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Interseasonal variation of Chrysodeixis includens (Walker, [1858]) (Lepidoptera: Noctuidae) populations in the Brazilian Savanna

Abstract

Chrysodeixis includens (Walker, [1858]) is currently the main plusiine pest in the Americas, not only because of the damage caused to soybean, but also with several crop species in a broad geographical range. However, its population dynamics is still poorly understood, despite outbreak records that are common across different locations in the Americas. The current study aimed at identifying phenological patterns of C. includens emphasizing its differences among the three years of sampling effort in an intercropping area of the Brazilian Savanna. Thereafter, we tested whether the El Niño size effect, meteorological factors, or soybean, corn and wheat cycles, are better predictors of its monthly abundance. The insects were collected with a light trap during five consecutive nights (repetitions) during 35 new moons. In total, 2026 specimens were collected in all months of the year although not consecutively. Across each year, monthly abundance of C. includens was non-uniform, characterized by sharp population peaks concentrated in the rainy season. These peaks varied from January until March, depending on the year sampled. We found that the local soybean cycle and El Niño effect to significantly influence the species abundance across the entire period of study. These results aid in understanding the species population dynamics and its status as a pest, providing evidence of factors that determine its phenological patterns. Although it presents a very defined phenology, the population dynamics of C. includens varies significantly between years and locations, which demonstrates the importance and need to monitor local populations of larvae and adults for its management.

Keywords:
Circular statistics; Phenology; Pest-species; Population outbreaks; Soybean phenology

Introduction

Since the beginning of last century, Chrysodeixis includens (Walker, [1858]) has been considered the main pest of soybean, occurring with higher frequency and intensity in different locations in Brazil (Rolim et al., 2013Rolim, A.A.S.G., Yano, S.A.C., Specht, A., Andrade, C.G.T.D.J., Sosa-Gómez, D.R., 2013. Morphological and molecular characterization of the eggs of some noctuid species associated with soybean in Brazil. Ann. Entomol. Soc. Am. 106, 643-651.; Sosa-Gómez and Omoto, 2013Sosa-Gómez, D.R., Omoto, C., 2013. Resistência a inseticidas e outros agentes de controle em artrópodes associados à cultura da soja. In: Hoffmann-Campo, C.B., Corrêa-Ferreira, B.S., Moscardi, F. (Eds.), Soja: Manejo Integrado de Insetos e outros Artrópodes-praga. Embrapa, Brasília, pp. 673–723.; Sosa-Gómez et al., 2010Sosa-Gómez, D.R., Omoto, C., 2013. Resistência a inseticidas e outros agentes de controle em artrópodes associados à cultura da soja. In: Hoffmann-Campo, C.B., Corrêa-Ferreira, B.S., Moscardi, F. (Eds.), Soja: Manejo Integrado de Insetos e outros Artrópodes-praga. Embrapa, Brasília, pp. 673–723.). However, even though its polyphagia and wide distribution across the Americas (e.g. Herzog, 1980Herzog, D.C., 1980. Sampling soybean looper on soybean. In: Kogan, M., Herzog, D.C. (Eds.), Sampling Methods in Soybean Entomology. Springer New York, New York, pp. 141–168.; Lafontaine and Poole, 1991Lafontaine, J.D., Poole, R.W., 1991. Noctuoidea, Noctuidae (Part), Plusiinae. The Moths of America North of Mexico, 25.1. The Wedge Entomological Research Foundation, Washington, pp. 1–182.; Wagner et al., 2011Wagner, D.L., Schweitzer, D.F., Sullivan, J.B., Reardon, R.C., 2011. Owlet Caterpillars of Eastern North America. Princeton University Press, Princeton.; Specht et al., 2015Specht, A., Paula-Moraes, S.V., Sosa-Gómez, D.R., 2015. Host plants of Chrysodeixis includens (Walker) (Lepidoptera, Noctuidae, Plusiinae). Rev. Bras. Entomol. 59, 343-345.), population increase of C. includens is commonly related to seasonal phenomena (i.e. hot and humid periods), or due to the period of increased hostplant availability (Alford and Hammond, 1982Alford, A.R., Hammond, A.M., 1982. Plusiinae (Lepidoptera: Noctuidae) populations in Louisiana soybeans ecosystems as determined with looplurebaited traps. J. Econ. Entomol. 75, 647-650.; Moraes et al., 1991Moraes, R.R., Loeck, A.E., Belarmino, L.C., 1991. Flutuação populacional de Plusiinae e Anticarsia gemmatalis Hübner, 1818 (Lepidoptera: Noctuidae) em soja no Rio Grande do Sul. Pesq. Agropec. Bras. 26, 51-56.; Marsaro et al., 2010Marsaro, A.L., Pereira, P.R.V.S., Silva, W.R., Griffel, S.C.P., 2010. Flutuação populacional de insetos-praga na cultura da soja no estado de Roraima. Rev. Acad. Ciênc. Agrár. Ambient. 8, 71-76.).

Plant phenology (Bencke and Morellato, 2002Bencke, C.S.C., Morellato, L.P.C., 2002. Comparação de dois métodos de avaliação da fenologia de plantas, sua interpretação e representação. Rev. Bras. Bot. 25, 269-275.; Ting et al., 2008Ting, S., Hartley, S., Burns, K.C., 2008. Global patterns in fruiting seasons. Glob. Ecol. Biogeogr. 17, 648-657.; Morellato et al., 2010Morellato, L.P.C., Alberti, L.F., Hudson, I.L., 2010. Applications of circular statistics in plant phenology: a case studies approach. In: Hudson, I.L., Keatley, M.R. (Eds.), Phenological Research: Methods for Environmental and Climate Change Analysis. Springer Science and Business Media, New York, pp. 339–359.) is of particular importance to phenological patterns exhibited by herbivore insects, especially when these plants are cultivated (Fietz and Rangel, 2008Fietz, C.R., Rangel, M.A.S., 2008. Época de semeadura da soja para a região de Dourados-MS, com base na deficiência hídrica e no fotoperíodo. Eng. Agríc. 28, 666-672.; Freitas et al., 2010Freitas, M.C.M., Hamawaki, O.T., Bueno, M.R., Marques, M.C., 2010. Época de semeadura e densidade populacional de linhagens de soja UFU de ciclo semitardio. Biosci. J. 26, 698-708.). The leaf flush period and the development of reproductive organs are of main concern to temporal distribution of specialized herbivores, but seeding and harvest periods of annual agricultural crops can drastically constrain heir abundance, or even presence of insects in a short time period. The contrasting seasons of the Brazilian Savanna are marked by differences of water availability, which requires an intensification of primary agricultural production during the period of highest rainfall (usually soybean and corn). The dry period is usually reserved for the growth of secondary crops (intercropped with soybean, corn or cotton), such as grasses (wheat, sorghum, millet and signalgrass) or forage legumes (pencil flower, common jack bean and pigeon pea), whose production is for feeding cattle during the dry season, or to simply protect the soil from solar radiation and to increase organic matter (Hoffmann et al., 2004Hoffmann, L.L., Reis, E.M., Forcelini, C.A., Panisson, E., Mendes, C.S., Casa, R.T., 2004. Efeitos da rotação de cultura, de cultivares e da aplicação de fungicida sobre o rendimento de grãos e doenças foliares em soja. Fitopatol. Bras. 29, 245-251.; Franchini et al., 2011Franchini, J.C., Costa, J.M., Debiasi, H., 2011. Rotação de culturas: prática que confere maior sustentabilidade a produção agrícola no Paraná. Inf. Agron. 134, 1-13.). These crop management needs led to the development of cultivars with characteristics such as drought resistance and long, medium, early and extra-early cycles. Crops in the Brazilian Savanna are therefore always present throughout the year, though constantly changing in species composition according to season. This scenario favours the presence and abundance of polyphagous insects whose populations make use of different cultivated hostplants (Paula-Moraes and Specht, 2013Paula-Moraes, S.V., Specht, A., 2013. Panorama para o manejo de Lepidópteros-praga em grandes culturas. In: Baldin, E.L.L., Fujihara, R.T., Cruz, P.L., Souza, A.R., Kronka, A.Z., Negrisoli, E. (Eds.), Tópicos especiais em proteção de plantas. FEPAF, Botucatu, pp. 137–164.). Although C. includens larvae are not very mobile, as Plusiinae in general (Bernarys and Singer, 2002Bernarys, E.A., Singer, M., 2002. Contrasted foraging tactics in two species of polyphagous caterpillars. Acta Zool. Acad. Sci. Hung. 48, 117-135.), C. includens presents a high degree of polyphagia, being reported feeding on at least 175 species of plants (Baldin et al., 2014Baldin, E.L.L., Lourenção, A.L., Schlick-Souza, E.C., 2014. Outbreaks of Chrysodeixis includens (Walker) (Lepidoptera: Noctuidae) in common bean and castor bean in São Paulo State, Brazil. Bragantia 73, 458-465.; Specht et al., 2015Specht, A., Paula-Moraes, S.V., Sosa-Gómez, D.R., 2015. Host plants of Chrysodeixis includens (Walker) (Lepidoptera, Noctuidae, Plusiinae). Rev. Bras. Entomol. 59, 343-345.).

Local climate factors are reported as one of the main drivers in yield oscillations (Marchiori et al., 1999Marchiori, L.F.S., Câmara, G.D.S., Peixoto, C.P., Martins, M.C., 1999. Desempenho vegetativo de cultivares de soja [Glycine max (L.) Merrill] em épocas normal e safrinha. Sci. Agríc. 56, 383-390.; Bergamaschi and Matzenauer, 2014Bergamaschi, H., Matzenauer, R., 2014. O milho e o clima. Emater/RS, Porto Alegre.). Likewise, the weather has been associated with population variations of pest insects (Moraes et al., 1991Moraes, R.R., Loeck, A.E., Belarmino, L.C., 1991. Flutuação populacional de Plusiinae e Anticarsia gemmatalis Hübner, 1818 (Lepidoptera: Noctuidae) em soja no Rio Grande do Sul. Pesq. Agropec. Bras. 26, 51-56. Heineck-Leonel and Corseuil, 1997Heineck-Leonel, M.A., Corseuil, E., 1997. Seasonal fluctuation of Cerotoma arcuata tingomariana (Bechyné) (Coleoptera: Chrysomelidae) in soybean. An. Soc. Entomol. Bras. 26, 183-185.). Temperature, for example, has an important influence over the development of crops such as soybean, corn and wheat (Marchiori et al., 1999Marchiori, L.F.S., Câmara, G.D.S., Peixoto, C.P., Martins, M.C., 1999. Desempenho vegetativo de cultivares de soja [Glycine max (L.) Merrill] em épocas normal e safrinha. Sci. Agríc. 56, 383-390.; Fietz and Rangel, 2008Fritz, L.L., Heinrichs, E.A., Pandolfo, M., Salles, S.M., Oliveira, J.V., Fiuza, L.M., 2008. Agroecossistemas orizícolas irrigados: insetos-praga, inimigos naturais e manejo integrado. Oecol. Bras. 12, 720-732.; Bergamaschi and Matzenauer, 2014Bergamaschi, H., Matzenauer, R., 2014. O milho e o clima. Emater/RS, Porto Alegre.), which in turn affects development and reproduction rates of insects (Porter, 1991Porter, M.E., 1991. Towards a dynamic theory of strategy. Strateg. Manag. J. 12, 95-117.). In the tropics however, a great part of the seasonal climatic variations is related to water availability during the year, evidenced by ecosystems with well defined dry and rainy seasons (Silva et al., 2014Silva, F.A.M., Evangelista, B.A., Malaquias, J.V., 2014. Normal climatológica de 1974 a 2003 da estação principal da Embrapa Cerrados. Embrapa Cerrados. Planaltina Documentos 321.). Thus, insect dynamics in natural environments and agroecosystems are highly dependent on tropical dry/wet seasons (Silva et al., 2011Silva, N.A.P., Frizzas, M.R., Oliveira, C.M., 2011. Seasonality in insect abundance in the "Cerrado" of Goiás State, Brazil. Rev. Bras. Entomol. 55, 79-87.; Kishimoto-Yamada and Itioka, 2015Kishimoto-Yamada, K., Itioka, T., 2015. How much have we learned about seasonality in tropical insect abundance since Wolda (1988)?. Entomol. Sci. 18, 407-419.).

Phenological oscillations also depend on supra-annual factors that influence the Earth's climate, such as hurricanes, earthquakes, cyclones and global temperature oscillations (i.e., La Niña and El Niño) (Torres, 1992Torres, J.A., 1992. Lepidoptera outbreaks in response to successional changes after the passage of Hurricane Hugo in Puerto Rico. J. Trop. Ecol. 8, 285-298.; Bravo et al., 2010Bravo Cabrera, J.L., Azpra Romero, E., Zarraluqui Such, V., Gay García, C., Estrada Porrúa, F., 2010. Significance tests for the relationship between "El Niño" phenomenon and precipitation in Mexico. Geofis. Int. 49, 245-261.). The El Niño effect, depending on the locality, is known to cause excessive rainfall, high winds, drought and temperature increase (Bravo et al., 2010Bravo Cabrera, J.L., Azpra Romero, E., Zarraluqui Such, V., Gay García, C., Estrada Porrúa, F., 2010. Significance tests for the relationship between "El Niño" phenomenon and precipitation in Mexico. Geofis. Int. 49, 245-261.), and is responsible for related agricultural losses (Sivakumar et al., 2005Sivakumar, M.V.K., Das, H.P., Brunini, O., 2005. Impacts of present and future climate variability and change on agriculture and forestry in the arid and semi-arid tropics. Clim. Change 70, 31-72.) and insect outbreaks (Rouault et al., 2006Rouault, G., Candau, J.N., Lieutier, F., Nageleisen, L.M., Martin, J.C., Warzée, N., 2006. Effects of drought and heat on forest insect populations in relation to the 2003 drought in Western Europe. Ann. For. Sci. 63, 613-624.). Nonetheless, effects caused by inter-annual phenomena are rarely investigated in insect population dynamics (Kishimoto-Yamada and Itioka, 2015Kishimoto-Yamada, K., Itioka, T., 2015. How much have we learned about seasonality in tropical insect abundance since Wolda (1988)?. Entomol. Sci. 18, 407-419.), and even less so when related to agricultural pest species (Sivakumar et al., 2005Sivakumar, M.V.K., Das, H.P., Brunini, O., 2005. Impacts of present and future climate variability and change on agriculture and forestry in the arid and semi-arid tropics. Clim. Change 70, 31-72.).

In order to contribute to the knowledge of pest-insect population dynamics in agroecosystems of the Brazilian Savanna (i.e. Cerrado), the current study aimed at identifying seasonality patterns of C. includens in an intercropping area during three years, testing: (1) significant major occurrence to a certain period of the year; (2) the same monthly abundance distribution among different years; (3) predictive power of the annual crop cycle, weather factors and El Niño effect on monthly moth abundance.

Material and methods

Sampling area

The experiment was performed in the ‘Estação Experimental da Embrapa Cerrados', located in the city of Planaltina, Distrito Federal, Brazil (15°35'30″ S and 47°42'30″ W, altitude: 1007 m). The area is located in the ‘Cerrado' biome (Ab'Sáber, 2003Ab'Sáber, A.N., 2003. Domínios de natureza no Brasil: potencialidades paisagísticas. Ateliê Editorial, São Paulo.), also known as the Brazilian Savanna. According to the climate classification of Köppen, it has a Subtropical-Dry Winter climate (Cwa), with average temperature of the coldest month below 18 °C and from the hottest month above 22 °C. The region is marked by two seasons that are defined by the differences in rainfall accumulation. The rainy period starts in September and extends until April, with the rainiest months being November, December and January. The dry period starts in May and ends in September, resulting in a hot and rainy summer and mild and dry winter (Silva et al., 2014Silva, F.A.M., Evangelista, B.A., Malaquias, J.V., 2014. Normal climatológica de 1974 a 2003 da estação principal da Embrapa Cerrados. Embrapa Cerrados. Planaltina Documentos 321.).

The sample landscape is totally devoid of natural areas, where several species of agricultural importance predominate, especially soybean, corn and wheat that occupies about 25%, 15% and 10% of the landscape. Part of the area is occupied with buildings and, to a lesser extent, crops of other species such as Andropogum, coffee, cassava, Crotalaria, Eucalyptus, oil palm, Panicum, passion fruit, cane. Wheat stands out because of its presence is restricted to the dry period, while soybean and corn cultivation is restricted to the rainy season. It is assumed that the other crops do not affect the phenology of C. includens because they are perennial, are not preferential hosts or are cultivated in small areas.

Collecting method

Because C. includens is strongly attracted to light sources (Wagner et al., 2011Wagner, D.L., Schweitzer, D.F., Sullivan, J.B., Reardon, R.C., 2011. Owlet Caterpillars of Eastern North America. Princeton University Press, Princeton.), we used a Pennsylvania light trap (Frost, 1957Frost, S.W., 1957. The Pennsylvania insect light trap. J. Econ. Entomol. 50, 287-292.) as a collection method, set with a black fluorescent light model BL T8 15W (Tovalight), with wavelengths varying between 290 and 450 nm with a peak around 340 nm. A plastic cone was set in the lower portion of the trap, with the widest diameter of 32 cm and narrowest of 16 cm, to which a plastic bucket was set with three litres of 96GL ethanol. The trap was set on a post, with its lower part approximately 3.5 m above the ground, and was lit from nightfall until the following morning.

The trap was lit 35 times during three years to represent all months during that period. The only month whose samples could not be considered was November of 2013, since the excess rainfall and a large number of Coleoptera, Hymenoptera and Isoptera attracted to the trap damaged the specimens preventing species identification. To minimize the effects of moonlight and meteorological effects on traps efficiency, each collecting event had five samples (nights) collected at the end of the waning moon and start of the new moon (Zanuncio et al., 1995Zanuncio, T.V., Zanuncio, J.C., Araújo, M.S.S., Evaristo, F.C., 1995. Influência da fase lunar na coleta de lepidópteros, em plantios de eucalipto, na região de Açailândia, Maranhão, Brasil. Rev. Árvore 19, 100-109.).

Chrysodeixis includens specimens are preserved in 96GL ethanol, and representative vouchers were pinned and deposited in the ‘Coleção de Insetos da Embrapa Cerrados'. Specific identification was based on the specialized bibliography (Eichilin and Cunningham, 1978Eichilin, T.D., Cunningham, H.B., 1978. The Plusiinae (Lepidoptera: Noctuidae) of America North of Mexico, emphasizing genitalia and larval morphology. Tech. Bull. USDA 1567., pp. 1–122.; Lafontaine and Poole, 1991Lafontaine, J.D., Poole, R.W., 1991. Noctuoidea, Noctuidae (Part), Plusiinae. The Moths of America North of Mexico, 25.1. The Wedge Entomological Research Foundation, Washington, pp. 1–182.).

Statistical analysis

Rao's Spacing test was used to test the uniformity of the temporal distribution of C. includens for each year. Taking into consideration that the Rao test rejected the hypothesis of an uniform distribution for C. includens, the estimated average angle of abundance in a certain period of the year was used to indicate the period of highest occurrence. The length of the average angle (r), which may vary from 0 to 1, was used to indicate how clustered the abundance data were around the average (Zar, 2010Zar, J.H., 2010. Biostatistical Analysis, 5th ed. Prentice Hall, New Jersey.). This value is correlated to the angular standard deviation calculated, which is used to represent the amplitude of a phenological pattern.

Once evidence of a phenological pattern of moth occurrence was observed, annual distributions (between harvests) were compared to each other to determine if the species maintains its patterns, even between distinct years. In this case, the average angles and abundance distributions were used as statistical parameters, associated to the Watson William (f) and Watson-U 2 tests, respectively.

We also tested for different variables as predictors of the phenological abundance variation of C. includens during the three years. Because abundance distribution is not normal and data showed overdispersed residuals, we used the generalized linear model using a negative binomial distribution. The variables tested include hostplant availability, El Niño size effect, and weather measurements. Since we could not access a quantitative estimate of available hostplants, soybean/corn and wheat were monthly coded as presence/absence according to local management of these cultures in the study area. Soybean and corn effect could not be distinguished because they are cultivated during the same season. However, since corn is only sporadically reported as a hostplant of C. includens (Herzog, 1980Herzog, D.C., 1980. Sampling soybean looper on soybean. In: Kogan, M., Herzog, D.C. (Eds.), Sampling Methods in Soybean Entomology. Springer New York, New York, pp. 141–168.), we discussed the effect of this factor by being solely provided by the soybean. Soybean and corn crops were available for C. includens between December and March, the months of its sowing and ripening, respectively. During April, C. includens cannot use the leaves of the soybean and corn because they dry and fall when the pod is ripening (Moscardi et al., 2012Moscardi, F., Bueno, A.F., Sosa-Gómez, D.R., Roggia, S., Hoffmann-Campo, C.B., Pomari, A.F., Corso, I.C., Yano, S.A.C., 2012. Artrópodes que atacam as folhas da soja. In: Hoffmann-Campo, C.B., Corrêa-Ferreira, B.S., Moscardi, F. (Eds.), Soja – Manejo integrado de insetos e outros artrópodes-praga. Embrapa, Brasília, pp. 214–334.). The wheat cycle, however, starts in March and extends until September. These hostplant cycles were selected because they represent non-perennial crops cultivated in the study area that are used by C. includens as hostplants.

Measurements from the previous month of average, maximum and minimum relative humidity, rainfall, average, maximum and minimum temperature, and insolation were selected to represent two main factors that could influence on the development of C. includens and, therefore, its abundance. Thus, to improve the interpretation of results and avoid collinearity in our data we used the interaction of the first four variables to represent water availability and the last four variables to represent temperature affecting abundance of the soybean looper. The linear model was fitted using glm function, available in R environment R Development Core (R Core Team, 2013, 2013. R development core team. R. A. Lang. Environ. Stat. Comput. 55, 275-286.).

Results

During the three years (July/2013 until June/2016) 2026 specimens of C. includens were collected (Table 1). The monthly abundance was marked by an exceptional peak occurring in February, elevated abundances between January and March depending on the year, and only occasional records in other months, when present. The species was not detected in October of the first and second crop seasons, and in May, June and November of the second and third crop seasons. A non-uniform pattern was observed for C. includens in all sampled years, as confirmed by the Rao Spacing test (Table 2).

Table 1
Monthly abundance of Chrysodeixis includens moths collected with light traps in three agricultural crop seasons in the 'Estação Experimental da Embrapa Cerrados', Planaltina, DF, Brazil.
Table 2
Descriptive statistics of the circular analysis of the abundance of Chrysodeixis includens in each harvest in the 'Estação Experimental da Embrapa Cerrados', Planantina, DF, Brazil. n, number of moths; µ, mean vector; CSD, circular standard deviation; r, length of mean vector; Concentration; U, Rao's spacing test; U 2, Watson's U 2 test.

Abundance and phenological patterns of C. includens differed between years. Although total abundance decreased through the years (1452 in the 2013/2014, 462 in the 2014/2015 and 112 in the 2015/2016), the average vector angle (the circular measurement that represents the phenological mean distribution of the species) delayed slightly from the first to the third year. In the first, the vector angle was directed towards the beginning of February. In the following years the average angle delays slightly to the middle of February and March, accordingly (Fig. 1), although always concentrated in a small portion of the rainy season and almost synchronic to soybean availability (Fig. 2). Circular statistical analyses confirmed the differences between the average angles and the abundance distributions between years (Table 3). When all variables are included to predict C. includens abundance, only soybean availability and El Niño effect showed significant influence, although both factors acts conversely. While soybean availability raises C. includens abundances, higher effects of El Niño reduces its populations. All other factors influence did not differ from zero (Table 4).

Fig. 1
Monthly abundance of Chrysodeixis includens moths during three crop seasons. Vectors angles represents circular mean abundance while vectors length represents how clustered is the abundance data around the average.

Fig. 2
Population variation of Chrysodeixis includens (bars) sampled through light traps, compared to monthly normal rainfall (mm/month) (dotted line), monthly accumulated rainfall (mm/month) (continuous line) and period of corn and soybean cultivation (grey area) during five nights each month (new moon), in the ‘Estação Experimental da Embrapa Cerrados', Planaltina, DF, Brazil.

Table 3
Comparison of abundance distribution of Chrysodeixis includens between crop seasons, based on Watson-Williams F-test and Watson's U 2 test.
Table 4
GLM coefficients from predictive power of weather and crop cycle on monthly abundances of Chrysodeixis includens. Theta value = 0.564 (±0.163SE).

Discussion

The phenological dynamic patterns of insect species has so far been focused on species with natural distributions (Wolda, 1988Wolda, H., 1988. Insect seasonality: why?. Annu. Rev. Ecol. Syst. 19, 1-18.), although such patterns can be easily translated to pest species. Recognizing the phenological patterns exhibited by pest species, such as C. includens, is particularly important to applied crop sciences, as this kind of information is necessary to develop and/or recommend methods to minimize economic losses (Hudson and Keatley, 2010Hudson, I.L., Keatley, M.R. (Eds.), 2010. Phenological Research: Methods for Environmental and Climate Change Analysis. Springer Science and Business Media, New York.). As it occurs to species in natural habitats, phenological patterns are dependent of the range of hostplant used by herbivorous species. For monophagous, oligophagous, or species particularly associated to certain annual agricultural crops, a higher degree of phenological association is expected due to the limited available resource (Novotny and Basset, 1998Novotny, V., Basset, Y., 1998. Seasonality of sap-sucking insects (Auchenorrhyncha, Hemiptera) feeding on Ficus (Moraceae) in a lowland rain forest in New Guinea. Oecologia 115, 514-522.). Thus, from harvest to the beginning of the next crop growth cycle, populations are expected to be absent. On the other hand, polyphagous or generalist species can also present significant major occurrence (population peaks) for certain periods of the year, but low abundance can still be recorded in the absence of the preferred hostplant (Wolda, 1988Wolda, H., 1988. Insect seasonality: why?. Annu. Rev. Ecol. Syst. 19, 1-18.; Kishimoto-Yamada and Itioka, 2015Kishimoto-Yamada, K., Itioka, T., 2015. How much have we learned about seasonality in tropical insect abundance since Wolda (1988)?. Entomol. Sci. 18, 407-419.), as they will feed on inter-annual crops, weeds or cover plants.

Throughout the Americas, C. includens presents sharp population peaks in different periods of the year (Alford and Hammond, 1982Alford, A.R., Hammond, A.M., 1982. Plusiinae (Lepidoptera: Noctuidae) populations in Louisiana soybeans ecosystems as determined with looplurebaited traps. J. Econ. Entomol. 75, 647-650.; Moraes et al., 1991Moraes, R.R., Loeck, A.E., Belarmino, L.C., 1991. Flutuação populacional de Plusiinae e Anticarsia gemmatalis Hübner, 1818 (Lepidoptera: Noctuidae) em soja no Rio Grande do Sul. Pesq. Agropec. Bras. 26, 51-56.; Marsaro et al., 2010Marsaro, A.L., Pereira, P.R.V.S., Silva, W.R., Griffel, S.C.P., 2010. Flutuação populacional de insetos-praga na cultura da soja no estado de Roraima. Rev. Acad. Ciênc. Agrár. Ambient. 8, 71-76.). During the three studied years, its abundance was always concentrated in a narrow period of the rainy season (between January and March), showing a strong phenological pattern. This pattern was here showed to be influenced by the soybean cycle, which is relatively short compared to other crop species (Freitas et al., 2010Freitas, M.C.M., Hamawaki, O.T., Bueno, M.R., Marques, M.C., 2010. Época de semeadura e densidade populacional de linhagens de soja UFU de ciclo semitardio. Biosci. J. 26, 698-708.). However, it is important to highlight that C. includens maintained small populations surviving in alternate hostplants throughout much of the year, probably due to its high degree of polyphagia. Its absence during occasional months may be explained by low population numbers, and stochastic factors related to light attraction traps (Muirhead-Thompson, 1991Muirhead-Thompson, R.C., 1991. Trap Responses of Flying Insects. The Influence of Trap Design on Capture Efficiency. Academic Press, London.; Vilarinho et al., 2011Vilarinho, E.C., Fernandes, O.A., Hunt, T.E., Caixeta, D.F., 2011. Movement of Spodoptera frugiperda adults (Lepidoptera: Noctuidae) in maize in Brazil. Fla. Entomol. 94, 480-488.). In the presence of soybean and favourable conditions, these populations might multiply rapidly, occasionally causing outbreaks, massively infesting other crops like bean and castor bean (Baldin et al., 2014Baldin, E.L.L., Lourenção, A.L., Schlick-Souza, E.C., 2014. Outbreaks of Chrysodeixis includens (Walker) (Lepidoptera: Noctuidae) in common bean and castor bean in São Paulo State, Brazil. Bragantia 73, 458-465.). Other characteristics of this species, such its migratory behaviour in certain regions (Ferguson et al., 1991Ferguson, D.C., Hilburn, D.J., Wright, B., 1991. The Lepidoptera of Bermuda: their food plants, biogeography, and means of dispersal. Mem. Entomol. Soc. Can. 158, 1-105.; Wagner et al., 2011Wagner, D.L., Schweitzer, D.F., Sullivan, J.B., Reardon, R.C., 2011. Owlet Caterpillars of Eastern North America. Princeton University Press, Princeton.), could also explain the dynamics of these population peaks. Nevertheless, other methodologies (e.g. molecular approaches) are required to detect the migratory influence on population dynamics (Palma et al., 2015Palma, J., Maebe, K., Guedes, J.V.C., Smagghe, G., 2015. Molecular variability and genetic structure of Chrysodeixis includens (Lepidoptera: Noctuidae), an important soybean defoliator in Brazil. PLOS ONE 10, e0121260.).

The strong phenological pattern of the adults of C. includens in central Brazil also corroborates observations from immature data. Evidently, larval populations also increase in the presence of soybean crops in very distinct Brazilian agriculture systems (Moraes et al., 1991Moraes, R.R., Loeck, A.E., Belarmino, L.C., 1991. Flutuação populacional de Plusiinae e Anticarsia gemmatalis Hübner, 1818 (Lepidoptera: Noctuidae) em soja no Rio Grande do Sul. Pesq. Agropec. Bras. 26, 51-56.; Didonet et al., 1998Didonet, J., Fragoso, D.B., Peluzio, J.M., Santos, G.R., 1998. Flutuação populacional de pragas e inimigos naturais em soja no Projeto Rio Formoso – Formoso do Araguaia – TO, Brasil. Acta Amaz. 28, 67-74.; Conte and Corrêa-Ferreira, 2014Conte, O., Corrêa-Ferreira, B.S., 2014. Resultados do Manejo Integrado de Pragas da Soja na Safra 2013/14 no Paraná. Londrina, Embrapa soja, Documentos 356.). Because of this direct association with the soybean cycle (Herzog, 1980Herzog, D.C., 1980. Sampling soybean looper on soybean. In: Kogan, M., Herzog, D.C. (Eds.), Sampling Methods in Soybean Entomology. Springer New York, New York, pp. 141–168.; Moscardi et al., 2012Moscardi, F., Bueno, A.F., Sosa-Gómez, D.R., Roggia, S., Hoffmann-Campo, C.B., Pomari, A.F., Corso, I.C., Yano, S.A.C., 2012. Artrópodes que atacam as folhas da soja. In: Hoffmann-Campo, C.B., Corrêa-Ferreira, B.S., Moscardi, F. (Eds.), Soja – Manejo integrado de insetos e outros artrópodes-praga. Embrapa, Brasília, pp. 214–334.), the period when species abundance is higher also follows the period when soybean is cultivated in different regions of America. In the northern hemisphere, for example (latitude around 30°), the soybean phenology is inverted. There the higher abundance peaks of C. includens occurs from July to September (e.g. Harding, 1976Harding, J.A., 1976. Seasonal occurrence, parasitism and parasites of cabbage and soybean loopers in the lower Rio Grande Valley. Environ. Entomol. 5, 672-674.; Alford and Hammond, 1982Alford, A.R., Hammond, A.M., 1982. Plusiinae (Lepidoptera: Noctuidae) populations in Louisiana soybeans ecosystems as determined with looplurebaited traps. J. Econ. Entomol. 75, 647-650.). The same occurs to regions close to the Equator, though still further north. In the state of Roraima, Brazil (latitude around 2°), Marsaro et al. (2010)Marsaro, A.L., Pereira, P.R.V.S., Silva, W.R., Griffel, S.C.P., 2010. Flutuação populacional de insetos-praga na cultura da soja no estado de Roraima. Rev. Acad. Ciênc. Agrár. Ambient. 8, 71-76. reported the higher abundance of larvae of C. includens in the month of June. Together, these reports highlight the phenological plasticity of this pest species, whose population variation is extremely adapted to the seasonal conditions of Earth's hemispheres.

Circular statistical analyses already demonstrated that different taxa of the Brazilian Savanna, including plants, present high mean vectors and concentration values (Pinheiro et al., 2002Pinheiro, F., Diniz, I.R., Coelho, D., Bandeira, M.P.S., 2002. Seasonal pattern of insect abundance in the Brazilian Cerrado. Austral Ecol. 27, 132-136.; Silva et al., 2011Silva, N.A.P., Frizzas, M.R., Oliveira, C.M., 2011. Seasonality in insect abundance in the "Cerrado" of Goiás State, Brazil. Rev. Bras. Entomol. 55, 79-87.; Pilon et al., 2015Pilon, N.A.L., Udulutsch, R.G., Durigan, G., 2015. Padrões fenológicos de 111 espécies de Cerrado em condições de cultivo. Hoehnea 42, 425-443.; Velasque and Del-Claro, 2016Velasque, M., Del-Claro, K., 2016. Host plant phenology may determine the abundance of an ecosystem engineering herbivore in a tropical savanna. Ecol. Entomol. 41, 421-430.). This means that this ecosystem is broadly characterized by plant species with strong phenological patterns, such as observed in C. includens. Vector length of reproductive phenology of plants varies from 0.101 to 0.919 (Velasque and Del-Claro, 2016Velasque, M., Del-Claro, K., 2016. Host plant phenology may determine the abundance of an ecosystem engineering herbivore in a tropical savanna. Ecol. Entomol. 41, 421-430.), 0.07 to 0.81 (Morellato et al., 2000Morellato, L.P.C., Talora, D.C., Takahasi, A., Bencke, C.C., Romera, E.C., Zipparro, V.B., 2000. Phenology of Atlantic rain forest trees: a comparative study. Biotropica 32, 811-823.), and 0.08 to 0.59 (Pilon et al., 2015Pilon, N.A.L., Udulutsch, R.G., Durigan, G., 2015. Padrões fenológicos de 111 espécies de Cerrado em condições de cultivo. Hoehnea 42, 425-443.). The values obtained for C. includens (0.93 to 0.96) indicate sharper population peaks in a shorter period when adults are present. Although these values are unknown for the majority of pest-species, the population dynamics already described for a few of them suggest smoother phenology patterns (Tarragó et al., 1977Tarragó, M.F.S., Silveira Neto, S., Carvalho, S., Barbin, D., 1977. Influência de fatores ecológicos na flutuação populacional das lagartas da soja, Anticarsia gemmatalis Hbn. e Rachiplusia ou (Guen.) em Santa Maria – RS. An. Soc. Entomol. Brasil 6, 180-193.; Moraes et al., 1991Moraes, R.R., Loeck, A.E., Belarmino, L.C., 1991. Flutuação populacional de Plusiinae e Anticarsia gemmatalis Hübner, 1818 (Lepidoptera: Noctuidae) em soja no Rio Grande do Sul. Pesq. Agropec. Bras. 26, 51-56.).

The attempt to correlate different annual crop cycles with the abundance of C. includens allows for the verification of different aspects of these relationships. Although it can feed on more than 175 species of plants, including soybean, corn, cotton, wheat, bean and tobacco (Specht et al., 2015Specht, A., Paula-Moraes, S.V., Sosa-Gómez, D.R., 2015. Host plants of Chrysodeixis includens (Walker) (Lepidoptera, Noctuidae, Plusiinae). Rev. Bras. Entomol. 59, 343-345.), the population peaks of C. includens in the Brazilian Savanna are clearly related to soybean availability, as mentioned elsewhere (e.g. Herzog, 1980Herzog, D.C., 1980. Sampling soybean looper on soybean. In: Kogan, M., Herzog, D.C. (Eds.), Sampling Methods in Soybean Entomology. Springer New York, New York, pp. 141–168.; Moraes et al., 1991Moraes, R.R., Loeck, A.E., Belarmino, L.C., 1991. Flutuação populacional de Plusiinae e Anticarsia gemmatalis Hübner, 1818 (Lepidoptera: Noctuidae) em soja no Rio Grande do Sul. Pesq. Agropec. Bras. 26, 51-56.; Moscardi et al., 2012Moscardi, F., Bueno, A.F., Sosa-Gómez, D.R., Roggia, S., Hoffmann-Campo, C.B., Pomari, A.F., Corso, I.C., Yano, S.A.C., 2012. Artrópodes que atacam as folhas da soja. In: Hoffmann-Campo, C.B., Corrêa-Ferreira, B.S., Moscardi, F. (Eds.), Soja – Manejo integrado de insetos e outros artrópodes-praga. Embrapa, Brasília, pp. 214–334.; Specht et al., 2015Specht, A., Paula-Moraes, S.V., Sosa-Gómez, D.R., 2015. Host plants of Chrysodeixis includens (Walker) (Lepidoptera, Noctuidae, Plusiinae). Rev. Bras. Entomol. 59, 343-345.). Likewise, other insect pests with preference for soybean present similar population peaks, as in R. nu (Guenée, 1852) and Anticarsia gemmatalis Hübner, 1818, Eushistus heros (Fabricius, 1794), Piezodorus guildinii (Westwood, 1837), Nezara viridula (Linnaeus, 1758) and Cerotoma arcuata tingomariana (Bechyné, 1951) (Tarragó et al., 1977Tarragó, M.F.S., Silveira Neto, S., Carvalho, S., Barbin, D., 1977. Influência de fatores ecológicos na flutuação populacional das lagartas da soja, Anticarsia gemmatalis Hbn. e Rachiplusia ou (Guen.) em Santa Maria – RS. An. Soc. Entomol. Brasil 6, 180-193.; Heineck-Leonel and Corseuil, 1997Heineck-Leonel, M.A., Corseuil, E., 1997. Seasonal fluctuation of Cerotoma arcuata tingomariana (Bechyné) (Coleoptera: Chrysomelidae) in soybean. An. Soc. Entomol. Bras. 26, 183-185.; Marsaro et al., 2010Marsaro, A.L., Pereira, P.R.V.S., Silva, W.R., Griffel, S.C.P., 2010. Flutuação populacional de insetos-praga na cultura da soja no estado de Roraima. Rev. Acad. Ciênc. Agrár. Ambient. 8, 71-76.). The use of wheat as an intercropping species did not influence C. includens abundances, although it could have a fundamental role in allowing the maintenance of C. includens populations during the dry season, even in low numbers. This population dynamic is particularly important to insect pest management since it has been hypothesized that the populations of C. includens benefit from crop rotation, especially in irrigated crops, to remain throughout the year (Fritz et al., 2008Fritz, L.L., Heinrichs, E.A., Pandolfo, M., Salles, S.M., Oliveira, J.V., Fiuza, L.M., 2008. Agroecossistemas orizícolas irrigados: insetos-praga, inimigos naturais e manejo integrado. Oecol. Bras. 12, 720-732.). In Brazil, there has been an increase in the use of wheat as an alternative for the production of grains and intercropping (Franchini et al., 2011Franchini, J.C., Costa, J.M., Debiasi, H., 2011. Rotação de culturas: prática que confere maior sustentabilidade a produção agrícola no Paraná. Inf. Agron. 134, 1-13.). Cotton and bean, on the other hand, are examples of preferred hostplants of C. includens, which are also used in intercropping with soybean. The use of these species could therefore reveal different population dynamics than observed in the present study, but more study is necessary to clarify this inference.

Despite the importance of crop cycles, weather factors can also be determinant in regulating the abundance of pest species (Tarragó et al., 1977Tarragó, M.F.S., Silveira Neto, S., Carvalho, S., Barbin, D., 1977. Influência de fatores ecológicos na flutuação populacional das lagartas da soja, Anticarsia gemmatalis Hbn. e Rachiplusia ou (Guen.) em Santa Maria – RS. An. Soc. Entomol. Brasil 6, 180-193.). In ecosystems marked by a dry and rainy season, such as the Brazilian Savanna (Silva et al., 2014Silva, F.A.M., Evangelista, B.A., Malaquias, J.V., 2014. Normal climatológica de 1974 a 2003 da estação principal da Embrapa Cerrados. Embrapa Cerrados. Planaltina Documentos 321.), it is expected that water availability factors play a more important role driving species abundances (Kishimoto-Yamada and Itioka, 2015Kishimoto-Yamada, K., Itioka, T., 2015. How much have we learned about seasonality in tropical insect abundance since Wolda (1988)?. Entomol. Sci. 18, 407-419.). Moreover, insects often present richer fauna during the rainy season (Pinheiro et al., 2002Pinheiro, F., Diniz, I.R., Coelho, D., Bandeira, M.P.S., 2002. Seasonal pattern of insect abundance in the Brazilian Cerrado. Austral Ecol. 27, 132-136.; Silva et al., 2011Silva, N.A.P., Frizzas, M.R., Oliveira, C.M., 2011. Seasonality in insect abundance in the "Cerrado" of Goiás State, Brazil. Rev. Bras. Entomol. 55, 79-87.). However, neither water availability (measured by humidity and precipitation) nor temperature were correlated to the abundances of C. includens. This lack of response is probably because their high abundance peaks concentrated during a narrow temporal distribution. Therefore, there are long periods in the year marked of high variability of weather conditions, when population abundance is zero or varies slightly above it.

Weather variation was predictive of C. includens population variations when measured as an inter-annual factor (e.g. effect of El-Niño). Among years sampled, the El Niño effect was considered "weak to moderate" in 2014/2015, but i "very strong" during 2015/2016, affecting specially the rainfall and temperature levels in the southern hemisphere (Null, 2016Null, J., 2016. El Niño and La Niña Years and Intensities: Based on Oceanic Niño Index (ONI), http://ggweather.com/enso/oni.htm/ (accessed 28.11.16).
http://ggweather.com/enso/oni.htm/...
). This clearly resulted on the decrease of C. includens monthly abundances. Thus, considering that both excess and lack of rain are known to raise larval mortality, especially in the first instars (Zalucki et al., 2002Zalucki, M.P., Clarke, A.R., Malcolm, S.B., 2002. Ecology and behavior of first instar larval Lepidoptera. Annu. Rev. Entomol. 47, 361-393.), supra-annual phenomena such as the El Niño can cause substantial variations in species populations (Rouault et al., 2006Rouault, G., Candau, J.N., Lieutier, F., Nageleisen, L.M., Martin, J.C., Warzée, N., 2006. Effects of drought and heat on forest insect populations in relation to the 2003 drought in Western Europe. Ann. For. Sci. 63, 613-624.; Kishimoto-Yamada and Itioka, 2015Kishimoto-Yamada, K., Itioka, T., 2015. How much have we learned about seasonality in tropical insect abundance since Wolda (1988)?. Entomol. Sci. 18, 407-419.), including those with economic importance. Such phenomena should not be omitted in studies that aim to predict the factors responsible for the population dynamics of pests. With this additional information, agricultural techniques will be able to estimate more precisely how pest populations should behave during unexpected weather oscillations.

Other factors responsible for population variations of pest species, such as natural enemies and agricultural management techniques (Lima et al., 2009Lima, E.A.B.F., Ferreira, C.P., Godoy, W.A.C., 2009. Ecological modeling and pest population management: a possible and necessary connection in a changing world. Neotrop. Entomol. 38, 699-707.), could not be estimated in the current study. However, the populations of C. includens are known to be negatively affected by pathogens, parasitoids and predators (Harding, 1976Harding, J.A., 1976. Seasonal occurrence, parasitism and parasites of cabbage and soybean loopers in the lower Rio Grande Valley. Environ. Entomol. 5, 672-674.; Maruyama et al., 2001Maruyama, W.I., Gravena, S., Pinto, A.S., 2001. Parasitóides e Nomurarea rileyi (Farlow) Samson em Lagartas Desfolhadoras (Lepidoptera) na Cultura da Soja. Bol. Sanid. Veg. Plagas 27, 561-567.; Sosa-Gómez et al., 2003Sosa-Gómez, D.R., Delpin, K.E., Moscardi, F., Nozaki, M.H., 2003. The impact of fungicides on Nomuraea rileyi (Farlow) Samson epizootics and on populations of Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae), on soybean. Neotrop. Entomol. 32, 287-291.), as well as positively by management techniques, such as the use of pesticides which directly affect these natural enemies (Ferron, 1978Ferron, P., 1978. Biological control of insect pests by entomogenous fungi. Annu. Rev. Entomol. 23, 409-442.; Sosa-Gómez et al., 2003Sosa-Gómez, D.R., Delpin, K.E., Moscardi, F., Nozaki, M.H., 2003. The impact of fungicides on Nomuraea rileyi (Farlow) Samson epizootics and on populations of Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae), on soybean. Neotrop. Entomol. 32, 287-291.). Studies including this kind of information are required, especially in the case of C. includens, where a considerable fraction of its population variation is still unexplained by weather and crop cycle factors.

Acknowledgements

To Pollyanna Nunes de Otanásio, Vander Célio de Matos Claudino, Márcia Danyelle Ribeiro Bernardes and Fernando Ferreira Martins, for collecting and sorting insects. Dr. Fernando Antônio Macena da Silva gently provided the meteorological data. To Instituto Chico Mendes (ICMBio) - Ministério do Meio Ambiente do Brasil – Authorization for scientific activities SISBIO 38547/(1-6); Conselho Nacional de Desenvolvimento Cientifico e Tecnológico (CNPq) (proc n°. 403376/2013-0, 476691/2013-3, 47304/2013-8, 308247/2013-2) and Empresa Brasileira de Pesquisa Agropecuária (SEG MP2 02.13.14.006.00.00) for research funding.

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Publication Dates

  • Publication in this collection
    Oct-Dec 2017

History

  • Received
    16 May 2017
  • Accepted
    26 June 2017
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