Abstract
Riptortus pedestris (Fabricius) (Hemiptera: Alydidae) is an economically important insect pest of soybean. We investigated the developmental periods of each life stage as well as adult longevity and female fecundity. The study was conducted at eleven constant temperatures (12.0, 14.0, 15.9, 17.3, 19.3, 23.6, 28.3, 31.2, 34.2, 35.1, and 36.1 °C) for temperature-dependent development, and six constant temperatures (15.8, 19.7, 24.0, 27.8, 32.6, and 35.5 °C) for adult longevity and oviposition. Riptortus pedestris females showed successful egg-to-adult development from 17.9 to 36.1 °C, but failed to complete development under 15.9 °C. Using linear regression, lower developmental threshold (LDT) and thermal constant (K) for the total immature stage were estimated as 14.1 °C and 336.7°-day (DD), respectively. Higher and lower temperature threshold (TH and TL, respectively) were calculated using Lobry–Rosso–Flandrois (LRF) and Sharpe–Schoolfield–Ikemoto (SSI) models; a wider TL-to-TH temperature range (31.4 °C) was observed for LRF than for SSI (18.6 °C). The adult emergence frequency over the full range of constant temperatures was simulated using nonlinear developmental rate functions and the Weibull function. The daily egg production was predicted with respect to temperature and adult age. Biological characteristics of R. pedestris from different local populations are discussed.
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Introduction
Riptortus pedestris (Fabricius) (Hemiptera: Alydidae) is one of the important pests in Asian countries including Korea, Japan, and India (Kono 1989; Leal et al. 1995; Lim 2013; Son et al. 2000; Visalakshi et al. 1976; Wada et al. 2006). Both adults and nymphs of R. pedestris feed on leguminous plants such as Chinese milk vetch (Astragalus sinicus L.), cowpea [Vigna unguiculata (L.)], hairy vetch (Vicia villosa Roth), kidney bean (Phaseolus vulgaris L.), mung bean (Vigna. radiata L.), red clover (Trifolium pretense L.), sesame (Sesamum indicum L.), and soybean (Glycine max L.), as well as fruit trees such as apples (Malus pumila Miller) and sweet persimmon (Diospyros kaki L.f.) (Bae et al. 2009; Chung et al. 1995; Kimura et al. 2008; Kono 1989; Mainali and Lim 2012; Seo et al. 2011; Son et al. 2000). They directly damage the soybean pod and seed by piercing and sucking, in addition to transmitting microorganisms to soybean, resulting in serious economic losses (Jung et al. 2005, 2010; Kimura et al. 2008; Kono 1989). The damage caused by R. pedestris was severe from middle pod-elongation to earlier seed-thickening of soybean. Specially, when the pod stage of soybean was injured by R. pedestris, the empty pods and undeveloped seeds were increased. The economic loss of soybean yield depended on the life stage and density of R. pedestris and the timing of their feeding (Jung et al. 2005; Kono 1989; Suzuki et al. 1991).
Life table analysis is an important tool for understanding and analyzing the biological process of insects, for studying population growth, and for establishing management programs. Life table studies describe the survival, reproduction, and rate of increase of a population (Birch 1948; Goodman 1982; Maia et al. 2000; Sánchez-Ramos et al. 2017). Although Rahman and Lim (2017) created a fertility life table for R. pedestris on a limited food resource, they did not assess the effects of temperature on the life table parameters for R. pedestris. Temperature is one of the main abiotic factors affecting development, growth, reproduction, and survival of insects and mites (Park et al. 2017; Ramalho et al. 2015; Sugawara et al. 2017). The previous studies have often overlooked the effect of the lower and higher temperature range on the development of R. pedestris (Bae et al. 2005; Kidokoro 1978; Kim et al. 2009; Kono 1989; Lee et al. 1997). Although Kim et al. (2009) developed temperature-dependent development and oviposition models for R. pedestris, they emphasized more on the goodness-of-fit and simplicity of models rather than the biological interpretation of models. The main objective of this study was to investigate the effects of temperature on the development and reproduction of R. pedestris, to construct temperature-dependent development and oviposition models for the species and to analyze a fertility life table for R. pedestris.
Materials and methods
Insect colony
Riptortus pedestris (about 200) were obtained from the National Institute of Agricultural Sciences (NIAS), Wanju-gun, Republic of Korea, in 2016. Colonies of R. pedestris were maintained in acrylic cages (30 cm × 30 cm × 35 cm) with one door and two meshed screens in the lateral sides for ventilation at 25 ± 1 °C, 60 ± 10% relative humidity and 16:8 h light:dark photoperiod. Dry soybean seeds and water were supplied as food sources. Three pieces of gauze (10 cm × 4.5 cm) were placed at the bottom of each cage as oviposition sites. Riptortus pedestris, which were captured seasonally in the field of Jeju, were added about 100 adults (we did not identify the sex) in the cage for mass rearing three times (spring, summer, and fall seasons) per year, to avoid inbreeding depression.
Experimental procedure for egg-to-adult development
New eggs (< 24 h old) on the gauze were randomly selected from the insect-rearing system and placed in Petri dishes (10.0 cm diameter and 4.0 cm height, with a 4.0 cm-diameter air hole on the lid covered with 0.05 mm mesh, SPL, Pocheon, Korea) with cotton soaked with water for maintaining humidity. When the eggs hatched, the first instar nymphs were randomly selected with a brush and placed individually in Petri dishes (5.0 cm diameter and 1.5 cm height with a 1.3 cm-diameter air hole on the lid covered with 0.05 mm mesh). Each dish was first filled with cotton soaked with water and three dried soybean seeds. The dried soybean seeds were placed in a small plastic band, so that seeds do not roll over in the Petri dishes. Soybean seeds and water were supplied as a food source for the nymphs.
The developmental periods of R. pedestris stages from egg-to-adult emergence were studied at temperatures of 12.0, 14.0, 15.9, 17.3, 19.3, 23.6, 28.3, 31.2, 34.2, 35.1, and 36.1 °C. The temperature inside the cages was very similar to that of the chamber (WTH-305, Daihan Scientific, Co. Ltd, Seoul, Korea). Sample sizes were greater than 200 eggs per treatment. Observations were made visually at 24 h intervals to distinguish between the nymph instars, which were identified using the exuviae. The eggs were allowed to complete development until adults within the Petri dishes, and the developmental time for each life stage was recorded. Dried soybean seeds were replaced with new ones whenever needed.
Experimental procedure for adult longevity and fecundity
To obtain newly emerged female and male adults (< 24 h old), fifth instar nymphs were chosen from the mass rearing system and transferred into acrylic cages (30 cm × 30 cm × 35 cm). The new female adults were paired with new males and placed in Petri dishes (10.0 cm diameter and 4.0 cm height, with a 4.0 cm-diameter air hole on the lid covered with 0.05 mm mesh). A given pair of R. pedestris adults was maintained in the same Petri dish. We replaced the female or male if they died within 1 week. The fecundity and longevity of R. pedestris individuals were studied at temperatures of 15.8, 19.7, 24.0, 27.8, 32.6, and 35.5 °C. We followed the same procedure as the developmental time experiment. Rolled pieces of gauze (10 cm × 4.5 cm) were placed in the bottom of each Petri dish as oviposition substrate. The longevity and fecundity of R. pedestris were examined and recorded at 24 h intervals using visual observation. To assess the daily fecundity and hatchability, eggs laid by the female were removed from the containers daily, and it was observed whether they hatch or not.
Data analysis
Developmental time, longevity, and fecundity data for R. pedestris were analyzed using the PROC GLM in SAS (SAS Institute 2002). Statistical differences in development periods, longevity, and fecundity across the tested temperatures were determined using the Tukey’s studentized range test (p < 0.05). The data for hatchability were normalized by arcsine–square-root transformation and were then analyzed using Tukey’s test. The parameters for the linear and nonlinear functions were estimated using least-square method in TableCurve 2D (Jandel Scientific 1996) or R-statistics (version 3.2.2; R Core Team 2015).
Analysis of developmental data
The relationship between temperature and developmental rates (1/developmental periods) was analyzed using linear and nonlinear functions. The lower developmental threshold \(\left( {{\text{LDT,}} - \frac{b}{a}} \right)\) and thermal constant \(\left( {{\text{K}}, \frac{1}{a} } \right)\) were estimated by linear function (y = aT + b: where y = developmental rate and T = temperature tested) (Campbell et al. 1974).
Many researchers have suggested and evaluated nonlinear equations that explain the relationship between developmental rates and temperature (Kim et al. 2017; Kontodimas et al. 2004; Mirhosseini et al. 2017; Ratkowsky and Reddy 2017; Roy et al. 2002; Shi et al. 2016, 2017). We selected two nonlinear equations, the Lobry–Rosso–Flandrois (LRF) model and the Sharpe–Schoolfield–Ikemoto (SSI) model, based on the evaluation by Ratkowsky and Reddy (2017) and Shi et al. (2017):
Equation (1) is the LRF model (Lobry et al. 1991; Ratkowsky and Reddy 2017; Rosso et al.1993). The LRF model has been generally considered in food microbiology and not previously well applied in population entomology before introducing by Ratkowsky and Reddy (2017). The model was developed by Lobry and colleagues and which has the important features that all parameters of the model have biological meaning. In this model, r(T) is the developmental rate (1/developmental time) at different temperatures (°K), T is the absolute temperature (K), μopt is the development rate at the optimum temperature, Tmax is the temperature above which no development occurs, Tmin is the temperature below which development is no longer observed, and Topt the optimal temperature for development:
Equation (2) is the SSI model (Ikemoto 2005; Schoolfield et al. 1981; Sharpe and DeMichele 1977). The SSI model based on thermodynamics was proposed by Sharpe and DeMichele (1977) and modified by Schoolfield et al. (1981) and Ikemoto (2008). The model has been developed to describe temperature-dependent reaction rates of a theoretical rate-controlling enzyme that is in its active temperature ranges. Parameters of the SSI model were estimated using an R script, which improved the fitting method of parameter estimates, developed by Shi et al. (2017). In this model, r(T) represents the developmental rate at absolute temperature T (°K), \(\Delta HA\), \(\Delta HL\), and \(\Delta HH\) are enthalpy changes (Jmol−1), R is the universal gas constant, \(\rho_{\phi }\) is the developmental rate at \(T_{\phi }\), TL and TH are temperatures at which the rate-controlling enzyme has equal probability to be active or inactive by low- or high-temperature inactivation, respectively, and \(T_{\phi }\) is the intrinsic optimum temperature. \(T_{\phi }\) is the optimal temperature at which the species can optimize its fitness to the environment (Sharpe and DeMichele 1977):
Equation (3) is the probability that the rate-controlling enzyme is in the active state. The maximum probability of \(P_{2} \left( T \right)\) is observed at \(T_{\phi }\).
The relationship between the cumulative proportion of adult emergence and normalized developmental times (developmental time/mean developmental period) was estimated using the three-parameter Weibull function (Wagner et al. 1984; Weibull 1951). The parameters for the Weibull function were estimated using least-square method:
where F(t) is the cumulative frequency at normalized time t, and \(\gamma\), \(\eta\), and \(\beta\) are the parameters of the Weibull function.
The emergence proportion of R. pedestris adults was simulated with respect to constant temperature (°C) and time (day) by combining the two nonlinear functions and Weibull function:
where F(x, T) is the emergence frequency of R. pedestris adults at time x and constant temperature T(°C), x is time (day), r(T) is the developmental rate from selected model, and \(\gamma\), \(\eta\), and \(\beta\) are parameters from the Weibull equation. The results of F(x, T) were estimated by subtracting the simulation result at time xt from the result at time xt+1.
Oviposition model structure and life table parameters
The oviposition model of R. pedestris was constructed using temperature-dependent adult aging rate, the age-specific survival rate, age-specific cumulative oviposition rate, and temperature-dependent total fecundity. The relationship between the temperatures and adult aging rates (1/longevity) was described by the Lactin model (Eq. 6) (Lactin et al. 1995):
where r(T) represents the aging rate at temperature T (°C), \(\rho\) is a constant that defines the rate of optimal temperature, TM is the higher threshold, and \(\Delta T\) is the temperature window for inducing physiological action of insect adult aging.
The age-specific survival rate of R. pedestris was fitted with a Weibull frequency distribution (Pinder et al. 1978):
where S(t) is the proportion of living females at a normalized time t, t is the normalized time (age of each adult female/average longevity of tested female), and a and b are parameters. Age-specific cumulative oviposition rate was analyzed using the three-parameter Weibull function (Eq. 4). The relationship between the mean total fecundity per female and temperatures was estimated by the equation proposed by Briere et al. (1999):
where f(T) is the number of total eggs laid by one female at each temperature (°C), T and TM are terms from the Lactin model. TL is the lower developmental threshold, and c and m are empirical constants of the equation.
The number of eggs produced by a cohort of females was estimated between ti (i.e., normalized age at ith day) and ti+1 using the equation (Kim and Lee 2003):
where f(T) and S(t) are already defined above and F(t) is the cumulative oviposition proportion of living females at a normalized time t.
The parameters of fertility life table for R. pedestris, including net reproductive rate (RO), mean generation time (T), doubling time (DT), finite rate of increase (λ), and intrinsic rate of natural increase (rm), were estimated using methods proposed by Maia et al. (2000). The statistical differences in life table parameters across the tested temperatures were determined using the two-tailed t test.
Results
Riptortus pedestris developed successfully from the egg to the adult stage in the range of 17.9–36.1 °C (Table 1). The eggs could not hatch at 12.0 and 14.0 °C, and nymphs could not develop into adult stage under 15.9 °C. The developmental periods of each life stage and total immature period were significantly influenced by temperatures (i.e., combined: Egg F8, 2204 = 24655.40, p < 0.0001, first nymph stage F8, 1877 = 1688.40, p < 0.0001, second nymph stage F8, 1631 = 1962.74, p < 0.0001, third nymph stage F8, 1532 = 1877.59, p < 0.0001, fourth nymph stage F7, 1461 = 2705.14, p < 0.0001, fifth nymph stage F7, 1428 = 1960.42, p < 0.0001, total nymph stage F7,1336 = 16804.70, p < 0.0001, and total immature stage F8, 1336 = 26840.50, p < 0.0001). The time required to complete development decreased when the temperature increased from 17.9 to 34.2 °C. The mean developmental time for egg-to-adult emergence ranged from 81.7 days at 17.9 °C to 16.9 days at 34.2 °C. The lower developmental threshold (LDT) and thermal constant (K) for each life stage of R. pedestris were obtained by the linear regression analysis. LDT values of egg, first, second, third, fourth, and fifth nymph stages were 13.2, 13.5, 13.2, 14.4, 14.8, and 14.6 °C, respectively. K values of egg, first, second, third, fourth, and fifth nymph stage were 104.7, 31.6, 51.2, 41.5, 45.0, and 70.6 DD, respectively. LDT and K of total immature period were 14.2 °C and 336.7 DD.
The estimated parameters of two nonlinear functions are presented in Table 2. The temperature-dependent development for total immature period was described by two functions, and the curve performance of two models was right-skewed bell-shape (Fig. 1a). The maximum developmental rate was observed at 37.1 and 36.8 °C from the LRF and SSI models, respectively. The three critical temperature thresholds of rate-controlling enzyme for R. pedestris total immature stage were estimated using the SSI model (Fig. 1b). The intrinsic optimum temperatures of the control enzyme for egg, first, second, third, fourth, fifth, and total immature period were 24.1, 33.5, 32.5, 26.0, 33.3, 33.4, and 32.6 °C, respectively. The temperature window for the development of R. pedestris could be approximated from TL to TH. The temperature range for the nymph stages was 29.8–33.1 and 17.0–20.6 °C based on the LRF and SSI models, respectively.
The cumulative proportion of development completion for R. pedestris total immature stage was analyzed using a three-parameter Weibull distribution function (Fig. 1c) (\(\gamma\) = 0.7071, \(\eta\) = 0.2893, \(\beta\) = 6.7314, F2, 62 = 1393.73, p < 0.0001, r2 = 0.98). Adult emergence proportion for R. pedestris over the full range of constant temperature was obtained using the two nonlinear models and the development completion process. The results of the simulation were assessed by two nonlinear models (Fig. 2).
Riptortus pedestris adults survived at all the tested temperatures. The longevity of R. pedestris females decreased with increasing temperature (Table 3). The longevity of R. pedestris males was longer than that of females at different temperatures (sex F1, 304 = 42.88, p < 0.0001, temperature F5, 304 = 32.45, p < 0.0001, and interaction effect of sex and temperature F1, 304 = 8.93, p < 0.0001). The fecundity (total egg production/female) increased with increasing temperature until 24.0 °C. Fecundity and hatchability were significantly affected by the temperature (total egg per female: F4, 125 = 10.91, p < 0.0001; hatchability: F4, 125 = 32.83, p < 0.0001). Riptortus pedestris female did not oviposit at 15.8 °C.
The relationship between adult aging rate and temperature was analyzed using the Lactin model (Fig. 3a and Table 4). Three important components of the oviposition model of R. pedestris are shown in Fig. 3 and Table 4. Each component was described well by the selected models. The estimated maximum number of eggs produced per female was 186.0 eggs at 25.2 °C. The estimated egg production per day in relation to adult age and temperature is presented in Fig. 4. Age-specific female survival and daily fecundity are presented in Fig. 5. The survival curve presents a sharp decline after 28 days at 19.7 °C, after 49 days at 24.0 °C, after 13 days at 27.8 °C, and after 10 days at 32.6 and 35.5 °C. The daily fecundity declined gradually after peaking.
The estimated values of life table parameters for R. pedestris are presented in Table 5. The net reproductive rate was similar at 24.0 and 27.8 °C. The mean generation time decreased with increasing temperature up to 32.6 °C. The finite rate of increase (λ = 1.12) and intrinsic rate of increase (\(r_{m}\) = 0.11) were the highest at 32.6 °C.
Discussion
We investigated a wide range of temperatures for R. pedestris development and reproduction, determined the developmental times and fecundity, estimated important parameters for understanding biological processes using linear and nonlinear functions, and calculated the life table parameters of R. pedestris. Temperature affects the developmental time of R. pedestris as in other insect pests, such as Acrosternum hilare (Say), Aphis glycines (Matsumura), Halyomorpha halys (Stål), and Megacopta cribraria (Fabricius) in soybean fields (Baek et al. 2017; Hirano et al. 1996; Nielsen et al. 2008; Shi et al. 2014; Simmons and Yeargan 1988). The developmental periods of R. pedestris for each life stage decreased as the temperature increased up to 34.2 °C (Table 1). These results disagree with those reported by Kim et al. (2009) for R. pedestris, who found that the developmental times for each life stage except the second instar nymph stage decreased continuously from 19.7 to 36.7 °C. Riptortus pedestris nymphs could not develop into adult stage under 15.9 °C in this study. This result was similar to those reported by Kidokoro (1978) (17 °C) and Lee et al. (1997) (15 °C). The developmental periods for each life stage from this study were shorter than those reported by Kidokoro (1978), Lee et al. (1997), Bae et al. (2005), and Kim et al. (2009). It is inferred that the difference among developmental times is attributable to the food source or variety consumed, source of the insect population, and environmental conditions before the experiment.
In contrast to our study, Bae et al. (2005) reported lower LDTs for different nymph stages (8.7–12.7 °C) and total immature stage (10.0 °C) than our results (13.2–14.8 °C, 14.2 °C, respectively). However, Kim et al. (2009) reported higher values (14.5–15.8 °C) than the results of this study. The thermal constant of the total immature period in our study (336.7 DD) was lower than those reported by Kidokoro (1978) (385.0 DD) and Lee et al. (1997) (429.2 DD), and higher than those reported by Kono (1989) (326.8 DD) and Kim et al. (2009) (312.5 DD). These differences may be related to the differences in experimental conditions such as the nutrient of food resources, the origin of populations, and measurement of temperature.
The developmental rate of R. pedestris was well fitted by two nonlinear models, which were then used to calculate the developmental thresholds. In our study, the least-squares estimators are 0.96–0.99 and the estimated parameters presented the minimum variance. The models explained well the pooled development rates throughout the biokinetic temperature ranges tested. In contrast to the LRF model, SSI model has clear biophysical meanings and gives thermodynamic information among model parameters. The intrinsic optimum temperature values in our study (32.6 °C) and that by Kidokoro (32.1 °C) using the SSI model were similar, and differed from those of Kim et al. (2009) (27.3 °C) and Bae et al. (2005) (26.9 °C). The temperature ranges for insect development were estimated from TL to TH using the SSI model (van der Have 2002; Dixon et al. 2009). The ranges were 18.3, 18.6, 19.9, and 20.9 for the present study, Kidokoro (1978), Bae et al. (2005), and Kim et al. (2009), respectively. The activation states of the rate-controlling enzyme from our study and Kidokoro (1978) were similar compared with other results. It can be inferred that the thermal tolerance for immature development of R. pedestris from our study and Kidokoro is similar compared with the other results.
This study presents substantial evidence that temperature has a significant effect on the longevity and fecundity of R. pedestris adults and that the provided models constitute a crucial step towards establishment of population dynamic model. The longest pre-oviposition, oviposition periods, and total longevity for R. pedestris were at 19.7 °C and no significant differences were found in the range from 27.8 to 35.5 °C. The female longevity values in our study were shorter than those of male longevity. The difference in longevity between females and males has also been reported in Corythucha cydoniae (Fitch) (Neal and Douglass 1990) and Monosteira unicostata (Mulsant & Rey) (Sánchez-Ramos et al. 2017). It could be attributed to the oviposition behaviors of females, who invest substantial resources and energy to produce eggs and search for oviposition sites (Gibbs et al. 2010; Jervis et al. 2008).
The reproductive capacity of R. pedestris increased up to 24.0 °C and gradually decreased at higher temperatures. High fecundity was observed at 24.0 and 27.8 °C, with 196.6 and 154.3 eggs/female produced, respectively. Therefore, the optimum temperature for reproduction is likely between 24.0 and 27.8 °C. Kim et al. (2009) found relatively higher values of fecundity from 22.0 to 31.0 °C (353.2–369.2 eggs/female), whereas Bae et al. (2005) reported lower values from 20.0 to 32.0 °C (21.1–67.0 eggs/female). The number of eggs produced in our study was lower than that reported by Kim et al. (2009), and higher than that presented by Bae et al. (2005). In our study, the egg production was the lowest at the highest temperature (35.5 °C). Bae et al. (2005) and Kim et al. (2009) found a low reproductive capacity for R. pedestris when the females were reared at 20.0 and 34.0 °C, respectively. The estimated temperature for maximum reproductive capacity from our study and Kim et al. (2009) was similar at around 25 °C, but the estimated number of eggs reported by Kim et al. (2009) (453.8) was higher in comparison with our study (186.0). Nitrogen quality and the quantity of soybeans consumed may be responsible for the observed variation in fecundity across studies (Barnes et al. 2008).
We found that the intrinsic rate of increase (rm) was three-fold higher when the temperature was increased from 19.7 to 32.6 °C. At 35.5 °C, the rm value was negative. It means that the population growth of R. pedestris would decrease when they are exposed to this temperature. The results (0.22 and 0.23) of Rahman and Lim (2017) were higher than those from our study. The highest net reproductive rates (Ro) were observed at 24.0 and 27.8 °C in this study. The mean generation time (T) decreased with increasing temperature up to 32.6 °C.
In conclusion, our results provide valuable information about the biological traits of R. pedestris at various temperatures compared to the previous study—development time of male and female nymphs, longevity of female and male, and life table analysis, in addition to the estimated parameters of temperature-dependent development and oviposition models. We present the simulated temperature-dependent adult emergence frequency and oviposition density curves of R. pedestris. They could serve as a basis to improve management programs directed at controlling R. pedestris in crop plant systems.
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Acknowledgements
We thank for Kwon Soo Kang and Gun Hee Kwon for their enthusiastic help. We are grateful to anonymous reviewers for valuable criticisms and suggestions on the manuscript. This research was supported by the research program of National Institute of Horticultural and Herbal Science (PJ012060), and Rural Development Administration.
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Ahn, J.J., Choi, K.S. & Koh, S. Effects of temperature on the development, fecundity, and life table parameters of Riptortus pedestris (Hemiptera: Alydidae). Appl Entomol Zool 54, 63–74 (2019). https://doi.org/10.1007/s13355-018-0593-5
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DOI: https://doi.org/10.1007/s13355-018-0593-5