Luciana Elizalde

Behavioral Strategies of Phorid Parasitoids and Responses of Their Hosts, the Leaf-Cutting Ants

Abstract Host-searching and oviposition behaviors of parasitoids, and defensive responses of the hosts, are fundamental in shaping the ecology of host-parasitoid interactions. In order to uncover key behavioral features for the little known interactions between phorid parasitoids (Diptera: Phoridae) and their leaf-cutting ant hosts (Formicidae: Attini), host-related behavioral strategies (i.e., host searching and oviposition) for 13 phorid species, and host defensive responses (i.e., hitchhikers and particular body postures) for 11 ant species, were studied. Data was collected at 14 localities, one of them characterized by its high species richness for this host-parasitoid system. Phorid species showed both great variation and specificity in attacking behaviors. Some chose their hosts using either an ambush or an actively searching strategy, while some species attacked ants on different body parts, and specialized on ants performing different tasks, such as when ants were foraging, removing wastes to refuse piles, or repairing the nest. Combining all the behaviors recorded, most phorid species differed in performance in at least one, making it possible to recognize species in the field through their behavior. Phorid species that attacked hosts with greater activity levels showed overall higher attack rates, although there was no significant correlation between attack rates by most phorid species and ant activity outside the nest while parasitoids were attacking. The presence of phorids was a significant determinant for the presence of defensive behaviors by the ants. Although ant species varied in the incidence levels of these defensive behaviors, most ant species reacted against different phorids by utilizing similar behaviors, in contrast to what parasitoids do. General features of the observed phorid-ant interactions were parasitoid specialization and corresponding high interspecific variation in their behaviors, while their hosts showed generalized responses to attacks with high intraspecific variation. Behavioral patterns as well as specific features of these ant-parasitoid interactions are described, and their ecological importance discussed.

To be or not to be faithful: flexible fidelity to foraging trails in the leaf-cutting ant Acromyrmex lobicornis

1. Ants using trails to forage have to select between two alternative routes at bifurcations, using two, potentially conflicting, sources of information to make their decision: individual experience to return to a previous successful foraging site (i.e. fidelity) and ant traffic. In the field, we investigated which of these two types of information individuals of the leaf‐cutting ant Acromyrmex lobicornis Emery use to decide which foraging route to take.

Social life and sanitary risks: evolutionary and current ecological conditions determine waste management in leaf-cutting ants.

Adequate waste management is vital for the success of social life, because waste accumulation increases sanitary risks in dense societies. We explored why different leaf-cutting ants (LCA) species locate their waste in internal nest chambers or external piles, including ecological context and accounting for phylogenetic relations. We propose that waste location depends on whether the environmental conditions enhance or reduce the risk of infection. We obtained the geographical range, habitat and refuse location of LCA from published literature, and experimentally determined whether pathogens on ant waste survived to the high soil temperatures typical of xeric habitats. The habitat of the LCA determined waste location after phylogenetic correction: species with external waste piles mainly occur in xeric environments, whereas those with internal waste chambers mainly inhabit more humid habitats. The ancestral reconstruction suggests that dumping waste externally is less derived than digging waste nest chambers. Empirical results showed that high soil surface temperatures reduce pathogen prevalence from LCA waste. We proposed that LCA living in environments unfavourable for pathogens (i.e. xeric habitats) avoid digging costs by dumping the refuse above ground. Conversely, in environments suitable for pathogens, LCA species prevent the spread of diseases by storing waste underground, presumably, a behaviour that contributed to the colonization of humid habitats. These results highlight the adaptation of organisms to the hygienic challenges of social living, and illustrate how sanitary behaviours can result from a combination of evolutionary history and current environmental conditions.

Biological attributes of Argentinian phorid parasitoids (Insecta: Diptera: Phoridae) of leaf-cutting ants, Acromyrmex and Atta

Little is known about the natural history of phorid parasitoids of leaf-cutting ants, an important pest in the Neotropics. This is particularly so for phorids attacking Acromyrmex species. We searched for phorids ovipositing and reared them from ants collected in the field. We found that these phorids formed a guild. Acromyrmex phorids selected ants from all sizes available outside the nests, whereas Atta phorids did not parasitize the smallest workers and soldiers. Maximum parasitism by phorids was 12% for Acromyrmex and 35% for Atta hosts, percentages higher than any reported previously. Some phorid species coexisting in a site showed differences in developmental times. Only 1.1% of phorids collected over hosts were males; however, as the male : female ratios from parasitoid rearing did not differ from one, mating is suspected to occur elsewhere. Our results helped to increase the knowledge of the phorids of leaf-cutters, and highlighted their potential use for the biocontrol of these ants.

Parasitoids of the endangered leafcutter ant Atta robusta Borgmeier in urban and natural areas

Parasitoids of the endangered leafcutter ant Atta robusta Borgmeier in urban and natural areas. Hosts of parasitoids in urban areas may suffer from a double threat of habitat destruction by urbanization and parasitism pressure. Moreover, the parasitoids themselves might be at risk if they are specialists. Here, we studied whether Atta robusta (Hymenoptera, Formicidae), which is on the red list of Brazilian threatened species, suffers from higher parasitism pressure in an urban area compared to a natural one. In addition, we determined whether their specialist parasitoids, Eibesfeldtphora breviloba and Myrmosicarius exrobusta (Diptera, Phoridae), are in risk and evaluated whether they are influenced by habitat structure, temperature, humidity, ant traffic, and time of the day. The study was carried out in an urban park and in a natural protected area in the city of Rio de Janeiro. In each site we chose an open area and a closed area (forest) and sampled nine nests in each area. We found that parasitism pressure was similar in urban and natural areas, with the same two parasitoid species present in both areas. The main difference was related to habitat structure, since M. exrobusta was mainly present in open areas while E. breviloba was almost exclusively found in closed areas. Myrmosicarius exrobusta was not present during the hottest midday times, and its abundance was negatively correlated to vapor pressure deficit. These results suggest that green areas can be an important component in efforts to conserve diversity in urban areas. However, the complexity of the habitats in those areas is a fundamental issue in designing urban parks.

Spatial and temporal variation in host–parasitoid interactions: leafcutter ant hosts and their phorid parasitoids

1. Parasitoid–host interactions are important components of ecological communities. Although parasitoid–host interactions are strongly shaped by evolutionary history, the abundance of both the parasitoid and the host may have a role in determining the nature of the interaction once phylogenetic relationships are considered.

Collective Response of Leaf-Cutting Ants to the Effects of Wind on Foraging Activity

One advantage of sociality is to mitigate environmental restrictions through collective behavior. Here we document a colony-level response of leaf-cutting ants to wind, an environmental factor that impedes foraging. Given that larger ants adhere more strongly to the substrate, increasing forager size in windy conditions should reduce the negative effect of wind. We tested this idea for Acromyrmex lobicornis in windy regions of Patagonia. We examined (1) whether the fraction of larger ants versus smaller ants increased in windy conditions and (2) whether the effect of wind on the ants’ movement was lower for larger ants. The size-frequency distribution of foragers was skewed more toward larger ants in nature under more windy conditions. Under windy conditions in the field, the mobility of smaller ants was more reduced than that of larger ants. The change toward larger foragers in windy conditions reduced the negative effect of wind by 32%, illustrating how a social organism can collectively mitigate the adverse effects of the environment.

A Breath of Fresh Air in Foraging Theory: The Importance of Wind for Food Size Selection in a Central-Place Forager

Empirical data about food size carried by central-place foragers do not often fit with the optimum predicted by classical foraging theory. Traditionally, biotic constraints such as predation risk and competition have been proposed to explain this inconsistency, leaving aside the possible role of abiotic factors. Here we documented how wind affects the load size of a central-place forager (leaf-cutting ants) through a mathematical model including the whole foraging process. The model showed that as wind speed at ground level increased from 0 to 2 km/h, load size decreased from 91 to 30 mm2, a prediction that agreed with empirical data from windy zones, highlighting the relevance of considering abiotic factors to predict foraging behavior. Furthermore, wind reduced the range of load sizes that workers should select to maintain a similar rate of food intake and decreased the foraging rate by ∼70% when wind speed increased 1 km/h. These results suggest that wind could reduce the fitness of colonies and limit the geographic distribution of leaf-cutting ants. The developed model offers a complementary explanation for why load size in central-place foragers may not fit theoretical predictions and could serve as a basis to study the effects of other abiotic factors that influence foraging.

La leña como vía para la introducción de insectos. ¿Cuáles son los riesgos de las invasiones de hormigas en la Patagonia?

Firewood can act as a long-distance dispersal vector for wood-infesting insects both within and among countries. Recently, we detected the alien carpenter ant Camponotus mus in firewood transported from central Argentina to Patagonia. This species generates significant economic losses in its native range and has invader potential. Moreover, global warming and the increasing anthropogenic disturbance in Patagonian ecosystems make them highly susceptible to insect invasions. This is especially alarming considering the current lack of sanitary controls of incoming goods into the region. To prevent insect introductions via firewood, it is crucial to implement a joint effort among the scientific community, control organisms, government and end user.https://doi.org/10.25260/EA.17.27.2.0.478