versão impressa ISSN 1519-566X
Neotrop. entomol. vol.40 no.5 Londrina set./out. 2011
ECOLOGY, BEHAVIOR AND BIONOMICS
Development and survival of the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Yponomeutidae) as a function of temperature: effect on the number of generations in tropical and subtropical regions
CA Marchioro; LA Foerster
Depto de Zoologia, Univ Federal do Paraná, Curitiba, PR, Brasil
The diamondback moth, Plutella xylostella (L.), is the most important pest of brassicaceous crops worldwide. Since temperature is the major abiotic factor influencing insect development and thermal requirements may vary among insect populations, it is important to know the effect of temperature on development and survival of a subtropical strain of P. xylostella. Development and survival of the diamondback moth was evaluated under seven constant temperatures ranging from 10°C to 35°C. Development was completed between 10°C and 32.5°C, but at 35°C all individuals died in the larval stage. Data were fitted to one linear and five nonlinear models. Considering as criteria the goodness of fit and the ability to estimate parameters of biological significance, the models Briere-1 and Briere-2 were the most adequate to describe the relationship between temperature and development of P. xylostella. The linear model demonstrated that P. xylostella required 312.5 degree-days above a lower threshold of 6.3°C to complete development. The degree-day model showed that the number of diamondback moth generations in the tropical region of Brazil is nearly twice the number in the subtropical region of the country. This result explains, at least in part, the higher population levels of this species in the tropical region of Brazil, and also demonstrates that P. xylostella is tolerant to a wide range of temperatures (6.1-32.5°C). Therefore, temperature cannot be considered a limiting factor for the occurrence of diamondback moth throughout the year in most regions of Brazil.
Keywords: Degree-day, development rate, lower development threshold, thermal requirement, upper development threshold
The diamondback moth, Plutella xylostella (L.), is the most destructive pest of brassicaceous plants worldwide (Talekar & Shelton 1993). High population levels can cause losses in yield up to 90% (Verkerk & Wright 1996) resulting in an estimated 1 billion US dollars to promote its annual management (Talekar & Shelton 1993). The high incidence of the diamondback moth is partially explained by the absence of effective natural enemies (Lim 1986), as well as by its high capacity to develop resistance to insecticides (Talekar & Shelton 1993).
Studies on the factors that affect field density and population dynamics are fundamental for the development of management strategies to control P. xylostella. Temperature is recognized as the most important environmental factor influencing development and survival of insects (Hallman & Denlinger 1998). Although the relationship between temperature and development of P. xylostella has been studied in other countries (Sarnthoy et al 1989, Shirai 2000, Liu et al 2002, Mohandass & Zalucki 2004, Golizadeh et al 2007), the thermal requirements may vary among different populations (Lee & Elliot 1998, Gomi et al 2003) mainly due to geographic differences in climate according to a gradient of latitude (Honék 1996, Addo-Bediako et al 2000, Chen & Kang 2004). Honék (1996) showed that in subtropical and temperate zones the lower development threshold decreases with increasing geographical latitude.
The incidence levels of P. xylostella on brassicaceous crops in the subtropical region of Brazil (unpublished data) are not as severe as those reported for tropical areas and other countries (Martínez-Castillo et al 2002, Guilloux et al 2003, Campos et al 2006). Thus, this study was conducted to evaluate the upper and lower temperature thresholds for development and survival of a subtropical population of P. xylostella, in order to investigate the differences in the population dynamics of the pest in comparison to its incidence levels in the tropical region of Brazil.
Material and Methods
Laboratory rearing of P. xylostella
A colony of P. xylostella was established with larvae and pupae collected in commercial crops of broccoli (Brassica oleracea cv. italica) and cauliflower (B. oleracea cv. botrytis). The collection area is located in Colombo, Paraná State, in the subtropical region of Southern Brazil (25°17' S; 49°13' W), a transitional zone between tropical and temperate climates, characterized by cold and dry winters and rainy and moderate temperatures in summer.
Larvae of P. xylostella were reared on broccolis leaves until pupation in 18 cm diameter Petri dishes containing 50 neonate larvae. Pupae were individually kept in 2 cm diameter by 4 cm high polyethylene tubes until adult emergence. Adults were kept in 10 cm diameter by 20 cm high polyethylene cages. A 5 x 5 cm leaf piece of broccoli placed between two superposed lids was used as a stimulant for oviposition. The lower lid had a 4 x 4 cm slit in the center to allow adults to reach the leaf inside the cage. The internal surface of the lower lid was lined with sulfite paper, where the eggs were laid around the exposed broccoli leaf. Every three days the paper containing the eggs was removed and the broccoli leaf on the lid was changed. Adults were fed with 10% honey diluted in water, provided in a cotton ball soaked in the solution. The colony was maintained in a climatic chamber at 20 ± 1°C, 70 ± 10% RH and 12:12 L:D photoperiod.
Development and survival of P. xylostella in relation to temperature
Development time and survival of the diamondback moth were evaluated at 10, 15, 20, 25, 30, 32.5 and 35 ± 1°C, 70 ± 10% RH and 12:12 L:D photoperiod. Sixty newly hatched larvae were transferred from the laboratory colony to each temperature and individually kept in 2 x 4 cm polyethylene vials lined with paper towel. Larvae were fed on broccoli leaves previously washed in a 1% sodium hypochlorite solution. Food was provided daily as well as the recording of mortality and development time. Eggs obtained from females reared at each temperature were used to evaluate the incubation period. Eggs laid at 32.5°C and 35°C did not hatch; thus in these treatments incubation period was assessed on eggs laid at 20°C and immediately transferred to either 32.5°C or 35°C. For each of these temperatures, 30 replicates each containing 40 eggs were tested.
Relationship between temperature and development
Based on development time for each immature stage in all temperatures evaluated, the development rate (1/development time) was recorded for each individual. The relationship between temperature and development rate of P. xylostella was fitted by one linear and five nonlinear models (Table 1). To correctly estimate the linear regression coefficients, only the linear part of the relationship between temperature and development was computed; thus, the data recorded for 32.5°C and 35°C were not used. Using the parameters estimated by the linear regression, the lower temperature threshold (T0) and thermal constant (K) were respectively calculated by means of the x-intercept method (T0 = -a/b), and by the reciprocal of the slopes (K = 1/b). In the nonlinear models proposed by Brière et al (1999), the optimum temperature (Topt) was calculated using the T0 and upper temperature threshold (Tmax) estimated by the model, according to the equation:
The evaluation of each mathematical model was based on its ability to describe the data accurately. The commonly used statistics for this purpose are the coefficient of determination (r2) and residual sums of square (RSS) (Roy et al 2002), that indicates better fits with higher and lower values, respectively (Aghdam et al 2009). The Akaike information criterion (AIC) was also used as an additional parameter to evaluate the goodness-of-fit of the mathematical models tested. The AIC was calculated using the equation:
AIC = nln(SSE/x) + 2p
where n is the number of treatments, SSE is the sum of the squared error, and p is the number of parameters in the model. Smaller AIC values were considered as an indicative of better fit (Sandhu et al 2010). All parameters employed in the regression models were estimated with the software Table Curve 2D (Systat Inc 2002).
Number of generations
The number of diamondback moth generations was used as a parameter to assess the role of temperature on population dynamics of the pest. The number of generations was calculated using the cumulative degree-days, according to the single sine method. This method uses daily minimum and maximum temperatures to produce a sine curve over a 24h period, and then estimates degree-days for that day by calculating the area above the threshold and below the curve (Herms 2004). The minimum and maximum daily temperature of different regions of Brazil were obtained from "Instituto Nacional de Metereologia (INMET)", considering only the months between June and November, which is the period of diamondback moth occurrence in Brazil (Guilloux et al 2003, Campos et al 2006).
The effect of temperature on development time of the immature stages was evaluated by analysis of variance (ANOVA). When differences were detected, Tukey's HSD test (P < 0.05) was applied to classify the means. Differences in survival rates were compared by Chi-square test (P < 0.05). Additionally survival curves were constructed for each temperature and compared using the survival function of Kaplan-Meier estimation (Kaplan & Meier 1958). All analyses were performed using the software Statistica 6.0 (Statsoft Inc 2001).
Plutella xylostella completed development from egg to adult in all temperatures evaluated, except at 35°C, which was lethal to the larvae (Table 1). The duration of the immature stages and the time required to complete the cycle from egg to adult were significantly affected by temperature (Table 2). In general, the development time of the immature stages decreased linearly with the increase of temperature between 10°C and 30ºC. Above 30ºC, the development rate was clearly reduced, indicating that the optimum temperature is close to this value.
The lowest and highest temperatures evaluated had a deleterious effect on the survival of P. xylostella. Larval survival at 10°C (80.0%), 30°C (76.7%) and 32.5°C (81.7%) was significantly lower (Χ2 = 6.12, P < 0.05) than at 15°C (95.0%), 20°C (96.7%) and 25°C (95.0%). Similarly, when P. xylostella was maintained at 10, 30 and 32.5°C, the percentage of survival from egg to adult was lower (80.0, 76.7 and 71.7%, respectively) than at 15°C (93.3%), 20°C (96.7%) and 25°C (95.0%) (Χ2 = 9.02, P < 0.01). In contrast, no significant differences in mortality were recorded during pupal stage. The survival curves obtained by Kaplan-Meier´s estimation showed significant differences according to the temperature (Χ2 = 232.26 P < 0.001), and an increase in temperature resulted in a decrease in survival time (Fig 1).
When data from 32.5°C and 35°C were excluded from the analysis, the linear regression suitably described the relationship between temperature and development rate of P. xylostella, as corroborated by the high r2 and low RSS and AIC (Table 3). According to the linear regression, the diamondback moth required 312.5 degree-days above the lower threshold of 6.3ºC to complete development from egg to adult stage (Table 3).
The mathematical models evaluated provided a good fit to describe the relationship between temperature and development rate of the different life stages of P. xylostella (Fig 2, Table 4). The models Brière-1, Brière-2, Lactin-1 and Polynomial showed r2 higher than 0.93, and low RSS and AIC values (Table 4). In contrast, Taylor's model did not adequately fit the data, especially for larval stage and total development, as indicated by the low r2 values.
Number of generations at different localities of Brazil
In general, the number of diamondback moth generations increased with decreasing latitude (Table 5). The highest number of generations was estimated for the state of Pernambuco, Northeastern Brazil (11.0), which was nearly twice the number of generations (5.8) estimated for Colombo, state of Paraná in Southern Brazil.
Temperature is the most important abiotic factor affecting insect growth, development rate and survival (Hallman & Denlinger 1998). The diamondback moth develops between 10°C and 32.5°C, but did not survive at the constant temperature of 35°C. Other studies performed with this species reported similar results (Liu et al 2002, Golizadeh et al 2007), although individuals of some tropical populations were able to complete development at 35°C, with a high mortality rate (Shirai 2000). Survival of P. xylostella was also affected by the extreme temperatures evaluated in the study. Diamondback moth mortality followed the pattern described by Liu et al (1995), represented by a "U" shaped curve, with highest mortality at 10°C followed by a reduction in mortality as the temperature increased between 15°C and 25°C, and by another increase between 30°C and 35°C.
The influence of temperature on development and survival of the diamondback moth may affect the population dynamics of the pest. Such influence can be quantified by calculating the number of generations for localities with different climatic conditions, based on parameters estimated by the linear model. In this study we demonstrated that a higher number of diamondback moth generations are expected for warmer regions of Brazil. This result confirms the field information, which demonstrate that the abundance of diamondback moth attacking brassicaceous crops in the tropical region of Brazil (Guilloux et al 2003) and other countries (Martínez-Castillo et al 2002, Ahmad et al 2009) is higher if compared with those recorded in the subtropical region (Marchioro 2011). These differences in the number of generations may be even greater if there are strains adapted to local climatic conditions in tropics of Brazil.
Predicting the development time of an insect pest in relation to temperature can be an important tool for pest management (Roy et al 2002). In this context, the selection of mathematical models that suitably describe this relationship is essential. The relationship between temperature and development in insects tends to be nonlinear over the full range of tolerable temperature (Logan et al 1976, Lactin et al 1995). In the present study, the linear regression provided a good fit to describe the data, but only when the linear part of the relationship between temperature and development was considered (10-30ºC). The development time of P. xylostella from egg to adult was longer in temperatures above 30ºC, demonstrating that the optimum temperature was exceeded. If the linear regression was used over the full range of tolerable temperature by P. xylostella, the results would have been inaccurate, and in this case nonlinear models would be more adequate.
The performance of nonlinear models varies according to the species under study, and in some cases the results can be quite different. The model proposed by Logan et al (1976) was suitable for some species (Coop et al 1993, Roy et al 2002, Fantinou et al 2003, Bonato et al 2007), whereas for other species better results were obtained using the model of Lactin et al (1995) (Kontodimas et al 2004, Castillo et al 2006) and Briere et al (1999) (Roy et al 2002, Aghdam et al 2009). In our study, the nonlinear models Brière-1, Brière-2, Lactin-1 and Polynomial best described the relationship between temperature and P. xylostella development, and can be used to predict development time.
Along with the statistics, another parameter that can be used to select a model is its capacity to estimate parameters of biological significance, such as T0, Topt and Tmax (Roy et al 2002). Despite the high number of parameters, the polynomial model did not estimate parameters of biological interest. The Lactin-1 model estimates Tmax, but because it predicts positive development rates even at 0ºC, this model could not accurately estimate the T0. In contrast, Brière 1 and 2 models estimate T0 and Tmax, and based on these parameters allows the calculation of Topt. Therefore, considering both the statistical criteria and the ability to estimate parameters of biological significance, the models proposed by Briere et al (1999) can be considered the most appropriate for P. xylostella development time prediction.
The estimated T0 through the nonlinear models showed subtle differences in comparison to the values obtained by linear regression. Studies performed with other species have shown similar results when comparing the T0 estimated by linear and nonlinear models (Herrera et al 2005, Golizadeh et al 2007, Jalali et al 2009). This difference is due to the fact that the linear regression uses only the linear part of the points to calculate thelower temperature threshold, whereas nonlinear models also uses the observed points above the Topt.
Studies conducted with populations from different geographical areas have shown slight variation in development time, lower threshold and thermal constant of P. xylostella. These differences can be attributed to multiple factors such as experimental conditions, host-plant quality and thermal adaptations to different geographical areas. Larval food can affect development time and survival of the diamondback moth (Hamilton et al 2005, Ayalew et al 2006, Thuler et al 2007), and can explain at least in part the differences reported in the literature. Another explanation is the existence of differences among populations from distinct geographical localities due to acclimatization. According to Honék (1996), the lower thermal limits reduces as latitude increases.
Although some studies have demonstrated variations in thermal response of insects along a gradient of latitude (Addo-Bediako et al 2000, Kimura 2004), the available information for P. xylostella is conflicting. For example, in a study with three populations of this species from geographically isolated localities of Japan, differences in the development rate among the populations were reported (Umeya & Yamada 1973). On the other hand, in a study comparing Japanese and Thai populations of the diamondback moth no difference in development time was recorded (Sarnthoy et al 1989). This view was confirmed in a study with nine populations of P. xylostella from tropical and subtropical regions of Asia (Shirai 2000). In this study, the author emphasized that it is unlikely that clear geographical differences in thermal response would be generated in a highly mobile species like P. xylostella. However, as pointed out by Mohandass & Zalucki (2004), the populations evaluated by Shirai (2000) were kept under laboratory conditions for a long time and the possibility of acclimatization of the strains to local conditions was not evaluated.
The minimum temperature tested in the work of Sarnthoy et al (1989) was 17°C, and 15°C in Shirai (2000), which were higher than the lowest one tested in the present study (10°C). According to Mohandass & Zalucki (2004), the inclusion of lower temperature regimes in such experiments would give an indication of the differences in development rate among strains from temperate zones against those from tropical and subtropical zones. In fact, the development time registered (72.6 days) at a temperature closer to the lower thermal limit evaluated in our study (10°C) was lower than the 88.8 days (Liu et al 2002), 85.1 and 81.2 days (Golizadeh et al 2007) reported in other studies at 10°C.
Another way to evaluate differences among populations in thermal response is through comparison of parameters such as lower temperature threshold and thermal constant. According to Trudgill (1995), species with low T0 develop faster at low temperatures, while warm adapted species develop faster at high temperatures. Therefore higher T0 and lower K are expected for populations of tropical regions, whereas in subtropical and temperate regions a lower T0 and higher K is expected (Trudgill & Perry 1994). The comparison of T0 and K estimated for diamondback moth populations from subtropics and temperate regions with those estimated for tropical populations clearly show this pattern. The parameters estimated for a tropical population from Indonesia (Latitude 3º S) were 8.1ºC and 232.5 DD, respectively (Shirai 2000). In contrast, T0 and K estimated for populations of China (Liu et al 2002, latitude 30º N), Iran (Golizadeh et al 2007, latitude 35º N), Japan (Shirai 2000, latitude 43º N) and Brazil (present study, latitude 25º S), were respectively: 7.4ºC and 268.2 DD, 7.0ºC and 263.7 DD, 6.7ºC and 285.7 DD and 6.3ºC and 312.5 DD.
Considering the lower and upper temperature thresholds estimated by the nonlinear models and the capacity of P. xylostella to survive at temperatures below 0ºC for up to two months (Gu 2009), it is unlikely that temperature limits the occurrence of the diamondback moth throughout the year in most regions of Brazil. Nevertheless, studies carried out in different regions of Brazil have shown that P. xylostella occurs in high levels only between June and November (Guilloux et al 2003, Campos et al 2006, Marchioro 2011), period in which temperatures are lower. The results indicate that local factors other than temperature must be considered, such as rainfall intensity and levels of parasitism. To avoid these unfavorable conditions, the moths might be adapted to abandon the habitat as soon as they emerge from the pupae (Campos et al 2006).
The results obtained in this study show that temperature play an important role on development and survival of the diamondback moth, and that mathematical models can be used to describe the relationship between temperature and development rate. Differences in temperature between tropical and subtropical regions affect the number of generations of the diamondback moth, and may be responsible for the differences in population levels recorded between these regions.
The authors are grateful to the MSc Flavia da Silva Krechemer for technical support and to CNPq and CAPES for the scholarships and financial support provided.
Addo-Bediako A, Chown SL, Gaston KJ (2000) Thermal tolerance, climatic variability and latitude. Proc R Soc Lond B 267: 739-745. [ Links ]
Aghdam HR, Fathipour Y, Radjabi G, Rezapanah M (2009) Temperature-dependent development and temperature thresholds of codling moth (Lepidoptera: Tortricidae) in Iran. Environ Entomol 38: 885-895. [ Links ]
Ahmad T, Ansari MS, Ali H (2009) Outbreak of diamondback moth, Plutella xylostella in Aligarh, India. Trends Biosci 2: 10-12. [ Links ]
Ayalew G, Löhr B, Ogol CKPO, Baumgärtner J (2006) Suitability of cultivated and wild crucifers for the development of diamondback moth, Plutella xylostella L. (Lepidoptera: Plutellidae). J Entomol 3: 82-88. [ Links ]
Bonato O, Lurete A, Vidal C, Fargues J (2007) Modeling temperature-dependent bionomics of Bemisia tabaci (Q-biotype). Physiol Entomol 32: 50-55. [ Links ]
Briere JF, Pracos P, Le Roux AY, Pierre JS (1999) A novel rate model of temperature-dependent development for arthropods. Environ Entomol 28: 22-29. [ Links ]
Campos WG, Schoereder LH, DeSouza OF (2006) Seasonality in neotropical populations of Plutella xylostella (Lepidoptera): resource availability and migration. Popul Ecol 48: 151-158. [ Links ]
Castillo J, Jacas JA, Peña JE, Ulmer BJ, Hall DG ( 2006) Effect of temperature on life history of Quadrastichus haitiensis (Hymenoptera: Eulophidae), an endoparasitoid of Diaprepes abbreviatus (Coleoptera: Curculionidae). Biol Control 36: 189-196. [ Links ]
Chen B, Kang L (2004) Variation in cold hardiness of Liriomyza huidobrensis (Diptera: Agromyzidae) along the latitudinal gradients. Environ Entomol 33: 155-164. [ Links ]
Coop LB, Croft, A, Drapek RJ (1993) Model of corn earworm (Lepidoptera: Noctuidae) development, damage, and crop loss in sweet corn. J Econ Entomol 86: 906-916. [ Links ]
Fantinou AA, Perdikis DC, Chatzoglou CS (2003) Development of immature stages of Sesamia nonagrioides (Lepidoptera: Noctuidae) under alternating and constant temperatures. Environ Entomol 32:1337-1342. [ Links ]
Fields PG (1992) The control of stored-products insects and mites with extremes temperatures. J Stored Prod Res 28: 89-118. [ Links ]
Golizadeh A, Kamali K, Fathipour Y, Abbasipour H (2007) Temperature-dependent development of diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) on two brassicaceous host plants. Insect Sci 14: 309-316. [ Links ]
Gomi T, Inudo M, Yamada D (2003) Local divergence in developmental traits within a trivoltine area of Hyphantria cunea Drury (Lepidoptera: Arctiidae). Entomol Sci 6: 71-75. [ Links ]
Gu H (2009) Cold tolerance and overwintering of the diamondback moth (Lepidoptera: Plutellidae) in Southeastern Australia. Environ Entomol 38: 524-529. [ Links ]
Guilloux T, Monnerat RG, Castelo-Branco M, Kirk AA, Bordat D (2003) Population dynamics of Plutella xylostella (Lep., Yponomeutidae) and its parasitoids in the region of Brasilia. J Appl Entomol 127: 288-292. [ Links ]
Hallman GJ, Denlinger DL (1998) Introduction: temperature sensitivity and integrated pest management, p.1-5. In Hallman GJ, Denlinger DL (eds) Temperature sensitivity in insects and application in integrated pest management. Boulder, Westview Press, 311p. [ Links ]
Hamilton AJ, Endersby NM, Ridland PM, Zhang J, Neal M (2005) Effects of cultivar on oviposition preference, larval feeding and development time of diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), on some Brassica oleracea vegetables in Victoria. Aust J Entomol 44: 284-287. [ Links ]
Herms DA (2004) Using degree-days and plant phenology to predict pest activity, p. 59-59. In Krischik V, Davidson J (eds) IPM of midwest landscapes. St Paul, University of Minnesota, 316p. [ Links ]
Herrera AM, Dahlsten DD, Tomic-Carruthers N, Carruthers RI (2005) Estimating temperature-dependent developmental rates of Diorhabda elongata (Coleoptera: Chrysomelidae), a biological control agent of saltcedar (Tamarix spp.). Environ Entomol 34: 775-784. [ Links ]
Honék A (1996) Geographical variation in thermal requirements for insect development. Eur J Entomol 93: 303-312. [ Links ]
Jalalai MA, Tirry L, Arbab A, De Clercq P (2009) Temperature-dependent development of the two-spotted ladybeetle, Adalia bipunctata, on the green peach aphid, Myzus persicae, and a factitious food under constant temperatures. J Insect Sci 10: 124. [ Links ]
Kaplan EL, Meier P (1958) Nonparametric estimation from incomplete observations. J Am Stat Assoc 53: 457-481. [ Links ]
Kimura MT (2004) Cold and heat tolerance of drosophilid flies with reference to their latitudinal distributions. Oecologia 140: 442-449. [ Links ]
Kontodimas DC, Eliopoulos PA, Stathas GJ, Economou LP (2004) Comparative temperature-dependent development of Nephus includes (Kirsch) and Nephus bisignatus (Boheman) (Coleoptera: Coccinelidae) preying on Planococcus citri (Risso) (Homoptera: Pseudococcidae): evaluation of a linear and various nonlinear models using specific criteria. Environ Entomol 33: 1-11. [ Links ]
Lactin DJ, Holliday NJ, Johnson DL, Craigen R (1995) Improved rate model of temperature-dependent development by arthropods. Environ Entomol 24: 68-75. [ Links ]
Lamb RJ, Gerber GH, Atkinsin GF (1984) Comparison of developmental rate curves applied to egg hatching data of Entomoscelis Americana Brown (Coleoptera: Chrysomelidae). Environ Entomol 13: 868-872. [ Links ]
Lee JH, Elliott NC (1998) Comparison of developmental responses to temperature in Aphelinus asycyhis (Walker) from two different geographic regions. Southwest Entomol 23: 77-82. [ Links ]
Lim GS (1986) Biological control of diamondback moth, p.159-171. In Diamondback moth Management: Proceedings of the First International Workshop. Taiwan, Asian Vegetable Research and Development Center. [ Links ]
Liu SS, Chen FZ, Zalucki MP (2002) Development and survival of the diamondback moth (Lepidoptera: Plutellidae) at constant and alternating temperatures. Environ Entomol 31: 221-231. [ Links ]
Liu SS, Zhang GM, Zhu J (1995) Influence of temperature variations on rate of development in insects: analysis of case studies from entomological literature. Ann Entomol Soc Am 88: 109-117. [ Links ]
Logan JA, Wollkind DJ, Hoyt SC, Tanigoshi LK (1976) An analytic model for description of temperature dependent rate phenomena in arthropods. Environ Entomol 5: 1133-1140. [ Links ]
Marchioro CA (2011) Flutuação populacional de Plutella xylostella (L.) (Lepidoptera : Yponomeutidae) e seus parasitóides no Sudeste do Paraná: biologia em plantas silvestres e cultivadas e exigências térmicas. Tese de doutorado, Universidade Federal do Paraná, 156p. [ Links ]
Martinez-Castillo M, Leyva JL, Cibrian-Tovar J, Bujanos-Muniz R (2002) Parasitoid diversity and impact on populations of the diamondback moth Plutella xylostella (L.) on Brassica crops in central Mexico. BioControl 47: 23-31. [ Links ]
Mohandass S, Zalucki MP (2004) DBM development: are we measuring the right temperatures?, p.117-122. In The Management of the Diamondback Moth and Other Crucifer Pests: Proceedings of the Fourth International Workshop. Victoria, The Regional Institute. [ Links ]
Roy M, Brodeur J, Cloutier C (2002) Relationship between temperature and developmental rate of Stethorus punctillum (Coleoptera: Coccinellidae) and its prey Tetranychus mcdanieli (Acarina: Tetranychidae). Environ Entomol 31: 177-187. [ Links ]
Sandhu HS, Nuessly GS, Webb SE, Cherry RH, Gilbert RA (2010) Temperature-dependent development of Elasmopalpus lignosellus (Lepidoptera: Pyralidae) on sugarcane under laboratory conditions. Environ Entomol 39: 1012-1020. [ Links ]
Sarnthoy O, Keinmeesuke P, Sinchaisri N, Nakasuji F (1989) Development and reproductive rate of the diamondback moth Plutella xylostella from Thailand. Appl Entomol Zool 24: 202-208. [ Links ]
Shirai Y (2000) Temperature tolerance of the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae) in tropical and temperate regions of Asia. Bull Entomol Res 90: 357-364. [ Links ]
Statsoft Inc (2001) Statistica for Windows. Tulsa, Statsoft Inc. [ Links ]
Systat Inc (2002) Table Curve 2D. Chicago, Systat Software Inc. [ Links ]
Talekar NS, Shelton AM (1993) Biology, ecology, and management of the diamondback moth. Annu Rev Entomol 38: 275-301. [ Links ]
Taylor F (1981) Ecology and evolution of physiological time in insects Am Nat 117:1-23. [ Links ]
Thuler RT, De Bortoli SA, Hoffman-Campo CB (2007) Classificação de cultivares de brássicas com relação à resistência à traça-das-crucíferas e à presença de glucosinolatos. Pesq Agropec Bras 42: 467-474. [ Links ]
Trudgill DL (1995) Why do tropical poikilothermic organisms tend to have higher threshold temperature for development than temperate ones? Funct Ecol 9: 136-137. [ Links ]
Trudgill DL, Giliomee JH (1994) Thermal tome and ecological strategies - a unifying hypothesis. Ann Appl Biol 125: 521-532. [ Links ]
Umeya K, Yamada H (1973) Threshold temperature and thermal constants for development of the diamondback moth, Plutella xylostella L., with reference to their local differences. Jpn J Appl Entomol Zool 17: 19-24. [ Links ]
Verkerk R H J, Wright D J (1996) Multitrophic interactions and management of the diamondback moth: a review. Bull Entomol Res 86: 205-216. [ Links ]
Worner S P (1992) Performance of phenological models under variable temperature regime: consequences of the Kaufmann or rate summation effect. Environ Entomol 21: 689-699. [ Links ]
Luís A Foerster
Depto de Zoologia
Univ Federal do Paraná CP 19.020
81531-990, Curitiba, PR, Brasil
Received 29 December 2010 and accepted 27 May 2011
Edited by Wesley A C Godoy - ESALQ/USP