Biology of Corythucha gossypii Fabricius, 1794 (Hemiptera: Tingidae) in Ricinus communis at different temperatures and thermal requirements

We studied the biology of Corythucha gossypii in Ricinus communis under different temperatures in climatic chambers adjusted at 20, 23, 25, and 28 °C, 60 ± 10% relative humidity, and a 12-h photoperiod. The development period and viability of eggs, the development period and survival rate of nymphs, and egg-adult cycle of C. gossypii as well as the adult longevity and fecundity were estimated. The thermal requirements (K) and temperature-base (Tb) were estimated for each of the immature stages and for the eggs-adults period. The duration of the eggs and nymphs phases and the egg-adult cycle of the C. gossypii on castor bean leaves at 20-28 °C were 7.6-17 days, 10.2-27.5 days, and 16.9-44.5 days, respectively. The lower temperature inhibited the oviposition of C. gossypii , whereas the higher temperatures were most favorable for its development. The municipalities of the Bahia state of Brumado, Irecê, Itaberaba, Jacobina, and Senhor do Bonfim were estimated to have a high potential for the population growth of C. gossypii . However, a greater number of generations per year of C. gossypii were observed in the municipalities of Brumado and Itaberaba.


Introduction
Brazil is the world's third-largest producer of castor bean (Ricinus communis L., Malpighiales: Euphorbiaceae) after China and India. The estimated castor production for 2015-2016 harvest in Brazil was 97,300 tons in 125,100-ha area, representing 52.4% growth in the national acreage as compared to the data from the previous year (CONAB, 2016). The northeast region comprises of >99% of the planted area, with a production of 96,800 tons in the 2015-2016 crop season. Among the states of this region, Bahia stands out with a production of around 95,000 tons, which accounted for over 98% of the castor oil production in Brazil (Costa et al., 2014).
Castor bean is highly adapted to the Brazilian soil and climatic conditions, especially in the semiarid region (Corrêa et al., 2006). In the northeast region, for example, planting this crop has been encouraged not only due to the low cost of implementation and production involved but also for its recognized tolerance to adverse conditions of climate and soil, such as in drought-related stress area (Severino et al., 2012). Nevertheless, the crop yield in Brazil is lower than in other countries due to the lack of information about the damages caused by species of insects and mites, which has compromised the economic exploitation of this crop (Ribeiro and Costa, 2008). Some species of Tingidae (Hemiptera, Heteroptera) have a great potential to become the major pests of this crop, among them, Corythucha gossypii (Fabricius, 1794) is notable (Varón et al., 2010).
Adults and nymphs of the lace bug C. gossypii feed on both sides of the castor bean leaves, causing injuries similar to the ones caused by other tingids. The damage is initially characterized by the formation of white punctuation that progresses to tanning, chlorosis, and, eventually, to premature dropping of the leaves (Li et al., 2007).
Temperature is a determining factor in the geographical distribution of species (Calosi et al., 2010;Kellermann et al., 2012a, b;Overgaard et al., 2014), particularly the metabolic activity and development time of insects (Damos and Savopoulou-Soultani, 2011;Pereira et al., 2011;Poncio et al., 2016). However, to understand the effect of temperature on the life cycle of insects, it is necessary to determine the base temperature and thermal constant of these arthropods Savopoulou-Soultani, 2008, 2011). Therefore, the information on the thermal requirements in the development of insect pests have important implications in the control programs of such organisms, because the temperature determines the growth and size of the pest population and its variation in different environmental conditions. Thus, the insight to this information would provide support for the prediction of population dynamics and spatial and seasonal distributions of these organisms in the main castor-producing regions of Brazil.
In this study, we evaluated the biology of the lace bug C. gossypii in castor beans under different temperatures.
The specimens of castor bean cultivar "BRS Paraguaçú" were first planted in 4-L-plastic pots filled with soil collected from the experimental field, which was classified as a mixture of entisol eutrophic and manure (3:1 ratio), as recommended by the Soils Laboratory of the Embrapa Cotton. The plants were kept in the greenhouse until 55 days of age and then transferred to the laboratory for evaluate tingids infestation.
The C. gossypii specimens used in the experiment were collected from castor bean plants attacked in the Embrapa Cotton field. A total of 30 specimens (20 females and 10 males) of the lace bugs were collected using a brush, transferred to dry glass jars, and sent to Dr. Luiz Antônio Alves Costa (National Museum of the Federal University of Rio de Janeiro in Rio de Janeiro State, Brazil) for identification. These specimens were identified based almost exclusively on external morphology, because genital traits are not usually described (Monte, 1941) and deposited at the National Museum. For each temperature condition, two leaves of a castor plant were infested with 40 C. gossypii females, which continued laying eggs for 24 h. The infested leaves were wrapped with voile to prevent the insects' escape. At the end of this period, the females were removed and their positions were marked with black paint to facilitate stereoscopic microscope inspections until the emergence of the nymphs.

Biology and thermal time bioassays
A castor bean plant containing 250 newly laid eggs inside the leaves by C. gossypii females were maintained in the biochemical oxygen demand (BOD) chambers adjusted at 20, 23, 25, and 28 °C under a relative humidity of 60 ±10% for a 12-h photoperiod. The eggs were observed daily. The total number of eggs hatched at each temperature and the duration of each egg development (incubation period) was recorded.
To evaluate the nymphal stage at each temperature, the newly emerged first-instar nymphs were kept individually in rearing units consisting of 25-mL, transparent, plastic containers (3 × 4 cm). Inside these units, a filter paper disk measuring 3.0 cm in diameter was placed and moistened with distilled water. On this disk, a disk of a castor bean leaf was placed, with the ventral side facing upward. Then, the rearing units were covered with a transparent plastic film and maintained at a given temperature until the insects emerged as adults. The castor bean leaf disks were replaced every 2 days, and the filter paper was moistened on a daily basis.
The development time and viability of eggs and the survival of nymphs and adults of C. gossypii as well as the adult longevity and fecundity were estimated. The longevity of males and females was determined by considering the couples. To determine the fertility and the sex ratio of the offspring at each temperature condition, the adults were divided into couples, and the newly emerged males were transferred separately to new arenas containing newly emerged female. The eggs laid in these areas were quantified daily by two observations made at 08:00 AM and 04:00 PM.

Data analysis
The differences in the development periods between C. gossypii males and females were compared by F test at 5% probability using the System of Statistical Analysis and Genetics (SAEG) (Ribeiro Júnior, 2001). The threshold temperature (Tb) and thermal constant (K) were estimated by the hyperbole method (Haddad et al., 1999) based on the duration of the immature stages and the life cycle (egg-adult) of C. gossypii. The annual accumulation of degree-days and the likely number of generations (NG) of the lace bug in five castor-producing municipalities of Bahia state were calculated based on the thermal constant (Wilson and Barnett, 1983). The NG was calculated using the following Equation 1: where: K = thermal constant; Tm = average temperature for each location studied; Tb = lower temperature threshold; and T = time (in days).

Results
The insect was identified as C. gossypii (Figures 1A-C).
The viability of C. gossypii eggs in castor bean leaves did not vary between the four studied temperatures (Table 1); however, the survival of the nymphal phase ranged from 26% to 60%. The maximum survival was observed at 25 °C and the minimum at 20 °C. Among the nymphal instars, the survival rates for the first, second, third, fourth, and fifth instars for the four temperatures studied were 50-82%, 75.6-100%, 76.5-89.2%, 76.9-93.8%, and 80-100%, respectively ( Table 2).
The developmental time of eggs and nymphs phases, and the egg-adult cycle of C. gossypii with castor bean leaves gradually decreased with the increase in the temperature (Table 1), but did not differ between the sexes. The incubation periods of eggs and development period of the nymphal phase and egg-adult cycle were 7.6-17 days, 10.2-27.5 days, and 16.9-44.5 days, respectively, at 20-28 °C.
The development time of the nymphal phase of C. gossypii in castor bean leaves varied within each instar stage and between the instars and sexes (  temperature. Within each instar, the duration gradually decreased with increasing temperature. On the other hand, longer periods between instars were observed for the fifth-instar nymphs and shorter periods for the second-and third-instar nymphs, except for similar amount of days for the first-and fifth-instar nymphs at 20 °C. Among the second-and third-instar nymphs at 20 °C, the nymphs that originated males showed a longer development time than those that originated females. The longevity of C. gossypii adults in castor bean leaves were 24.3-46.8 days and 21.3-42.3 days for females and males nymphs, respectively (Table 3). The greatest longevity period was observed for females nymphs at 23 °C, followed by those kept at 25 °C. The smallest longevity of C. gossypii adults was observed for those kept at 28 °C.
The fecundity of C. gossypii in castor bean leaves varied with temperature (Table 3), with a better performance demonstrated at higher temperatures. At 20 °C, the females did not lay any eggs. Similarly, the sex ratio in castor bean leaves varied with the temperature, with values of 0.57, 0.58, 0.50, and 0.38 at temperatures of 20, 23, 25, and 28 °C, respectively.
The development rate to the egg and nymph stages and the egg-adult cycle of C. gossypii with castor bean leaves   (Table 4). Within this temperature range, the second-and third-instar nymphs showed higher development rate, which could be confirmed by larger angular coefficients of the regression equations estimated for these instars. Thermal constants for the egg and nymph stages and the egg-adult cycle of C. gossypii with castor leaves showed a linear and positive correlation with the temperature of 20-28 °C ( Table 4).
The likely number of generations of C. gossypii throughout the year in the municipalities of Brumado, Irecê, Itaberaba, Jacobina, and Senhor do Bonfim (the largest castor bean producers in Brazil; Bahia state) ranged from 14.4 to 17.5 (Table 5). The municipalities of Itaberaba and Brumado, two of the hottest cities in the region, possess the greatest potential of annual generations of C. gossypii, while municipalities with cooler temperatures such as Irecê, Jacobina, and Senhor do Bonfim are predicted to yield fewer numbers of generations per year.

Discussion
The high viability rate of eggs with castor bean leaves is similar to the >90% value observed for the viability of C. ciliata eggs (Ju et al., 2011a) in the studied temperature range with hybrid plane leaves of Platanus × acerifolia (Aiton). This observation can be attributed to C. ciliate's oviposition behavior. The females often lay their eggs on both the sides of the leaf and next to the midvein or lateral veins, inserted partially in the leaf parenchyma; this site of oviposition protects the eggs from abiotic stress factors such as water loss and extreme temperatures and biotic ones such as attack by natural enemies (Southwood, 1973).
The shorter incubation period of C. gossypii eggs at temperature between 20 °C and 28 °C as compared to those of 12-19 days by C. cydoniae on leaves of Crataegus phaenopyrum (L.f.) Medik. (Neal Junior and Douglass, 1990), 11.3-26.5 days by C. cydoniae on leaves of Cotoneaster dammeri (Braman and Pendley, 1993), and 8.8-20 days by C. ciliata on hybrid plane leaves (Ju et al., 2011b) can be attributed to differences among the oviposition sites in the plant tissue of the host leaves. The oviposition of C. gossypii is endophytic, while those of C. cydoniae and C. ciliata are pseudo-endophytic and exophytic, respectively. In the endophytic posture, the eggs are inserted into the spongy mesophyll with only the operculum left outside the vegetable tissue, while, in the pseudo-endophytic posture, the eggs are partially inserted in the plant tissue. In the exophytic posture, the eggs are deposited on the surface of the plant tissue (Guidoti et al., 2015).
The differences in the development time of the second-and third-instar nymphs of C. gossypii at 20 °C that originated males and females may be attributed to the reduced number of individuals used to calculate this development period of this lace bug at this temperature. However, the development time of the phases of egg, nymph, and egg-adult did not differ between the sexes at all temperatures, indicating that nymphs at a more advanced instar stage of development can compensate for the possible differences between the sexes in the development time Table 4. Linear regression equations between the rates of development r(T) and temperature (20 °C, 23 °C, 25 °C and 28 °C) to determine the base temperature (Tb) and thermal constant (K) for egg and nymph stages and egg-adult cycle of development of Corytucha gossypii in castor leaves.

Phase
Instar Tb (°C) K a (1) ± standard error b (2) ± standard error (1) The base temperature or low development threshold (Tb) is calculated as Tb =2a/b; (2) The thermal constant, k (day-degrees) is calculated as k = 1/b.a is the intercept, and b is the regression line slope. The values of Tb and k were calculated for each instar and nymph stage (from hatching to the adult stage).  (Braman and Pendley, 1993), respectively, and of 11.3-27.6 days and 20.0-47.6 days for the same development period of C. ciliata on the hybrid plane leaves (19-30 °C) (Ju et al., 2011a). Moreover, the durations were greater, ranging from 14.7 to 23.4 days and 26.6 to 42.5 days for the nymph stage and the egg-adult cycle of C. cydoniae on the leaves of Crataegus phaenopyrum (Neal Junior and Douglass, 1990). The survival rates for the first-, second-, third-, fourth-, and fifth-instars for the four temperatures studied were less than those in survival from 63% to 90%, 95% to 100%, 96% to 99%, 96% to 97.5%, and 85% to 95% observed for the respective instars of C. ciliata on hybrid plane leaves (19-30 °C). On the other hand, the improved survival of C. gossypii at 25 °C and its reduction at 20 °C indicates that these nymph species preferably survive in warmer temperatures.
Variations in the development time of C. gossypii within each instar and between instars and sexes according to the temperature confirm that temperature is an important climatic factor that influences the development of these insects. The developmental period gradually decreases with increasing temperature conditions. On the other hand, the longest period observed for the fifth-instar nymphs and shortest for the second-and third-instar nymphs, except for similar durations for the first-and fifth-instar nymphs at 20 °C, are in concordance with the previous results observed for other species of Tingidae (Vogt and McPherson, 1986;Douglass, 1988, 1990;Braman et al., 1992;Braman and Pendley, 1993;Cividanes et al., 2004;Silva, 2004;Aysal and Kivan, 2008;Ju et al., 2011a;Zhang et al., 2011;Carr and Braman, 2012;Moreira et al., 2013;Sánchez-Ramos et al., 2015), thereby confirming this to be the pattern of development for the nymphal stages of lace bugs, as proposed by Sanchez-Ramos et al. (2015).
In this study, adult longevity and fecundity were prolonged and increased with decreasing temperature. At 25 °C, the life spans of the male and female C. gossypii were found to be similar to the life spans of 33.2 days and 34.7 days for the male and female C. ciliate, respectively, on hybrid plane leaves at 26 °C (Ju et al., 2011a).
The positive linear correlation between the development rate and the temperature and between the thermal constant and the temperature for the egg, nymph, and egg-adult stages of C. gossypii at 20-28 °C indicated the thermophilic nature of Tingidae species. The number of degree-days required for the development of egg and nymph stages and the egg-adult cycle were similar to those observed for the Tingidae species Monosteira unicostata on the leaves of Phyllostachys nigra (Sánchez-Ramos et al., 2015) to those observed for Gargaphia torresi on cotton leaves (Silva, 2004) and for C. cydoniae on the leaves of Cotoneaster dammeri (Braman and Pendley, 1993). On the other hand, the number of degree-days required for the three developmental stages were superior to the lower limits of 10.5, 10.9, and 11.2 °C obtained for the respective stages of C. ciliata (Ju et al., 2011a).
The largest number of annual generations estimated for C. gossypii in the warm municipalities of Itaberaba and Brumado as compared to those in the colder municipalities of Irecê, Jacobina, and Senhor do Bonfim indicate that the municipalities of Itaberaba and Brumado are most susceptible to population outbreaks and, consequently, to damage caused by castor bean lace bug.

Conclusion
From this study, it can be concluded that temperature influences the development time of the egg and nymph stages and the egg-adult cycle as well as the longevity and fecundity of C. gossypii on the leaves of castor beans. The temperatures of 25 °C and 28 °C were found to be the most favorable for the development of this lace bug. The study indicated that the municipalities of the Bahia state of Brumado, Irecê, Itaberaba, Jacobina, and Senhor do Bonfim have a greater potential for the population growth of C. gossypii. However, the greater number of generations per year of C. gossypii observed in Brumado and Itaberaba indicated that C. gossypii has more potential to be a pest in these municipalities.