1. Introduction
The fall armyworm (FAW)
Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) is native to the tropical regions of the western hemisphere (Brazil and Argentina) to the southern United States [
1]. This species is polyphagous, feeding on more than 350 plants belonging to 76 plant families, including several economically important crops such as maize, rice, and sorghum and various weeds [
2]. Recently, the FAW has rapidly invaded Africa and Asia, thereby crucially threatening crop production and food security [
1,
3,
4]. FAW invasion could be attributed to its strong long-distance flight capability, fecundity, and quick adaptability, further modulated by the prevailing meteorological conditions [
5,
6].
Considering the increasing significance of the FAW as an agricultural pest, it is crucial to understand the factors that affect its fitness and ecology for developing management measures. Temperature is a key abiotic factor in insect growth and development in the environment [
7]. Ntiri et al.’s [
8] findings suggest that temperature affects resource utilization and intraspecific and interspecific interactions and influences the geographic distribution of ectothermic organisms such as insects [
8]. Knowledge regarding the effect of temperature on insect development is critical for modeling their development under environmental conditions.
Mathematical models can be used to evaluate the development rate of an insect pest in response to variations in temperature [
9]. A nonlinear curve simulates a lower thermal threshold (T
L), optimum temperature (T
opt), and upper thermal threshold (T
H) [
10]. This curve best describes the effect of temperature on the development duration of insects. In this curve, the development rates increase above the lower thermal threshold (T
L) until they reach the optimum temperature (T
opt) and then decline to zero at the upper thermal threshold (T
H) [
10]. Because only the highest development rate is attained at T
opt, certain more elaborated mathematical models also consider parameters that predict the intrinsic optimum temperature [
11]. Considering that thermal thresholds can differ among insect species throughout their life cycle, it is essential to select a model that best describes the effect of temperature on the development rate to understand how the insect responds to temperature changes [
12].
Based on the best-fit model selection, insect development in environmental conditions can be simulated using temperature time series data [
13]. Insect pest control measures can be more successful in some life stages than in others. Hence, inappropriate planning in implementing control measures may lead to failures in pest control [
14]. Implementing pest control measures at the ideal time can be cost- and time-effective in the use of pesticides and can thus increase the income for farmers and reduce environmental contamination [
15]. Prior planning in implementing the pest control measures approach has been used effectively against various agricultural pests [
14,
16,
17].
Implementing pest control measures depends on mathematical models that reliably predict the development of a pest in environmental conditions. Therefore, models may be used to simulate the phenology of insects, enabling us to set the time of control measures that mimic the presence of vulnerable stages of the pest in the field [
18]. Previous studies have investigated the effect of temperature on the development of
S. frugiperda [
19,
20,
21,
22]. However, those studies estimated the temperature thresholds of
S. frugiperda using linear regression despite the known nonlinear response of ectotherms to temperature. Moreover, few studies on nonlinear models of
S. frugiperda have either used a single model or focused on environmental parameters other than temperature [
23,
24,
25]. Since its global invasion, the FAW has become a major pest of several crops. Moreover, the effect of temperature on its development has been insufficiently investigated, particularly with respect to the selection of mathematical models for describing this relationship. Therefore, this study aimed to investigate the effect of temperature on the fitness (survival, development time, and growth rate) of the FAW and select mathematical models that describe its development rate.
4. Discussion
To achieve a better understanding of the phenological change that insect populations go through, it is important to have a clear understanding of how abiotic elements, such as temperature, affect their development rate [
47]. This information is especially crucial for invasive species that are expanding their distribution range in invaded areas, such as the FAW. Therefore, understanding the determinants influencing FAW population dynamics is critical for integrated pest management. In this regard, this study could significantly contribute toward understanding the effect of temperature on the development of the FAW.
Our findings demonstrated that temperature significantly affected the development duration and survival rate of the FAW. The effect was observed when the response was compared between individuals at extreme temperatures in this study. For instance, a difference of 27 days was found in the mean development duration between individuals reared at 20 °C and 34 °C. Furthermore, a significant difference in pupal weight was observed between 20 °C and 34 °C, and a lower larval survival rate was observed at 15 °C, 32 °C, and 34 °C. Previous studies have reported similar differences in the development duration of the FAW at different temperatures, wherein lower survival rates of larvae were recorded at high temperatures [
21,
34]. Interestingly, the number of larval instars (7th instar larvae) increased at 15 °C and 20 °C, which are the lower temperatures at which development was studied, suggesting the biological plasticity of the FAW to survive under adverse conditions [
21,
29].
Based on biological characteristics such as development time, survival, and pupal weight, our findings imply that the T
opt for the FAW is between 28 °C and 30 °C. Our results are consistent with those of previous studies that reported that the most favorable temperature range for FAW development, survival, and reproduction was 27–30 °C [
21,
22].
Understanding the temperature thresholds of insects is crucial for predicting their potential distribution [
48]. In this study, the lower threshold temperature for the development of the egg was estimated at 15.92 °C, which was in the range (15.6–18.3 °C) reported by Barfield et al. [
49] but was higher than the threshold temperature of 12.1 °C reported by Prasad et al. [
21], 13.01 °C reported by Du Plessis et al. [
22], and 12.69 °C reported by Ali et al. [
34]. Knowledge regarding the thermal requirements of an insect can help interpret its current geographical distribution and predict its future distribution [
50]. Each developmental stage has specific temperature requirements for survival and development in a particular environment [
48]. This study demonstrated that the DD requirements for the larvae and pupae of FAW were 193.80 and 124.70, respectively, which were lower than those (204 and 150, respectively) reported by Du Plessis et al. [
22]. According to Ali et al. [
34], these differences in DD may be attributed to the different larval diets used in the two investigations.
The recent invasion in continents with diverse climatic conditions, such as Asia and sub-Saharan Africa, indicates that the FAW is regularly facing temperatures that are probably outside the linear range of the relationship between temperature and development rate [
1,
3]. Therefore, linear models become unrealistic to predict the temperature-dependent development rate, which may then necessitate the use of nonlinear models to estimate the development rate of the FAW. In this study, the nonlinear models demonstrated significant variability in their ability to characterize the correlation between temperature and
S. frugiperda growth rate. In this particular investigation, the level of “goodness-of-fit” was considered alongside the accuracy of the projected thermal thresholds to select the most effective models. The best-fit model in this investigation generated valid estimations of thermal thresholds. The multiple criteria selection method showed that among the seven models assessed, Shi and Taylor can be used to describe the temperature-dependent development of the FAW. Based on the accuracy of the thermal threshold estimation, Shi was considered the best model because it fitted well in all developmental stages. Previous studies have also demonstrated that the Shi model can accurately describe the relationship between temperature and development rate in other lepidopteran species [
9,
44,
51].
We observed differences in the predicted thermal thresholds between the models as well as between the developmental stages. For instance, the TL estimated by the Shi model for the larval stage was 12.78 °C, compared with 8.83 °C and 9.94 °C estimated by the Taylor and Briere-2 models, respectively. For the egg-to-adult life cycle, a difference of 3.1 °C was observed between the TL estimated using the Shi and Taylor models. Interestingly, linear regression estimated a TL value similar to those estimated via the Shi and Briere-1 models but higher than that estimated via the Taylor and Briere-2 models for the larval stage.
The best-fit model obtained in this study can be used in integrated pest management to set a good time to implement management measures. Previously, the same method was used in the management of the oriental fruit moth
Grapholita molesta (Busck, 1916) (Lepidoptera: Tortricidae) in orchards in North Carolina, the U.S.A. The method contributed to a decrease in pesticide use and decreased the contamination of the environment [
52]. Similarly, the findings of this study can be applied to simulate FAW development in the field and provide information on efficient and effective methods for applying control measures. The best-fit model can be used to determine the ideal time to implement control measures as well as assess the effects of climate change on pest voltinism [
53]. For example, in a study by Santos et al. [
53], the nonlinear model (Lactin-2) predicted a higher number of generations in warmer regions than in colder regions for the small tomato borer
Neoleucinodes elegantalis (Guenée, 1854) (Lepidoptera: Crambidae). In another study, the nonlinear model predicted a decrease of up to 33.1% in the number of generations of
S. cosmioides in warmer regions where temperatures often exceeded the optimum temperature required for the species’ survival [
54]. The application of mathematical models in pest management might encounter several limitations, including the prediction accuracy of the life stage of the insect in the field and ambiguity in selecting a suitable date to start estimating the development rates [
55]. Another potential limitation is associated with the practical application of the model for different crops. In this study, the best-fit model was selected based on development data obtained using the corn plant as the host and only seven mathematical models. Further experiments in different host plants of
S. frugiperda and evaluation of a greater number number of temperature-dependent development models are essential.