that buildup of the natural elucidation and manipulation of enemy population for control later factors constraining or enhancing during the same season is pursued. natural enemy abundance and Thus, it requires several generations activity, and evaluation of biological of natural enemies and pest control efficacy (Naranjo 2001). insects in a crop. The approach is successfully applied in the control (2) The inoculative release method. of T. vaporariorum by E. formosa in Beneficial organisms are collected protected tomato crops (Lenteren in a region from which the pest and Woets 1988). insect originates and introduced in relatively small numbers in a region Any control method alone is where the pest was introduced. The not able to manage with the complex aim is a long term control effect and problematic situation described above. the method has been successful Futhermore, many of the management when a continuous existence of the strategies are applied without taking natural enemy was possible (Onillon into account local knowledge, farmer’s 1990). perceptions and other actors’ initiatives in rural areas (Santamaría Guerra 2012). (3) The inundative release method. In the framework of the contextual Beneficial organisms are released theory of action, Integrated Knowledge periodically in large numbers in a and Innovation Management, from a crop for immediate control. This holistic, systemic and committed to the requires mass rearing of the natural context of its application and implications enemy. Illustrating examples are perspective offers alternatives to the need the release of E. formosa against to improve efficiency and relevancy levels B. tabaci in poinsettia and the of development organizations and their application of entomopathogenic contribution to a productive and institutional fungi against T. vaporariorum (Albert innovation (Santamaría Guerra 2011). 1990, Fransen 1990, Meekes 2001).

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Final Recommendations for the whitefly pest species and their Integrated Pest Management Research natural enemies. As advanced previously this review 5. Determine the population dynamics allows recommending research topics to of the most important whitefly develop sustainable safe and effective pest species in Panamanian control strategies for whitefly attacking greenhouses. tomatoes in Panama under protected 6. Determine and compare efficiency cultivation. Moreover, the results will of Eretmocerus sp. (Chalcidoidea: be broadly applicable in view of the Aphelinidae), a naturally present importance and wide distribution of this parasitoid genus in Panama. insect pest throughout the country. The 7. Present a proposal of a strategy on result may have application in a range integrated tomato crop management of cropping system. It may help also to with emphasis on Biological Control establish biological control as a reliable under Integrated Knowledge and alternative in devising pest management Innovation Management with the strategies under protected cultivation in active participation of the local main Panama. stake holders.

The following research activities should be Rational choices regarding pest implemented management strategies require by definition a thorough understanding of the 1. Identification of the most abundant basic life history parameters of the insect whitefly pest species present in pest. Present information on whitefly tomato in Panama. pest species of whitefly is inadequate 2. Identification of the most abundant in Panama to implement any control naturally present parasitoids of strategy, chemical, biological or other. whiteflies in tomato and other host Since control efficacy can vary with life plants in Panama. stages and whiteflies species, a study of 3. Review, develop and apply all life stages of the whitefly pest species identification molecular techniques is necessary. Further, optimal application on the important pest’s parasitoids of any control agent requires the capability species of whiteflies based on the of predicting patterns of abundance PCR technique. (temporal and geographical). Information 4. Describe the basic life history derived from the above recommendations parameters of the most important will serve the dual function of (1) providing

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 100 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA) a basis for biological control, (2) providing Institut für Phytopathologie und the framework for the development of Angewandte Zoologie der Justus- contextual managerial strategies. Liebig-Universität Giessen. 136 p.

LITERATURE Brown, JK; Coats, SA; Bedford, ID; Albert, R. 1990. Experiences with biological Markkham, P; Bird, J; Frolinch, DR. control measures in glasshouses in 1995. Biochemical Genetics. 33: Southwest Germany. Bull. IOBC/ 205-214. [Biotype B]. WPRS 13(5):1-5. Brunt, AA. 1986. Transmission of Arnal, E; Russell, LM; Debrot, E; Ramos, F; diseases. In Cock, MJW. (Ed.) Cermeli, M; Mercano, R; Montagne, Bemisia tabaci: a literature survey A. 1993. A listing of white flies and on the cotton whitefly with an their host plants in Venezuela. annotated bibliography. 121 p. CAB Florida Entomologist 76:365-381. International Institute of Biological Control, Ascot, UK. p. 43-50. Babcock, CS; Heraty, JM. 2000. Molecular marker for the discrimination of Butler, GD; Henneberry, TJ; Clayton, TE. Encarsia formosa and Encarsia 1983. Bemisia tabaci (Homoptera: luteola (Hymenoptera:Aphelinidae). Aleyrodidae): development, Annals of the Entomological Society oviposition, and longevity in relation of America. 93:738-744. to temperature. Annals of the Entomological Society of America Berlinger, MJ; Dahan, R; Mordechi, 76:310-313. S. 1985. Photoperiodism in the tobacco whitefly, Bemisia tabaci. Byrne, DN; Bellows, TS. 1991. Whitefly Phytoparasitica 13:74. biology. Annual Review of Entomology 36:431-457. Bernal V., JA. 2001. Untersuchung zum Einsatz natürlicher und CABI/EEPPO. CAB International. synthetischer Insektizide und 1999a. Bemisia tabaci. biotype B. zur Parasitierung von Bemisia Distribution Maps of Plant Pest N° tabaci (Gennadius) (Homoptera: 284. CAB International, Wallingford, Aleyrodidae) im Tomatenanbau U.K. in Panama. Dissertationsschrift,

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 101 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA)

CABI/EEPPO. CAB International. 1999b. Castle, SJ. 1999. Agricultural and pest Bemisia tabaci. biotype B. Distribution outbreaks: a reappraisal of events Maps of Plant Pest N° 591.CAB in the Sudan Gezira. Ann. Entomol. International, Wallingford, U.K. Soc. Am. 92(6):840-852.

Campbell, BC; Duffus, JE; Baumann, P. Cock, MJW. 1986. Bemisia tabaci: a 1993. Determining whitefly species. literature survey on the cotton Science 261: 1333. whitefly with an annotated bibliography. In Commonwealth Campbell, B; Heraty, J; Rasplus, JY; Chan, Institute of Biological Control, Ascot, K; Steffen-Campbell, J; Babcock, U.K. 121 p. C. 2000. Molecular systematics of the Chalcidoidea using 28S-D2 Costa, HS; Brown, JK; Byrne, DN. 1991. rDNA. In Hymenoptera—evolution, Life history traits of the whitefly, biodiversity and biological control. Bemisia tabaci on six virus- Andrew, A; Dowton, M (eds). CSIRO infected or healthy plant species. Publishing, Collingwood, Australia. Environmental Entomologist p. 59-73. 20(4):1102-1107.

Campbell, BC; Steffen-Campbell, JD; Coudriet, DL; Prabhaker, N; Kishaba, Gill, RJ. 1996. Origin and radiation AN; Meyerdirk, DE. 1985. Variation of whiteflies: an initial molecular in developmental rate on different phylogenetic assessment. In hosts and over wintering of the D. Gerling (ed.). Bemisia 1995: sweetpotato whitefly, Bemisia Taxonomy, Pest Status and tabaci (Homoptera: Aleyrodidae). Management. Intercep, Andover, Environm. Entomol. 14: 516-519. Hants. p. 29-52. De Barro, PJ; Driver, F; Naumann, ID; Clarke, Carreiro H, R. 1994. Análisis del complejo GM; Curran, J. 2000. Descriptions de enemigos naturales de Bemisia of three species of Eretmocerus tabaci (Gennadius) (Homoptera: Haldeman (Hymenoptera: Aleyrodidae), en la península de Aphelinidae) parasitising Bemisia Azuero, Panamá. Tesis de Maestría tabaci (Gennadius) (Hemiptera: en Entomología. Universidad Aleyrodidae) and Trialeurodes Nacional de Panamá. 89 p. vaporariorum (Westwood)

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 102 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA)

(Hemiptera: Aleyrodidae) in Eveleens, KG. 1983. Cotton-insect control Australia based on morphological in the Sudan Gezira: analysis of a and molecular data. Journal Aust. J. crisis. Crop Prot. 2:273-287. Entomol. In press. FAO (World Organization for Food Plant Dittrich, V; Ernt, GH. 1990. Chemical control Protection Bulletin). 1994. Plant and insecticide resistance of whitefly. Prot. Bull. v. 42/1-2:1. In Whiteflies: their Bionomics. Pest Status and Management. Ed. D. Ferguson G, OL. 1994. Dinámica Gerling, Intercept Ltd, Andover UK. poblacional de Bemisia tabaci p. 263-285. (Gennadius) (Homoptera: Aleyrodidae), en la península de Ehler, LE. 1990. Some contemporary Azuero, Panamá. Tesis de Maestría issues in biological control of insects en Entomología. Universidad and their relevance to the use of Nacional de Panamá. 98 p. entomopathogenic nematodes. In R. Gaugler and H.K. Haya (eds.). Flint, ML; Bosch, R van den. 1981. Entomopathogenic nematodes in Introduction to Integrated Pest biological control. CRC Press, Boca Management. New York: Plenum Raton, USA. p. 1-19. Press. 240 p.

Ehler, LE. 1998. Conservation biological Fransen, JJ. 1990. Natural enemies of control: past, present, and future. whitefly: Fungi. In D. Gerling (ed.), In Barbosa, P. (Ed.), Conservation Whiteflies: Their bionomic, Pest Biological Control. Academic Press, Status and Management, Intercept New York, p. 1-8. Ltd, Andover, Hants, p.187-210.

Ekbom, BS. 1979. Investgations on Gaugler, R. (Ed.). 2002. Entomopathogenic the potential of a parasitic fungus Nematology. CABI. 388 p. (Verticillium lecanii) for biological control of the greenhouse whitefly Gerling, D (ed.).1990. Whiteflies: Their Trialeurodes vaporariorum. Swedish Bionomics, Pest Status and Journal of Agriculture Research Management. Intercep, Andover, 9:129-138. Hants.

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 103 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA)

Gerling, D; Mayer, RT (eds.) 1996. Bemisia parasitoides de la mosca blanca en 1995: Taxonomy, Biology, Damage, Panamá. Instituto de Investigación Control and Management. Intercep, Agropecuaria de Panamá. Nota Andover, Hants. de Investigación en Progreso, N°2 febrero 2009. ISSN 0257-7127. 4 p. Gidin, G; Ben Ze’ev, IS. 1994. Virulence and persistence of Conidiobolus Greathead, AH. 1986. Host Plants. In coronatus and Conidiobolus sp. In Cock, MJW. (Ed.) Bemisia tabaci : a glasshouse populations of Bemisia literature survey on the cotton whitefly tabaci. IOBC Bulletin 17/3:185-188. with an annotated bibliography. CAB International Institute of Biological Gill, RJ. 1990. The morphology of Control, Ascot, UK. p. 17-25. whiteflies. In D.Gerling (ed.). Whiteflies: Their Bionomics, Pest Hanson, P. 1995. Potencial para la Status and Management. Intercep, implementación del control biológico Andover, Hants. p.13-46. de la mosca blanca por parasitoides. Comisión Nacional de Moscas González D, GI. 1998. Proyecto sobre blancas MAG-UCR-UNA-CATIE, Investigación en Control Biológico San José, Costa Rica. In 2. Taller en tomate y cebolla: una oportunidad Nacional sobre Moscas Blancas. de desarrollo sostenible. Instituto Alajuela, CR. 4-7 de Investigación Agropecuaria de Panamá. IDIAP. 11 p. Heinz, KM. 1996. Predators and parasitoids as biological control González D, GI; Serrano, C; Sánchez, agents of Bemisia in greenhouses. E; Zeballos, F; Espinoza, A. 1994. In Gerling and R. T. Mayer (eds.), Fluctuación poblacional de plagas Bemisia 1995: Taxonomy, Biology insectiles en tomate. Boquete, 1994. Damage, Control and Management, In Resultados de Investigación: Intercept, Andover, Hants, p. 435-449. Hortalizas. Instituto de Investigación Agropecuaria de Panamá. p. 481-484. Hillis, DM; Dixon, MT. 1991. Ribosomal DNA: molecular evolution and González D, GI; Guerra, JA; Villarreal, N; phylogenetic inference. Q. Rev. Biol. Adames, K; Araúz L; Núñez, J. 2009. 66:411-453. Contribución al conocimiento de los

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 104 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA)

Hoddle, MS; Driesche, R van. 1996. Breeding for resistance, Springer. Evaluation of Encarsia formosa Dordrecht, The Netherlands. p. 305- (Hymenoptera: Aphelnidae) 325. to control Bemisia argentifolii (Homoptera: Aleyrodidae) on Hoy, MA. 1994. Insect Molecular Genetics: poinsettia (Euphorbia pulcherrima): an introducction to principles and a lifetable analysis. Florida Entomol. applications. Academic Press. San 79:1-12. Diego, California. USA. 546 p.

Hoelmer, KA; Osborne, LS; Yocomi, IDIAP (Instituto de Investigación RK. 1991. Foliage disorders in Agropecuaria de Panamá). 1996. Florida associated with feeding by Proyecto de Investigación y sweetpotato whitefly,Bemisia tabaci. Transferencia en Mejoramiento Florida Entomologist 74(1):162-166. Genético del cultivo de tomate industrial. Instituto de Investigación Horiwitz, AR; Gerling, D. 1992. Seasonal Agropecuaria de Panamá. Panamá. variation of sex ratio in Bemisia tabaci 48 p. on cotton in Israel. Environmental Entomology 21: 556-559. King, ABS; Saunders, JL. 1984. Las plagas invertebradas de los cultivos Horiwitz, AR; Mendelson, Z; Weintraub, anuales y alimenticios en América PG; Ishaaya, I. 1988. Comparativa Central. TDRI/CATIE, Turrialba, toxicity of foliar and systemic CR. 182 p. applications of two chloronicotinyl insecticides, acetamiprid and Kuperus, WR; Chapco, W. 1994. imidacloprid, against the cotton Usefulness of internal transcribed whitefly, Bemisia tabaci. Bull. spacer regions of ribosomal DNA in Entomol. Res. 8:110-114. Melanopline (Orthoptera, Acrididae) systematics. Ann. Entomol. Soc. Horiwitz, AR; Denholm, I; Morin,S. 2007. Am. 87: 751–754. Resistance to insecticides in the TYLCV vector Bemisia tabaci. Lacey, LA; Fransen, JJ; Carruthers, RI. In Henryk. Czonek (ed.) Tomato 1995. Global distribution of naturally Yellow Leaf Curl Virus Desease: occurring fungi of Bemisia, their Management, molecular biology, biologies and use as biological

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 105 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA)

control agents. In D. Gerling and genus Aschersonia against whitefly. R. T. Mayers (eds.), Bemisia: 1995 IOBC/WPRS bulletin 19(1):103-106. Taxonomy, biology, damage, control and management. Intercept, Meekes, E.T.M. 2001. Entomopathogenic Andover, UK. p. 401-433. fungi against whiteflies: tritrophic interections between Aschersonia Lenteren, JC van; Woet, J. 1988. Biological species, Trialeurodes vaporariorum and integrated pest control in and Bemisia argentifolii, and greenhouses. Annu. Rev. Entomol. glasshouse crops. PhD Thesis. 33:239-269. Wageningen University. 181 p.

Lenteren, JC van; Roermund, HJW van; Menn, JJ. 1996. The Bemisia complex, an Sutterlin, S. 1996. Biological Control international crop protection problem of greenhouse whitefly (Trialeurodes waiting for a solution. In Bemisia vaporariorum) with the parasitoid 1995: Taxonomy, Pest Status and Encarsia formosa: How does it Management. Intercep, Andover, work? Biol. Control 6:1-10. Hants. p. 381-384.

Lenteren, JC van; Drost, YC; Roermund, MIDA (Ministerio de Desarrollo HJW van; Posthuma-Doodeman, Agropecuario de Panamá). 2009. CJAM. 1997. Aphelinid parasitoids Insumos fitosanitarios importados en as sustainable biological control la república de Panamá. Dirección agents in greenhouses. J. of Applied Nacional de Sanidad Vegetal, Entomology 121:473-458. Departamento de Agroquímicos.

Martin, JH. 1987. An identification guide Mound, LA; Halsey, SH. 1978. Whitefly of to common whitefly pest species of the world: A systematic catalogue of the world (Homoptera, Aleyrodidae). the Aleyrodidae (Homoptera) with Tropical Pest Management 33:298- host plant and natural enemies data. 322. British Museum (Natural History). 340 p. Meekes, ETM; Fransen, JJ; Lenteren, JC van. 1996. Pathogenicity of Name, BA. 2000. Determinación de entomopathogenic fungi of the las especies de mosca blanca (Homoptera: Aleyrodidae) que

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 106 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA)

atacan los cultivos hortícolas en systems for Bemisia tabaci. Crop la provincia de Chiriquí. Tesis de Protection 20:835-852. Ing. Agr. Fitotecnia. Universidad de Panamá. 57 p. Neal Jr, JW; Bentz, J. 1999. Evidence for the stage inducing phenotypic Naranjo, SE; Ellsworth, PC; Chu, CC; plasticity in pupae of the Henneberry, TJ; Riley, DG; Watson, polyphagous whiteflies Trialeurodes TF; Nichols RL. 1998. Action vaporariorum and Bemisia thresholds for the Management argentifolii (Homoptera:Aleyrodidae) of Bemisia tabaci (Homoptera: and the raison d’être. Ann. Entomol. Aleyrodidae) in cotton. J. Econ. Soc. Am. 92 (6): 774-787. Entomol. 91(6):1415-1426. Oliveira, MRV; Henneberry, TJ; Anderson, Naranjo, SE; Butler Jr, GD; Henneberry, P. 2001. History, current status, and TJ. 1999. Bibliography of Bemisia collaborative research projects for tabaci (Gennadius) and Bemisia Bemisia tabaci. Crop Protection argentifolii Bellows and Perring. 20(1):709-723 National research, action and technology transfer plan. Onillon, JC. 1990. The use of Natural enemies for the biological control Naranjo, SE; Butler Jr, GD; Henneberry, of whiteflies, In D. Gerling (ed.), TJ. 2002. Complete bibliography Whiteflies: Their bionomic, Pest of Bemisia tabaci and Bemisia Status and Management, Intercept argentifolii (on line). P. 227-415. Ltd, Andover, Hants, p. 287-313. In Silverleaf whitefly: National research, action and technology Osorio, O. 1998. Identificación de transfer plan, 1997-2001; Fourth malezas hospederas de Geminivrus annual review of the second 5-year del tomate. Tesis Ing. Agr. con plan and final report for 1992-2002. especialidad en Protección Vegetal. USDA-ARS June 2002. Consultado Panamá, Facultad de Ciencias mayo 2013. Disponible en http:// Agropecuaria de la Universidad de www.ars.usda.gov/News/docs Panamá. 65 p.

Naranjo, SE. 2001. Conservation and Orrego, C; Agudelo-Silva, F. 1993. evaluation of natural enemies in IPM Genetic variation in the parasitoid

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 107 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA)

wasp Trichogramma (Hymenoptera, Bulletin of Entomological Rsearch Trichogammatidae) revealed by 82:375-392. DNA amplification of a section of the nuclear ribosomal repeat. Fla Polston, JE; Anderson, PK. 1999. Entomol. 76:519-524. Surgimiento y distribución de geminivirus transmitidos por mosca Pachón, MP; Cotes, AM. 1997. Efecto de blanca en tomate en el Hemisferio Verticillium lecanii entomopatógeno Occidental. Manejo Integrado de de la mosca blanca Trialeurodes Plagas. no. 53:12-17. vaporariorum sobre la actividad parasítica de Amitus fuscipennis Powell, DA; Bellows, TS. 1992a. en un cultivo de fríjol. Revista Preimaginal development and Colombiana de Entomología 23(3- survival of Bemisia tabaci on cotton 4):171-175. and cucumber. Environmental Entomology 21:359-363. Perring, TW; Cooper, AD; Rodriguez, RJ; Farrar, CA; Bellows Jr., TS; 1993. Powell, DA; Bellows, TS. 1992b. Adult Identification of a whitefly species longevity, fertility and population by genomic and behavioral studies. growth rates for Bemisia tabaci on Science 259:74-77. two host plant species. Journal of Applied Entomology 113:68-78. Pinto, JD; Stouthammer, R; Platner,

GR. 1997. A new cryptic specie Prabhaker, N; Coundriet, DL; Meyerdirk, of Trichogramma (Hymenoptera, DE. 1985. Insecticide resistance in Trichogammatidae) from the Mojave the swetpoptato whitefly, Bemisia desert of California as determined tabaci (Homoptera:Aleyrodidae). J. by morphological, reproductive and Econ. Entomol. 78:748-752. molecular data. Proc. Entomol. Soc.

Washington 99:238-247. Rosell, RC; Bedford, ID; Markham; Frohlich, DR; Brown, JK. 1996. Polaszek, A; Evans, GA; Bennett, FD. 1992. Morphological variations in Bemisia Encarsia parasitoids of Bemisia populations. In Gerling, D. Bemisia tabaci Hymenoptera: Aphelinidae, 1995: Taxonomy, Pest Status and Homoptera: Aleyrodidae): a Management. Intercep, Andover, preliminary guide to identification. Hants. p. 147-152.

González y Santamaría. CONTROL BIOLÓGICO: UNA ALTERNATIVA DE MANEJO INTEGRADO DE Trialeurodes vaporariorum EN INVERNADEROS EN PANAMÁ 108 2015. CIENCIA AGROPECUARIA no. 22:86-109. (REVISIÓN BIBLIÓGRAFICA)

Russell, LM. 1962. The citrus blackfly. FAO Schilthuizen, M; Stouhamer, R. 1997. Plant Protection Bulletin 10(2):36- Horizontal transmission of 38. (Whiteflies 34). parthenogenesis-inducing microbes in Trichogramma wasps. Proc. R. Santamaría Guerra, J. 2011. Gerencia Soc. Lond. B, 264:361-366. por desafíos y sostenibilidad de intervenciones para el desarrollo Sánchez, E; Serrano, C. 1994. Manual inclusivo. Tegucigalpa, Honduras. del cultivo de la cebolla para las Universidad Nacional Autónoma de tierras altas de Chiriquí. Instituto Honduras, Facultad de Ciencias de Investigación Agropecuaria de Sociales, Programa de Doctorado en Panamá. IDIAP. 42 p. Ciencias Sociales con orientación en Gestión del Desarrollo. Consultado Valderrama, A; Velásquez, A; Fernández 13 mayo 2013. Disponible en http:// G, O. 1994. Trasmisión y ámbito issuu.com/doctoradoccssgd/docs/ de hospederos de un geminivirus gerencia_por_desafios_para_la_ asociado con B. tabaci en tomate. sostenibilidad_de_in In V Jornada Agropecuaria Región Oriental, Instituto de Investigación Santamaría Guerra, J. 2012. Metodología Agropecuaria. Panamá. 17 p. IDIAP- Agricultura Familiar. Panamá, Panamá. IDIAP (Instituto Vega, FE; Infante F; Castillo F; Jaramillo de Investigación Agropecuaria de J. 2009. The berry borer, Panamá). Consultado 19 ene. 2014. Hypothenemus hampei (Ferrari) Disponible en https://www.youtube. (Coleoptera: Curculionidae): a short com/watch?v=wWHWuiRss0o. review, with recent findings and future research directions. Terrestrial Sappal, NP; Jeng, RS; Hubbes, M; Liu, F. Arthropod Reviews 2:129–147. 1995. Restriction fragment length polymorphisms in polymerase Wardlow, LR; Ludlam, FAB; Bradley, chain reaction amplified ribosomal LF. 1976. Pesticide resistance in DNAs of three Trichogramma glasshouse whitefly (Trialeurodes (Hymenoptera, Trichogammatidae) vaporariorum Westwood). Pestic. species. Genome 38:419-425. Sci. 7:320–324.

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