Phorid flies are small-sized, highly diverse insects, found in Neotropical regions with varying larval lifestyles (Disney 1994). Many species of this family parasitize bees (Core et al. 2012), termites (Neoh & Lee 2010), and leaf-cutting ant pests of several crops (Della Lucia et al. 2014; Farder-Gomes et al. 2016). Leaf-cutting ants are managed principally with insecticidal baits (Zanetti et al. 2003; Montoya-Lerma et al. 2012). Increasing global awareness regarding sustainable cultivation and pest control methods that are safer for the environment (Bale et al. 2008; Zheng et al. 2017) has driven the search for alternative methods to manage leaf-cutting ants.

Leaf-cutting ant parasitoids in the family Phoridae are specialists or generalists, coexisting in the environment and attacking ants of different head sizes (Bragança & Medeiros 2006). Additionally, these parasitoids can reduce plant material transported into the nests and ant traffic on trails (Martinez et al. 2014; Guillade & Folgarait 2015). Females of these insects lay an egg into the body of each ant with the larva subsequently feeding on host tissues (Bragança & Medeiros 2006; Farder-Gomes et al. 2016). Phorid flies have an evolutionary relationship with host ants, and require them as the only food source for their entire development. Therefore, fly richness correlates with ant richness (Elizalde & Folgarait 2010).

Landscape structure is important for parasitoid-host interaction (Thies et al. 2005; Liu et al. 2016b), and fragmentation and loss of environmental complexity may decrease natural enemy abundance (Elizalde & Queiroz 2013; Zhao et al. 2015). Highly diversified landscapes may provide multiple resources, such as nest sites, temporary refuges, and food (Alignier et al. 2014; Liu et al. 2016b), whereas agricultural landscapes, e.g., pasture and field crops, have fewer resources due to reduced habitat complexity (Kleijn et al. 2009; Thies et al. 2w011).

Changes in landscape structure also modifies microclimate, thereby affecting insect populations (Alignier et al. 2014; Aranda & Graciolli 2015). Climatic variables, such as temperature and humidity, influence the abundance, activity period, diversity, distribution, and reproduction of insects (Folgarait et al. 2005, 2007; Aranda & Graciolli 2015). Preferred climatic conditions differ between parasitoid species (Bragança & Medeiros 2006; Reese & Philpott 2012). For example, Pseudacteon laciniosus Brown (Diptera: Phoridae) was found to be more abundant in the wet season than in the dry, whereas Pseudacteon planidorsalis Brown (Diptera: Phoridae) showed the opposite pattern (Reese & Philpott 2012). Therefore, knowledge of parasitoid seasonal patterns is important for success of biological control. The objective of our study was to evaluate the parasitism of the leaf-cutting ant Atta sexdens Linnaeus (Hymenoptera: Formicidae) by the phorids Apocephalus attophilus Borgmeier and Eibesfeldtphora tonhascai Brown (both Diptera: Phoridae) across seasons throughout a yr in a Brazilian Cerrado-Atlantic Forest ecotone, and compare their ant parasitism in a semi-deciduous seasonal forest fragment and urban area.

Materials and Methods

Results

Parasitism of ants by phorid species was significantly influenced by season (χ² = 74.6; df = 3; P < 0.05). The number of ants parasitized by A. attophilus was higher in the winter (χ² = 33.3; df = 1; P < 0.05), and those by E. tonhascai in the spring (χ² = 27.6; df = 1; P < 0.05) (Fig. 1). However, the number of ants parasitized by both parasitoids in summer (χ² = 0.7; df = 1; P > 0.05) and fall (χ² = 7.22; df = 1; P > 0.05) was similar (Fig. 1).

The number of ants parasitized by A. attophilus was negatively correlated with temperature (r = –0.722; df = 9; P < 0.05), but not with relative humidity (r = 0.150; df = 9; P > 0.05) (Fig. 2). The number of ants parasitized by E. tonhascai did not correlate with temperature (r = 0.040; df = 9; P > 0.05) or relative humidity (r = 0.243; df = 9; P > 0.05). In addition, parasitism by A. attophilus and E. tonhascai was significantly greater in the semi-deciduous (364 ants parasitized) (χ² = 234.4; df = 1; P < 0.05) than the urban landscape (32 ants parasitized).

Fig. 1.

Number of leaf-cutting ants Atta sexdens parasitized by Apocephalus attophilus and Eibesfeldtphora tonhascai in a Brazilian Cerrado-Atlantic Forest ecotone. The seasons are as follows: spring (Sep–Nov), summer (Dec–Feb), fall (Mar–May), and winter (Jun–Aug).

Discussion

We found that an increase in number of leaf-cutting ants parasitized by A. attophilus occurred with decreasing temperature, whereas the highest parasitism by this species appeared during winter, which indicated this species has a greater tolerance to low temperatures, similar to that reported for the phorids Pseudacteon borgmeieri Schmitz (Diptera: Phoridae) (Folgarait et al. 2003) and Lucianaphora folgaraitae Disney (Diptera: Phoridae) (Elizalde et al. 2018). A negative correlation between parasitism by A. attophilus and temperature also was reported from Viçosa, Minas Gerais, Brazil (Martins 2015). Phorid flies commonly disappear during colder mo (Folgarait et al. 2003). Thus, a preference for lower temperatures may benefit A. attophilus by allowing it to explore hosts during periods where few parasitoids of other species may be present. In addition, results of our work showed that parasitism rates of A. attophilus on A. sexdens were not correlated with the relative humidity; conversely, other studies have reported an increase in parasitism by this species in the hottest and rainy seasons (Arruda et al. 2018; Farder-Gomes et al. 2018). This suggests that A. attophilus possesses a wide range of tolerance for some environmental conditions. On the other hand, greater leaf-cutter ant parasitism during the spring by E. tonhascai suggested better adaptation of this species to the climatic conditions of that season. Differences in the number of ants parasitized between seasons may allow for temporal segregation of parasitoid species throughout the yr with reduced interspecific competition (Guillade & Folgarait 2011; Arruda et al. 2018; Elizalde et al. 2018).

Fig. 2.

Correlation between temperature and the number of leaf-cutting ants Atta sexdens parasitized by Apocephalus attophilus (r = –0.722; df = 9; P < 0.05).

As in our study, lack of correlation between E. tonhascai parasitism with either temperature or humidity may indicate that this parasitoid is more resistant to changes in climatic conditions. Apocephalus attophilus can parasitize leaf-cutting ants during the d and night, but E. tonhascai is active only during the d (Bragança et al. 2008). We hypothesize that light intensity may be an important determinant of abundance and parasitism, similar to that reported for Pseudacteon litoralis Borgmeier (Diptera: Phoridae) attacking Solenopsis saevissima (Smith) (Hymenoptera: Formicidae) in Rio Claro, São Paulo, Brazil (Pesquero et al. 1996), but this hypothesis would need further investigation. The highest number of ants parasitized in the semi-deciduous forest fragment may be due to the landscape diversity of this area with alternative sites for feeding and refuge, enhancing parasitoid populations (Pozzebon et al. 2015; Liu et al. 2016b; Damien et al. 2017). This agrees with the higher number of ants parasitized by E. tonhascai, Eibesfeldtphora bragancai Brown (Diptera: Phoridae), and A. attophilus in a Cerrado fragment containing Eucalyptus sp. (Myrtaceae), showing that these parasitoids are sensitive to changes in landscape composition (Pesquero et al. 2010). Similarly, high landscape diversity increased the Trichogramma chilonis Ishii (Hymenoptera: Trichogrammatidae) parasitism rates on Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) eggs (Liu et al. 2016a). The failure of the parasitoid Pseudacteon curvatus Borgmeier (Diptera: Phoridae) to establish itself in the states of Florida and Tennessee, USA, was attributed to insufficient vegetation cover and harsh environmental conditions (Graham et al. 2003). Therefore, the maintenance of native vegetation fragments is important to enhance natural enemy populations.

In summary, our study provides important ecological information about the interaction between the leaf-cutting ant A. sexdens and its parasitoids. Generally, the parasitism by phorid flies varied with season; A. attophilus parasitized more ants in winter and E. tonhascai in spring. Parasitism by A. attophilus was negatively correlated with temperature, and corroborates the preference of this species for lower temperatures. In addition, reduction of landscape complexity in urban areas may decrease the parasitism by parasitoid species. Therefore, biotic and abiotic factors that influence the population dynamics of phorids in the field must be understood to design mass rearing and releasing protocols for these parasitoids.