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Neotropical Entomology

Print version ISSN 1519-566XOn-line version ISSN 1678-8052

Neotrop. entomol. vol.38 no.4 Londrina July/Aug. 2009 



Life history parameters of Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) at different environmental conditions on two bean cultivars


Estadísticos vitales de Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) a diferentes condiciones ambientales en dos cultivares de fríjol



Maria R ManzanoI; Joop C van LenterenII

IDepto. de Ciencias Agrícolas, Univ. Nacional de Colombia, sede Palmira, Cra. 32 Chapinero via a Candelaria, Colombia;
IILab. of Entomology, Wageningen University, PO Box 8031, 6700 EH Wageningen, The Netherlands;




Life-history parameters of the greenhouse whitefly Trialeurodes vaporariorum (Westwood), an important pest of bean crops in Colombia, were determined in environmental control chambers on two dry bean (Phaseolus vulgaris) cultivars (cv.). Trialeurodes vaporariorum longevity on cv. Chocho decreased as temperature increased from 22.6 d at 19ºC to 5.9 d at 26ºC. Fecundity was significantly lower at 19ºC (8.6 eggs/female), as compared to 22ºC (32.6 eggs/female) and 26ºC (33.3 eggs/female) on cv. Chocho. Fecundity on cv. ICA-Pijao was much higher (127.2 eggs/female) than on cv. Chocho (32.6 eggs/female) at 19ºC. The intrinsic rate of population increase (rm) was highest at 22ºC (0.061), intermediate at 19ºC (0.044) and lowest at 26ºC (0.035) on cv. Chocho, and was 0.072 on cv. ICA-Pijao at 19ºC. Life history parameters of T. vaporariorum are compared to those of one of its natural enemies, the parasitoid Amitus fuscipennis MacGown & Nebeker. Finally, data are presented on the distribution of the parasitoid related to the altitude for the Valle del Cauca, Colombia.

Key words: Greenhouse whitefly, fecundity, Phaseolus vulgaris, Amitus fuscipennis, IPM


Se determinaron los estadísticos vitales de la mosca blanca Trialeurodes vaporariorum (Westwood), una plaga importante del cultivo del fríjol en Colombia, en cámara ambiental en dos cultivares (cv.) de fríjol. La longevidad media de T. vaporariorum en el cv. Chocho fue mayor a 19ºC (22.6 d), intermedia a 22ºC (17.5 d) y menor a 26ºC (5.9 d). En el cv. ICA-Pijao la longevidad media fue de 35.5 d a 19ºC. La fecundidad media total fue 8.6, 32.6 y 33.3 huevos por hembra a 19, 22 y 26ºC, respectivamente en el cv. Chocho. La fecundidad en el cv ICA-Pijao fue mucho más alta, 127. 2 huevos por hembra, a 19ºC, que la del cv. Chocho. La tasa intrínseca de crecimiento poblacional (rm) fue más alta a 22ºC (0.061), intermedia a 19ºC (0.044) y más baja a 26ºC (0.035) en el cv. Chocho. Ella fue de 0.072 a 19ºC en el cv. ICA-Pijao. Se comparan los estadísticos vitales de T. vaporariorum con los de su enemigo natural, el parasitoide Amitus fuscipennis MacGown & Nebeker y se zonifica la distribución del parasitoide en el Valle del Cauca, Colombia.

Palabras clave: Mosca blanca de los invernaderos, fecundidad, Phaseolus vulgaris, Amitus fuscipennis



The greenhouse whitefly, Trialeurodes vaporariorum (Westwood), is an important pest especially in vegetable and ornamental crops (van Lenteren & Martin 2000). Adults and nymphs feed on phloem sap, excreting large amounts of honeydew that favors the development of sooty mould, which reduces plant photosynthesis (Lindquist et al 1972). In Colombia, greenhouse whitefly is a key pest on dry and snap kidney beans (Phaseolus vulgaris) (Rodriguez & Cardona 2001, Quintero et al 2001). As a result, Colombian bean crops are heavily sprayed (average of 10 times per cropping season) with chemical insecticides to control this pest (Rodriguez & Cardona 2001).

The presence of three mountain ranges of the Andean mountain range in Colombia offers a landscape of kidney bean cultivation at different altitudes. Surveys in Colombia and Ecuador have shown that T. vaporariorum is the dominant whitefly species distributed in the tropical highlands of the Andean region between 2000 m.a.s.l. and 2830 m.a.s.l. (meters above sea level) (Quintero et al 2001) where the average temperature and relative humidity (RH) are around 19ºC and 80%, respectively. The pest is also present on crops established around 1000 m (inter-Andean valleys) in combination with other whitefly species (Quintero et al 2001), where average temperature ranges from 22ºC to 24ºC, with a relative humidity around 74%.

In Colombia, the greenhouse whitefly is parasitized by an endemic natural enemy, the parasitoid Amitus fuscipennis MacGown & Nebeker (Hymenoptera: Platygasteridae), which has been evaluated as a potential biological control agent of the greenhouse whitefly on kidney beans (Manzano et al 2000) and tomato in Colombia (De Vis et al 2002). One criterion used to evaluate the potential of natural enemies for controlling a pest is that the intrinsic rate of population increase (rm) of the control agent has to be at least equal to the pest's population growth rate, thereby making biological control feasible (van Lenteren & Woets 1988).

At least 37 commercial kidney bean cultivars are grown in Colombia and more than 60 bean lines have been improved agronomically (Voysest 1983). To test the potential effect of host plant on the rm value of T. vaporariorum, two different cultivars were used, cv. Chocho and cv ICA-Pijao. Chocho is an important commercial cultivar that is grown mainly in the hillside areas of Tenerife, Valle del Cauca, Colombia, while cv. ICA-Pijao is well adapted to greenhouse conditions and is less susceptible to microbial infections.

We measured the rm values of T. vaporariorum in environmental control chambers, which were set to simulate the climate found at the hillside and lowland bean-cropping regions. The rm values of the parasitoid and its host were compared to determine those altitudinal zones and kidney bean cultivars where A. fuscipennis is likely to be most efficient as a biological control agent of the greenhouse whitefly. The earlier published rm values of A. fuscipennis were obtained under similar climatic conditions on cultivars ICA-Pijao and Chocho with T. vaporariorum as a host (Manzano et al 2002).


Material and Methods

Plant and whitefly cultures. Plants of the kidney bean P. vulgaris cv. Chocho and cv. ICA-Pijao were grown in a greenhouse at 25 ± 5ºC, 40-80% RH and at least 12h light per day. Plants used were 15 days old and were not fertilized or sprayed with chemicals.

Trialeurodes vaporariorum adults were obtained from a colony established on kidney bean plants (cv. ICA-Pijao) at the Centro Internacional de Agricultura Tropical (CIAT). The whitefly colony at CIAT was originally collected from snap bean fields in Fusagasugá, Colombia. The whiteflies were reared at 23 ± 1ºC, 40-80% RH and 12L:12D.

Adult longevity and reproduction. Trialeurodes vaporariorum newly emerged adults were sexed and caged by pairs in clip-cages (inner diameter = 2.5 cm). Every 48h, the clip-cage with the test insects was moved to a new leaf area until all the female insects died. Fecundity was estimated by counting the number of eggs laid in each period of 48h. The caged adults were kept in environmental control chambers under different temperature and humidity conditions. Cultivar Chocho was kept at 19ºC, 75 ± 5% RH; 22ºC, 72 ± 6% RH; 26ºC, 75 ± 5% RH, and cv. ICA-Pijao was kept at 19ºC, 75 ± 5% RH.

Immature development and survival. Approximately 40 adults of T. vaporariorum were placed in clip-cages (inner diameter = 2.5 cm), which were then put on leaves of each cultivar. After 10h, adults were removed and about 100 eggs coming from two or three different groups of T. vaporariorum females were allowed to develop under the same conditions as previously described. Developmental time, percentage immature survival and proportion of females of T. vaporariorum were recorded.

Demographic parameters. Immature developmental time, percentage of immature survival and proportion of females were combined with reproduction experimental data to estimate life table parameters for calculation of T. vaporariorum demographic parameters, as defined by Price (1997): net reproductive rate (Ro), which represents the number of female descendants that an average female produces in one generation, and generation time (T) that is equivalent to the mean period between the birth of parents and birth of offspring. The intrinsic rate of population increase (rm) for T. vaporariorum at different climatic conditions was also calculated using the equation given by Carey (1993): Σ exp(-rmx)lxmx = 1, in which x is the age, lx is the age-specific survival and mx is the proportion of females produced by a female at age x. According to Carey (1993), pivotal age, which is x + 0.5, was used in the calculation of rm values.

The rm values of T. vaporariorum were measured simultaneously for ICA-Pijao and Chocho cultivars at 19ºC and 75 ± 5% RH. These conditions were chosen for ICA-Pijao in order to compare this rm value with that of A. fuscipennis previously determined (Manzano et al 2002). For the T. vaporariorum experiment, the rm value at 22ºC, 72 ± 6% RH was calculated assuming 25% as the proportion of females based on the proportion of females reported at 19ºC and 26ºC.

Distribution of T. vaporariorum and A. fuscipennis in Valle del Cauca, Colombia. Amitus fuscipennis and T. vaporariorum were collected on dry and snap kidney beans in different areas of Valle del Cauca, Colombia. Based on tested life history parameters of T. vaporariorum, a zoning map was made for Valle del Cauca. Localities where A. fuscipennis was collected in Valle del Cauca were drawn in the map to match parasitoid-host climatic adaptation.

Data analyses. Differences between mean longevity and fecundity values were compared using the Kruskal-Wallis One Way Analysis of Variance (ANOVA) on Ranks followed by all pairwise multiple comparison procedures (Student-Newman-Keuls test). Oviposition rates were compared using one-way ANOVA followed by Student-Newman-Keuls test. Differences in developmental time were tested using the Kruskal-Wallis One Way ANOVA on Ranks followed by pairwise multiple comparisons (Dunn's method). For comparison of survival rates, χ2- tests were used.



Adult longevity and fecundity. Longevity of T. vaporariorum females decreased as temperature increased. T. vaporariorum longevity on cv. Chocho was shortest at 26ºC (5.7 d), and the longest longevity on cv. ICA-Pijao was observed at 19ºC (35.5 d). Mean longevity differed significantly among temperatures and kidney bean cultivars, except for values on cv. Chocho at 19ºC and 22ºC (P < 0.0001) (Table 1, Fig 1).



Fecundity was affected by temperature and kidney bean cultivars (P < 0.0001), except for values on cv. Chocho at 19ºC and at 22ºC (Table 1, Fig 2). Differences in fecundity between cv. Chocho and cv. ICA-Pijao at 19ºC can be clearly observed in the reproduction curves: oviposition on cv. ICA-Pijao is much higher and oviposition continues for a longer period of time (Fig 3). Oviposition rate was significantly different among treatments (one-way ANOVA, P < 0.0001), except for the comparison between females on cv. Chocho at 19ºC and 26ºC (1.4 for both conditions, P > 0.05) (Table 1).





Trialeurodes vaporariorum had similar longevity and fecundity at tropical highland conditions (19ºC, 80% RH) as at inter-Andean valley conditions (22ºC, 74% RH). However, at a constant temperature of 26ºC, combined with a relative humidity of 75%, longevity, fecundity and survival rates were much lower than at 19ºC and 22ºC (Table 1).

Immature development and survival. Trialeurodes vaporariorum survival (χ2 = 77.7, df = 3, P < 0.0001) and development time (Kruskal-Wallis one way ANOVA on ranks P < 0.0001, followed by Dunn's method, P < 0.05) were affected by climatic conditions and the kidney bean cultivars tested (Table 2). Female emergence was only around 20% at 19ºC on both cultivars, and a little higher (28%) at 26ºC on cv. Chocho (Table 2).

Demographic parameters. There were no large differences between reproduction data on cv. Chocho at 19ºC (Ro = 6.2) and at 22ºC (Ro = 8.3). The rm value was lower (0.044) at 19ºC than at 22ºC (0.061). Reproduction decreased for the same cultivar at 26ºC with Ro and rm values at 2.3 and 0.035, respectively. The main difference was found for values of cv. Chocho at 19ºC (Ro = 6.2, rm = 0.044) and those of cv. ICA-Pijao under the same environmental conditions (Ro = 26.7 and rm = 0.072). Generation time (T) was highest (49.6) on cv. ICA-Pijao and shortest (24.7) for cv. Chocho at 26ºC (Table 2).

Distribution of T. vaporariorum and A. fuscipennis in Valle del Cauca, Colombia. Distribution of A. fuscipennis in combination with a temperature zone map for T. vaporariorum is shown in Fig 4. Amitus fuscipennis matches its distribution to 19-22ºC except for Lomitas (Pradera) where average temperature is above 22ºC. The average temperature of Tenerife is lower than 19ºC, but the parasitoid is present.



The temperature effects observed for T. vaporariorum follow the same trend of that reported by several authors, whom reported a negative effect on whitefly survival and adult longevity as temperature increased (Madueke 1979, Collman & All 1980, van Roermund & van Lenteren 1992). There are few data concerning the effects of kidney beans as a host on the reproductive capacity of T. vaporariorum at similar conditions as tested here (e.g., Madueke 1979), making any specific comparisons difficult. However, the drastic effect of different hosts on greenhouse whitefly reproduction and population growth potential can easily be observed when looking at the differences in rm values for T. vaporariorum on different host plants (Zabudskaya 1989, Yano 1989, Romanow et al 1991).

Trialeurodes vaporariorum is well adapted to tropical highland conditions (19ºC, 80% RH) as well as at inter-Andean valley conditions (22ºC, 74% RH); an outcome supported by field surveys carried out by Quintero et al (2001). However at higher temperature and relative humidity conditions, survival of whitefly decreases. These latter climatic conditions are found in the northern coastal area of Colombia with tropical lowland conditions where RH can be higher than 80%. Trialeurodes vaporariorum is absent in this area but other whitefly species are present, like Bemisia tabaci (Gennadius) biotype B on vegetable crops (Rodriguez et al 2005), Bemisia tuberculata Bondar, Trialeurodes variabilis (Quaintance) and Aleurotrachelus socialis Bondar on cassava (Cardona et al 1998). Recently, it was found that T. vaporariorum possesses less tolerance to higher temperatures than B. tabaci biotype B, probably linked to the expression of heat shock protein genes (Wan et al 2009).

In our experiments, a strongly male-biased sex ratio was found for T. vaporariorum. We did not find the 'normal' sex ratio of 1:1 mentioned by van Lenteren & Noldus (1990). Our results cannot be easily explained because sex ratio in T. vaporariorum is thought to be independent of temperature and host-plant species (van Lenteren & Noldus 1990, van Roermund & van Lenteren 1992). Van Roermund & van Lenteren (1992) summarized several data from different authors on different host plants including kidney bean and reported an average value for sex ratio of T. vaporariorum of 0.538 (or 53.8% females).

Our results show considerable differences in life-history parameters between the kidney bean cultivars ICA-Pijao and Chocho. One possible explanation for this outcome is that whiteflies used in our experiments came from a colony established at CIAT for five years on cv. ICA-Pijao, and T. vaporariorum may have been adapted to this bean cultivar and, thus, performed better on cv. ICA-Pijao than on cv. Chocho.

Van Lenteren & Noldus (1990) found that a T. vaporariorum strain originating from tomato and reared for three generations on sweet pepper had a higher fecundity on sweet pepper than did the original strain. A different whitefly species, B. tabaci biotype B increased its oviposition rate after being reared for five generations on different host plants starting with bean and finishing with cassava passing through two Euphorbiaceae species (Carabali et al 2005). These results indicate that rearing for some generations on a host plant may facilitate the adaptation of whiteflies to a different host plant. Based on the above discussion concerning the possible adaptation of whitefly strains during exposure for several generations to a new cultivar, we propose further testing to find out if the poor performance found for T. vaporariorum on cv. Chocho is permanent or disappears within a few generations.

According to field surveys, parasitoid distribution in Valle del Cauca matches with areas along 19ºC to 22ºC where its host T. vaporariorum is also well adapted, corresponding to both inter-Andean and tropical highland conditions. Longevity of A. fuscipennis is negatively affected by dry or warm environments (Manzano et al 2000). As shown in the map localities as Lomitas (1180 m.a.s.l.) where average temperature is above 22ºC, the parasitoid is scarce and Encarsia nigricephala Dozier is the dominant parasitoid species of T. vaporariorum (Manzano et al 2003). On the other hand, in Tenerife, Valle del Cauca, located at tropical highland were average temperature is below 19ºC, both the parasitoid and T. vaporariorum are abundant (Manzano 2000). Besides Valle del Cauca, A. fuscipennis has been collected in Rionegro (Antioquia) and Sumapaz (Cundinamarca) at altitudes above 1500 m in the tropical highlands (Manzano 2000).

We measured the rm value of A. fuscipennis under the same experimental conditions and with the same kidney bean cultivars as in the present study, and found that the rm values of the parasitoid were higher than the rm values of T. vaporariorum (Manzano et al 2002). On cv. Ica-Pijao the parastioid's rm value was 0.117; on cv. Chocho rm values were 0.102 and 0.144 at 19ºC and 22ºC respectively. Van Lenteren & Woets (1988) proposed that an efficient parasitoid should have a potential maximum rate of population increase (rm) equal to or larger than that of its host to keep up with growth of the pest population in inoculative or seasonal inoculative biological control programs.

Our results suggest that based on the reproductive parameters alone, A. fuscipennis may control T. vaporariorum populations at inter-Andean and tropical highland conditions.



We thank Cesar Cardona (CIAT) for allowing us to work at the Laboratory of Bean Entomology and to Hector Morales (CIAT) for his support in greenhouse activities. Thanks to Bregje Wertheim (Wageningen University) for her critical review that improved an early version of the manuscript. Thanks to John Selvaraj (UNAL sede Palmira) for preparing the map. Thanks to Takumasa Kondo (Corpoica, Palmira) and Fernando L Consoli (ESALQ/USP) for their comments and reviews. This research was financed by the Netherlands Foundation for the Advancement of Tropical Research (WOTRO).



Carabali A, Bellotti A C, Montoya-Lerma J, Cuellar M E (2005) Adaptation of Bemisia tabaci biotype B (Gennadius) to cassava, Manihot esculenta (Crantz). Crop Prot 24: 643-649.         [ Links ]

Cardona C, Rendón F, Rodríguez I (1998) Chemical control and insecticide resistance of whiteflies in the Andean zone: a progress report. In International Workshop on Bemisia and Geminivirus, June 7-12, San Juan, Puerto Rico, L-70.         [ Links ]

Carey J R (1993) Applied demography for biologists. New York, Oxford University Press, 206p.         [ Links ]

Collman G L, All J N (1980) Quantification of the greenhouse whitefly life cycle in a controlled environment. J Georgia Entomol Soc 15: 432-438.         [ Links ]

de Vis R M J, Fuentes L E, van Lenteren, J C (2002) Life history of Amitus fuscipennis (Hym., Platygastridae) as parasitoid of the greenhouse whitefly Trialeurodes vaporariorum (Hom., Aleyrodidae) on tomato as function of temperature. J Appl Entomol 126: 24-33.         [ Links ]

Lindquist R K, Bauerle W L, Spadafora R (1972) Effect of the greenhouse whitefly on yields of greenhouse tomatoes. J Econ Ent 65:1406-1408.         [ Links ]

Madueke E (1979) Biological control of Trialeurodes vaporariorum. PhD thesis, University of Cambridge, 114p.         [ Links ]

Manzano M R (2000) Evaluation of Amitus fuscipennis as biological control agent of Trialeurodes vaporariorum on bean in Colombia. PhD thesis, Wageningen University, The Netherlands, 149p.         [ Links ]

Manzano M R, van Lenteren J C, Cardona C (2002) Intrinsic rate of population increase of Amitus fuscipennis MacGown & Nebeker (Hym., Platygasteridae) according to climatic conditions and bean cultivar. J Appl Entomol 126: 34-39.         [ Links ]

Manzano M R, van Lenteren J C, Cardona C (2003) Influence of pesticide treatments on the dynamics of whiteflies and associated parasitoids in snap bean fields. Biocontrol (Dordrecht) 48: 685-693        [ Links ]

Manzano M R, van Lenteren J C, Cardona C, Drost Y C (2000) Developmental time, sex ratio, and longevity of Amitus fuscipennis MacGown & Nebeker (Hymenoptera: Platygasteridae) on the greenhouse whitefly. Biol Control 18: 94-100.         [ Links ]

Price P (1997) Insect ecology. New York, John Wiley & Sons, 874p.         [ Links ]

Quintero C, Rendón F, García J, Cardona C, López-Avila A, Hernández P (2001) Especies y biotipos de moscas blancas (Homoptera: Aleyrodidae) en cultivos semestrales de Colombia y Ecuador. Rev Colomb Entomol 27: 27-31.         [ Links ]

Rodriguez I V, Cardona C (2001) Problemática de Trialeurodes vaporariorum y Bemisia tabaci (Homoptera: Aleyrodidae) como plagas de cultivos semestrales en el Valle del Cauca. Rev Colomb Entomol 27: 21-26.         [ Links ]

Rodriguez I, Cardona C, Morales H, Bueno J M (2005) El biotipo B de Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) adquiere mayor importancia en el Valle del Cauca. Rev Colomb Entomol 31: 21-28.         [ Links ]

Romanow L R, de Ponti O M B, Mollema C (1991) Resistance in tomato to the greenhouse whitefly: analysis of population dynamics. Entomol Exp Appl 60: 247-259.         [ Links ]

van Lenteren J C, Martin N A (2000) Biological control of whiteflies, p.202-214. In Albajes R, Gullino M, van Lenteren J C, Elad Y (eds) Integrated pest and disease management in greenhouse crops. Dordrecht, Kluwer Publishers, 568p.         [ Links ]

van Lenteren J C, Noldus L (1990) Whitefly-plant relationships: behavioural and ecological aspects, p.47-89. In Gerling D (ed) Whiteflies: their bionomics, pest status and management. Andover, Intercept, 352p.         [ Links ]

van Lenteren J C, Woets J (1988) Biological and integrated pest control in greenhouses. Annu Rev Entomol 33: 239-269.         [ Links ]

van Roermund H J W, van Lenteren J C (1992) Life-history parameters of the greenhouse whitefly, Trialeurodes vaporariorum and the parasitoid Encarsia formosa. Wageningen, Wageningen Agricultural University Paper 92-3, 147p.         [ Links ]

Voysest O (1983) Variedades de frijol en América Latina y su origen. Cali, Centro Internacional de Agricultura Tropical (CIAT), 87p.         [ Links ]

Yano E (1989) Factors affecting population growth of the greenhouse whitefly, Trialeurodes vaporariorum (Westwood) (Homoptera: Aleyrodidae). Jpn J Appl Entomol Zool 33: 122-127.         [ Links ]

Wan F, Zhang G, Liu S, Luo C, Chu D, Zhang Y, Zang L, Jiu M, Lü Z, Cui X, Zhang L, Zhang F, Zhang Q, Liu W, Liang P, Lei Z, Zhang Y (2009) Invasive mechanism and management strategy of Bemisia tabaci (Gennadius) biotype B: Progress report of 973 Program on invasive alien species in China. Sci China Ser C- Life Sci 52: 88-95.         [ Links ]

Zabudskaya I A (1989) Biological control of the greenhouse whitefly, Trialeurodes vaporariorum (Homoptera, Aleyrodidae). Acta Entomol Fenn 53: 73-76.         [ Links ]



Received 13/II/07.
Accepted 26/VI/09.



Edited by André L Lourenção - IAC

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