Biotic Potential and Reproductive Parameters of Biotic Potential and Reproductive Parameters of Spodoptera Spodoptera (J. E. Smith, 1797) (Lepidoptera: Noctuidae) (J. E. Smith, 1797) (Lepidoptera: Noctuidae)

The fall armyworm, Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae), a native to the Americas and recently reported in Africa, Germany, the Netherlands and India, is a significant pest of many crop species. Although a widespread and important pest, information on its biology and development are incomplete and require detailed study. In this study, the biotic potential and reproductive parameters of S. frugiperda were evaluated under controlled conditions (25±1 °C, 70±10% RH and 14 hour photophase). The longevity, pre-, post-and oviposition periods, fecundity, and fertility of 30 pairs were evaluated. The longevity of females (10.87 days) was not significantly different from that of males (10.90 days). The mean durations of the pre-, post- and oviposition periods were 2.63, 0.53 and 7.70 days, respectively. The mean fecundity was 2,370.66 eggs per female and mean fertility was 2,309.03 larvae per female. On average, a female copulated 1.6 times. The biotic potential of S. frugiperda was estimated at 2.086 × 10 29 individuals/female/year. The net reproductive rate (Ro) was 1,079.73 times per generation and the mean generation time (T) was 32.00 days. The intrinsic rate of increase (rm) was 0.22, with a finite rate of increase ( λ ) of 1.24 per day. This study evaluates and describes the biological parameters of S. frugiperda with special emphasis on its biotic potential and reproductive parameters. This information will improve the development of integrated pest management (IPM) and insect resistance management (IRM) for this species.

Although S. frugiperda is such a widespread pest of many crop species, detailed biological parameters of its adult stage and biotic potential is lacking.As demonstrated for other species of Spodoptera, factors related to the reproductive behavior, such as the number of matings, is an important factor in adult longevity and fecundity (Kehat & Gordon, 1975;Etman & Hooper, 1979;Ellis & Steele, 1982;Rogers & Marti Jr., 1997;Montezano et al., 2013bMontezano et al., , 2014bMontezano et al., , 2015b;;Specht & Roque-Specht, 2016), and such information can influence population parameters and help to understand pest development.This information is necessary for the improvement of S. frugiperda integrated pest management (IPM) and insect resistance management (IRM).
To evaluate the effect of pupal weight on reproductive characteristics (Tisdale & Sappington, 2001;Specht et al., 2016), pupae were weighed on the second day after metamorphosis, and fecundity was correlated with pupal weight.Adults were kept in pairs (n = 30) within cylindrical plastic containers (10 cm in diameter and 15 cm high) with long filter paper strips attached to stimulate oviposition.The tops of the containers were closed with plastic film and the bottoms were closed with Petri dishes (10.5 cm diameter) lined with filter paper.The adult diet was composed of honey (10 g), sorbic acid (1 g), methylparaben (1 g), sucrose (60 g), and distilled water (1000 ml) (Hoffmann-Campo et al., 1985).All components were dissolved in distilled water and the resulting solution was kept under refrigeration (7 °C).Pilsen beer (Cerveceria Costa Rica, Heredia, Costa Rica) was added to the solution daily at a proportion of 1:4 beer to diet, and made available to the insects in a 5 cm Petri dish lined with cotton wool.Autoclaved water was provided in another 5 cm cotton wool lined Petri dish.Containers were examined daily to record adult survival and to remove and count the number of eggs.Dead females were dissected to determine the number of spermatophores received during copulation.Fecundity (number of eggs per female), fertility (number of hatched larvae per female), longevity, and the duration of the pre-oviposition, post-oviposition and oviposition periods were determined.
To estimate fertility, the viability of 27 egg masses (including the first and the last egg mass, totaling 8,508 evaluated eggs) taken from eight mated pairs was evaluated.Each egg cluster was placed in a Petri dish lined with filter paper moistened with distilled water until larval eclosion.All the evaluated egg masses were from females that had at least one spermatophore in the bursa copulatrix.The determination of the presence of spermatophores was done after death to verify fertilization of females during the experiment.All experiments were performed in a rearing room (25±1 ºC, 70±10% RH and a 14 hour photophase) with evaluations performed daily at 2:00 PM.
All biological parameters were analyzed using descriptive statistics.The fecundity, longevity of both sexes, and the duration of pre-and post-oviposition periods were correlated with the number of copulations for each couple: unmated females (n = 3 pairs), mated once (n = 11 pairs), mated twice (n = 11 pairs), and mated three times (n = 5 pairs).Shapiro-Wilk was used to confirm normality of data, and Levene's test to assess the equality of variances.Analysis of variance (ANOVA) was used to verify the significance of the treatments and Tukey's post-hoc test was used for the comparison of the means at a 5% probability level (α = 0.05).
Pearson's linear correlation method was used to verify possible association between fecundity and pupal weight followed by simple linear regression to assess how fecundity was influenced by pupal weight.To verify the significance of the coefficients of the model (linear coefficient and linear coefficient), a t-test was used.To verify the quality of the adjusted model, the coefficient of determination (R 2 ) was used.All statistical procedures were performed in SPSS version 19.
Biotic Potential (BP) was calculated using the equation described in Silveira-Neto et al. (1976): where, (sr) sex ratio is the number of females divided by the number of females plus number of males; (d) viable individuals per female consisting of the number of eggs per female (or fecundity) multiplied by total survival; (n) number of generations per year or 365 days divided by the total lifespan; and (er) environmental resistance, in this case considered as null.
The biotic potential and fertility life table were developed using data from the immature stages of S. frugiperda reared in accordance with the methodology of Montezano et al. (2015a).The data is graphically presented by plotting the probability of survival values at the midpoint of each time interval, (survival rate-l x ), and the total number of eggs per female per week which became females (specific fertility-m x ).
Using the life table, the values of S. frugiperda reproductive parameters were calculated.The net reproductive rate (R 0 ), given by the ratio between the number of females in two successive generations; the mean generation time (T), which is the mean number of days from the birth of the parents to the birth of offspring; the daily intrinsic rate of increase (r m ), and the daily finite rate of increase (λ) followed the formulas in Silveira-Neto et al. (1976).

Results
The mean longevity, mean length of pre-, post-and oviposition periods, and mean fecundity of 30 male-female pairs of moths are presented in Table 1.The mean fertility (calculated using 97.40% egg viability from Montezano et al. (2019) was 2,309.030larvae per S. frugiperda female.The average number of copulations per female was 1.60, while three (10%) did not copulate, eleven copulated only once (36.67%), eleven copulated twice (36.67%) and five copulated three times (16.67%).
Unmated females had a lower mean daily number of unfertilized eggs and the length of the pre-and oviposition periods were significant later and longer when compared with females that mated (Figure 1).The pre-and oviposition periods were significantly higher for females that did not mate (F = 33.427,P < 0.001, and F = 6.539,P = 0.002, respectively; Figures 2 and 3).Such differences were responsible for the increased longevity of the unmated females and males with respect to those that mated (F = 7.167, P < 0.001; Figure 4).Fecundity was positively affected by the number of matings (F = 4.809, P = 0.009), as females which were not mated oviposited less than half of those which were fertilized, with significant differences between unmated females, and those mating once, twice, or three times (Figure 5).2015a, 2015b, 2019;Specht & Roque-Specht, 2016).Therefore, the results indicate that S. frugiperda presents the fastest development among all Spodoptera species studied to date (Pogue, 2002).
The maximum number of matings observed in this study (three matings with one moth pair per container) was less than that reported in other studies: five matings when moths were maintained under similar conditions (Garcia & Clavijo, 1989), eight when 25 pairs were maintained per container (Milano et al., 2008), and eleven with one female and two males per container (Simmons & Marti Jr., 1992).However, considering the mean number of matings with just one couple per container in this study (1.6), this is similar to the data reported for the same species by Garcia and Clavijo (1989), with 1.7 matings, and Murúa et al. (2008), where variability was observed between different S. frugiperda populations in Argentina (0.78 to 2.32 matings).Regarding the absence of mating for some S. frugiperda pairs, studies with single pairs (Garcia & Clavijo, 1989;Murúa et al., 2008), multiple pairs (Milano et al., 2008), and one female and two males (Simmons & Marti Jr., 1992) have also reported unmated females.When compared with other Spodoptera species under similar conditions, the number of matings per pair was similar to what was described for S. albula, S. eridania, S. cosmioides and S. dolichos (Montezano et al., 2013b(Montezano et al., , 2014a(Montezano et al., , 2016;;Specht & Roque-Specht, 2016).The strong positive correlation between the number of matings and fecundity observed for S. frugiperda is similar to that for one female with two males per cage (Simmons & Marti Jr., 1992) and multiple pairs per cage (Burton & Perkins, 1972;Milano et al., 2008).This suggests that in nature, where the possibility of encounters between moths is high, the number of matings will be high, thus increasing fecundity.Simmons and Marti Jr. (1992) state in a personal communication from Silvian and Remillet that most field-mated (French Guiana) females had 2-4 spermatophores, and one contained nine spermatophores.
The significant reduction in the oviposition period for moths that had mated one or more times is related to the interaction between egg production and metabolism (Hou & Sheng, 1999).It is suggested that multiple matings stimulate egg production and accelerate the use of energy and resources, reducing the resources available for somatic maintenance.However, the reduction of the oviposition period associated with a greater number of matings, as described by Hou and Sheng (1999), is likely related to the increase of the reproductive activity in females which copulated more.
The presence of a pre-oviposition period indicates that S. frugiperda, as with S. albula and S. eridania (Montezano et al., 2013b(Montezano et al., , 2014b) ) under the same conditions, need at least two days after emergence to begin oviposition.However, the sexual maturity of S. frugiperda occurs soon after emergence (Simmons & Marti Jr., 1992;Rogers & Marti Jr., 1994;Busato et al., 2006), as in other Spodoptera species (e.g., Etman & Hooper, 1979;Habib et al., 1983;Tisdale & Sappington, 2001).Our results confirm that the initial mating of S. frugiperda occurs between the first and second day after emergence.The onset of oviposition, at least in the first days after emergence, is conditioned on the occurrence of the first mating, as observed for S. albula (Montezano et al., 2014a), S. cosmioides (Specht & Roque-Specht, 2016), S. dolichos (Montezano et al., 2016), S. eridania (Montezano et al., 2013b) and S. exigua (Roger & Marti Jr., 1997).However, as already reported by Martin et al. (1989), andSimmons andMartin Jr. (1992) and reported in Figure 5, the importance of multiple mating may be marginal for S. frugiperda egg production because it is not a prerequisite for continued egg production.
Results presented in this study demonstrate that S. frugiperda females that did not mate delayed the beginning of the oviposition period.Results also reported by Kehat and Gordon (1975), and Ellis and Steele (1982) which showed that in Spodoptera littoralis the delay of the first mating negatively influences population parameters.These results illustrate the possible importance of studies on the identification and use of S. frugiperda pheromones (e.g., Sekul & Sparks, 1967;Jones & Sparks, 1979;Mitchell et al., 1985;Tumlinson et al., 1986;Meagher & Mitchell, 1998;Andrade et al., 2000;Batista-Pereira et al., 2006) to delay or disrupt mating (Carde & Minks, 1995) as a strategy for the integrated management of this species.
When comparing the results obtained in this study to others conducted under the same conditions with S. albula, S. cosmioides, S. dolichos and S. eridania (Montezano et al., 2013a(Montezano et al., , 2013b(Montezano et al., , 2014a(Montezano et al., , 2014b(Montezano et al., , 2015a(Montezano et al., , 2015b(Montezano et al., , 2019;;Specht & Roque-Specht, 2016), S. frugiperda presents higher biotic potential from the combination of faster development, higher survival and high fecundity.Such factors should be considered in all areas of occurrence of this pest, which now includes the African, European and Asian continents (Goergen et al., 2016;CABI, 2017), and especially in areas where major host plants of S. frugiperda are cultivated.Results presented in this study represent optimum developmental conditions for the pest, including temperature, photoperiod, suitable diet, and absence of natural enemies.However, it is possible that additional factors that favor S. frugiperda and improve the chances of mating and reproductive success exist in nature, which are not possible to reproduce in the laboratory, such as daily variations of temperature and luminosity, pheromone release, and availability of host plants.Therefore, all observations made under laboratory conditions must be compared with detailed studies examining population temporal effects for field collected specimens when considering genetics (e.g., biotype identification), individual size (e.g., wingspan correlated with suitability of host plant and/or starvation) and number of mating events.
Figure 1 twice (n

Table 1 .
Means, standard deviation (SD) and range of longevity, pre-, post-and oviposition periods and fecundity of 30 Spodoptera frugiperda pairs under controlled conditions (25±1 °C, 70±10% RH and a 14 hour photophase) Note.Comparison of male and female mean longevity using a Student t-test, considering different variances, at 5% level of significance (ns, p = 0.163).jas.ccsenet.