Variation in insect pest and virus resistance among habanero peppers (Capsicum chinense Jacq.) in Yucatán, México

Variación en resistencia a insectos herbívoros y virosis en líneas de chile habanero (Capsicum chinense Jacq.) en Yucatán, México

Jorge C. Berny–Mier y Teran^1,4, Luis Abdala–Roberts^2*, Antonio Durán–Yáñez³, Felipe Tut–Pech¹

¹Campo Experimental Mocochá, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias. 97454. Km. 25 Carretera Mérida–Motul, Mocochá, Yucatán, México. (jcberny@yahoo.com).

³ Departamento de Apicultura Tropical, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán. 97000. Apartado Postal 4–116. Itzimná, Mérida, Yucatán, México. (locomotion.plus@gmail.com).

⁴ Present address: Department of Plant Sciences, University of California–Davis, 1 Shields Avenue, Davis, CA 95616.

Received: June, 2012.
Approved: April, 2013.

Abstract

The evaluation of crop genetic variation for herbivore resistance is a relevant tool that can provide information about plant breeding strategies and biological control. The objective of this study was to provide a field–based assessment of pest resistance in five lines of habenero pepper (Capsicum chinense Jacq.). Weekly surveys were conducted at an experimental site in Mocochá (Yucatán, México) from July 2010 to December 2010, including incidence of Bemisiatabaci nymphs and Liriomyza trifolii leafmines, fruit infestation by the pepper weevil (Anthonomus eugenii), and the presence and severity of symptoms of viral infection. The experimental design was completely randomized with five 5X5 m replicate plots, each containing an equal number of plants of each C. chinense line. There were significant differences (p≤0.05) among C. chinense lines for the number of mines per leaf and the proportion of fruits infested by the pepper weevil. Genotype 36 (a South American habanero) exhibited the highest incidence of leaf mines but the lowest incidence of fruit attack by the weevil, while genotype 110 (Antillean yellow habanero) showed a reverse pattern. In addition, there were differences among lines in the severity of virosis symptoms, suggesting differencial susceptibility to viruses. These results provide novel evidence of pest resistance variation in C. chinense lines under field conditions, to be used in selecting for pest resistance in this crop.

Key words: Capsicum chinense, plant resistance, plant genetic variation.

Resumen

La evaluación de la variación genética en cultivos para la resistencia a herbívoros es una herramienta importante que puede aportar información acerca de estrategias de mejoramiento genético y control biológico. El objetivo de este estudio fue evaluar en campo la resistencia a plagas de cinco líneas de chile habanero (Capsicum chinense Jacq.). En un sitio experimental en Mocochá (Yucatán, México) se realizaron encuestas semanales entre julio y diciembre del 2010, de incidencia de ninfas de Bemisia tabaci y minas foliares de Liriomyzatrifolii, infestación de frutos por el gorgojo del chile (Anthonomus eugenii), y presencia y severidad de síntomas de infección viral. El diseño experimental fue completamente al azar replicado en cinco parcelas de 5X5 m, cada una con un número igual de plantas de cada línea de C. chinense. Hubo diferencias significativas (p≤0.05) entre las líneas respecto al número de minas por hoja, y la proporción de frutos infestados por el gorgojo del chile. El genotipo 36 (un habanero de América del Sur) presentó la mayor incidencia de minas de hoja, pero la menor incidencia de ataque de frutos por el gorgojo, mientras que el genotipo 110 (habanero amarillo de las Antillas) mostró un patrón inverso. Además, hubo diferencias entre líneas de la gravedad de síntomas de virosis, sugiriendo susceptibilidad diferencial a virus. Estos resultados dan nueva evidencia de variación en resistencia a plagas en líneas de C. chinense bajo condiciones de campo, para usar al seleccionar para resistencia a plagas en chiles.

Palabras clave: Capsicum chinense, resistencia de las plantas, variación genética de las plantas.

INTRODUCTION

The use of insecticides is the most common method for pest control in horticultural crops such as peppers (Capsicum spp.) (Soria–Fregoso et al., 1996; Bosland and Votava, 2000). However, it is recognized that insecticides negatively affect populations of natural enemies (Theiling and Croft, 1988), lead to resistance of target insect pests (Nauen and Denholm, 2005), and have harmful impacts on human health and the environment (Eskenazi et al., 1999). A viable strategy to reduce pest damage and minimize insecticide application is the use of pest–resistant crops (Cuartero et al., 1999; Cortesero et al., 2000), which can serve as a complementary tool to other methods targeted for integrated pest management (Eigenbrode and Trumble, 1994). Accordingly, evaluations of pest resistance across plant genotypes are a fundamental step towards the study of crop pest resistance (Smith, 2005). Although studies by Kim et al. (2010) and Fridaus et al. (2011) as well as multinational efforts (Sarath Babu et al., 2011) address plant genotypic variation in resistance to arthropod pests and pathogens in the genus Capsicum, evaluations are scarce for Latin America (Morales, 2011) and lacking for some cultivated peppers such as the habanero pepper (Capsicum chinense Jacq.).

Habanero pepper is one of the main horticultural crops in southeast México owing to its cultural, culinary and economic value, as well as its high potential for exportation and industrialization (Soria–Fregoso et al., 1996; Tun–Dzul, 2001). In Yucatán, the state in México with the greatest production of C. chinense, the total area planted with this crop has progressively increased during the last decade (SIAP, 2011). However, C. chinense yields remain low and this is largely due to the negative impact of insect pests and pathogens. The main pests of peppers in México's lowland tropics are the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae), the pepper weevil Anthonomus eugenii Cano (Coleoptera: Curculionidae), leafminers of the genus Liriomyza (Diptera: Agromyzidae), as well as some species of mites (Tetranychus sp., Polyphagotarsonemuslatus) (Soria–Fregoso et al., 1996; Tun–Dzul, 2001). Among these pests, B. tabaci is the most damaging because it is a vector of several species of Begomovirus (Geminiviridae) (Torres–Pacheco et al., 1996; Morales and Anderson, 2001) which cause yellowing and deformation in leaves, plant stunting, reduced fruit–set and fruit deformation (Polston and Anderson, 1997).

The goal of this study was to provide a field assessment of resistance to multiple pests in five lines of C. chinense in Yucatán, México. To this end, detailed surveys of abundance and damage by three major pests of habanero pepper were conducted, as well as the onset and severity of symptoms of virosis was recorded.

The study was conducted from July 2010 to November 2010 at the Mococha Research Station of the Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias (INIFAP), in Yucatán (21° 6' 40'' N, 89° 26' 35'' W). A 30X50 m area was used to establish five 5X5 m plots of C. chinense, each of which included an equal number of plants of all five lines. Within each plot, positions were randomly assigned to plants of each line. Distance between plots was 2.5 m, and within each plot the planting design was 30 cm between plants within rows, and 1.25 m between rows within plots. Planting density was 2.64 plants m^–2 (66 plants per plot), for 330 plants. Of these, eight plants per line, per plot, were randomly chosen and monitored throughout the growing season, resulting in 40 sampled plants per line, and 200 sampled plants. The fertilization and irrigation regime were the same across all plots and followed standard agricultural practices for C. chinense in the region (Tun–Dzul, 2001); the only exception was that insecticides were not used.

Capsicum chinense lines were selected a priori to include a wide range of phenotypic variation in vegetative and reproductive traits. A typical orange habanero (G84), a Belizean red habanero (G149), an Antillean yellow habanero (G110), a South American habanero of small fruits (G36), and the Cuban habanero (G37) were utilized. These lines differ in vegetative (plant size, architecture) and reproductive traits (flowering phenology, fruit size and yield) (Trujillo–Aguirre and Pérez–Llanes, 2004).

The variables measured for each plant were: 1) number of leaf mines of L. trifolii on six randomly chosen leaves, with surveys being conducted on different leaves every two weeks from July 2010 to September 2010; 2) presence of whitefly B. tabaci nymphs on the abaxial surface of four leaves, recorded once every two weeks (on different leaves each survey) from July 2010 to September 2010, as well as an additional survey in November 2010; both leafminer and whitefly nymph data were recorded on young, fully–expanded leaves; 3) the number of weeks until the appearance of symptoms of virosis based on weekly surveys from July 2010 to November 2010; 4) severity of virosis, scored from one (low severity) to nine (high severity) based on infection symptoms (Gonzalez–Perez et al., 2011) at the end of the experiment (November 2010); 5) fruit infestation by the pepper weevil A. eugenii based on weekly harvests of all fruits per plant from late September 2010 to mid November 2010. Infested fruits were identified based on the presence of yellowing of the fruit petiole which is a reliable indicator of weevil presence (>95 % of the cases based on a random subsample; data from this study).

Surveys of B. tabaci at the study site confirmed the presence of whitefly biotypes A and B during the sampling season through barcoding mitochondrial cytochrome c oxidase subunit I (Papayiannis et al., 2009) and sequence similarity in the GenBank database (Benson et al., 2013). However, we did not discern between these two biotypes when recording nymph presence (although resistance to both is frequently positively related; Wilhoit, 1992; Nombela et al., 2001). In the case of virus infection trasmitted by B. tabaci, a wide range of symptoms were observed in the field and co–infections by begomoviruses are common in cultivated Solanaceae plantations (Mendez–Lozano et al., 2001; Anaya–Lopez et al., 2003; Mendez–Lozano et al., 2003); there is no evidence to support the presence of mixed infections in this study. Therefore, documentation of virosis in the field represented a measure of resistance to either one or multiple virus species (e.g. resistance to the Begomovirus complex or Tospovirus), or both.

Statistical analyses

Generalized linear models in Proc GLIMMLX, SAS version 9.1 (SAS Institute, 2002, Cary, NC) were used to test for differences among C. chinense lines in number of mines per leaf (number of mines per plant/number of leaves sampled per plant), proportion of fruits attacked by the pepper weevil (number of weevils per plant/number of fruits sampled per plant), and number of weeks until the appearance of symptoms of virosis and severity of virosis. In all three cases, data were not normally distributed even after transformation; therefore, alternative error distributions which best fitted the raw data were selected. The model number of leaf mines assumed a gamma distribution (log link), the weevil attack model assumed an exponential distribution (log link), and models for number of weeks until appearance of symptoms and severity of virosis both assumed a Poisson distribution (log link) which is appropriate for count data. The gamma and exponential distributions are appropriate for continuous data and handle different types of non–normal distributions (Zuur et al. 2009). In addition, Proc LOGISTIC was used to test for pepper line differences in the likelihood of whitefly nymph presence based on presence/absence data.

Proc GLIMMIX was used to test for differences among C. chinense lines in the number of fruits produced, total yield (g) and mean fruit weight (g; number of fruits/total yield). Fruit number and total yield models assumed a Poisson distribution (log link), while the fruit weight model assumed a gamma distribution (log link).

For all statistical models, the effect of plot was included to account for spatial variation in insect attack and spread of virosis. Previously, the plotX line interaction was removed owing to its non–significance. The only exception was the model for number of weeks until appearance of symptoms of virosis. For all models results for type 3 analysis are reported. Whenever the line effect was significant, tests were run for differences among line least–square means (using corrected P–values). In all cases, back–transformed least–square means and 95 % confidence limits are shown as descriptive statistics. All models treated C. chinense line as fixed effect given that this study was based on the a priori selection and examination of resistance of pepper lines of interest in breeding programs at INIFAP as well as for commercial purposes.

Fruit number, yield, and fruit weight

There were significant differences among habanero lines for fruit number (Table 1); G36 produced the greatest number of fruits and differed significantly from all other lines (p≤0.05). Then followed G110 and G37 with intermediate values that did not differ significantly (p>0.05) from G37 and G110, neither among each other (Table 2).

Mean fruit weight also differed significantly among habanero lines (Table 1), with G149 showing the greatest weight, compared to all other lines (p≤0.05). G110 and G84 had the following greatest values, differing significantly from G37 and G36 (p≤0.05), but not among each other (p>0.05). G37 had the following lowest weight and differed from G36 with the lowest value of all lines (p≤0.05)(Table 2).

There were weaker differences (marginal) for total yield among habanero lines (Table 1). G110 and G84 showed the highest and lowest average yield, and G149, G37, and G36 showed intermediate values (Table 2). These findings show how G84 by having an intermediate mean fruit weight, but one of the lowest fruit outputs, exhibited the lowest yield of all five lines. In contrast, line G36, despite producing the smallest fruits, had the highest fruit output and an intermediate yield. Line G110 showed the highest yield by producing the second largest amount of fruits and intermediate–size fruits.

Pest incidence and virosis among C. chinense lines

There were significant differences among lines for number of mines per leaf, proportion of fruits attacked by the pepper weevil, degree of severity of virosis, and number of weeks up to appearance of symptoms of virosis (Table 1). Differences among lines were not significant for the likelihood of presence of whitefly nymphs (logistic regression: X²=7.59; d.f. =4,197; p=0.06).

Line G36 was the most attacked by the leafminer, followed by G149 from which it did not differ significantly (p> 0.05). These two lines showed a greater amount of leaf mines relative to G110, G37 and G84 (p≤0.05); the latter three lines did not differ signficantly (Figure 1A). In contrast, G36 exhibited the lowest proportion of attacked fruits by the pepper weevil (p≤0.05, compared with the other lines); the following line with the lowest proportion of attacked fruits showed more than a three–fold difference relative to G36. Line G110 showed the highest proportion of attacked fruits (p≤0.05, compared with the other lines), followed by lines G149, G37 and G84, which were similar between them (p>0.05; Figure 1B). By showing the highest incidence of fruit infestation but a tendency for the lowest number of mines per leaf, line G110 showed a reverse pattern of attack for these two pests relative to G36. Such reverse patterns of attack by leaf miners relative to the weevil may suggest trade–offs in resistance against pests for these two lines (Koricheva et al., 2004; Lankau, 2007). Although of preliminary nature due to the limited number of lines used in this study, there was a significant negative correlation between the number of leaf mines and the proportion of weevil–attacked fruits using pepper line means (r=–0.89, p=0.03). Nonetheless, to formally test this hypothesis, further experiments are needed using prescribed levels of infestation rates of each pest (including control plants), comparing results at several sites and across two or more years.

Because G36 produced the smallest fruits of all five lines and showed the lowest proportion of attacked fruits by A. eugenii, it is possible that fruit selection by ovipositing female weevils is dictated by plant traits such as fruit size. Female beetles may prefer to oviposit on larger fruits for two reasons: greater resource availability or decreased risk of predation. To support the latter idea, G36 showed higher parasitism rates of weevils (1.2 to 6.3–fold greater relative to the other lines), presumably due to easier access of the female parasitoid to weevil larvae during oviposition. On the contrary, Porter et al. (2007) report that weevils prefered smaller fruits of a Jalapeño cultivar, which could be due to differences in fruit developmental time. Besides, other fruit traits such as pericarp thickness were proposed as important predictors of parasitism risk of pepper weevil in bell pepper (Riley and Schuster, 1992) and remain to be tested in C. chinense. In addition to fruit traits per se, high fruit production may cause an effect of satiation on the pepper weevil (Elzinga et al., 2007), which may have influenced results in this study. These and other plant traits influencing weevil attack deserve further examination.

The mean number of weeks until the appearance of symptoms of virosis was similar among most lines, except G149, which was the earliest to show symptoms of infection but not significantly different from G110 (Figure 2A). In contrast, line G84 showed the highest mean score for severity of virosis by the end of the experiment, but there were no differences (p> 0.05) among all other lines (Figure 2B). Considering that lines appeared to show similar levels of antiobiosis or antixenosis or both to whitefly (i.e. weak differences in nymph presence/ absence), the fact that G84 showed a much higher mean score of severity suggests a lower degree of virus resistance by this line. Whitefly nymphs showed a very low abundances during the first half of the sampling period (July to September), and higher abundances of this pest may uncover stronger among–line differences in female oviposition choice and feeding. Hence, additional research is warranted to distinguish between B. tabaci antixenosis and antibiosis patterns, as well as how this relates to incidence and susceptiblity to virosis in habanero peppers. Only, Godinez–Hernandez et al. (2001) and Anaya–Lopez et al. (2003) report differences in virus susceptiblity among habanero lines. In the present study there is no evidence to support single virus species or co–infections in the field. Regardless of this limitation, providing a field–based assessment of habanero resistance to viruses transmitted by B. tabaci is important even when symptoms of infection cannot be linked to particular species of virus as in co–infection patterns frequently observed in the field (Janick and Jansky, 2000).

CONCLUSIONS

Results from this study provide evidence of field–based variation for pest attack levels as well as virus susceptibility among the studied Capsicum chinense lines. In particular, variation among habanero lines for incidence of L. trifolii and A. eugenii represents novel information for this crop species. Thus, these results provide baseline information for the selection of C. chinense lines for cultivar development purposes as well as research on crop traits associated with insect resistance and their inheritance.

ACKNOWLEDGMENTS

We thank Chenco Chale Macias and Carlos Cervera Herrera who provided assistance in the field, Emiliano Loeza Kuk who shared information on B. tabaci biotype identification and Victor Lopez–Martinez who contributed to the species identification of Liriomyza specimens. This study was funded by INIFAP (060047F).

LITERATURE CITED

Anaya–Lopez, J. L., I. Torres–Pacheco, M. Gonzalez–Chavira, J. A. Garzon–Tiznado, J. L. Pons–Hernandez, R. G. Guevara–Gonzalez, C. I. Muñoz–Sanchez, L. Guevara–Olvera, R. F. Rivera–Bustamante, and S. Hernandez–Verdugo. 2003. Resistance to geminivirus mixed infections in Mexican wild peppers. Hortscience 38: 251–254.         [ Links ]

Benson, D. A., M. Cavanaugh, K. Clark, I. Karsch–Mizrachi, D. J. Lipman, J. Ostell, and E. W. Sayers. 2013. GenBank. Nucleic Acids Res. 41(D1): D36–D42.         [ Links ]

Bosland, P. W., and E. Votava. 2000. Peppers: Vegetable and Spice Capsicums. CAB International. Wallingford. United Kingdom. 204 p.         [ Links ]

Cortesero, A. M., J. O. Stapel, and W. J. Lewis. 2000. Understanding and manipulating plant attributes to enhance biological control. Biol. Control 15: 35–49.         [ Links ]

Cuartero, J., H. Laterrot, and J. C. van Lenteren. 1999. Host–plant resistance to pathogens and arthropod pests. In: Albajes, R., M. Lodovica G., J. C. van Lenteren, and Y. Elad (eds). Integrated Pest and Disease Management in Greenhouse Crops. Kluwer. Netherlands. pp: 124–138.         [ Links ]

Eigenbrode, S. D., and J. T. Trumble. 1994. Host plant resistance to insects in integrated pest management in vegetable crops. J. Agric. Entomol. 11: 201–224.         [ Links ]

Elzinga, J. A., A. Atlan, A. Biere, L. Gigord, A. E. Weis, and G. Bernasconi. 2007. Time after time: flowering phenology and biotic interactions. Trends Ecol. Evol. 22: 432–439.         [ Links ]

Eskenazi, B., A. Bradman, and R. Castorina. 1999. Exposures of children to organophosphate pesticides and their potential adverse health effects. Environ. Health Persp. 107: 409–419.         [ Links ]

Fridaus, S., A. van Heusden, A. Harpenas, E. D. J. Supena, R. G. F. Visser, and B. Vosman. 2011. Identification of silverleaf whitefly resistance in pepper. Plant Breed. DOI: 10.1111/j.1439–0523.2011.01894.x.         [ Links ]

Godinez–Hernandez, Y., J. L. Anaya–Lopez, R. Díaz–Plaza, M. González–Chavira, and I. Torres–Pacheco. 2001. Characterization of resistance to pepper huasteco geminivirus in chili peppers from Yucatán, México. Hortscience 36: 139–142.         [ Links ]

González–Pérez, J. L., M. C. Espino–Guidiño, I. Torres–Pacheco, R. G. Guevara–González, G. Herrera–Ruiz, and V. Rodríguez–Hernández. 2011. Quantification of virus syndrome in chili peppers. Afr. J. Biotechnol. 10: 5236–5250.         [ Links ]

Janick, J., and S. Jansky. 2000. Breeding for diseases resistance in potato. In: Janick, J. (ed).         [ Links ] Plant Breed. Rev. 19: 69–155.         [ Links ]

Kim, J. S., H. J. Jee, J. G. Gwag, and C. K. Shim. 2010. Evaluation on red pepper germplasm lines (Capsicum spp.) for resistance to anthracnose caused by Colletotrichumacutaum. Plant Pathol. J. 26: 1598–2254.         [ Links ]

Koricheva, J., H. Nykänen, and E. Gianoli. 2004. Meta–analysis of trade–offs among plant antiherbivore defenses: are plants jacks–of–all–trades, masters of all? Am. Naturalist 163: E64–75.         [ Links ]

Lankau, R. A. 2007. Specialist and generalist herbivores exert opposing selection on chemical defense. New Phytol. 175: 176–184.         [ Links ]

Méndez–Lozano, J., R. F. Rivera–Bustamante, C. M. Fauquet, and R. de la Torre–Almaraz. 2001. Pepper huasteco virus and Pepper golden mosaic virus are geminiviruses affecting tomatillo (Physalis ixocarpa) crops in México. Plant Dis. 85: 1291.         [ Links ]

Mendez–Lozano, J., I. Torres–Pacheco, C. M. Fauquet, and R. F. Rivera–Bustamante. 2003. Interactions between geminiviruses in a naturally occurring mixture: Pepperhuasteco virus and Pepper golden mosaic virus. Virology 93: 270–277.         [ Links ]

Morales, F. J., and P. K. Anderson. 2001. The emergence and dissemination of whitefly–transmitted geminiviruses in Latin America. Arch. Virol. 146: 415–441.         [ Links ]

Morales, F. J. 2011. Interaction between Bemisia tabaci, Begomoviruses, and plant species in Latin America and the Caribbean. In: Thompson, W. (ed). The Whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) Interaction with Geminivirus–Infected Host Plants. Springer. Netherlands. pp: 15–49.         [ Links ]

Mundt, C. C. 2002. Use of multiline cultivars and cultivar mixtures for disease management. Ann. Rev. Phytopathol. 40: 381–410.         [ Links ]

Nauen, R., and I. Denholm. 2005. Resistance of insect pests to neonicotinoid insecticides: Current status and future prospects. Arch. Insect Biochem. Physiol. 58: 200–215.         [ Links ]

Nombela, G., F. Beitia, and M. Muñiz. 2001. A differential interaction study of Bemisia tabaci Q–biotype on commercial tomato varieties with or without the Mi resistance gene, and comparative host responses with the B–biotype. Entomol. Exp. Appl. 98: 339–344.         [ Links ]

Papayiannis, L. C., J. K. Brown, N. A. Seraphides, M. Hadjistylli, N. Ioannou, and N. I. Katis. 2009. A real–time PCR assay to differentiate the B and Q biotypes of the Bemisia tabaci complex in Cyprus. Bull. Entomol. Res. 99(06): 573–582.         [ Links ]

Parella, M. P. 1987. Biology of Liriomyza. Ann. Rev. Entomol. 32: 201–224.         [ Links ]

Peacock, L., T. Hunter, H. Turner, and P. Brain. 2001. Does host genotype diversity affect the distribution of insect and disease damage in willow cropping systems? J. Appl. Ecol. 38: 1070–1081.         [ Links ]

Polston, J. E., and P. K. Anderson. 1997. The emergence of whitefly transmitted geminiviruses in tomato in the western hemisphere. Plant Dis. 81: 1358–1369.         [ Links ]

Porter, P., B. E. Lewis, R. Scanion, and S. Murray. 2007. Pepper weevil infestation of cv. Early Jalapeno peppers of different size classes. Southwestern Entomol. 32: 1–6.         [ Links ]

Riley, D. G., and D. J. Schuster. 1992. The occurrence of Catolaccushunteri, a parasitoid of Anthonomus eugenii, in insecticide treated bell pepper. Southwestern Entomol. 17: 71–72.         [ Links ]

Riley, D. G., D. J. Schuster, and C. S. Barfield. 1992. Sampling and dispersion of pepper weevil (Coleoptera: Curculionidae) adults. Environ. Entomol. 21: 1013–1021.         [ Links ]

Sarath Babu, B., S. R. Pandravada, R. D. Prasada Rao, K. Anitha, S. K. Cakrabarty, and K. S. Varasprasad. 2011. Global sources of pepper genetic resources against arthropods, nematodes and pathogens. Crop Protection 30: 389–400.         [ Links ]

SAS. 2002. SAS, Version 9.1. SAS Institute Inc., North Carolina.         [ Links ]

SIAP (Servicio de Información Agroalimentaria y Pesquera). 2011. Agricultura, Producción Anual. http://www.siap.sagarpa.gob.mx (Accessed: January 2012.         [ Links ])

Smith, C. M. 2005. Plant Resistance to Arthropods. Molecular and Conventional Approaches. Springer. Netherlands. 423 p.         [ Links ]

Soria–Fregoso, M. J., J. M. Tun–Suarez, R. H. Trejo, y S. R. Terán.1996. Tecnología para la Producción de Hortalizas a Cielo Abierto en la Península de Yucatán. Tercera edición, CIGA–Instituto Tecnológico Agropecuario No. 2. Conkal, México. 430 p.         [ Links ]

Theiling, K. M., and B. A. Croft. 1988. Pesticide side–effects on arthropod natural enemies: A database summary. Agric. Ecosys. Environ. 21: 191–218.         [ Links ]

Torres–Pacheco, I., J. A. Garzon–Tiznado, J. K. Brown, A. Becerra–Flora, and B. F. Rivera–Bustamante. 1996. Detection and distribution of geminiviruses in México and southern United States. Phytopathology 86: 1186–1192.         [ Links ]

Trujillo–Aguirre, J. J., and C. del R. Pérez–Llanes. 2004. Chile habanero Capsicum chinense Diversidad varietal. Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias. Folleto Técnico. México. 24 p.         [ Links ]

Tun–Dzul, J. C. 2001. Chile habanero. Características y tecnología de producción. Folleto técnico. Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias. México. 74 p.         [ Links ]

Wilhoit, L. R. 1992. Evolution of virulence to plant resistance: Influence of variety mixtures. In: Fritz, R. S., and E. L. Simms (eds). Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics. University of Chicago Press. Chicago. pp: 91–119.         [ Links ]

Zuur, A. F., E. N. Ieno, N. J. Walker, A. A. Saveliev, and G. M. Smith. 2009. Mixed Effects Models and Extensions in Ecology with R. Springer. New York. 574 p.         [ Links ]