Article

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

Authors:
To read the full-text of this research, you can request a copy directly from the author.

Abstract

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 internalwaste 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. © 2016 The Author(s) Published by the Royal Society. All rights reserved.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the author.

... Unlike most ants of the Atta genus, Atta colombica (G. Meneville) ants do not deposit waste inside the nest but need around 11% of all workers to execute this task outside the nest (Hart and Ratnieks, 2002;Farji-Brener et al., 2016). In this study, the formation of waste chambers was observed in nests aged 18 months (Fig. 1a). ...
... Most likely, due to the complexity of the structure, A. capiguara prefers to build waste chambers over recruiting a larger number of workers to deposit waste outside the nest. Another hypothesis is that, although the construction of waste chambers is influenced by phylogeny (close species, A. sexdens, A. robusta, A. bisphaerica, A. capiguara, A. laevigata, A. saltensis and A. vollenweideri, build waste chambers), the habitat of ants is the main fact that determines waste site (Farji-Brener et al., 2016). In environmental conditions that are harmful to pathogenic organisms, that is, desert habitats, leaf-cutting ants usually avoid excavation costs, with minimal sanitary risk when depositing waste outside the nest. ...
... In environmental conditions that are harmful to pathogenic organisms, that is, desert habitats, leaf-cutting ants usually avoid excavation costs, with minimal sanitary risk when depositing waste outside the nest. On the other hand, humid habitats such as tropical and subtropical forests or Cerrado provide suitable conditions for pathogen proliferation (Farji-Brener et al., 2016). Table 1 Matrix based on Spearman's correlation between the number of fungus chambers (FC), number of waste chambers (WC), number of foraging tunnels (FT), nest depth (ND), total fungus chamber volume (FCV), total waste chamber volume (WCV), foraging tunnel volume (FTV) and total nest volume (NV) along the development of Atta capiguara nests, in Botucatu, SP. ...
Article
Full-text available
Atta capiguara grass-cutting ants are commonly found in the Cerrado biome, in open fields. Although grass-cutting ants build giant nests, little has been elucidated about this building pattern and when chambers and tunnels emerge. The present study describes the nest architecture development of A. capiguara grass-cutting ants from data on 31 cement-molded nests. A. capiguara nests grow with increases in the number of fungus chambers and emergence and increase of waste chambers and foraging tunnels. The structural growth of A. capiguara nests in the first year and a half of age (18 months) is vertical, with the building of the first chambers in the soil profile. After 18 months, the nests grow sideways with the addition of chambers and tunnels, and the first waste chambers appear. Between 18 and 54 months, the number of fungus chambers increases from 1-3 to 21-32, and the chambers are concentrated at the soil surface, although they can be found more than 3 m deep. In addition, the total volume of the waste chambers increases with the increment in the fungus chambers volume. Thus, this study contributes to understanding the nest architecture development of A. capiguara grass-cutting ants and demonstrates that the total volume of waste chambers is proportional to the total volume of fungus chambers suitable for the colony.
... During these steps, plant volatiles might diffuse from the leaf fragments and locally scent the fungus garden. Then, naïve foragers that visit this compartment might learn the odors of those plants currently harvested Due to the turnover of the fungus, exhausted plant material and dead fungus are removed from the garden and disposed of at the colony dump (Herz et al., 2007;Jonkman, 1980;Bot et al., 2001;Hart and Ratnieks, 2001;Farji-Brener et al., 2016). If the harvested plant is harmful for the fungus, presumably due to compounds with fungicidal effect, foragers can learn to avoid the cues of the plant in question (Thiele et al., 2014;Ridley et al., 1996;North et al., 1999;Herz et al., 2008;Saverschek and Roces, 2011) and later discontinue its harvesting. ...
... Although little is known about the architecture of A. ambiguus nests, Fowler (1985) described that A. ambiguus deposits the waste in underground chambers, as a number of Acromyrmex spp. does (Haines, 1983;Verza et al., 2007;Farji-Brener et al., 2016). Whether the conditions that prevail in underground dumps enable plant volatiles to last longer than under open air conditions, is unlikely. ...
... Whether the conditions that prevail in underground dumps enable plant volatiles to last longer than under open air conditions, is unlikely. In fact, some authors argue that external refuse dumps might be advantageous for the ants, as open-air conditions are detrimental for microorganisms involved in the decomposition of discarded leaf fragments (Farji-Brener et al., 2016). ...
... Garden contamination relies on distinct aspects of waste management. For example, the location of waste (in underground chambers or on external refuse piles) may affect the probability of fungal infections, as well as the quantity of organic waste deposited (Farji-Brener et al. 2016). Since refuse dumps are known as a source of fungal pathogens, some authors suggest that waste disposal should be located as far as possible from the nest foraging entrances to avoid contamination (Weber 1972;Bot et al. 2001; al. 2016). ...
... nest-dump distances can restrict foraging territories, as foraging workers often avoid paths that cross waste piles and contact with midden workers (Farji-Brener et al. 2016). Actually, larger (>350 cm 2 ) and more distant (>50 cm) dumps had almost no activity ( Figure 2b), which might indicate its desertion. ...
... This material, along with other colony detritus such as ant necromass, is then transported to designated colony refuse dumps [4,12]. Depending on the LCA species, these refuse dumps can be located in subterranean chambers (many Atta genera, including the widespread A. cephalotes), or as a single aboveground pile in the open or at the base of a tree at the periphery of the colony (e.g. A. colombica [13]; figure 1c). These refuse piles play host to diverse microbial and litter arthropod communities, including species that & 2019 The Author(s) Published by the Royal Society. ...
... The significance of LCA-driven emissions could increase notably when considering either a broader range of habitat types or the potential for similar N 2 O production across a greater range of refuse-concentrating LCA species. Other Acromyrmex and Atta species form refuse piles that can be located both aboveground (e.g. A. mexicana, many Acromyrmex) or belowground (common species A. cephalotes and A. sexdens) and are widely distributed within the latitudinal extents of Neotropical forests, from the southern USA to Argentina [13]. Overall colony density is also 50-150% greater when considering multiple co-occurring Atta species compared with A. colombica alone (electronic supplementary material, table S1). ...
Article
Full-text available
Though tropical forest ecosystems are among the largest natural sources of the potent greenhouse gas nitrous oxide (N2O), the spatial distribution of emissions across landscapes is often poorly resolved. Leaf cutter ants (LCA; Atta and Acromyrmex, Myrmicinae) are dominant herbivores throughout Central and SouthAmerica, and influencemultiple aspects of forest structure and function. In particular, their foraging creates spatial heterogeneity by concentrating large quantities of organic matter (including nitrogen,N) fromthe surrounding canopy into their colonies, and ultimately into colony refuse dumps. Here, we demonstrate that refuse piles created by LCA species Atta colombica in tropical rainforests of Costa Rica provide ideal conditions for extremely high rates of N2O production (high microbial biomass, potential denitrification enzyme activity, N content and anoxia) and may represent an unappreciated source of heterogeneity in tropical forest N2O emissions. Average instantaneous refuse pile N2O fluxes surpassed background emissions by more than three orders of magnitude (in some cases exceeding 80 000 mg N2O-N m22 h21) and generating fluxes comparable to or greater than those produced by engineered systems such as wastewater treatment tanks. Refuse-concentrating Atta species are ubiquitous in tropical forests, pastures and production ecosystems, and increase density strongly in response to disturbance. As such, LCA colonies may represent an unrecognized greenhouse gas point source throughout the Neotropics.
... While it is obvious that the nests of social insects have specialized functional dimensions [111][112][113], the question of whether they are also built aesthetically is difficult to address scientifically. There is no doubt that in the eyes of a human observer, social insect nests are beautiful objects [16]. ...
... The result of this indirect coordination is a round-shaped comb with approximately 150 cells and, more importantly, without holes. Other examples of social insect construction relying on stigmergic coordination include internal and external structures of nests in ants and honeybees [14,163], trail networks in ants and termites [234][235][236] and cemeteries and refuse piles in ants [113,224]. ...
Article
Full-text available
The similarities between the structures built by social insects and by humans have led to a convergence of interests between biologists and architects. This new, de facto interdisciplinary community of scholars needs a common terminology and theoretical framework in which to ground its work. In this conceptually oriented review paper, we review the terms ‘information’, ‘space’ and ‘architecture’ to provide definitions that span biology and architecture. A framework is proposed on which interdisciplinary exchange may be better served, with the view that this will aid better cross-fertilization between disciplines, working in the areas of collective behaviour and analysis of the structures and edifices constructed by non-humans; and to facilitate how this area of study may better contribute to the field of architecture. We then use these definitions to discuss the informational content of constructions built by organisms and the influence these have on behaviour, and vice versa. We review how spatial constraints inform and influence interaction between an organism and its environment, and examine the reciprocity of space and information on construction and the behaviour of humans and social insects. This article is part of the theme issue ‘Interdisciplinary approaches for uncovering the impacts of architecture on collective behaviour’.
... Leaf-cutting ant behaviors such as self-and allogrooming, that is, the removal of contaminants from itself or another individual, respectively (Morelos-Juárez et al., 2010;Richard & Errard, 2009), preparation and cleaning of plant material used as a substrate for the fungus crop (Mangone & Currie, 2007;Quinlan & Cherrett, 1977), and the removal of foreign conidia or infected pieces of the fungus garden (grooming and weeding, respectively, Currie & Stuart, 2001;Nilssøn-Moller et al., 2018), are prophylactic and suppressive strategies against invasions from various pathogens. Spatial avoidance (Cremer et al., 2007;Stroeymeyt et al., 2014) and division of labor (Farji-Brener et al., 2016;Hart & Ratnieks, 2001;Waddington & Hughes, 2010) also reduce the likelihood of infection by decreasing contact between infected and healthy workers. ...
Article
Full-text available
Leaf-cutting ants and their fungal crops are a textbook example of a long-term obligatory mutualism. Many microbes continuously enter their nest containing the fungal cultivars, destabilizing the symbiosis and, in some cases, outcompeting the mutual-istic partners. Preferably, the ant workers should distinguish between different microorganisms to respond according to their threat level and recurrence in the colony. To address these assumptions, we investigated how workers of Atta sexdens sanitize their fungal crop toward five different fungi commonly isolated from the fungus gardens: Escovopsis sp., Fusarium oxysporum, Metarhizium anisopliae, Trichoderma spirale, and Syncephalastrum sp. Also, to investigate the plasticity of these responses toward recurrences of these fungi, we exposed the colonies with each fungus three times fourteen days apart. As expected, intensities in sanitization differed according to the fungal species. Ants significantly groom their fungal crop more toward F. oxyspo-rum, M. anisopliae, and Syncephalastrum sp. than toward Escovopsis sp. and T. spirale. Weeding, self-, and allogrooming were observed in less frequency than fungus grooming in all cases. Moreover, we detected a significant increase in the overall responses after repeated exposures for each fungus, except for Escovopsis sp. Our results indicate that A. sexdens workers are able to distinguish between different fungi and apply distinct responses to remove these from the fungus gardens. Our findings also suggest that successive exposures to the same antagonist increase hygiene, indicating plasticity of ant colonies' defenses to previously encountered pathogens. K E Y W O R D S Atta sexdens, disease, pathogens, secondary exposures, social immunity
... One reason could be that the excavated subsoil diluted the ant-affected (and perhaps nutrientrich) soil, and so our mound samples showed similar soil properties to the control soil (Holec and Frouz, 2006). Ants can also deposit their waste outside of the nest at a specific place so these nutrients would not be included in our mound sample (Farji-Brener et al., 2016). Alternatively, our mound sample could have been in fact an "inverted" version of the control sample as the mineral soil excavated by ants simply overlayed the top organic layer of the original soil surrounding the ant nest entrance, thus resulting in a mixed sample with similar soil properties. ...
Article
Ants and termites reach high abundances in the tropics and substantially affect the environment through a range of their activities. Because of foraging and decomposition of organic matter at their nesting sites, these locations show fundamentally altered soil properties compared to the adjacent soil. However, such changes are typically studied only within one species or taxon and in one habitat type. Consequently, it is not clear how these effects vary across different taxa and in relation to anthropogenic habitat change. In this study we assess the impacts of different mound-building taxa across a gradient of tropical habitat change in SE Asia comprising primary forest, logged forest and oil palm plantation. To do this we analysed chemical soil properties of mounds of multiple taxa of social insects, with some taxa spanning the full habitat change gradient, and where taxa differ in their mound construction type. Our results show that soils in mounds and adjacent soils have consistently different properties. However, these patterns differ both between social insect taxa and across habitat types. Specifically, mounds of soil-feeding termites Dicuspiditermes spp. were substantially enriched in basic soil nutrients such as C, N, P, especially in oil palm, while mounds of the leaf litter-feeding termite Macrotermes gilvus were depleted. Ant mounds did not show a clear pattern. This indicates that different social insect taxa in a particular habitat affect soil properties in differing ways, and furthermore that such impacts can change when a habitat is anthropogenically altered. Our research highlights the importance of termites for driving the heterogeneity of soil properties and nutrient redistribution across tropical landscapes.
... Finalmente, encontramos que el comportamiento de enterrar o acumular basura en la superficie estaba en parte determinado por la filogenia, pero también por la ecología. Como predijimos, las especies de cortadoras que habitaban ambientes más desérticos depositaban la basura en montículos externos, y las especies que habitaban en ambientes más húmedos generalmente enterraban sus desechos (Farji-Brener et al. 2016). En resumen, las ideas novedosas aparecieron porque intentamos explicar un aspecto contrastante de la historia natural de las hormigas cortadoras. ...
... Some early studies suggested that this parasite is highly virulent to its host, capable of causing the death of infected colonies and reducing the fungus garden biomass as well as the production of new ant individuals (Currie et al., 1999a;Currie, 2001). Based on the results of these studies, it has become disseminated in the literature that this fungus actually represents a highly virulent parasite (Currie et al., 1999a(Currie et al., , 2003aCurrie, 2001;Currie and Stuart, 2001;Stearns and Hoekstra, 2005;Hölldobler and Wilson, 2009;Farji-Brener et al., 2016;Verza et al., 2017). However, it is important to consider some points related to this. ...
Article
Full-text available
Eusocial insects interact with a diversity of parasites that can threaten their survival and reproduction. The amount of harm these parasites cause to their hosts (i.e., their virulence) can be influenced by numerous factors, such as the ecological context in which the parasite and its host are inserted. Leaf-cutting ants (genera Atta, Acromyrmex and Amoimyrmex, Attini: Formicidae) are an example of a eusocial insect whose colonies are constantly threatened by parasites. The fungi Escovopsis and Escovopsioides (Ascomycota: Hypocreales) are considered a highly virulent parasite and an antagonist, respectively, to the leaf-cutting ants’ fungal cultivar, Leucoagaricus gongylophorus (Basidiomycota: Agaricales). Since Escovopsis and Escovopsioides are common inhabitants of healthy colonies that can live for years, we expect them to have low levels of virulence. However, this virulence could vary depending on ecological context. We therefore tested two hypotheses: (i) Escovopsis and Escovopsioides are of low virulence to colonies; (ii) virulence increases as colony complexity decreases. For this, we used three levels of complexity: queenright colonies (fungus garden with queen and workers), queenless colonies (fungus garden and workers, without queen) and fungus gardens (without any ants). Each was inoculated with extremely high concentrations of conidia of Escovopsis moelleri, Escovopsioides nivea, the mycoparasitic fungus Trichoderma longibrachiatum or a blank control. We found that these fungi were of low virulence to queenright colonies. The survival of queenless colonies was decreased by E. moelleri and fungus gardens were suppressed by all treatments. Moreover, E. nivea and T. longibrachiatum seemed to be less aggressive than E. moelleri, observed both in vivo and in vitro. The results highlight the importance of each element (queen, workers and fungus garden) in the leaf-cutting ant-fungus symbiosis. Most importantly, we showed that Escovopsis may not be virulent to healthy colonies, despite commonly being described as such, with the reported virulence of Escovopsis being due to poor colony conditions in the field or in laboratory experiments.
... Therefore, workers actively manage their waste by moving it away from their living space (Bot et al., 2001;Diez, Le Borgne, Lejeune, & Detrain, 2013;. A wide variety of waste can be discarded out of the nest, including inorganic items (Gordon & Mehdiabadi, 1999) such as nest-building material (Pielstr€ om & Roces, 2013), food-related waste such as dead mycelium in fungus-growing ants (Ballari, Farji-Brener, & Tadey, 2007;Farji-Brener, Elizalde, Fern andez-Marín, & Amador-Vargas, 2016;Verza, Diniz, Chiarelli, Mussury, & Bueno, 2017), faeces (reviewed in: Jackson & Hart, 2009;Weiss, 2006) or even corpses of dead nestmates (i.e. necrophoresis: Diez, Deneubourg, & Detrain, 2012, Diez et al., 2013reviewed in Sun & Zhou, 2013). ...
Article
Insect societies are challenged by harmful pathogens that originate from waste, such as faeces, food leftovers or corpses. The discarding of waste to outside the nest reduces these sanitary risks and contributes to the social immunity of ant colonies. In this study, we tested whether the nest-cleaning behaviour in Myrmica rubra colonies differed depending on the pathogenicity of waste or the presence of brood as well as over successive exposure to waste. We introduced waste items covered with entomopathogenic Metarhizium brunneum conidia and items without conidia in either broodright or broodless colonies. The greater the pathogenicity of waste, the faster it was discarded by the ants, although this did not prevent higher mortality rates in workers and larvae. When exposed a second time to waste items, ant colonies improved the discarding of nonpathogenic waste but became less efficient at removing infected waste, probably due to morbidity in the workers’ population. Most surprisingly, we found that the presence of brood enhanced the hygienic responses of workers, with ant colonies doubling their probability of discarding waste items to outside the nest. Overall, we show that ants can detect entomopathogenic conidia on waste and take steps accordingly to hasten the removal of infected items. Furthermore, we demonstrate the upregulating role of larvae which results in enhanced performance of hygienic tasks and reinforces sanitary control inside the colony.
... A turret could also prevent dangerous material or organisms such as non-colony members or predators from entering the nest. Many leaf-cutting ant species dispose of their colony waste by external deposits [43] and the waste pile of Ac. fracticornis nests is located in very close proximity to the nest entrance. This pathogen-loaded waste material [44] could easily be blown back into a nest opening located at the ground level. ...
Article
Full-text available
Ants build complex nest structures by reacting to simple, local stimuli. While underground nests result from the space generated by digging, some leaf-and grass-cutting ants also construct conspicuous aboveground turrets around nest openings. We investigated whether the selection of specific building materials occurs during turret construction in Acromyrmex fracticornis grass-cutting ants, and asked whether single building decisions at the beginning can modify the final turret architecture. To quantify workers' material selection, the original nest turret was removed and a choice between two artificial building materials, thin and thick sticks, was offered for rebuilding. Workers preferred thick sticks at the very beginning of turret construction, showed varying preferences thereafter, and changed to prefer thin sticks for the upper, final part of the turret, indicating that they selected different building materials over time to create a stable structure. The impact of a single building choice on turret architecture was evaluated by placing artificial beams that divided a colony's nest entrance at the beginning of turret rebuilding. Splitting the nest entrance led to the self-organized construction of turrets with branched galleries ending in multiple openings, showing that the spatial location of a single building material can strongly influence turret morphology.
... In a LCA colony, most waste originates from the fungus chamber. Here, workers weed and groom the fungus garden, i.e., pick-up exhausted substrate and pathogen-infected fungus (Currie and Stuart 2001), and relocate large quantities of waste to aboveground heaps, as in most Acromyrmex and a few Atta species, or to voluminous underground chambers as in most Atta species (Stahel and Geijskes 1939;Jonkman 1980;Hart and Ratnieks 2002;Bollazzi et al. 2012;Farji-Brener et al. 2016). These are usually excavated in deep soil layers below the fungus-garden zone. ...
Article
Full-text available
Social insects often use olfactory cues from their environment to coordinate colony tasks. We investigated whether leaf-cutting ants use volatiles as cues to guide the deposition of their copious amounts of colony refuse. In the laboratory, we quantified the relocation of a small pile of colony waste by workers of Atta laevigata towards volatiles offered at each side of the pile as a binary choice, consisting of either waste volatiles, fungus volatiles, or no volatiles. Fungus volatiles alone did not evoke relocation of waste. Waste volatiles alone, by contrast, led to a strong relocation of waste particles towards them. When fungus and waste volatiles were tested against each other, waste particles were also relocated towards waste volatiles, and in a high percentage of assays completely moved away from the source of fungus volatiles as compared to the previous series. We suggest that deposition and accumulation of large amounts of refuse in single external heaps or a few huge underground waste chambers of Atta nests is due to both olfactory preferences and stigmergic responses towards waste volatiles by waste-carrying workers.
... Waste is removed from the nest by specific ant workers that do not perform other tasks [147,148] and will not go on to perform other tasks before they die [149]. Interestingly, leaf cutter ant species that live in wet environments will dig special waste chambers inside their nest, while leaf cutter ant species from arid environments will dispose of their waste outside the nest [150]. One potential explanation for this difference is that in wet environments, microorganisms in the waste are more likely to spread and so confining waste in chambers that can be closed off reduces the risk of spreading pathogens. ...
Article
The environment plays an important role in disease dynamics and in determining the health of individuals. Specifically, the built environment has a large impact on the prevention and containment of both chronic and infectious disease in humans and in non-human animals. The effects of the built environment on health can be direct, for example, by influencing environmental quality, or indirect by influencing behaviours that impact disease transmission and health. Furthermore, these impacts can happen at many scales, from the individual to the society, and from the design of the plates we eat from to the design of cities. In this paper, we review the ways that the built environment affects both the prevention and the containment of chronic and infectious disease. We bring examples from both human and animal societies and attempt to identify parallels and gaps between the study of humans and animals that can be capitalized on to advance the scope and perspective of research in each respective field. By consolidating this literature, we hope to highlight the importance of built structures in determining the complex dynamics of disease and in impacting the health behaviours of both humans and animals. This article is part of the theme issue ‘Interdisciplinary approaches for uncovering the impacts of architecture on collective behaviour’.
... Additionally, they are highly territorial and forage mostly in the area around their nests, meaning that if they do not clear it of dead and potentially infectious nestmates, they are likely to be reencountered (Boomsma et al., 2005;Cremer et al., 2017). Ants tend therefore to place corpses onto specific midden (trash) sites that are located inside or outside near the nest, but these sites are still regularly visited by midden workers (Verza et al., 2017;Hart and Ratnieks, 2002;Farji-Brener et al., 2016). Consequently, although middens likely reduce a colony's exposure to corpses, they still represent a potential route for disease transmission back into the colony; hence the need to destroy infected corpses rather than simply taking them out of the nest. ...
Article
Full-text available
In social groups, infections have the potential to spread rapidly and cause disease outbreaks. Here, we show that in a social insect, the ant Lasius neglectus, the negative consequences of fungal infections (Metarhizium brunneum) can be mitigated by employing an efficient multicomponent behaviour, termed destructive disinfection, which prevents further spread of the disease through the colony. Ants specifically target infected pupae during the pathogen's non-contagious incubation period, utilising chemical 'sickness cues' emitted by pupae. They then remove the pupal cocoon, perforate its cuticle and administer antimicrobial poison, which enters the body and prevents pathogen replication from the inside out. Like the immune system of a metazoan body that specifically targets and eliminates infected cells, ants destroy infected brood to stop the pathogen completing its lifecycle, thus protecting the rest of the colony. Hence, in an analogous fashion, the same principles of disease defence apply at different levels of biological organisation.
... Fungus cultivation produces a considerable amount of waste due to the decomposition of the substrate. According to the ant species, waste is disposed of outside the nest or inside specific underground chambers (waste dumps) along with exhausted fungus, dead ants, soil particles, and other debris [28][29][30][31]. The transport, manipulation and spatial isolation of waste in a dump are thought to be adaptive responses aimed at reducing the spread of pathogens within the nest [32][33][34][35]. ...
Article
Plants initially accepted by foraging leaf-cutting ants are later avoided if they prove unsuitable for their symbiotic fungus. Plant avoidance is mediated by the waste produced in the fungus garden soon after the incorporation of the unsuitable leaves, as foragers can learn plant odors and cues from the damaged fungus that are both present in the recently produced waste particles. We asked whether avoidance learning of plants unsuitable for the symbiotic fungus can take place entirely at the colony dump. In order to investigate whether cues available in the waste chamber induce plant avoidance in naïve subcolonies, we exchanged the waste produced by subcolonies fed either fungicide-treated privet leaves or untreated leaves and measured the acceptance of untreated privet leaves before and after the exchange of waste. Second, we evaluated whether foragers could perceive the avoidance cues directly at the dump by quantifying the visits of labeled foragers to the waste chamber. Finally, we asked whether foragers learn to specifically avoid untreated leaves of a plant after a confinement over 3 hours in the dump of subcolonies that were previously fed fungicide-treated leaves of that species. After the exchange of the waste chambers, workers from subcolonies that had access to waste from fungicide-treated privet leaves learned to avoid that plant. One-third of the labeled foragers visited the dump. Furthermore, naïve foragers learned to avoid a specific, previously unsuitable plant if exposed solely to cues of the dump during confinement. We suggest that cues at the dump enable foragers to predict the unsuitable effects of plants even if they had never been experienced in the fungus garden.
Article
Full-text available
Species of the genus Trichoderma sp. are used to control leaf-cutting ants. However, knowledge about the collective immune responses of ants against this antagonist is scarce. Therefore, this study assessed the frequency of hygienic behaviors deployed by medium workers of Atta cephalotes. For this purpose, suspensions of Trichoderma sp. spores were sprayed on sub-colonies composed of workers and a portion of the mutualist. As a control, the sub-colonies were sprayed with water. Independent of whether the workers were treated with spores of Trichoderma sp. or water, they increased the frequency of self-grooming while reducing the frequency of fungus grooming. These findings suggest that medium workers prioritize the removal of contaminants from their bodies over the interaction with the mutualist, possibly to avoid further contamination in the garden. In the field, this strategy may minimize the possibility that foraging ants exposed to contaminants from the exterior can transfer potentially hazardous materials to the nest where they can reach the garden, risking the colony’s productivity.
Article
Leaf‐cutting ants (LCA) try to reduce the risk of contamination in their colonies by avoiding contact with their nest refuse (NR), as it can harbor substances harmful to them and their symbiotic fungi. Here, we tested whether an aqueous extract with 10% vol/vol of NR of the leaf‐cutting ant Atta opaciceps Borgmeier (Hymenoptera: Formicidae, Attini) causes a deterrent effect. We placed leaves of Hibiscus rosa‐sinensis L. (Malvaceae) sprayed with NR extract or distilled water (control) in the foraging areas of 12 colonies – eight colonies of A. opaciceps and four of Atta sexdens (L.) – for 60 min, on three consecutive days. The fresh weight of remaining leaf fragments between treatments was compared using linear‐mixed effect models. Leaf consumption was significantly lower in the presence of NR extract for 48 h, indicating that the NR odor impregnated in the leaves may have been the responsible factor for the deterrence. Further studies are needed to establish a deterrent extract with a broad spectrum and lasting effect on plants, and to better understand the mechanisms involved in deterrence.
Article
Leaf-cutting ants of the genus Atta are widely distributed throughout the American tropics and subtropics and rival other herbivores in the consumption of surrounding foliage. Although numerous studies have been conducted on the role these insects play in herbivory and organic matter dynamics, only a handful of studies have examined their impacts on soil greenhouse gas emissions. Our study investigated fluxes of carbon dioxide (CO2) and methane (CH4) from three nests of Atta cephalotes using a portable greenhouse gas analyzer, and measured CO2 and CH4 emissions from soils containing nest holes that ranged 5.2 to 152.1 g CO2-C and -1.1 to 15,264.7 mg CH4-C m⁻² day⁻¹, respectively. Fluxes of CO2 and CH4 were positively correlated above nest holes, but not in patches of soil away from leaf-cutting ant nests. Nearby non-nest soil emissions were significantly lower, ranging from 0.6 to 6.0 g CO2-C and -1.3 to 0.77 mg CH4-C m⁻² day⁻¹. Fluxes of both gases among nests and among holes within a single nest were highly variable. This preliminary dataset is small in scale both temporarily and geographically, but the discovery of substantial greenhouse gas fluxes from Atta cephalotes nests may have important implications for carbon budgets of tropical and subtropical American forests. Further work will be necessary to determine the mechanisms behind enhanced greenhouse gas emissions from leaf-cutting ant nests, and how this may alter ecosystem-scale CO2 emissions and CH4 sink strength in tropical forest soils.
Article
Many animals consume the feces of their conspecifics. This allo-coprophagy can have benefits, such as access to nutrients and symbionts, but also risks for consumers, mainly due to direct contact with pathogens that develop on feces. In the European earwig Forficula auricularia, mothers and juveniles live in nests lined with their feces. This surprising habit allows juveniles to consume the feces of their siblings during family life and provides them with nutritional benefits when mothers provide low care. However, it was unclear whether earwig mothers also practice allo-coprophagy, and whether this behaviour is motivated by their nutritional needs. Here, we set up four types of experimental families in which we manipulated the nutritional needs of mothers and/or juveniles and measured the effects on the production of feces by the juveniles, and the consumption of these feces by the mothers. Our results first show that fed juveniles produced more feces pellet in presence of fed compared to food-deprived mothers. We also found that, overall, about 50% of the mothers consumed juveniles feces. This consumption was both more likely and larger when the feces were produced by fed compared to food-deprived juveniles, while the proportion of feces pellets eaten was larger in food-deprived compared to fed mothers. Overall, our results reveal that allo-coprophagy involves every family member and suggest that it can have both nutritional and non-nutritional benefits for earwig mothers. Allo-coprophagy could thus favour the maintenance of mothers in the nest and, more generally, promote the early evolution of family life. This article is protected by copyright. All rights reserved
Article
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 Atta opaciceps are species of very restricted occurrence. Southeastern region was characterized by the occurrence of A. capiguara and A. laevigata. Atta laevigata exhibited a generalized pattern of occurrence in the Center-West and North. Our study contributes to a better understanding of the so far unknown occurrence of leaf-cutting and grass-cutting ants within Brazil.
Article
Myrmecochory, a type of ant-mediated seed dispersal, is a diffuse, widespread mutualism in which both partners are purported to benefit from the services or rewards of the other. However, ant benefits in this interaction are conflicted and understudied, especially in the context of microbial third parties. Here, we investigate the effect of a myrmecochore plant-produced antimicrobial chemical (sanguinarine) on the growth of a common entomopathogenic fungus (Beauveria bassiana). We then explore whether sanguinarine, through its effect on entomopathogen growth, might influence ant survival and foraging behavior. At high concentrations, sanguinarine increased the growth of B. bassiana, but fungal growth was not affected at concentrations of sanguinarine near natural levels produced in seeds. When ant colonies were exposed to B. bassiana, survival was not affected by a sanguinarine-supplemented diet. Furthermore, ant foraging patterns (preference for or avoidance of food items with sanguinarine) did not change when ants were exposed to the entomopathogen. Though sanguinarine promotes the growth of an entomopathogen at higher concentrations, which might pose an additional risk for ants in myrmecochory, we assert that social immune behavioral defenses (such as grooming or redispersal of seeds after elaiosome consumption) help ants mitigate this risk. By incorporating a microbial third party into this ant-plant interaction, we seek to more fully understand the risks and benefits provided to both partners in this mutualism. We encourage the investigation of third-party influences in reciprocal pairwise interactions to assist in the understanding of the evolution and persistence of mutualisms.
Article
Forest plantations represent the fourth largest crop by planted area in Brazil. However, leaf-cutting ants can compromise their establishment and development. Atta and Acromyrmex (Hymenoptera: Formicidae) ant genera are the main pests in Eucalyptus and Pinus plantations, and their management is fundamental to maintain the forestry sector. Here, we describe biological aspects of leaf-cutting ants in Brazilian commercial forest plantations and the feasibility of different methods to control these insects. Physical and biological control methods are not effective in suppressing leaf-cutting ants nests of any size. Chemical control is the most used method and is based mainly on ant baits with high efficiency, easy application, and low operational cost. Ant baits comprise a carrier, usually citrus pulp, and an active ingredient. Dodecachlor was the first active ingredient used on a large scale in ant baits in Brazil. The use of this chemical was suspended because of its toxicity and persistence and replaced by sulfluramid, which is currently the most used active ingredient in ant baits. Although this compound controls leaf-cutting ants effectively, the raw material used in the manufacture of sulfluramid (perfluorooctane sulfonyl fluoride) was listed at the Stockholm Convention in 2009 as a persistent organic pollutant. Diverse alternative control methods have been tested without success and for this reason, sulfluramid is still used to control leaf-cutting ants. Regardless of the effectiveness of sulfluramid-based baits, researchers should put more effort into developing control methods safer to the environment.
Article
Full-text available
Several worker subcastes may occur in ant colonies, including physiological, morphological, and temporal subcastes. Leaf-cutting ants present intricate division of labor among worker subcastes during brood care, fungus garden maintenance, substrate foraging and processing. For colony survival, the fungus garden must be healthy, and tasks efficiently shared among worker subcastes. Therefore, worker behavior is key for colony maintenance in fungus-farming ants. Here we provide a qualitative and quantitative account of intracolonial behavior in Acromyrmex subterraneus, a common leaf-cutter in Brazilian Cerrado savanna. Quantitative ethograms showed that performance of major behavioral categories (e.g., “Brood and Queen Care,” “Foraging,” “Fungus Care”) and the composition of behavioral repertoires are important parameters distinguishing labor among A. subterraneus worker subcastes. Media and major subcastes are behaviorally more similar to one another than to minors. Minors regularly executed brood- and fungus-related tasks, whereas media and majors executed mostly foraging-related tasks. Grooming was frequent in all subcastes. Overall, the behavioral patterns reported in A. subterraneus are similar to those reported for other leaf-cutters. The tasks executed by different subcastes of A. subterraneus closely resemble the division of labor observed in Atta colonies, suggesting that alongside the use of fresh leaves as culturing substrates, a highly conserved set of worker behaviors persist since the origin of the leaf-cutting lineage. Our work highlights the importance of detailed analyses of the composition of behavioral repertoires in polymorphic fungus-farming ants to better understand their social organization, and the mechanisms mediating division of labor among worker subcastes in the Attina.
Article
Full-text available
1. Leaf‐cutting ants remove copious amounts of colony waste, a potential pathogen source for workers and reared symbiotic fungus, to above‐ground heaps or deep underground chambers. However, the dumpsite may also contain information about plants initially harvested and disposed of because of unsuitability for the fungus. 2. The underground environment presents climatic gradients across the soil profile and it is an open question whether leaf‐cutting ants use microclimatic cues to choose suitable sites for waste disposal, as displayed for other in‐nest tasks. 3. Climatic preferences in leaf‐cutting ants were investigated for the deposition of colony waste. In the laboratory, deposition of waste particles by workers of Atta laevigata was quantified by offering them, in different experiments, a binary choice of temperatures (range, 15–30 °C), levels of air humidity (range 10–98%), and CO2 concentrations (range, atmospheric values to 10%). 4. Leaf‐cutting ants used temperature and air humidity, but not CO2 levels, as cues for the deposition of their waste. They consistently preferred a dry (≤ 33% air humidity) environment. Less consistent, temperature preferences varied depending on colony (15–25 °C for one colony and 25–30 °C for the other). Although workers showed clear preferences for high levels of CO2 for themselves, they were CO2‐indifferent for waste deposition. 5. It is argued that the observed climatic preferences for underground waste disposal might aid nest hygiene by providing unsuitable dry conditions for pathogen growth, with thermal preferences that do not hinder worker activities for further waste management and inspection of discarded plants.
Article
Full-text available
The nutrient‐rich organic waste generated by ants may affect plant reproductive success directly by enhancing fruit production but also indirectly, by affecting floral traits related with pollinator attraction. Understanding how these soil‐nutrient hot spots influence floral phenotype is relevant to plant–pollination interactions. We experimentally evaluated whether the addition of organic waste from refuse dumps of the leaf‐cutting ant Acromyrmex lobicornis (Hymenoptera: Formicidae: Attini) alters floral traits associated with pollinator attraction in Eschscholzia californica (Ranunculales: Papaveraceae), an entomophilous herb. We analysed flower shape and size using geometric morphometric techniques in plants with and without the addition of refuse‐dumps soil, under greenhouse conditions. We also measured the duration of flowering season, days with new flowers, flower production and floral display size. Plants growing in refuse‐dumps soil showed higher flower shape diversity than those in control soil. Moreover, plants in refuse‐dumps soil showed bigger flower and floral display size, longer flowering season, higher number of flowering days and flower production. As all these variables may potentially increase pollinator visits, plants in refuse‐dumps soil might increase their fitness through enhanced attraction. Our work describes how organic waste from ant nests may enhance floral traits involved in floral attraction, illustrating a novel way of how ants may indirectly benefit plants.
Article
Full-text available
en Anthropogenic disturbances are known to modify plant–animal interactions such as those involving the leaf‐cutting ants, the most voracious and proliferating herbivore across human‐modified landscapes in the Neotropics. Here, we evaluate the effect of chronic anthropogenic disturbance (e.g., firewood collection, livestock grazing) and vegetation seasonality on foraging area, foliage availability in the foraging area, leaf consumption and herbivory rate of the leaf‐cutting ant Atta opaciceps in the semiarid Caatinga, a mosaic of dry forest and scrub vegetation in northeast Brazil. Contrary to our initial expectation, the foraging area was not affected by either disturbance intensity or the interaction between season and disturbance intensity. However, leaf consumption and herbivory rate were higher in more disturbed areas. We also found a strong effect of seasonality, with higher leaf consumption and herbivory rate in the dry season. Our results suggest that the foraging ecology of leaf‐cutting ants is modulated by human disturbance and seasonality as these two drivers affect the spectrum and the amount of resources available for these ants in the Caatinga. Despite the low productivity of Caatinga vegetation, the annual rates of biomass consumption by A. opaciceps are similar to those reported from other leaf‐cutting ants in rain forests and savannas. This is made possible by maintaining high foraging activity even in the peak of the dry season and taking benefit from any resource available, including low‐quality items. Such compensation highlights the adaptive capacity of LCA to persist or even proliferate in human‐modified landscapes from dry to rain forests. RESUMO pt Perturbações antrópicas podem modificar as interações entre plantas e animais tais como aquelas envolvendo as formigas cortadeiras, os herbívoros mais vorazes da região neotropical e que proliferam em paisagens antrópicas. Nesse estudo nós avaliamos o efeito de perturbações antrópicas crônicas (e.g. coleta de lenha, sobrepastoreio por animais domésticos) e sazonalidade na área de forrageamento, disponibilidade da vegetação na área de forrageamento, consumo de vegetação e taxa de herbivoria da formiga cortadeira A. opaciceps na Caatinga, um mosaico de florestas secas e vegetação arbustiva que ocorre no Nordeste do Brasil. Contrário às nossas expectativas, a área de forrageamento das colônias não foi afetada pela perturbação nem pela interação entre estação e perturbação. Contudo, o consumo de vegetação e a taxa de herbivoria foram mais altos em áreas mais perturbadas e durante a estação seca. Nossos resultados sugerem que o forrageamento das formigas cortadeiras na Caatinga é modulado por perturbações antrópicas e sazonalidade, pois estes dois fatores afetam a diversidade e a quantidade de recursos disponíveis para as colônias. Apesar da baixa produtividade da Caatinga, as taxas anuais de consumo de biomassa de Atta opaciceps são similares àquelas reportadas para outras espécies de formigas cortadeiras em florestas úmidas e savanas. Isso é possível porque as formigas mantêm uma alta atividade de forrageamento mesmo no pico da estação seca, utilizando todos os recursos disponíveis, incluindo diversos itens de baixa qualidade. Tal compensação ressalta a capacidade de adaptação das formigas cortadeiras para persistir ou até mesmo proliferar em paisagens antrópicas de florestas secas a úmidas.
Article
Full-text available
Understanding how environmental factors modulate foraging is key to recognizing the adaptive value of animal behavior, especially in ectothermic organisms such as ants. We experimentally analyzed the effect of rain on the foraging of leaf-cutting ants, a key ant group that is commonly found in rainy habitats. Specifically, we experimentally discriminate among direct and indirect effects of rain on laden ants and explore whether ants respond to rain predictors by incrementing their speed. Watered loads were frequently dropped although ants were not wet, and watered ants also dropped their loads although loads were not wet. Watered leaf fragments increased their weight by 143% and were dropped independently with regards to area or symmetry. Watering the trail did not affect the proportion of ants that dropped their loads. Ants increased their speed by 30% after experimental increments in relative humidity and the noise of raindrops on leaves near the trail. Our experimental results confirm earlier anecdotic evidence of the negative effect of rainfall on the foraging of leaf-cutting ants. We demonstrate that rain can strongly limit ant foraging through different mechanisms, affecting both the ant itself, and the maneuverability of laden ants, by increasing the weight of their loads. We also depict behavioral responses that may mitigate this negative effect on foraging: walking faster at signals of rainfall to reduce the portion of leaf fragments lost. Our results illustrate how environmental factors can directly and indirectly constrain ant foraging and highlight the relevance of behavioral responses to mitigate these effects.
Article
Leaf-cutting ants produce large quantities of waste that harbor bacteria and fungi that are harmful to the colony. To be protected from these pathogens, the workers of Atta species present a sophisticated organization to manage harmful material, which can be deposited outside the nest or in internal chambers. However, little is known about the behavior of Acromyrmex species in handling and disposal of waste. Due to some observations, we assume that the same species of Acromyrmex can deposit waste outside the nest and into internal chambers and raise the following question: what determines the occurrence of internal waste chambers in Acromyrmex? To address this question, we verified whether nest depth influences the waste-chamber occurrence. We also verified the nest structure and the abiotic factors of soil beside each waste-chamber: pH and water content of the soil. For this, eight nests were excavated for Acromyrmex balzani and Acromyrmex rugosus rugosus. We verified that not only can the same leaf-cutting ant species deposit debris both outside and inside the nest but also the same nest can present internal chambers and external waste deposit. The soil beside the waste chamber always presented an acidic pH, while the humidity varied widely. Our results showed that the nest depth was highly correlated with the depth of the waste chamber (p = 0.0003) and probably has some influence on waste disposal. The characteristics of the nest and the role of depth in the choice of waste chamber location are discussed.
Article
Civilization and Industrialization are two main side effects of overpopulation. Production of food and living requirement for new generations needs raw materials and production process as well as changing natural environment for infrastructure construction. Huge municipal solid waste, anthropological pollution in terrestrial, aquatic and atmosphere media are responses of numerous industries for engaging with humankind requirement. Economic circumstances, ecological condition as well as effective management of production process by selecting smart managing methods in order to decreasing hazardous wastes which produce throughout the manufacturing human living requirements, will be a suitable or even favorable target for green living and environmental protection. This manuscript will discuss on wastes sources, production and practical strategies for decreasing their hazard effect throughout current human activities. In other words, how civilization and industrialization can engage with emerging requirements of humankind as well as concerning to environmental protection?
Article
Full-text available
An important issue in the evolution of group living is the risk of pathogen and predator exposure entailed by the inherent accumulation of feces within a nesting site. While many group living species limit this risk by cleaning the nest, others do not, raising questions about the benefits of maintaining feces in the nest and their importance in social evolution. Here, we investigated whether one of these benefits could be mediated by coprophagy in families of the European earwig, Forficula auricularia. In this insect species, mothers and mobile juveniles (nymphs) line their nests with feces and consume them. In a first experiment, we tested whether access to feces produced by either nymphs or mothers affects nymph survival in both presence and absence of food. The results showed that access to sibling feces, but not mother feces, enhanced offspring survival under food deprivation. Such an effect did not occur when regular food was available. We then conducted a food-choice experiment to reveal whether nymphs prefer food to feces, and if they discriminate between feces from their mother, unrelated adult females, unrelated nymphs, or their siblings. We found that offspring generally preferred regular food to feces, but nevertheless always consumed some feces. By contrast, nymphs showed no preference between related sibling or mother feces and did not discriminate between feces from related and unrelated individuals. Overall, our results suggest that the benefits of coprophagy could favor the maintenance of feces within the nest and promote the evolution of social life.
Article
Full-text available
Fungus-gardening (attine) ants grow fungus for food in protected gardens, which contain beneficial, auxiliary microbes, but also microbes harmful to gardens. Among these potentially pathogenic microorganisms, the most consistently isolated are fungi in the genus Escovopsis, which are thought to co-evolve with ants and their cultivar in a tripartite model. To test clade-to-clade correspondence between Escovopsis and ants in the higher attine symbiosis (including leaf-cutting and non-leaf-cutting ants), we amassed a geographically comprehensive collection of Escovopsis from Mexico to southern Brazil, and reconstructed the corresponding Escovopsis phylogeny. Contrary to previous analyses reporting phylogenetic divergence between Escovopsis from leafcutters and Trachymyrmex ants (non-leafcutter), we found no evidence for such specialization; rather, gardens from leafcutters and non-leafcutters genera can sometimes be infected by closely related strains of Escovopsis, suggesting switches at higher phylogenetic levels than previously reported within the higher attine symbiosis. Analyses identified rare Escovopsis strains that might represent biogeographically restricted endemic species. Phylogenetic patterns correspond to morphological variation of vesicle type (hyphal structures supporting spore-bearing cells), separating Escovopsis with phylogenetically derived cylindrical vesicles from ancestral Escovopsis with globose vesicles. The new phylogenetic insights provide an improved basis for future taxonomic and ecological studies of Escovopsis.
Article
Full-text available
Fungus-farming (attine) ant agriculture is made up of five known agricultural systems characterized by remarkable symbiont fi- delity in which five phylogenetic groups of ants faithfully cultivate five phylogenetic groups of fungi. Here we describe the first case of a lower- attine ant cultivating a higher-attine fungus based on our discovery of a Brazilian population of the relictual fungus-farming ant Aptero- stigma megacephala, known previously from four stray specimens from Peru and Colombia. We find that A. megacephala is the sole sur- viving representative of an ancient lineage that diverged ∼39 million years ago, very early in the ∼55-million-year evolution of fungus- farming ants. Contrary to all previously known patterns of ant-fungus symbiont fidelity, A. megacephala cultivates Leucoagaricus gongylo- phorus, a highly domesticated fungal cultivar that originated only 2–8 million years ago in the gardens of the highly derived and recently evolved (∼12 million years ago) leaf-cutting ants. Because no other lower fungus-farming ant is known to cultivate any of the higher- attine fungi, let alone the leaf-cutter fungus, A. megacephala may pro- vide important clues about the biological mechanisms constraining the otherwise seemingly obligate ant-fungus associations that charac- terize attine ant agriculture.
Article
Full-text available
Sanitary behaviour is an important, but seldom studied, aspect of social living. Social insects have developed several strategies for dealing with waste and faecal matter, including dumping waste outside the nest and forming specialised waste-storage chambers. In some cases waste material and faeces are put to use, either as a construction material or as a long-lasting signal, suggesting that faeces and waste may not always be dangerous. Here we examine a previously undescribed behaviour in ants - the formation of well-defined faecal patches. Lasius niger ants were housed in plaster nests and provided with coloured sucrose solution. After two months, 1-4 well defined dark patches, the colour of the sucrose solution, formed within each of the plaster nests. These patches never contained other waste material such as uneaten food items, or nestmate corpses. Such waste was collected in waste piles outside the nest. The coloured patches were thus distinct from previously described 'kitchen middens' in ants, and are best described as 'toilets'. Why faeces is not removed with other waste materials is unclear. The presence of the toilets inside the nest suggests that they may not be an important source of pathogens, and may have a beneficial role.
Article
Full-text available
Colonially nesting Cliff Swallows (Passeriformes: Hirundo pyrrhonota) in southwestern Nebraska, USA, are commonly parasitized by hematophagous swallow bugs (Hemiptera: Cimicidae: Oeciacus vicarius) and fleas (Siphonaptera: Ceratophyllidae: Ceratophyllus celsus). We examined to what degree these ectoparasites represent a cost of coloniality for Cliff Swallows. The number of swallow bugs per nest increased significantly with Cliff Swallow colony size. Body mass of nestling swallows at 10 d of age declined significantly as the number of bugs per nestling increased. By fumigating half of the nests in some colonies, killing the bugs, and leaving half of the nests as nonfumigated controls, we showed that swallow bugs lower nestling body mass and nestling body mass and nestling survivorship in large Cliff Swallow colonies but not in small ones. Bugs cost nestlings, on average, up to 3.4 g in body mass, and reduced survivorship by up to 50%. Parasitism by fleas showed no consistent relationship with colony size during the nestling period but increased significantly with colony size early in the season, when birds were first arriving in the study area. Flees did not affect nestling body mass or survivorship and thus, unlike swallow bugs, are probably not important costs of coloniality to Cliff Swallows. Field observations and nest fumigation experiments showed that Cliff Swallows apparently assess which nests are heavily infested with swallow bugs early each spring and select parasite-free nests, leading sometimes to alternate-year colony site usage. Cliff Swallows were more likely to construct new nests (rather than reusing old ones) in large colonies than in small colonies, probably in response to heavier infestations of ectoparasites in the existing nests of large colonies.
Article
Full-text available
Sociality increases exposure to pathogens. Therefore, social insects have developed a wide range of behavioural defences, known as 'social immunity'. However, the benefits of these behaviours in terms of colony survival have been scarcely investigated. We tested the survival advantage of prophylaxis, i.e. corpse removal, in ants. Over 50 days, we compared the survival of ants in colonies that were free to remove corpses with those that were restricted in their corpse removal. From Day 8 onwards, the survival of adult workers was significantly higher in colonies that were allowed to remove corpses normally. Overall, larvae survived better than adults, but were slightly affected by the presence of corpses in the nest. When removal was restricted, ants removed as many corpses as they could and moved the remaining corpses away from brood, typically to the nest corners. These results show the importance of nest maintenance and prophylactic behaviour in social insects.
Article
Full-text available
Emigration of a colony of the leaf-cutting ant Acromyrmex heyeri Forel (Hymenoptera, Formicidae). Colony migration is a poorly studied phenomenon in leaf-cutting ants. Here we report on the emigration of a colony of the leaf-cutting ant A. heyeri in Brazil. The colony emigrated to a new location 47.4 m away from the original nest site, possibly because it had undergone considerable stress due to competitive interactions with a colony of Acromyrmex crassispinus.
Article
Full-text available
During colony growth, leaf-cutting ants enlarge their nests by excavating tunnels and chambers housing their fungus gardens and brood. Workers are expected to excavate new nest chambers at locations across the soil profile that offer suitable environmental conditions for brood and fungus rearing. It is an open question whether new chambers are excavated in advance, or will emerge around brood or fungus initially relocated to a suitable site in a previously-excavated tunnel. In the laboratory, we investigated the mechanisms underlying the excavation of new nest chambers in the leaf-cutting ant Acromyrmex lundi. Specifically, we asked whether workers relocate brood and fungus to suitable nest locations, and to what extent the relocated items trigger the excavation of a nest chamber and influence its shape. When brood and fungus were exposed to unfavorable environmental conditions, either low temperatures or low humidity, both were relocated, but ants clearly preferred to relocate the brood first. Workers relocated fungus to places containing brood, demonstrating that subsequent fungus relocation spatially follows the brood deposition. In addition, more ants aggregated at sites containing brood. When presented with a choice between two otherwise identical digging sites, but one containing brood, ants' excavation activity was higher at this site, and the shape of the excavated cavity was more rounded and chamber-like. The presence of fungus also led to the excavation of rounder shapes, with higher excavation activity at the site that also contained brood. We argue that during colony growth, workers preferentially relocate brood to suitable locations along a tunnel, and that relocated brood spatially guides fungus relocation and leads to increased digging activity around them. We suggest that nest chambers are not excavated in advance, but emerge through a self-organized process resulting from the aggregation of workers and their density-dependent digging behavior around the relocated brood and fungus.
Article
Full-text available
We developed a linear-time algorithm applicable to a large class of trait evolution models, for efficient likelihood calculations and parameter inference on very large trees. Our algorithm solves the traditional computational burden associated with two key terms, namely the determinant of the phylogenetic covariance matrix V and quadratic products involving the inverse of V. Applications include Gaussian models such as Brownian motion (BM) derived models like Pagel's lambda, kappa, delta and the early-burst model; Ornstein-Uhlenbeck models to account for natural selection with possibly varying selection parameters along the tree; as well as non-Gaussian models such as phylogenetic logistic regression, phylogenetic Poisson regression and phylogenetic generalized linear mixed models. Outside of phylogenetic regression, our algorithm also applies to phylogenetic principal component analysis, phylogenetic discriminant analysis or phylogenetic prediction. The computational gain opens up new avenues for complex models or extensive resampling procedures on very large trees. We identify the class of models that our algorithm can handle as all models whose covariance matrix has a 3-point structure. We further show that this structure uniquely identifies a rooted tree whose branch lengths parametrize the trait covariance matrix, which acts as a similarity matrix. The new algorithm is implemented in the R package phylolm, including functions for phylogenetic linear regression and phylogenetic logistic regression.
Article
Full-text available
Symbiotic relationships modulate the evolution of living organisms in all levels of biological organization. A notable example of symbiosis is that of attine ants (Attini; Formicidae: Hymenoptera) and their fungal cultivars (Lepiotaceae and Pterulaceae; Agaricales: Basidiomycota). In recent years, this mutualism has emerged as a model system for studying coevolution, speciation, and multitrophic interactions. Ubiquitous in this ant-fungal symbiosis is the "weedy" fungus Escovopsis (Hypocreales: Ascomycota), known only as a mycoparasite of attine fungal gardens. Despite interest in its biology, ecology and molecular phylogeny-noting, especially, the high genetic diversity encountered-which has led to a steady flow of publications over the past decade, only two species of Escovopsis have formally been described. We sampled from fungal gardens and garden waste (middens) of nests of the leaf-cutting ant genus Acromyrmex in a remnant of subtropical Atlantic rainforest in Minas Gerais, Brazil. In culture, distinct morphotypes of Escovopsis sensu lato were recognized. Using both morphological and molecular analyses, three new species of Escovopsis were identified. These are described and illustrated herein-E. lentecrescens, E. microspora, and E. moelleri-together with a re-description of the genus and the type species, E. weberi. The new genus Escovopsioides is erected for a fourth morphotype. We identify, for the first time, a mechanism for horizontal transmission via middens. The present study makes a start at assigning names and formal descriptions to these specific fungal parasites of attine nests. Based on the results of this exploratory and geographically-restricted survey, we expect there to be many more species of the genus Escovopsis and its relatives associated with nests of both the lower and higher Attini throughout their neotropical range, as suggested in previous studies.
Article
Full-text available
Material brought to midden piles of leaf-cutting ants is considered to be hazardous. It is therefore expected that midden workers should not re-enter the colony, to reduce pathogen transmission. Here, we examined whether the midden workers of Atta sexdens rubropilosa remain confined to the waste compartment and, if not, whether they could perform many different behaviors in the absence of specialized nestmates. Eleven subcolonies received either midden workers or non-midden workers in addition to pupae and 50 mL of fungus garden. Survival, fungal and brood care, foraging and waste manipulation were observed daily until subcolonies death. Subcolonies maintained by midden workers died earlier: average survival times were 13.92 and 22.66 days for midden and non-midden workers, respectively. Midden workers cared for the brood and foraged as non-midden workers did but they were not as efficient in caring for the garden. Activities related to waste manipulation were more frequently performed by midden workers. These results show that midden workers are not a behaviorally rigid caste and retain many labor capabilities being able to leave the waste compartment and perform internal activities in the absence of specialized internal workers.
Article
Full-text available
The mounds of ant nests have been characterized as structures that facilitate the colonization of habitats subject to extreme temperatures. My objective was to investigate the importance of the mound of Acromyrmex lobicornis (Formicidae, Attini) in this process. In the most climatically rigorous environment that this ant genus lives (northwestern Patagonia), I determined (1) the temperature range within Acromyrmex lobicornis nest-mounds, (2) the influence of mound damages on the mortality or abandonment rate of Acromyrmex lobicornis nests, and (3) compared, from the existing literature, the distribution limits between the species of Acromyrmex that do and do not construct mounds. The mounds of A. lobicornis function as 'thermal buffers' by diminishing the effects of external thermal variations, and previous mound damage increased mortality or abandonment only of colonies with nest mounds constructed on bare ground. Mounds constructed on tussock plants increased their diameter faster and recovered better from perturbations. This may be due to the structural support of plant stems facilitating repair. At a larger scale, the species of Acromyrmex with mounds have more southerly range limits than species that do not construct mounds, indicating an important function of this nest structure for the colonization of temperate environments.
Article
Full-text available
Hygienic behaviour is an important aspect of social organisation because living in aggregations facilitates the spread of disease. Leaf-cutting ants face the additional problem of an obligatory dependency on a fungus, which itself is also susceptible to parasites. In this study we provide evidence for the importance of effective waste management in colonies of several Panamanian species of Atta and Acromyrmex leaf-cutting ants, differing in colony size and typical mode of waste accumulation (external or internal dumps). We show that: (1) waste is dangerous for the ants, which die at a higher rate in the presence of waste; (2) waste is dangerous for the mutualistic fungus because waste in field colonies is infected with the specialised fungal parasite Escovopsis; (3) the ants allocate considerable effort to active management of waste in order to reduce these dangers. This management follows a “conveyer belt” model according to which increasingly dangerous tasks are performed by older workers, who are less valuable to their colony. Our approach is kaleidoscopic, as different species of leafcutting ants are unequally suitable for direct observation and experimental manipulation, and suggests that more in depth studies of waste management in attine ants would be highly rewarding.
Article
Full-text available
Animals adjust their behaviors in response to changing environmental conditions because the costs and benefits of such behaviors change as conditions change. The reuse of materials from waste (i.e., recycling) rarely occurs in social insects because it may imply significant health risks and behavioral difficulties. However, the benefit of reusing may exceed its costs under certain circumstances. For the first time, we document that ants recycle refuse materials to repair nest-mound damage. We conducted a series of field measurements and experiments to test the hypotheses that fluctuations in this behavior in the leaf-cutting ant Acromyrmex lobicornis depend on 1) seasonal changes in the tendency to reject refuse (a proxy of changes in their pathogen levels), and/or 2) seasonal foraging restrictions. We 1) measured the rejection of foraging ants toward experimental refuse piles among seasons and 2) analyzed how mound condition, temperatures of fungus chamber and soil surface, and foraging activity explained this behavior using a classification tree, a powerful recursive partitioning method. Foraging ants showed similar rejection levels toward refuse piles in different seasons. Colonies repaired mound damage with refuse materials only during the hottest season and when they had low foraging rates, suggesting that ants recycle their refuse by a hierarchical set of decisions dependent on the risk of fungal damage and foraging restrictions. Repairing the mounds is essential during summer, when temperatures inside damaged mounds are lethal to their fungus cultures. However, these high temperatures also restrict the foraging activity, reducing the collection of building materials. Thus, colonies with lower foraging rates apparently use their refuse to repair mounds because this substrate requires less searching and carrying time. The use of refuse did not affect the colony growth rate. This illustrates how ants integrate information about food, hygienic and nest conditions through a novel and plastic behavior: recycling of their discarded materials.
Article
Full-text available
The Chaco leaf-cutting ant Atta vollenweideri (Forel) inhabits large and deep subterranean nests composed of a large number of fungus and refuse chambers. The ants dispose of the excavated soil by forming small pellets that are carried to the surface. For ants in general, the organisation of underground soil transport during nest building remains completely unknown. In the laboratory, we investigated how soil pellets are formed and transported, and whether their occurrence influences the spatial organisation of collective digging. Similar to leaf transport, we discovered size matching between soil pellet mass and carrier mass. Workers observed while digging excavated pellets at a rate of 26 per hour. Each excavator deposited its pellets in an individual cluster, independently of the preferred deposition sites of other excavators. Soil pellets were transported sequentially over 2 m, and the transport involved up to 12 workers belonging to three functionally distinct groups: excavators, several short-distance carriers that dropped the collected pellets after a few centimetres, and long-distance, last carriers that reached the final deposition site. When initiating a new excavation, the proportion of long-distance carriers increased from 18% to 45% within the first five hours, and remained unchanged over more than 20 hours. Accumulated, freshly-excavated pellets significantly influenced the workers’ decision where to start digging in a choice experiment. Thus, pellets temporarily accumulated as a result of their sequential transport provide cues that spatially organise collective nest excavation.
Article
Full-text available
A medium-sized nest of the Texas leafcutting ant, Atta texana (Buckley), in northern Louisiana was excavated completely, and a three-dimensional model of its external and subterranean features was constructed. In total, 97 fungus gardens, 27 dormancy cavities, and 45 detritus cavities were located. At the lower center of the funnel-shaped nest was a large central cavity, which in winter functions as a domicile for the colony and where the alate brood is reared. Vertical tunnels, possibly as deep as 32 m, may serve as wells leading to the water table. Winter mean annual temperatures within the central cavity may limit the northern geographical range of A. texana to ≈33° N latitude. The inquilines Attaphila fungicola Wheeler, Pholeomyia comans Sabrosky, Ceuthophilus sp., Lobopoda subcuneatus Campbell, Geomysaprinus nr. formicus (Hinton), species of Aleocharinae, and a species of Annelida were seen in nest cavities and galleries.
Article
Full-text available
Frequencies of social grooming recorded from 44 species of free-living primates correlate with group size but not body size. This is interpreted as evidence for the social function of grooming and against the purely hygienic function. However, there is some evidence to suggest that body size is a more important determinant of grooming time among platyrrhine primates. This might imply that there has been a shift in the functional system governing grooming during primate evolution.
Article
Full-text available
Living in groups raises important issues concerning waste management and related sanitary risks. Social insects such as ants live at high densities with genetically related individuals within confined and humid nests, all these factors being highly favorable for the spread of pathogens. Therefore, in addition to individual immunity, a social prophylaxis takes place, namely, by the removal of risky items such as corpses and their rejection at a distance from the ant nest. In this study, we investigate how Myrmica rubra workers manage to reduce encounters between potentially hazardous corpses and nestmates. Using both field and laboratory experiments, we describe how the spatial distribution and the removal distance of waste items vary as a function of their associated sanitary risks (inert item vs. corpse). In the field, corpse-carrying ants walked in a rather linear way away from the nest entrance and had an equal probability of choosing any direction. Therefore, they did not aggregate corpses in dedicated areas but scattered them in the environment. In both field and laboratory experiments, ants carrying corpses dropped their load in more remote-and less frequented-areas than workers carrying inert items. However, for equidistant areas, ants did not avoid dropping corpses at a location where they perceived area marking as a cue of high occupancy level by nestmates. Our results suggest that ants use distance to the nest rather than other occupancy cues to limit sanitary risks associated with dead nestmates.
Article
Full-text available
Leaf-cutting ants often avoid contact with their waste because it harbors microorganisms that are dangerous to the ants and their symbiotic fungus. Therefore, the use of ant waste (i.e., refuse dumps) has been proposed as a deterrent method against leafcutter attack. We tested experimentally whether the age of the refuse dump (fresh vs. old) affects the herbivory-deterrent effect against the leaf-cutting ant Acromyrmex lobicornis Emery (Hymenoptera: Formicidae). Refuse placed around seedlings significantly delayed the initiation attacks of leaf-cutting ants, and this deterrent effect decreased gradually over a period of 30 days. The initial strength of this decrease was the same for newly-discarded ( ‘new’) refuse and refuse from the bottom of the ants’ waste pile (‘old’ refuse). However, the loss of deterrent effect over time was more rapid for new than old refuse. A further experimental manipulation, replacement of refuse every 3 days, had no effect on the deterrent effect for old refuse, but increased this effect for new refuse, although the amount of this increase gradually weakened over the course of the 30-day experiment. We speculate on the possible causes of these effects, their consequences for the hygienic behavior of leaf-cutting ants, and on the use of ant debris as short-term control method against leaf-cutting ants.
Article
Full-text available
We revise and key Trachymyrmex ants occurring in North America north of Mexico. We recognize nine species, including one new species from southern Arizona: T. arizonensis (Wheeler), T. carinatus Mackay & Mackay, T. desertorum (Wheeler), T. jamaicensis (André), T. nogalensis Byars, T. pomonae Rabeling & Cover sp. nov., T. septentrionalis (McCook), T. smithi Buren, and T. turrifex (Wheeler). Two infraspecific taxa are synonymized: T. smithi neomexicanus Cole syn. nov. (= T. smithi) and T. turrifex caroli Wheeler syn. nov. (= T. turrifex). We briefly characterize the previously undescribed queens of T. desertorum and T. nogalensis, and the males of T. desertorum and T. turrifex. We include keys for the identification of workers, queens and males, along with distribution maps for all species. A phylogenetic analysis of DNA sequence information for parts of the mitochondrial gene Cytochrome Oxidase 1 and the first intron of the F1 Attini, Formicidae, phylogeny and species boundaries, taxonomy, Trachymyrmex, United States copy of the nuclear protein-coding gene Elongation Factor 1-α, is used to characterize the intra- versus inter-specific genetic variation of several populations per species. The molecular phylogenetic analysis supports our taxonomic con-clusions concerning the North American Trachymyrmex species.
Article
Full-text available
The location of the nutrient-rich organic refuse produced by a leaf-cutting ant colony varies among ant species. Atta cephalotes locate their organic refuse in subterranean chambers, whereas A. colombica place their organic refuse on the soil surface near the nest. We studied the effect of the absence or presence of external organic refuse on the abundance of fine roots and seed bank composition in the superficial horizons of ant nests. We sampled soils from ant nests or dumps and adjacent areas of 15 adult nests of A. cephalotes at La Selva (LS), Costa Rica, and of 15 of A. colombica nests on Barro Colorado Island (BCI), Panama. Soils from A. cephalotes nests did not differ from adjacent soils in abundance of fine-root and seed diversity. In contrast, organic refuse from A. colombica nests was less diverse in seed composition (due to the great abundance of Miconia argentea) and had a greater abundance of fine roots than adjacent areas. Thus the external location of the ant-nest organic refuse is potentially important in determining the different types of plant recolonization in abandoned or dead ant nests. The relative abundance of these Atta species may influence the structure and/or composition of tropical forests.
Article
Full-text available
Foundresses of the leaf-cutting ant Acromyrmex octospinosus in central Panam forage for leaves as garden substrate (semi-claustral foundation). The fungal pellet and substrate usually are attached to rootlets, which are used as a platform for the garden. This arrangement keeps the garden suspended away from the earthen chamber of the underground nest during early colony growth, and we hypothesize that it serves to minimize contact between the garden and contaminants. A. octospinosus foundresses produce from 3 to 7 workers in 2.7 months after founding the nest, but workers do not forage for substrate at this time. Incipient nests died or were abandoned at a monthly rate of ca. 50%. We show that ants routinely clean their legs before manipulating the garden substrate. We also describe how foundresses use their fore-legs to rub the surface of the metapleural gland (MPG), and they then use typical grooming behaviors to pass the forelegs through the mouthparts, after which the ant then licks the garden substrate. Similarly, ants apparently use their mouths to transfer fecal droplets to their legs. We briefly discuss the functional significance of these grooming behaviors, and hypothesize that they are prophylactic behaviors that may help the foundress maintain a hygienic garden.
Article
Full-text available
A task is said to be partitioned when it is split into two or more sequential stages and material is passed from one worker to another; for instance, one individual collects a material from a source and passes it to another for transportation back to the nest. In this study, we review the existence of task partitioning in leafcutting ants (Attini) and find that, across species, this form of work organisation occurs in all stages of leaf collection, leaf transportation, and leaf processing within the nest; in the deposition of refuse (leaves and spent fungal garden) to internal or external dumps; and in colony emigration. Thus, task partitioning is shown to be a very important component of work organisation in leafcutting ants. Examples mostly concern Atta but task partitioning is also known in Acromyrmex. The costs and benefits of task partitioning of the various stages are discussed and suggestions for further research are highlighted.
Article
Full-text available
Emerys rule predicts that social parasites and their hosts share common ancestry and are therefore likely to be close relatives. Within the leaf-cutting ant genus Acromyrmex, two taxa of social parasites have been found, which are thought to occupy opposite grades of permanent social parasitism, based on their contrasting morphologies: Acromyrmex insinuator differs little in morphology from its free-living congeneric host species and produces a worker caste, and is thus thought to represent an early grade of social parasitism. At the other extreme, Pseudoatta spp. exhibit a very specialised morphology and lack a worker caste, both of which are characteristics of an evolutionarily derived grade of social parasitism. Here we present a molecular phylogeny using partial sequences of cytochrome oxidase I and II of about half of the known Acromyrmex species including two social parasites, their hosts and all congeneric species occurring sympatrically. We show that the two inquiline parasites represent two separate origins of social parasitism in the genus Acromyrmex. The early-grade social parasite A. insinuator is highly likely to be the sister species of its host Acromyrmex echinator, but the derived social parasite Pseudoatta sp. is not the sister species of its extant host Acromyrmex rugosus.
Article
Full-text available
The prominent nests mounds of many ant species are one of the most obvious signs of their presence, yet the subterranean architecture of nests is often poorly known. The present work aimed to establish the external and internal structure of nests of a species of leaf-cutting ant, Acromyrmex rugosus rugosus, by either marking the interior of nests with talcum powder, or forming casts with cement. Twelve nests were excavated and surveyed, with eight being marked with talcum powder and four cast with cement. The external and internal structure of the nests was highly variable. The largest and smallest nests had mound areas of 9.89 m2 and 0.01 m2 respectively. The number of chambers found ranged from 1 to 26, with maximum dimensions of between 6 and 70 cm. Chambers were found close to the soil surface (6 cm) down to a maximum depth of 3.75 m. In addition to chambers containing fungus garden, some chambers were found to be empty, filled with soil or filled with waste, the first time this has been recorded in a species of Acromyrmex. The nests of A. rugosus rugosus appear to be unusually complex for the genus, containing a diversity of irregular chambers and tunnels.
Article
Full-text available
Division of labour is the hallmark of the success of many social animals. It may be especially important with regard to waste management because waste often contains pathogens or hazardous toxins and worker specialisation can reduce the number of group members exposed to it. Here we examine waste management in a fungus-farming, leaf-cutting ant, Acromyrmex echinatior, in which waste management is necessary to protect their vulnerable fungal crop. By marking ants with task-specific paint colours, we found clear division of labour between workers that engage in waste management and those that forage, at least during the fine timescale of the 3-day marking period. This division of labour was influenced by both age and size, with waste management workers tending to be smaller and younger than foragers. The role of preventing contaminated ants from entering the colony was fulfilled mainly by medium-sized workers. When the level of waste was experimentally increased, most of the ants that responded to remove the waste were workers previously engaged in tasks inside the nest rather than external waste workers or foragers. These responding workers tended to be young and medium-sized. Surprisingly, the responding ants were subsequently able to revert back to working within the fungus garden, but the probability of them doing so depended on their age and the length of time they were exposed to waste. The results demonstrate the importance of division of labour with regard to waste management in A. echinatior and show that this is adaptable to changing needs. KeywordsSocial insect-Hygiene-Caste-Polyethism-Stimulus-response threshold
Article
Full-text available
We studied the organisation of garbage disposal and management in the leafcutting ant Atta cephalotes. The nest of this species has an internal garbage heap to which waste from the fungus garden is taken. The transport of waste from the fungus gardens to the garbage heaps is an example of task partitioning. Ninety-four percent of the garbage loads transferred from the fungus garden to the garbage heap were transferred indirectly via a caching site just outside the garbage heap entrance. A further 3% were transferred directly from a fungus garden worker to a garbage heap worker, again just outside the heap entrance. Only 3% were taken directly to the garbage heap without task partitioning. This is the first described example of task partitioning in insect societies for work other than foraging and the first example of task partitioning occurring entirely within the nest. Furthermore, there is a strong division of labour between the fungus garden workers and the garbage heap workers, with garbage workers hardly ever leaving the heap. Division of labour is reinforced by aggressive behaviour directed towards workers contaminated with garbage. This pattern of work organisation minimises contact between garbage heap workers, who are probably contaminated with pathogens hazardous to both the ants and their symbiotic fungus, and both fungus garden workers and the fungus garden. Task partitioning, division of labour (reinforced by aggression) and nest compartmentalisation act synergistically to isolate the hazardous garbage heap from the fungus gardens.
Article
Full-text available
Leaf-cutting ant queens excavate a founding nest consisting of a vertical tunnel and a final horizontal chamber. Nest foundation is very time consuming, and colony success depends on the excavated depth. Although shallow nests may be energetically cheaper to dig, queens may be more exposed to the changing environment. Deeper chambers, in contrast, may be climatically more stable, but are more expensive to dig. We investigated the mechanisms underlying the control of nest depth in queens of the leaf-cutting ant Atta vollenweideri. We focused on the use of internal information for the control of nest depth, and therefore maintained the soil and environmental conditions invariant during the different laboratory experiments. We compared the tunnel lengths excavated by queens that were able to complete their nests earlier, faster or slower than under standard conditions. An earlier and faster nest completion was obtained by offering queens either pre-excavated tunnels of different lengths, soils at different temperatures, or soft sandy soils. A slower nest excavation was induced by offering queens harder dry soils, and by delaying the start of digging several days after the nuptial flight. Results indicate that the determination of nest depth was a regulated process involving the use of internal references: queens excavated their tunnels either until a particular depth was reached or for some predetermined length of time. Queens appear to monitor their movements while walking up und down the tunnel, and to compare this sensory information with a motor command that represents a preset tunnel length to be excavated before switching to chamber digging. In addition to this form of idiothetic control, results indicate that the elapsed digging time also feeds back onto the control system. It is argued that the determination of nest depth, i.e. the transition from tunnel to chamber digging, is initiated either after a preset tunnel length is reached, or as soon as a maximal time interval has elapsed, irrespective of the excavated tunnel length. A control system using both idiothetic and temporal information, as demonstrated in the present study, allows queens to flexibly react to different soil conditions, and therefore avoid excessive time and energy investments. Possible mechanisms underlying the control of chamber size are also discussed.
Article
Full-text available
The thermal limits of individual animals were originally proposed as a link between animal physiology and thermal ecology. Although this link is valid in theory, the evaluation of physiological tolerances involves some problems that are the focus of this study. One rationale was that heating rates shall influence upper critical limits, so that ecological thermal limits need to consider experimental heating rates. In addition, if thermal limits are not surpassed in experiments, subsequent tests of the same individual should yield similar results or produce evidence of hardening. Finally, several non-controlled variables such as time under experimental conditions and procedures may affect results. To analyze these issues we conducted an integrative study of upper critical temperatures in a single species, the ant Atta sexdens rubropiosa, an animal model providing large numbers of individuals of diverse sizes but similar genetic makeup. Our specific aims were to test the 1) influence of heating rates in the experimental evaluation of upper critical temperature, 2) assumptions of absence of physical damage and reproducibility, and 3) sources of variance often overlooked in the thermal-limits literature; and 4) to introduce some experimental approaches that may help researchers to separate physiological and methodological issues. The upper thermal limits were influenced by both heating rates and body mass. In the latter case, the effect was physiological rather than methodological. The critical temperature decreased during subsequent tests performed on the same individual ants, even one week after the initial test. Accordingly, upper thermal limits may have been overestimated by our (and typical) protocols. Heating rates, body mass, procedures independent of temperature and other variables may affect the estimation of upper critical temperatures. Therefore, based on our data, we offer suggestions to enhance the quality of measurements, and offer recommendations to authors aiming to compile and analyze databases from the literature.
Article
Full-text available
Nest foundation in the leaf-cutting ant Atta sexdens is claustral, and the single queen completely relies on its body reserves throughout, approximately, 9 weeks until the first workers emerge and initiate foraging. Nest digging is much time- and energy-consuming, and it is an open question how queens decide on the length of the tunnel they dig and therefore the depth of the initial chamber. Shallow founding nests may be energetically cheaper to dig, but queens may be more exposed to changing environmental variables. Deeper nests, on the other hand, may be climatically more stable and suitable, but more expensive to dig. We hypothesized that the maximal nest depth excavated by Atta founding queens may represent the outcome of an evolutionary trade-off between maximizing nest depth and minimizing energy expenditure during digging, so as to save energy for the long claustral phase. We tested this hypothesis by comparing the fitness consequences of increased digging effort in queens that were experimentally stimulated to excavate a complete founding nest either once, twice or three times consecutively compared to control queens that did not dig. Fitness was quantified as mortality rates, rates of egg-laying and offspring production, and size of the fungus garden until the emergence of the first workers. Results showed that, in contrast with the initial expectations, fungus growth, egg-laying rates and offspring production were not affected by the increased digging effort in the experimentally induced successive excavations. However, a significant higher mortality was observed in queens with increased digging effort, i.e., those that dug two or three nests consecutively. It is argued that in queens a behavioral mechanism for the control of nest depth has evolutionary been selected for as a trade-off between maximizing nest depth, to favor protection of the queen against unsuitable environmental variables, and minimizing energy expenditure during digging, which significantly affects survival.
Article
Full-text available
In leaf-cutting ants, the handling of waste materials from the fungus culture increases the risk of infection. Consequently, ants should manage their waste in a way that minimizes the spread of diseases. We investigated whether in Acromyrmex lobicornis, waste-worker ants (a) also perform roles in foraging or mound maintenance, (b) are morphologically different than other ant workers, and (c) are aggressively discriminated by other worker ants from the same colony. In addition, we investigated whether the location of external waste piles minimizes the probability that wastes spread to the ant nest. In the field, we (a) marked with different colours waste-workers, foragers and mound-workers and monitored whether these ants interchanged their tasks; (b) measured head width, head length, hind femur length and total length of waste-workers; foragers and mound-workers; (c) forced field encounters between waste-workers and foragers, and (d) measured the cardinal orientation of the waste piles in relation to the colony mound. Waste-worker ants did not perform other function outside the nest; neither foragers nor mound-workers managed the waste. Moreover, waste-workers were smaller than foragers and mound-workers, and were attacked if they tried to enter their nest using foraging entrances. The location of external refuse dumps also appears to reduce contamination risks. Waste piles always were down-slope, and often followed the prevailing wind direction. The importance of behaviours such as the division of labour, aggressions against waste-workers and nest compartmentalization (i.e., the orientation of external waste piles) to minimize the spread of pathogens is discussed.
Book
This chapter introduces key themes from the book, reflecting the topics of the 'Awareness of the Health Impacts of Waste Management Policies' Seminar, in Kos, Greece. November, 1998. The waste management and health scene is introduced by an outline of concems relating to persistent organic pollutants, as well as through perspectives from Less Developed Countries and from industry. An overview of policy lines for waste management includes an assessment of recent proposals by the European Commission, as well as selected examples from European countries and the USA. Descriptions of developments in research, tools and conceptual approaches for waste management and health issues are provided. Research into health effects of dioxins and PCBs is outlined, as are reviews of technological options for waste management, proposed developments in health impact assessment, environmental taxes as a waste management tool, and integrated regional waste management approaches. A series of case studies provide real­ world examples of research and policy development including a review of the effects of waste management on wildlife and domestic animals. In conclusion, important crossover themes and challenges are outlined. Topical issues include differences between technological capacity and actual performance, burden of proof and the precautionary principle, hazard versus risk assessment, and societal dimensions of awareness and attitudes. Time-lag, intergenerational effects and the introduction of the chemical hygiene concept are highlighted as important considerations, as well as the general need for prioritisation of the child and infant in all regulatory procedures.
Article
The numbers of chewing lice were determined for adult bee-eaters and related to different measures of breeding density. Bee-eaters are infested by three species of chewing lice (Meropoecus meropis, Meromenopon meropis and Brueelia apiastri). Meropoecus meropis is the most common species and 94% of all adult bee-eaters were infested. This species also shows a significant variation between colonies, namely, infestation rate increases with colony size. Using different measures to describe colony size, a stepwise regression analysis showed that inter-nest distance is the best predictor for ecoparasite load. Average infestation rate per individual decreased significantly with increasing inter-nest distance. This relationship was even more pronounced for the maximum number of parasites found within a colony and with the variation in parasite load among members of a colony (controlling for number of breeding pairs). There was no difference in ectoparasite load between the sexes and no general patterns related to the position of the breeding site within the colony.
Article
Foraging by marked Trachymyrmex turrifex ants was examined over a 3-week period in Austin, Texas. Ants foraged nocturnally and collected plant debris and insect frass, but they did not cut live vegetation. Individual ants showed no fidelity to food type or foraging route.
Article
The size of groups formed by social animals is thought to result from a combination of selection pressures acting on individuals to maximize their fitness. In addition to commonly-invoked selective agents (e.g., predation), a growing number of studies suggest that levels of parasitism may be related to host group size and that parasites may influence optimal group size. We used a meta-analysis to quantify the intraspecific association found in published studies between prevalence and intensity of parasitism and host group size in a variety of taxa. We considered separately contagious parasites, which are transmitted via contact with infected individuals or feces, and mobile parasites which do not need proximity among hosts for transmission. In addition to mode of transmission, host group mobility was examined as a potential correlate of the association. Consistent positive correlations were found between host group size and both the prevalence and intensity of contagious parasites. By contrast, the intensity of infection by mobile parasites consistently decreased as host group size increased. Host group mobility had no apparent effect on either the strength or the direction of these correlations. Although few experimental studies examined the causal effect of parasitism on host group size, strong circumstantial evidence was provided, at least for mobile parasites, by many reports of larger host group sizes following increases in parasite abundance. Our results therefore suggest that parasites with different modes of transmission can exert conflicting selection on host group size. The trends found in the meta-analysis, however, do not hold in interspecific comparative studies, possibly owing to differences among related species in the relative importance of parasitism as a selective force.
Article
En un bosque de pino, Pinus palustris Mill., del norte de Florida se llevó a cabo la investigación de ciertos aspectos ecológicos relacionados con la producción de la hormiga Trachymyrmex septentrionalis McCook. Este tipo de hormiga es muy abundante en hábitats secos y arenosos (sandhills) del Bosque Nacional Apalachicola (Apalachicola National Forest); una hectárea contiene una media de 1.000 colonias, 235.000 hormigas obreras T. septentrionalis y 3,5 kg de jardín de hongos. Tras calcular el tamaño y la productividad de la colonia a partir de nuestras excavaciones y del peso de la arena en el túmulo, se observó que los nidos eran más grandes y que la mayor parte de las crías se producían en hábitats descubiertos, sin árboles. Por el contrario, los nidos más pequeños y menos productivos se encontraban en zonas arboladas. Nuestros datos indican que la tierra caliente de espacios abiertos estimula la actividad de la hormiga obrera y el crecimiento de la colonia, mientras que la tierra fría de zonas en sombra reduce la actividad de las mismas. Asimismo, las tierras calientes en extremo pueden llegar a ser fatales para estas hormigas y su jardín de hongos. Todo ello sugiere que la especie T. septentrionalis es indicadora de hábitats secos y arenosos intactos en los bosques de pino, ya que su actividad se relaciona de manera positiva con las principales alteraciones naturales del bosque; por ejemplo, los incendios que se producen con frecuencia en el verano. El desplazamiento de la tierra es uno de los principales efectos producidos por este tipo de hormiga en el ecosistema forestal—una colonia excava más de una tonelada métrica de tierra en una hectárea de bosque de pino cada año. Probablemente, esta rotación de la tierra tiene efectos significativos en estas zonas arenosas y pobres en nutrientes. Es necesario realizar experimentos para determinar cuál es el papel de este tipo de hormiga tan abundante en los bosques de pino.
Article
Leaf-cutting ants (genera Atta and Acromyrmex) are considered dominant herbivores of Neotropical forests. However, so far quantitative, long-term, and large-scale assessments of their impact on these ecosystems are rare, because the available assessment methods were laborious and/or destructive. We describe a rapid, nondestructive, and inexpensive method to estimate the long-term harvest of Atta colombica colonies. Workers of A. colombica dump the colony refuse (exhausted fungal substrate) outside the nest. A single trail connects the refuse pile and the nest. In contrast to the foraging activity, the refuse deposition rate (the number of deposited refuse particles per minute) is diurnally constant and varies little on subsequent days. The number of refuse particles deposited per day was tightly correlated with the number of harvested fragments in nests of differing sizes (R-2 = 0.77, P < 0.0001). Therefore, the daily harvest of a particular colony can be calculated from short-term counts (5 min) of the refuse deposition rate at any time of the day. Combining these data with information on average fragment size (weight and/or area) allows the calculation of the total daily amount of biomass and/or foliage area harvested by the colony. This new method facilitates quantifying A. colombica herbivory on scales of populations and ecosystems, or over long-term scales.
Article
The prevalence and impact of a specialized microfungal parasite (Escovopsis) that infects the fungus gardens of leaf-cutting ants was examined in the laboratory and in the field in Panama. Escovopsis is a common parasite of leaf-cutting ant colonies and is apparently more frequent in Acromyrmex spp. gardens than in gardens of the more phylogenetically derived genus Atta spp. In addition, larger colonies of Atta spp. appear to be less frequently infected with the parasite. In this study, the parasite Escovopsis had a major impact on the success of this mutualism among ants, fungi, and bacteria. Infected colonies had a significantly lower rate of fungus garden accumulation and produced substantially fewer workers. In addition, the extent of the reduction in colony growth rate depended on the isolate, with one isolate having a significantly larger impact than two others, suggesting that Escovopsis has different levels of virulence. Escovopsis is also spatially concentrated within parts of ant fungus gardens, with the younger regions having significantly lower rates of infection as compared to the older regions. The discovery that gardens of fungus-growing ants are host to a virulent pathogen that is not related to any of the three mutualists suggests that unrelated organisms may be important but primarily overlooked components of other mutualistic associations.
Article
Leave cutting ants rely on a fungus garden as their main food supply. This garden produces debris that must be disposed by workers, as it may favor the contamination of the fungus. We assumed that the growth of undesired microorganisms on garbage would increase with humidity, therefore drier areas should be more suitable for garbage disposal. Accordingly, we tested the hypothesis that leave-cutting ants Atta sexdens rubropilosa choose drier chambers for garbage disposal. We found that 30 out of 30 sub-colonies tested for hygropreference chose drier chambers for garbage disposal when offered a choice between dry (RH=25±5% SD) and humid (RH=95±5% SD) chambers.
Article
Parasitism is widely viewed as the primary cost of sociality and a constraint on group size, yet studies report varied associations between group size and parasitism. Using the largest database of its kind, we performed a meta-analysis of 69 studies of the relationship between group size and parasite risk, as measured by parasitism and immune defenses. We predicted a positive correlation between group size and parasitism with organisms that show contagious and environmental transmission and a negative correlation for searching parasites, parasitoids, and possibly vector-borne parasites (on the basis of the encounter-dilution effect). Overall, we found a positive effect of group size (r = 0.187) that varied in magnitude across transmission modes and measures of parasite risk, with only weak indications of publication bias. Among different groups of hosts, we found a stronger relationship between group size and parasite risk in birds than in mammals, which may be driven by ecological and social factors. A metaregression showed that effect sizes increased with maximum group size. Phylogenetic meta-analyses revealed no evidence for phylogenetic signal in the strength of the group size-parasitism relationship. We conclude that group size is a weak predictor of parasite risk except in species that live in large aggregations, such as colonial birds, in which effect sizes are larger.
Article
Division of labour was studied in a colony ofM. favosa with individually age-marked workers. The average longevity of these workers was 40 days. Construction and provisioning of brood cells, and operculation of provisioned cells, is performed most by bees aged 8–12 days. Worker ovipositions occur between 9–27 days of age, while workers of 15–16 days are most active in this respect. Waste-processing at the rubbish dump ic carried out by bees of nearly all ages. Guarding is performed by bees aged 19–48 days. From the study of egg-laying behaviour of individual workers, and from the occurrence of ovary development in fixed age-marked bees, we inferred that all workers were once layers. About 50% of the workers may lay one egg and the other 50% may lay two eggs. The laying of three eggs by one worker was observed once. The successive eggs of a single worker may be laid at varying intervals, ranging from 0–8 days. Laying workers are not the main provisioners of the cell in which they lay. Regularly they do not even discharge larval food in this cell at all, since they generally lay their eggs at the end of the period of several days in which they are active dischargers. The evolution of egg-laying by workers is discussed. In this respect reference is also made to our recent finding of an as yet unknown form of queen dominance in bees. This pertains to her control of the quality of the worker-laid eggs. The comparison between the ontogenetic division of labour in stingless bees and honeybees reveals distinct disparities with respect to the temporal organization of nest activities and the general occurrence of queenright worker oviposition.