Papers by Roberto da Silva Camargo
Figure 8. Nest 3a (A–E). General view of the subnests of colony 3 of Acromyrmex balzani. Scale: 4... more Figure 8. Nest 3a (A–E). General view of the subnests of colony 3 of Acromyrmex balzani. Scale: 40 cm.
Figure 9. Nests 4 and 5a. (A) General view of subnest 1, nest 4; (B) general view of subnest 1, n... more Figure 9. Nests 4 and 5a. (A) General view of subnest 1, nest 4; (B) general view of subnest 1, nest 5; (C) general view of subnest 2, nest 5; (D) general view of subnest 3, nest 5. Scale: 40 cm.

Emirates Journal of Food and Agriculture, 2020
Asclepias curassavica L. plant is toxic for vertebrates, and little is known about its effects on... more Asclepias curassavica L. plant is toxic for vertebrates, and little is known about its effects on invertebrates, as well as whether its secondary metabolites have an influence on food preference and survival of insects. Thus, a study was conducted to verify the action of A. curassavica on Spodoptera frugiperda J.E.Smith. The plants were collected, dried and ground to compose a crude ethanolic extract. Food tests were carried out with and without opportunity of choice, using corn leaf discs immersed in the extract at concentrations of 1%, 2% and 4%, for assessment of food consumption (g) and preference index. Later, the extract was topically applied on second- and fifth-instar caterpillars, at concentrations of 1%, 2%, 4% and 6%, in order to observe its effect on survival. In parallel, analysis was conducted to verify the presence and measure the amount of total polyphenols and flavonoids in the extract. There was contact action between the extract and second-instar caterpillars at a...
Figure 1. The clustering of males and females of Attacobious attarum.
Figure 2. Behavioural repertoire of Attacobius attarum for dispersion in Atta sexdens: (A) female... more Figure 2. Behavioural repertoire of Attacobius attarum for dispersion in Atta sexdens: (A) female spider in bunch of loose soil from the nest of leaf-cutting ant, in search of a winged male; (B) approximation of female of leaf-cutting ants before the mating flight; (C) climbing of the spider to the dorsal region of winged female; (D) spider detail on the back of the queen; (E, F) winged male and female of leaf-cutting ants are preparing for the mating flight with phoretic spiders on their pronota.

Insects, 2020
In 2009, sulfluramid, the main ingredient in toxic baits for leaf-cutting ant control, was includ... more In 2009, sulfluramid, the main ingredient in toxic baits for leaf-cutting ant control, was included in Annex B of the Stockholm Convention on Persistent Organic Pollutants. This resulted in interest in the use of entomopathogenic fungi such as Beauveria bassiana and Trichoderma harzianum for leaf-cutting ant control. The efficiency of these fungi in controlling these insects and the way that ants react individually or in group to the biological risks posed by these fungi is poorly understood. For this reason, we assessed the effects of B. bassiana and T. harzianum on Atta sexdens rubropilosa larvae, pupae and workers. Moreover, we investigated whether the number of contaminated individuals within a group has an influence in controlling the spread of fungi among workers. We found that the fungus T. harzianum showed high pathogenicity against A. sexdens rubropilosa larvae and pupae, leading to faster mortality and a survival rates. On the other hand, the fungus B. bassiana was respons...

Pest Management Science, 2021
BACKGROUND Leaf-cutting ants (LCA) of the genera Atta and Acromyrmex (Hymenoptera: Formicidae) ar... more BACKGROUND Leaf-cutting ants (LCA) of the genera Atta and Acromyrmex (Hymenoptera: Formicidae) are important pests in forest plantations, agriculture and livestock. Toxic baits with the active ingredients fipronil or sulfluramid are the main method to controlling these insects. The dispersion of insecticides between the members of colonies during the control using toxic baits is not well understood. The objective was to determine if self-grooming, allogrooming or touching behavior among the ant Atta sexdens (Hymenoptera: Formicidae) workers disperse the insecticides fipronil and sulfluramid among members of the colony. The insecticides were topically applied on groups of the ant A. sexdens workers and the social interactions between them with and without insecticide and the group mortality evaluated. RESULTS A behavioral analysis showed increasing interaction as the numbers of individuals increased, with touches between workers being the most frequent behavior. The frequency of behaviors observed in groups with sulfluramid was higher compared to those with fipronil. The mortality of groups with fipronil is practically twice higher compared to those with sulfluramid. Probably, the insecticides are dispersed due to excessive touches among workers and subsequent self-grooming and allogrooming. CONCLUSION These behaviors were responsible for the rapid dispersion of the insecticides among members of the colony. The corroboration of the hypothesis that social interactions contaminate nestmates is a model for future studies on contamination of ant workers with active insecticide ingredients. This article is protected by copyright. All rights reserved.

Sociobiology, 2019
Chemical control of leaf-cutting ants is widely used, but alternative control with toxic plant ex... more Chemical control of leaf-cutting ants is widely used, but alternative control with toxic plant extracts is promising. Substances with insecticidal potential extracted from plants have numerous ecological advantages. This study evaluated the insecticidal and/or fungicidal potential of the plants Asclepias curassavica (tropical milkweed), Rosmarinus officinalis L. (Lamiaceae) (rosemary) and Equisetum spp. (horsetail) for control of the leaf-cutting ant Atta sexdens rubropilosa Forel, 1908 (Hymenoptera: Formicidae). Forty laboratory-reared colonies of Atta sexdens rubropilosa were used. The plants were collected, dried out in a circulating air oven for 48 hours, ground, and macerated in 96o ethanol until exhaustion. After filtration, the products were evaporated under reduced pressure to obtain the ethanolic extracts. Acceptance of the reagent, topical application of the extracts, and application of baits containing 4% of the plant extracts were tested. The results showed that all plan...

The Complex World of Ants, 2018
The attini tribe comprises fungusgrowing ants, such as the basal Apterostigma and other more spec... more The attini tribe comprises fungusgrowing ants, such as the basal Apterostigma and other more specialized genera, including the higher attine and the ones that cut the fresh plant tissue (Atta and Acromyrmex), maintaining an obligatory mutualistic relation with the fungus Leucoagaricus gongylophorus, which serves as a food source for the ants. Leaf-cutter ants are considered agriculture pests and populate the soil, a rich environment, especially due to the presence of several microorganisms. Some of these microorganisms are natural enemies that may cause epizootics (quickly spreading opportunistic diseases). Such defence strategies include polyethism, that is, division of labor among the individuals. The older ants take on the responsibility of foraging, as their integument is harder and heavily sclerotized, serving as a protective barrier against pathogens (including bacteria and antagonistic fungi). The younger ants, whose metapleural glands synthetize important secretions to eliminate and control microorganisms that could attack the colony fungus garden and the immature (larvae and pupae), remain inside the colony cultivating symbiont fungi. The sum of the survival strategies of ants in general, including social immunity and nest-cleaning behavior, represents a barrier for the application of biological control programs, mainly microbial ones.

Sociobiology, 2020
Leaf-cutting ants are widely distributed in Brazil, particularly species of the genus Atta. We th... more Leaf-cutting ants are widely distributed in Brazil, particularly species of the genus Atta. We therefore described the occurrence of leaf-cutting and grass-cutting ant species of the genus Atta. Five routes comprising some of the main highways in the South, Southeast, Center-West, and North of Brazil were sampled, in addition to ants received from other 82 municipalities, composing 300 municipalities sampled. This is the first comprehensive study of Atta in Brazil. The following species were found: A. laevigata, A. capiguara, A. sexdens rubropilosa, A. sexdens piriventris, A. sexdens sexdens and A. cephalotes. Atta laevigata and A. capiguara were the species present in the largest number of the Brazilian municipalities sampled. Atta laevigata assumed the position of species of greatest occurrence in the Brazilian territory. Atta sexdens piriventris was only recorded in the southern region of Brazil. Atta bisphaerica presented lower expansion than A. capiguara. Atta cephalotes and At...

Revista Brasileira de Entomologia, 2018
Leaf-cutting ants live symbiotically with a fungus that they cultivate on the plant leaves that t... more Leaf-cutting ants live symbiotically with a fungus that they cultivate on the plant leaves that they cut. The innumerous studies on the plant selection mechanism used by leaf-cutting ants show the researchers' interest in this issue. Many classical studies propose that plants are selected according to the fungus garden nutritional needs and the absence of potentially harmful substances. This hypothesis is corroborated by behavioral experiments using cycloheximide (fungicide) with citric pulp or forage plants greatly accepted by leaf-cutting ants. According to this hypothesis, under the action of a fungicide, the fungus emits an allomone that informs worker ants that some food is inadequate to its growth. Although some authors state that the cycloheximide "fungicide" used is specific and non toxic to ants, our findings are distinct. In our study, various concentrations of cycloheximide were administered orally to leaf-cutting worker ants in a citric pulp paste diet. After the ingestion period, the ants were isolated and offered the symbiotic fungus for 21 days and the mortality rate was evaluated. As expected, the treatment with 0.01% cycloheximide showed a low mortality rate (8.86%). At 0.1%, the mortality rate was mild (27.85%), and treatment with 1% cycloheximide resulted in moderate mortality (45.57%). In contrast, the positive control with 0.1% sulfluramid showed a high mortality rate (91.14%). Therefore, we concluded that the ingestion of high concentrations of cycloheximide results in a moderate mortality rate in leaf-cutting worker ants.

Revista Brasileira de Entomologia, 2018
During foraging, worker ants are known for making use of many information sources to guide themse... more During foraging, worker ants are known for making use of many information sources to guide themselves in external environments, especially individual (memory) and social (trail pheromone) information. Both kinds of information act in a synergic way, keeping the foraging process efficient and organized. However, when social and individual information is conflicting face a trail bifurcation, it is necessary to establish a hierarchical order so prioritizing one of them. This study aims to verify which information (social or individual) is prioritized by Acromyrmex subterraneus workers when facing a bifurcation in a Y-trail system. Only one branch of the Y-trail leads to food resource and it had a section covered by filter paper where trail pheromone was deposited by workers. Pheromone deposition was here estimated by worker flow. After an individually marked forager (target-worker) made 1, 3 or 5 trips to the food resource, the filter paper was transferred to the branch which did not lead to the food. The time spent by target workers on branch selection and their right choice (branch with food) frequency were registered. Regardless of the target worker's previous trips to the resource, right choice frequency stood over 70%. In addition, the number of previous trips did not influence the time spent on decision making. However, the higher the flow of workers, the longer the time spent on decision making. By simulating a situation with conflicting information, it was possible to verify that a hierarchical order is established by A. subterraneus, which prioritized individual information (memory).

Tropical Zoology, 2019
The success of incipient colonies of leaf-cutter ants depends on multiple factors such as tempera... more The success of incipient colonies of leaf-cutter ants depends on multiple factors such as temperature, humidity, soil type, the queen's fertility and vigor, frequency of harmful microfungi, among others. Based on this observation, three factors related to Atta sexdens were characterized: (1) initial nest morphology (depth and volume); (2) queen oviposition rate; and (3) prevalence of Escovopsis (parasitic fungus) and other fungi in incipient colonies. Our observation showed a variation in chamber dimensions and volume, indicating differences in colony development rates. The oviposition rate of queens from nests of the same age showed a difference among queens. About microfungi prevalence, it was found that many are potentially deleterious. In particular, the parasite Escovopsis was present in 16.7% of the colonies. Our study shows positive correlations between queen condition and nest size/fungus garden size. These correlations collectively suggest that ecological factors such as plant availability can generate substantial variation between nests and thus shape the success of incipient colonies.

Revista Brasileira de Entomologia, 2018
Atta bisphaerica is a species of grass-cutting ants commonly found in the Cerrado biome. The Braz... more Atta bisphaerica is a species of grass-cutting ants commonly found in the Cerrado biome. The Brazilian Cerrado (savanna) biome covers 2 million km representing 23% of the area of the country. It is an ancient biome with rich biodiversity, estimated at 160,000 species of plants, fungi and animals. However, little is known about their nest architecture development. This study investigated the architecture of fourteen A. bisphaerica nests from Botucatu, São Paulo, Brazil. Molds were made of the nests by filling them with cement to allow better visualization of internal structures such as chambers and tunnels. After excavation, the depth and dimensions (length, width, and height) of the chambers were measured. As expected, there was a lateral development in the nests and increase in the number of chambers over time. Results showed that in nests with an estimated age of 14 months, the average depth was 1.6 ± 0.4 m; for those with 18 months it was 2.2 ± 0.7 m and at 28 months it was 2.5 ± 0.7 m. The number of chambers varied from 4 to 7 in 28-month nests, 2 to 4 in 18-month nests, and from 2 to 3 in 14-month nests. With respect to the dimensions of the internal tunnels, there were variations in their average width, increasing with time. The fungus chambers were located beneath the largest mound of loose soil. This study contributes to a better understanding of the so far unknown nest architecture development of A. bisphaerica grass-cutting ants.

Behavioural processes, Jan 22, 2018
Social information exchange through physical contacts and chemical trail deposition forms the bas... more Social information exchange through physical contacts and chemical trail deposition forms the basis of food recruitment in leaf-cutting ants. The scout initiates the process and passes the information to nestmates that recruit more foragers, thus amplifying the stimulus and ensuring the success of foraging. An interruption of the contact between workers and a reduction in trail laying can diminish the effectiveness of mass recruitment and alter scouting activity and forager flow. This study verified an increase in scout trips as a consequence of inbound workers (with or without a plant load) removal during Atta sexdens foraging, sustaining the outbound flow of foragers, and consequently foraging activity, either through direct contact or chemical trail deposition. Data indicate as one of the roles of unladen workers along the foraging trail must be to stimulate other workers to go out and so speed up the recruitment process The remarkable ability to organize themselves without centr...

Revista Brasileira de Entomologia, 2017
Social animals are faced with an intriguing dilemma. On the one hand, interactions between indivi... more Social animals are faced with an intriguing dilemma. On the one hand, interactions between individuals are essential to exchange information and to promote cohesion, while on the other hand such interactions carry with them the risk of catching and transmitting parasites. This trade-off is particularly significant for social insects because low within-colony genetic diversity makes their colonies potentially vulnerable to parasites while frequent interactions are essential to the development of the colonial odor profile necessary for nestmate recognition. Here we investigate whether social interactions between young and old leaf-cutting ant workers show evidence of this trade-off. We find that old workers engage in more selfgrooming and mandibular scraping than young workers, both in keeping with old workers having been more exposed to parasites. In contrast, we find that young workers engaged in more allogrooming than old workers, which seems likely to have a different motivation possibly the transfer of recognition cues. Furthermore, young workers tended to engage in allogrooming with other young workers, although it was the old workers that were most active and with whom allogrooming would seem likely to optimize information or chemicals transfer. This suggests that young workers may be attempting to minimize the risk of parasite transmission during their social interactions. Although limited to behavioral data, these results hint that ant workers may be sensitive to the trade-off between the transmission of recognition cues and disease, and adjust their social interactions accordingly.

Insects, Jan 9, 2017
The aim of this study was to determine whether worker self-grooming, allogrooming, and direct con... more The aim of this study was to determine whether worker self-grooming, allogrooming, and direct contact promotes the dispersal of substances among members of the colony. For this purpose, a tracer (Sudan III dye) was applied topically to a worker ant and the social interactions between the worker with the tracer and workers without the tracer were studied. Additionally, the worker heads were dissected to visualize whether or not the post-pharyngeal gland was stained. The post-pharyngeal glands from 50% to 70% of workers were stained depending on the size of the group. With the increase in the experimental group size, the frequency of interactions between workers increased, with touching being the most frequent behavior. The tracer dye was probably passed on by direct contact between workers, followed by self-grooming and allogrooming. These behaviors are responsible for the rapid dispersal of substances among colony members as observed in our experiment. The results therefore support ...

Atta capiguara is a grass-cutting ant species frequently found in Cerrado biome. However, little ... more Atta capiguara is a grass-cutting ant species frequently found in Cerrado biome. However, little is known about the giant nest architecture of this ant. In this study, we investigated the architecture of three A. capiguara nests from the fragment of cerrado in Botucatu, São Paulo, Brazil. Casts were made of the nests by filling them with cement to permit better visualization of internal structures such as chambers and tunnels. After excavation, the depth and dimensions (length, width, and height) of the chambers were measured. The results showed the typical shape of Atta capiguara nests consisting of mounds of loose soil with unique features resembling a conic section. The fungus chambers were found outside the apparent main part of the nest and were spaced apart and distributed laterally at ground level. The waste chambers were located beneath the largest mound of loose soil. Both the fungus and waste chambers exhibited a sectoral distribution. Our study contributes to a bet...

Sociobiology, 2016
Feed adaptation is crucial for the ecological success of animals, which explore specific or varie... more Feed adaptation is crucial for the ecological success of animals, which explore specific or varied resources according to the suitability of the selected feature. We hypothesized that the mandibles of leaf-cutting ants exhibit a greater degree of specialization because of the specific food preference of some species. The objective of this study was to highlight possible morphological differences between the mandibles of leaf-cutting ants of the genus Atta related to the food preference of the species, i.e., to investigate the morphofunctionality of mandibles in conjunction with a study of the leaf anatomy of plants selected. A detailed description of the mandibles of workers of the grass-cutting ant Atta bisphaerica and of the leaf-cutting ant Atta sexdens rubropilosa was provided, and the anatomy and chemical composition of the plant material foraged by these species were investigated. For morphometric analysis, 50 individuals of each of the four size classes were dissected for rem...

Journal of Natural History, 2015
Attacobius attarum spiders exhibit a phoretic behaviour on the winged sexual of Atta leaf-cutting... more Attacobius attarum spiders exhibit a phoretic behaviour on the winged sexual of Atta leaf-cutting ants during their mating flight. However, it is unclear if this behaviour is for dispersion or to facilitate the predation of ants in the new colonies. A nest of Atta sexdens was monitored on the day of the mating flight, and the winged ants, as well as the spiders, were collected. The results obtained corroborate the hypothesis that phoretic behaviour is commonly used for dispersion of the spider A. attarum, predominantly females. Of these spiders, 64 individuals of A. attarium were collected, of which 62 were females (96.9%) and two were males (3.1%). Regarding the winged leafcutting ants sampled, 378 females and 361 males were collected, totaling 739 individuals. Of these, 64 individuals (8.7%) had a spider attached to its back for phoretic dispersal and none was observed on the queens after the nuptial flight. In our study, A. attarum females perform phoretic dispersal into the environment on winged leafcutting ants but do not settle in the new nests.
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Papers by Roberto da Silva Camargo