Abstract
Leaf-cutter ants (Atta and Acromyrmex species) exhibit complex social organizations that have fascinated scientists for decades. The leaf-cutter ants belong to a subgroup of fungus-growing ants, which live with fungus inside their nests. The behaviours exhibited by these ants are closely linked to their social organization, which involves intricate division of labour, caste systems, and cooperative tasks. This review article provides an overview of the behaviors associated with the social organization of leaf-cutter ants. It explores various aspects of their social organization, including foraging behavior, hitchhiking behaviour, hygienic behaviour, social organization and environmental influences. The leaf cutter ants have the instinct to forage, as they walk around the nest to cut leaf fragments from plants, then transport those fragments with their jaws and go back to the nest to cultivate a special fungus garden within the colony. By synthesizing existing knowledge, this review highlights the intricate relationships between behaviors and the social structure of leaf-cutter ants, shedding light on the underlying mechanisms and evolutionary implications. Furthermore, it identifies research gaps and proposes future directions for studying leaf-cutter ant behaviors, including emerging techniques and interdisciplinary approaches. The behaviors correlating with the social organization of leaf-cutter ants showcase the intricate mechanisms underlying their highly organized societies. In conclusion, this review contributes to our understanding of the fascinating behaviors exhibited by leaf-cutter ants and their implications in the broader context of social insect societies.
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1 Introduction
The most dominant members of many terrestrial ecosystems are ants, which could indicate the many environmental changes that have occurred [1]. The ants comprise up to 20% of all terrestrial animal biomass involving rise up to 20% of all terrestrial animal biomass involving ants, constituting around 25% of all animal biomass in the new world tropics [2]. Recently, it has been estimated the total biomass of ants equals 20% of human biomass [3]. The most important and unique Neotropical ants are leaf-cutting ants, which belong to a subgroup: fungus-growing ants, also known as tribe “Attini” [4]. This species of ant lives compulsively with fungus in their nest. Moreover, the tribe “Attini” consists of 16 genera, with just two genera known as leaf-cutting ants, which are of 16 genera, with just two known as leaf-cutting ants, referred to as Atta and Acromyrmex [5].
Leaf-cutter ants (genera Atta and Acromyrmex) are fascinating social insects known for their complex and highly organized societies [6]. They form large colonies with a strict division of labor and intricate caste systems. The behaviors exhibited by leaf-cutter ants are closely intertwined with their social organization, and understanding this correlation is of utmost importance in unravelling the mechanisms that drive their remarkable success [7]. In this review, we comprehensively explore the behaviours that correlate with the social organization of leaf-cutter ants [7]. The importance of the leaf-cutting ants is underlined by their efficiency to alter foliage by cutting leaves [6]. Indeed, leaf-cutting ants have been considered agriculture pests due to them causing substantial damage to crops by cutting the leaves [7, 8]. Consequently, this will result in significant annual economic losses [6]. In contrast, some positive effects are brought about by leaf-cutting ants in the rain forest ecosystems, such as plant outgrowth development, contributing to the recycling of organic carbon, as well as their nest-digging formations, aiding quick soil reaction [6].
Social organisms, such as ants, obtain a division of labour as individuals have different tasks to perform regarding their age, location, morphological cast, genotype and experience [9]. Thus, effective work organization will lead to success and improve the colony's efficiency [2, 9]. The leaf-cutting ants’ cast system is a more difficult and complex system when compared with other social insects [10]. Atta colonies consist of huge numbers of workers that amount to up to one million, which individually have a head width range between 0.6 and 5.5 mm. In general, the head width 2.4 mm is the most common width in Atta forage workers, while the largest head width in soldiers specialising in colony defense could reach up to 3.0 mm [10]. Concerning the Acromyrmex species, the measurements are certainly similar to the Atta species, although the head width range is 0.6 and 3.0 mm, with 100,000 workers in the colony [11]. Moreover, the Acromyrmex species have a lower range regarding the number of forager workers than Atta within the colonies [12]. Furthermore, 90% of the most energetic and efficient forager workers have a head width range of 1.8 and 2.2 mm [10, 13].
This review aims to deepen our understanding of leaf-cutter ants’ behaviour correlating with social organization by synthesising current knowledge.
2 Foraging behaviour
This section will focus on certain aspects that contribute to the success of foraging from leaf-cutting ants. Initially, it will describe the foraging behaviour, then plant selection, followed by the load size selection in leaf-cutting ants.
The ants’ foraging behaviour could be defined as “a collective process composed of the activities of individuals as well as behaviourally integrated groups” [14]. The leaf-cutter ants can walk up to 100m around the nest to cut leaf fragments from plants, where they will then transport those fragments with their jaws and return to the nest [15]. Nevertheless, leaf–cutter ants do not use these leaf fragments as a food resource, even though they do actively cut the plants, as they use the leaf fragment as a substrate to cultivate a special fungus garden within the colony [16]. Subsequently, this is utilized as a primary food resource for the ants [7].
Traniello (1989) [14] believes that the success in foraging for the ants’ colony depends on the workers' foraging strategies to involve the available plants. Moreover, the success in that behaviour during recruitment ants depends on; choosing appropriate food and avoiding possible threats in the environment [17]. In terms of the key aspects of foraging behaviour, it was found that it is altered by the location of plants around the nest, the quantity and the quality of plant fragments collected, and the activity time for foraging in 24-h cycles [18, 19].
Wilson (1983) [10] examined the flexibility of the foraging behaviour in Atta Cephalotes by removing 90% of the most energetic and efficient forager workers from four colonies, including 8000 workers in the forest had a head width range size of 1.8 and 2.2 mm. Following this, the observations indicate that the colonies ignore ant removal, as they do not add other workers from relative size classes. However, the harvesting leaf rate remains unaffected, even after removing so many ants, due to the workers in the relative size classes being prepared to forage; likewise, the survivor workers of that size increased their efficiency by 5 times the normal amount [10].
Another study has investigated the identity of fragment size and size matching in the Atta species as a function of the distance of the forage area from the nest. The results of that study indicate that a specialized group exists within the ants because the comparison between the foraging size from different trails shows a considerable difference in worker ants, as the leaf-cutting ants were longer and bigger than the carrying ants, as well as those bigger workers possess larger heads and greater strength of jaw muscles [20]. Hence, this indicates a difference in the ants’ cast related to the size of the ants.
The nests of the leaf-cutting ants have a high level of organization which splits the labour regarding the collection and processing of the leaves, although some additional environmental aspects affect the workers’ forage time when gathering the leaf fragments. These aspects could result from heavy rainfall in the forest or day-night cycles [21]. Also, it has been indicated that there is a significant difference in tasks performed in relation to the Acromyrmex workers’ size [21]. For instance, on the one hand, the minor workers with a head width equal to or less than 2.0mm were responsible for brood care and the garden's main entrance, whereas the major workers with a head width bigger than 2.0mm primarily fulfilled the duty of cutting the leaf fragments. Contrastingly, the performance of tasks from minor and major workers was similar when the foragers were not part of the colony. Hence, this study suggests other factors, rather than the head width size, control polytheism in major workers [21].
2.1 Plant selection
An early study investigated the selective plants of a possible host species by Atta ants, together with the determinants of this selection [22]. Other studies have suggested that many evolutionary and phonological reasons underlie the reason for leaf-cutting ants selecting plants, as those ants prefer new leaves of native plant species and flowers rather than mature leaves [23]. Moreover, a study found that only 27 out of 86 mature leaves of possible species were consumed by Atta in a foraging area [22]. Furthermore, Atta ants concentrate on 49%-60% of woody species and upon a smaller subset of plant species [22].
In determining plant selection, a theory suggests that abundant plant species are the most acceptable for Atta ants. However, the rarest plant species were attacked. In contrast, ants ignored the abundant plant species ignored the abundant plant species during the foraging process [22]. Additionally, the plants which contain a high proportion of water are palatable for Atta ants [23].
There is a varied selection of plants from different ant colonies, even though the processed data has shown certain selectivity at particular times. One plant species can be completely acceptable to one colony, while other colonies of the same Atta species can reject the same species [22].
There are two possible expositions for the selection of plants to be cut by the Atta species, which could be a result of innate cyclical changes from the ants’ activity or preference, or that might be caused by the repeated changes in the plurality, physical or chemical characteristics of the plants [24].
In terms of rate cutting, a study by Rockwood (1976) [22] focused on the overall plants that were cut during the year and which were overridden by the number of attacks that the ants attempted on the plant. Likewise, the plant species, cut at elevated rates and visited regularly by ants, are the most palatable for ants. Additionally, the edible plant species and seasonal sources, such as new flowers, leaves and fruits, occupy the highest cutting rate for Atta ants. However, there is a variation in cutting rates for the same plant species among Atta colonies [22].
2.2 Load size selection
Leaf-cutting ants faced various changes in food quality and availability during foraging trails, as well as many changes in physical trial circumstances, that led to individual flexibility in load selection to face the changes caused by environmental factors [25]. Similarly, leaf–cutting ants have shown considerable flexibility in load size selection, which attracted many behavioural ecologists [26]. Regarding worker leaf-cutter ants, they have a significant size difference that leads to ants' dispread ability of ants to transport varied load sizes [27].
The leaf-cutter ant species, while walking for around a hundred meters around the nest and during this journey, cope with many hurdles and gradients, such as vertical trees to cut and carry the leaf fragment back to the nest; hence those physical characteristics cause load transport size [25]. In addition, travelling on different gradients and irregular surfaces has a pronounced effect on foraging costs rather than on smooth, flat surfaces [28]. Likewise, travelling on irregular surfaces influences the walking speed of leaf-cutting ants; hence the time is increased for foraging, and the locomotion of biomechanics likely to change, which subsequently affects the stability and the ability to carry load [25]. Furthermore, it has been suggested that the ants incur more energetic costs when they walk on gradient trails rather than flat trails [29].
Even though the early studies that investigated load size selection in relation to travel distance in leaf-cutting ants have failed to identify a consistent relationship [30], recent studies have examined the load size selection for Atta cephalotes and foraging behaviour related to trail gradient [26]. All previous studies on load size selection for Atta cephalotes were tested on smooth, horizons section trails. In contrast, in the real trails, the ants faced many uphill and downhill sections, which affected the ants’ load carrying and speed walking.
In addition, a study has emerged that investigates load size selection relating to gradient trails [26]. This study found a significant effect of gradient trails on Atta cephalotes load size selection; on uphill gradients, the leaf transport rates were reduced due to the reduction of walking speeds, and downhill sections illustrated the important factor on many foraging trails. In addition, it is believed that the leaf-cutting ants reduce the speed of walking back to the nest when they carry heavy loads, and in contrast, they will walk faster when they carry a smaller load. Generally, it is expected that the ants might select the fragment mass of the plant to carry and maximize the leaf fragments imparted per unit of time [26].
Another study by Norton et al. (2014) [25] on Acromyrmex octospinosus has shown individual flexibility in load mass selection and walking speed related to gradient trails, which is a similar behaviour pattern that was observed on Atta cephalotes by Lewis et al. (2008) [26]. Similarly, the results indicated a reduction in the ants’ foraging return speed with an increase in loading rates, which coincides with the results of Lewis et al. (2008) [26].
On the other hand, the effect of fragment mass and length on the energy cost of load transport has been investigated by testing the effect of mass when ants carry light or heavy fragments of the same size. Secondly, the investigators tested the effect of shape when ants carry short or long fragments in the same mass. The results indicated that not only does the walking speed not differ significantly with either light or heavy fragments, but there is also no difference in the cost of carrying per unit of body mass [31]. Likewise, taking long fragments reduces the walking speed rather than carrying short fragments of the same fragment mass [31]. In addition, it has been suggested that workers choose shorter fragments to avoid reducing speed and minimize transport costs [31]. Even the ants can choose between long or short fragments and may choose shorter fragments [20].
2.3 Hitchhiking behaviour
This behaviour is common in leaf-cutter ants, as the smallest (minima) workers in the colony often ride or “hitchhike” on the leaf fragments, which are carried back to the nest by larger workers [32]. The Hitchhiking behaviour has been recognized in 7 Atta species [33]. To explain this behaviour, it has been suggested that the minima workers hitchhike back to the nest to conserve energy [34]. However, this hypothesis is not strongly supported, as the minima spend energy when they move out of the nest and while riding the fragments [33].
The hitchhiking behaviour has several functions in Atta leaf cutter ants, including defensive and nutritional functions [35, 36]. As this behaviour could mainly involve the defence against phorid flies and the defence against fungal contamination [36]. While obtaining leaf sap function could be a secondary function in hitchhiking behaviour [36].
However, it appears unlikely that the minims given costs for walking out of the nest to the cutting sites to obtain sap [36]. Also, it was found that hitchhiking behaviour does not increase significantly with the presence of phorids [36]. Thus, hitchhiking behaviour could be an important defence mechanism against only some species of parasitoids [36].
Therefore, the possible explanation of the hitchhiking behaviour in leaf cutter ants in most cases is leaf cleaning [36].
2.4 Hygienic behaviour
Hygienic behaviour has a vital role in the organisms that live in social organization because living in aggregation enables disease spread [37]. Also, this behaviour is essential to protect the important brood, queen, adults and workers [9]. The leaf-cutter ants have an essential dependency on a fungus, increasing susceptibility to parasites such as Escovopsis, which could damage the fungal growth and destroy the colony [37, 38]. Thus, the hygienic behaviour or waste management in Atta and Acromyrmex ants’ colonies is important in protecting their vulnerable fungal crop [9, 37]. So, to decrease the contamination hazard in the colony, the leaf-cutting ants depose the waste efficiently, as the waste is accumulated in deep underground cavities or in batches out of the nest [9, 39].
Moreover, the hygienic behaviour in Atta and Acromyrmex ants’ colonies has been affected by the division of labour by age and size between workers. It was found that hygienic behaviour appears more commonly in small and young workers than foragers [9, 40]. However, the medium-sized workers have a role in preventing the contaminating ants from entering the colony [9]. Thus, the division of labour impacts the hygienic behaviour of leaf-cutter ants.
2.5 Social organization of leaf-cutter ants
The social organization of leaf-cutter ants (Atta and Acromyrmex species) is a subject of great fascination and scientific inquiry [41]. These remarkable insects exhibit intricate behaviours and structures that contribute to the success of their colonies. In this self-contained unit, we delve into four key aspects of their social organization: division of labour, caste system and roles, communication mechanisms, and nest architecture and maintenance. Leaf-cutter ant colonies operate through a highly specialized division of labour. Different castes of workers perform distinct tasks essential for colony survival [41, 42]. Foragers venture out to cut leaf fragments, while others carry leaf fragments, cultivate fungus gardens, care for the brood, and defend the nest. The coordination and allocation of tasks within the colony are finely tuned, ensuring the efficient functioning of society [41, 42]. The caste system in leaf-cutter ants consists of queens, males, and workers. Queens are responsible for reproduction, laying eggs that give rise to new colony members. Males have the role of mating with queens to ensure genetic diversity [43]. Workers, the largest caste, are involved in a multitude of tasks. Their roles change as they age, starting with tasks within the nest and progressing to foraging and defense [43, 44]. Genetic and environmental factors influence castes differentiation, with some plasticity observed in certain circumstances [44]. Effective communication is crucial for coordinating and synchronizing activities within leaf-cutter ant colonies. Chemical signals like pheromones are pivotal in conveying information about food sources, nest conditions, and danger alerts. Tactile cues, including antennation and trophallaxis, facilitate information exchange among individuals. Vibrational signals transmitted through the substrate enable communication over longer distances. These sophisticated communication mechanisms ensure efficient task allocation, optimize resource utilization, and maintain colony cohesion [45]. Leaf-cutter ants construct and maintain elaborate nests that cater to the specific needs of the colony. The nest architecture consists of intricate networks of chambers, tunnels, and galleries serving various functions. Fungus gardens are carefully maintained, providing a vital food source for the colony [46]. Brood chambers accommodate the developing larvae and pupae. Waste management areas help to maintain hygiene within the nest. The collective effort of workers ensures the integrity and functionality of the nest structure, allowing the colony to thrive [47].
3 Environmental influences on social behaviors
Understanding the environmental influences on social behaviors is crucial for comprehending the dynamics of social organisms. In this self-contained unit, we examine three key aspects of environmental influence: the impact of resource availability and distribution, responses to abiotic factors, and the influence of biotic factors. Investigating these factors gives us valuable insights into the complex interactions between the environment and social behaviors across various organisms. Resource availability and distribution profoundly shape social behaviours within a population. Limited resources often lead to competition and conflict among individuals or groups, resulting in strategies such as territoriality and resource defense [48]. Unequal access to resources can establish social hierarchies, where dominant individuals or groups have priority access while subordinates must adapt their behaviors accordingly [49].
Conversely, abundant resources can foster cooperation, collaboration, and division of labour within social groups, promoting collective survival and efficiency [48, 49]. Abiotic factors play a significant role in shaping social behaviors. Temperature, for instance, affects social organisms' activity patterns, foraging strategies, and reproductive behaviours. Humidity levels influence nesting site selection, brood development, and survival rates [50]. Light availability can impact social interactions, daily routines, and circadian rhythms. Substrate quality and composition affect nest construction, sheltering behaviours, and foraging techniques. Social organisms exhibit adaptive responses to these abiotic factors, adjusting their behaviours to optimize fitness and reproductive success [50]. Biotic interactions, including predation and parasitism, profoundly influence social behaviours. The presence of predators can lead to increased vigilance, collective defense, and altered foraging patterns within social groups [51]. Parasites and pathogens can disrupt social organization, compromise individual health, and affect reproductive success. Social organisms may develop various defense strategies, such as alarm signals, grooming behaviours, or cooperative nest guarding, to mitigate the negative effects of biotic factors. Understanding the intricate interplay between social behaviours and biotic factors enhances our knowledge of the adaptive strategies employed by organisms to navigate their ecological niches [51, 52].
4 Conclusion
In conclusion, the behaviours correlating with the social organization of leaf-cutter ants showcase the intricate mechanisms underlying their highly organized societies. The division of labor within the colony, where different castes perform specialized roles, enables efficient foraging, resource allocation, and colony maintenance. It is evident from the literature that leaf–cutter ants have a different cast in the colony, and foraging behaviour is related to size. However, they have flexibility in their cast to get the benefit for the colony. In addition, they select the palatable fresh plant as the one to gather, even if it is far away from the nest, rather than the nearest plant, as this relates to reasons such as innate and cycle change in the ants. Moreover, leaf-cutter ants have flexibility in load size related to the workers' size, which will also cause changes in the ants' walking speed. In most cases, hitchhiking behaviour in leaf cutter ants involves leaf cleaning. For hygienic behaviour, the division of labour influences the behaviour of leaf cutter ants. Further research in this area holds promise for uncovering additional complexities and enhancing our knowledge of the social organization in leaf-cutter ants and other social insect societies.
Data availability
All datasets generated or analyzed during this study are included in the manuscript.
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Khayat, R.O. The interplay between leaf-cutter ants behaviour and social organization. J.Umm Al-Qura Univ. Appll. Sci. 10, 225–231 (2024). https://doi.org/10.1007/s43994-023-00074-1
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DOI: https://doi.org/10.1007/s43994-023-00074-1