Spatio-temporal variation of Mocis latipes (Guenée, 1852) (Lepidoptera: Erebidae) populations in Brazil according to meteorological factors

Spatio-temporal variation of Mocis latipes (Guenée, 1852) (Lepidoptera: Erebidae) populations in Brazil according to meteorological factors. Biota Abstract: Mocis latipes (Guenée, 1852) (Lepidoptera: Erebidae) has been recognized as a major owlet caterpillar associated to the herbivory of gramineaceous plants across the American continent. During outbreaks, the caterpillars are capable of completely consuming preferred hosts (grasses) and, when these hosts are destroyed, they can move to adjacent non-grass plants and cause similar damage. Meteorological variable such as temperature and humidity are described as factors that affect the development and abundance of M. latipes . This paper aimed to describe and compare the spatial and temporal distribution of M. latipes in different locations in Brazil and to evaluate the influence of meteorological variables on the temporal range. A total of 12 locations were evaluated, in each collection point light traps were installed near cultivated areas. In order to understand the influence of meteorological variables on the abundance of M. latipes , the data were analyzed using a Generalized Linear Model according to Poisson regression. A linear regression was also used to verify the relation between the abundance and the latitude. A total of 1,985 moths were collected. The highest collections were in Amazon and Cerrado biomes. Results show that abundance was inversely related to increasing latitude and Poisson regression analysis indicated that the main meteorological variables were significantly related to abundance at each site. This study shows that due to the high preference for gramineas and the high temperature requirements (30°C), M. latipes is an important species in hot regions and regions with hight humidity. Furthurmore, even in higher latitudes, in subtropical areas, during summer months, populations can Rapidly growth being able to cause economic damages.

Usually, M. latipes is reported as a cyclic pest (e.g. Calderón et al. 1981, Saunders et al. 1998) whose abundance is influenced by environmental factors such as humidity, precipitation and temperature (Calderón et al. 1982, Ferreira & Parra 1985, Gibbs 1990). Therefore, under favorable weather conditions and food availability, their populations increase rapidly.
Temperature and humidity are the main environmental factors that influence occurrence, distribution and complete development of M. latipes biological cycle. Therefore, the imbalance of these conditions directly interferes in population size (Bertels 1970, Bernardi et al. 2011. Understanding spatial and temporal distribution of pest species is important to reduce risks of Outbreaks and to develop sustainable management control (Pedigo & Rice 2009). There is a lack of studies on population dynamics of M. latipes in different regions in Brazil. Population outbreaks are known to occur early in the rainy season, especially in the Amazon (Teixeira & Townsend 1997, Fazolin et al. 2009). However, the factors that cause these occurrences are still unknown. Thus, this paper reports the influence of meteorological variables and latitude on spatio-temporal abundance of M. latipes in different regions in Brazil.

Moth sampling
Mocis latipes moths were captured in systematized collections at 12 regions in Brazil (Table 1), being those regions representatives of the main Brazilian biomes and on a latitudinal range (2° North to 31° South). At each collection point, a light trap (Light Trap -Bio Controle®), adapted to Pennsylvania model (Frost 1957), was placed on a pole 3 meters from the ground. Collections were made once a month, from July 2015 to June 2016, during each novilunium repeated for five nights (repetitions). Collection methodology followed Specht et al. (2005) and Piovesan et al. (2018). Traps were placed in areas surrounded by several agricultural crops, especially cotton, soybean, corn and pastures (Table  1). Corn was the only crop presented in all regions.

Statistical analysis
To evaluate the relationship between the abundance of M. latipes and the latitude (Decimal Degrees -DD) used the generalized linear model (GLM) according to Poisson regression with eleven collections points established in the Southern Hemisphere (Table 1). In the same way, as abundance data considers moth count, a GLM Poisson regression was used in order to determine the conjunct influence of meteorological variables on the expected abundance of M. latipes at each collecting points. The analysis includes the estimates and respective significance, and the standard errors of the estimate for each collecting point and a general estimate with all points, except for Londrina, Passo Fundo and Bagé, due to the non-significance of the coefficients of the variables when studied individually. The analysis was performed on R version 3.4.0 (R Development Core Team 2017).

Results
In total, 1,985 moths of M. latipes were collected with greater abundance concentrated in the lower latitudes, in the Amazon and Cerrado biomes. Almost half of the insects (42.11%) were collected in Alto Alegre-RR, followed by Rio Branco-AC (13.55%) and Mojuí dos Campos-PA (11.33%) (Table 2; Figure 1). Moths were found in all sampled locations, most of the year and in 92 collections (63.88%) from the 144 collected. Disregarding the southernmost locations (Bagé, Passo Fundo and Londrina), where it is cold during the winter time, M. latipes were collected in 84 out of 108 events, which corresponds to more than ¾ (77.78%) of the collections.
The monthly occurrence data (Table 2) indicated that, despite occurring in practically the whole year, M. latipes populations varied differently in each location.
Poisson regression analysis indicated for most locations that the conjunct of accumulated monthly precipitation, the monthly averages of minimum and maximum temperature and the monthly average    of relative humidity positively influenced abundance (Table 3). As observed between monthly abundance (Table 2), the relations between the number of moths and meteorological variables varied between locations (Table 3).

Discussion
The occurrence of M. latipes throughout Brazil ( Figure 1) was expected due to the wide distribution previously mentioned in the bibliography (ex. Reinert 1975, Carvalho 1976, Saunders et al. 1998, Bentancourt & Scatoni 2006, Wagner et al. 2011. The simultaneous occurrence of this species in such a wide and diverse territory is correlated with several biological aspects attributed to insects presenting great geographic distribution that includes: great capacity for dispersion and migration (Ferguson et al. 1991 Labrador 1964, Reinert 1975, Cruz & Santos 1983, Ferreira & Parra 1985, Silva & Carvalho 1986, Silva et al. 1991, Piedra & Carrilo 1999, Wagner et al. 2011, and polyphagy, which allows food to be obtained anywhere and at any time. In this last aspect, M. latipes is better classified as an oligophytophage because it develops preferentially in grasses (Ogunwolu & Habeck 1975) despite consuming other vegetables especially at the end of larval development (Hayward 1960, Labrador 1964, Kimball 1965, Silva et al. 1968, Costilla et al. 1973, Biezanko et al. 1974, Kleyla et al. 1979, Pastrana 2004, Formentini et al. 2015. Despite being an oligophagous, M. latipes has in its favor that grasses are vegetables that have a relatively preserved physical and chemical structure throughout evolutionary history (Kellogg 2001). Thus, this determines that M. latipes, like most insects associated with grasses can develop satisfactorily in most species (Tscharntke & Greiler 1995). Moreover, both annual and perennial grasses are found in almost all environments throughout the year, except for closed forest areas, deserts or very cold regions (Strömberg 2011, Dixon et al. 2014). In addition, cultivated grasses often become invasive, having additional amounts of nutrients in their tissues and less physical or chemical defense structures (Tamiru et al. 2015).
This relation between greater abundance and higher temperature is in line with the significance of the negative regression between latitude and abundance found in this study (Figure 2). Indeed, despite the wide range of occurrences in the American continent, the largest number of studies that emphasize the importance of M. latipes as a pest refers to areas located in lower latitudes or that have climates characterized by high temperatures, especially in Central American countries and the Caribbean (e.g. Bodkin 1914, Fennah 1947, Labrador 1964, Capriles & Ferrer 1973, Hseih 1979, Calderón et al. 1981, 1982, Silvain 1984, Silvain & Dauthuille 1985, Gibbs 1990, Jiménez et al. 1997, Teixeira & Townsend 1997, Correia et al. 1999, Sánchez Soto & Ortiz Garcia 1999, Minno & Snyder 2008. Considering the specific area of this study the greatest importance of M. latipes as a pest is highlighted by several studies in hot and humid regions, especially the Amazon (Silva et al. 1994, Teixeira & Townsend 1997, Fazolin et al. 2009), northeastern coast (Mendonça Filho 1972, Costa et al. 1983, Correia et al. 1999) and Southeast of Brazil (Hempel 1914, 1920a, 1920b, Fonseca 1944, Lopes 1955, 1961, Cavalcante 1977, Ferreira 1984, Cruz 1991.
Considering the higher latitudes sampled in this study (Table 2, Figure 1) it is important to note that even in places below the tropical line there are outbreaks with significant production losses, both in the Northern hemisphere (Vickery 1924, Watson 1933, Genung & Allen Jr. 1974, Ogunwolu & Habeck 1975, Reinert 1975, Koehler et al. 1977, Minno & Snyder 2008, and in the southern hemisphere, in Argentina (Costilla et al. 1973, Salvatore & Willink 2004, Acosta et al. 2005, Salvatore et al. 2009) and in Uruguay (Bentancourt & Scatoni 1996). However, the greater occurrence of M. latipes and outbreaks are conditioned to the hottest times of the year. This is due to the fact that, even in high latitudes, in the subtropic, during summer solstice temperatures can be high, conditioning a favorable environment to increasing the development of population, which may cause outbreaks in specific years (Cavalcanti et al. 2009). On the other hand, it should be considered, in addition to the photoperiod, that winter temperatures are close to or below the base development temperature of 13.7°C (Ferreira & Parra 1985). This determines that in addition to prolonging the life cycle, as reported in the Northern Hemisphere, to survive against adverse weather conditions, instars need to develop pupal diapause (to be confirmed in Brazil) or adults must migrate to regions where temperatures are higher, and return when local conditions become favorable to their development (ex. Ferguson et al. 1991, Brou Jr. 2004, Wagner et al. 2011. The numbers presented in this study consist of a small sample represented by the moths caught in the range of the traps covers (estimated at 400m to Spodoptera frugiperda - Vilarinho et al. 2011) at just twelve points in Brazil. These samples represent only adults that survived the weather conditions and all natural enemies present during all stages and collection time. It is also not possible to associate adults with the host plants on which the caterpillars fed and developed. Despite all these limitations, the high number of adults of M. latipes collected in all locations (Figure 1, Table 2) highlights its importance as a key specimes in grass-insect interactions in most of Brazil (e.g. Costa 1944a, 1944b, Fonseca 1944, Pugliese 1954, Lopes 1955, 1961, Queiroz 1965, Mendonça Filho 1972, Cavalcante 1977, Planalsucar 1982, Costa et al. 1983, Ferreira 1984, Ferreira & Parra 1985, Cruz 1991, Silva et al. 1994, Teixeira & Townsend 1997, Correia et al. 1999, Fazolin et al. 2009), as well as in most countries of the American continent (e.g. Dine 1913, Bodkin 1914, Holloway 1933, Watson 1933, Fennah 1947, Dinther 1960, Guagliumi 1962, Labrador 1964, Capriles & Ferrer 1973, Costilla et al. 1973, Genung & Allen Jr. 1974, Ogunwolu & Habek 1975, Koehler et al. 1977, Mahadeo 1977, Hseih 1979, Calderón et al. 1981, 1982, Silvain 1984, Silvain & Dauthuille 1985, Miret 1986, Jiménez et al. 1997, Milán et al. 1990, Portillo et al. 1991, Saunders et al. 1998, Piedra & Carrilo 1999, Páliz-Sánchez & Mendoza-Mora 1999, Sánchez Soto & Ortiz García 1999, Pitre et al. 1999, Vergara et al. 2001, Brou Jr. 2004, Salvatore & Willink 2004, Acosta et al. 2005, Marquez 2013). Regarding the fact that it is one of the most predominant specimes, it is important to consider its role in natural ecosystems, especially in agroecosystems where there is a greater proportion or intensification of grass planting, including grains, forages, pastures and sugar cane (e.g. Labrador 1964, Koehler et al. 1977, Calderón et al. 1981, 1982, Costa et al. 1983, Cruz & Santos 1983, Ferreira 1984, Silvain 1984, Silvain & Dauthuille 1985, Miret 1986, Silva & Carvalho 1986, Gibbs 1990, Milán et al. 1990, Cruz 1991, Jiménez et al. 1997, Teixeira & Townsend 1997, Páliz-Sánchez & Mendonza-Mora 1999, Pitre et al. 1999, Vergara et al. 2001, Acosta et al. 2005, Salvatore et al. 2009, Marquez 2013, Hickel et al. 2018. Among the roles to be considered for this species, it is also considered a primary consumer, nutrient cycling promoter, food source for pests (including insects, birds and mammals), parasitoids and pathogens (Wagner et al. 2011).
In relation to the natural enemy organisms of M. latipes, there are studies about the relationship of a countless number of species associated with their natural biological control (predators, parasitoids and pathogens), in different stages of development, in different countries of the American Continent (e.g. Sauer 1946, Silva et al. 1968, Lopes 1969, Gonçalves & Gonçalves 1974a, 1974b, Genung et al. 1976, Guimarães 1977, De Santis 1979, 1989, Lourenção et al. 1982, Collins & Watson 1983, King & Saunders 1984, Hall 1985, Santos 1989, Rogers et al. 1990a, 1990b, Galán & Rodríguez 1991, Cave 1992, Rogers & Marti Jr. 1993, Whitaker Jr. et al. 2007, Rolfe et al. 2014. These studies mention that the action of several natural enemies is important when analyzing the abundance data of M. latipes in any area of its distribution. As shown for other owlet moths (Pereira et al. 2018), their population levels are maintained, at least most of the time, by the action of natural enemies. This might be related to the different population levels, between locations and in different months presented in this study (Table 2).
In relation to ecological balance promoted by the association and the presence of natural enemies, it is important to note that throughout the American continent M. latipes occurs in conjunction with other owlet moths associated with grasses, including congeneric species (Babayan et al. 1975, Ogunwolu & Habek 1975, Koehler et al. 1977, Brou Jr. 2004) and, specially, S. frugiperda (J.E. Smith) (e.g. Fonseca 1944, Pugliese 1954, Lopes 1955, 1961, Guagliumi 1962, Queiroz 1965, Mahadeo 1977, Hseih 1979, Calderón et al. 1981, Costa et al. 1983, Silvain 1984, Silvain & Dauthuille 1985, Portillo et al. 1991, Páliz-Sánchez & Mendoza-Mora 1999, Pitre et al. 1999, Sánchez Soto & Ortiz Garcia 1999, Fazolin et al. 2009 ) forming species complexes. Spodoptera frugiperda is a polyphagous species (Montezano et al. 2018) with high biotic potential (Montezano et al. 2019a(Montezano et al. , 2019b and, as in this study (Table 2, fig. 1) it was collected in all the locations presented here (Piovesan et al. 2018). It is important that M. latipes and other owlet moths, including S. frugiperda share the same predators, pathogens, also egg, larvae and pupae parasitoids (Silva et al. 1968, Rogers & Marti Jr. 1993, Camera et al. 2010. This determines that the presence of M. latipes, even in low populations, allows the maintenance of populations of different groups of natural enemies in natural ecosystems and agroecosystems. Thus, the occurrence of immature M. latipes allows the maintenance of a wide range of natural enemies, it is essential for the maintenance of natural biological control over time, for the entire species complex.
The significant relationship between the abundance of M. latipes with at least one of the meteorological variables (Table 3), in practically all Brazilian territory except in the three most southern locations ( Figure  1) reinforces the strong association between population variations and climatic conditions mentioned in several studies (e.g. Bertels 1970, Genung & Allen Jr. 1974, Babayan et al. 1975, Calderón et al. 1981, Gibbs 1990, Jiménez et al. 1997, Pitre et al. 1999, Salvatore & Willink 2004, Fazolin et al. 2009, Hickel et al. 2018. The relationship between population variations and climatic conditions, is evidenced by the large number of moths collected in rainy months (July, August and September), in Alto Alegre, RR, located in the Northern Hemisphere (Table 2) while all the other places are located in the Southern Hemisphere, these same months correspond to winter time (dry or cold), with very low population levels. Indeed, studies always relate the highest population levels with warm months, preferably during the rainy season in the Northern Hemisphere (Bodkin 1914, Vickery 1924, Watson 1933, Fennah 1947, Capriles & Ferrer 1973, Calderón et al. 1981, Gibbs 1990, Minno & Snyder 2008 as in the Southern Hemisphere (Lopes 1955, Costilla et al. 1973, Carvalho 1976, Lourenção et al. 1982, Teixeira & Townsend 1997, Correia et al. 1999, Salvatore & Willink 2004, Acosta et al. 2005.
Regarding the different numbers of moths collected each month, in each location (Table 2) besides the climatic characteristics (Cavalcanti et al. 2009), biogeographic and phytophysiognomic variations should also be considered (Heppner 1991). Although M. latipes is an oligophytophagous species with a preference for grasses (ex. Ogunwolu & Habeck 1975, Wagner et al. 2011, in each location the moths were able to choose to lay eggs on plants arranged as a space-time mosaic containing different native and/or cultivated species that served as food for their larvae.
The M. latipes abundance spatial variations described in this study, combined with the knowledge of its great dispersion capacity, including migration (ex. Barth 1958, Ferguson et al. 1991, Wagner et al. 2011, Alves et al. 2019) point to the need for studies related to the molecular characterization of populations in order to allow assessments of local populations, migration routes and/or gene flow as done for other owlet moths (e.g. Palma et al. 2015, Nagoshi et al. 2017). This information is extremely important to assess whether the occurrence of population outbreaks of this species is related only to the fast reproduction of local populations or whether it involves dispersion or migration events. Thus, it should be noted that even in Southmost areas, where the abundance of M. latipes was extremely low, there are several registers of its occurrence (ex. Tarragó et al. 1975, Link 1977, Specht & Corseuil 2002, Specht et al. 2004, Zenker et al. 2010 indicating that the species was present in more than 50% of weekly collections between July 1994 and June 1995 (Specht & Corseuil, 2002). Furthermore, further to the South, Bentancourt & Scatoni (2006) relate sporadic population outbreaks of this species in Uruguay, noting that, even at greater latitudes, the occurence of this species is relatively constant with increases in population linked to favorable conditions to its development. Especially in these places it is questioned whether the presence of the species is due to a local population or as a result of migration as described for the Northern Hemisphere (Brou Jr. 2004, Wagner et al. 2011. The results of this study as well as most previous publications (ex. Carvalho 1976, Lourenção et al. 1982, Fazolin et al. 2009, Bentancourt & Scatoni 1996, Saunders et al. 1998, Wagner et al. 2011 indicates that M. latipes, besides having a wide distribution, it has low population levels during most of the year, with sporadic population outbreaks during favorable weather conditions, food availability and inadequate cultural management. Therefore, it must be considered that agricultural occupation has modified most of the ecosystems where the effect of seasonal variations on native host plants is minimized by cultivating grasses that serve as alternative hosts more resistant to drought in the savanna and to the cold in greater latitudes. These plants can serve as a green bridge between the most favorable seasons to the development of M. latipes and other insects (Favetti et al. 2017). Considering grasses as host plants, it must be taken into consideration that M. latipes has food available both in open native environments and in the most diverse combinations of forage, grain and sugar production. In addition to these plants directly related to production, other crops should be considered for soil protection and biomass production to be incorporated in crop rotation systems (Dias et al. 2016, Favetti et al. 2017, integrated crop-livestock systems (Vilela et al. 2011) and even when introduced grasses become pests occupying most ecosystems for most of the year (Minno & Snyder 2008).
Even though this study shows an inverse relationship between latitude and M. latipes abundance along with other meteorological variables, it should be considered that abiotic factors are conditional to species development, and not necessarily associated with the decrease of abundance. Therefore, additional hypotheses need to be tested considering specific abundance and environmental factors. One example is the high abundance of M. latipes in tropical areas, it can be related to favorable conditions, while that in subtropical regions only summer months present favorable conditions. On the other hand, areas presenting favorable conditions all year long also provide a high number of natural enemies. Thus, due to the large number of variables related to M. latipes itself (which includes developmental biology in different conditions, the ability to diapause, migrate, defend against natural enemies) and biotic factors associated with each location (availability of different host plants native or cultivated, presence and abundance of natural enemies, interspecific competition) cause the associations established between population levels, latitude and environmental factors to be explored continuously. A better understanding of these associations will allow a more accurate understanding of the effects of local environmental variations and global climate changes on insect populations, pests or not.

Authors Contributions
Vander C. M. Claudino: Substantial contribution in the concept and design of the study; contribution to data collection; data analysis and interpretation; manuscript preparation and critical revision, adding intelectual content. Alexandre Specht: Substantial contribution in the concept and design of the study; contribution to data collection; data analysis and interpretation; manuscript preparation and critical revision, adding intelectual content.
Elisângela G. Fidelis: Contribution to data collection; data analysis and interpretation; manuscript preparation and critical revision.
Vânia F. Roque-Specht: Contribution to data collection; data analysis and interpretation; manuscript preparation and critical revision. Débora G. Montezano: Contribution to data analysis and interpretation; manuscript preparation and critical revision, adding intelectual content.
Pedro R. Martins: Contribution to data analysis and interpretation; manuscript preparation and critical revision; Fernando A.M. Silva: Contribution to data collection; data analysis and interpretation; manuscript preparation and critical revision.
Juaci V. Malaquias: Substantial contribution in the concept and design of the study; contribution to data analysis and interpretation; manuscript preparation and critical revision.