Sperm Storage Costs Determine Survival and Immunocompetence in Newly Mated Queens of the Leaf-Cutting Ant Atta colombica

In the leaf-cutting ant Atta colombica, queens receive ejaculates from multiple males during one single mating event early in their lives. A queen’s fertility and fitness therefore depend on maximizing the number of sperm cells she can store and maintain inside her spermatheca. Previous studies implied significant physiological mating costs, either originating from energetic investments maximizing sperm survival, or from resolving sexual conflicts to terminate male-driven incapacitation of rival sperm via serine proteases found in seminal fluid. Here we conducted an artificial insemination experiment, which allowed us to distinguish between the effects of sperm and seminal fluid within the queen’s sexual tract on her survival and immunocompetence. We found significantly higher mortality in queens that we had inseminated with sperm, independently of whether seminal fluid was present or not. Additionally, after receiving sperm, heavier queens had a higher probability of survival compared to lightweight queens, and immunocompetence decreased disproportionally for queens that had lost weight during the experiment. These findings indicate that queens pay significant physiological costs for maintaining and storing sperm shortly after mating. On the other hand, the presence of seminal fluid within the queens’ sexual tract neither affected their survival nor their immunocompetence. This suggests that the energetic costs that queens incur shortly after mating are primarily due to investments in sperm maintenance and not costs of terminating conflicts between competing ejaculates. This outcome is consistent with the idea that sexually selected traits in social insects with permanent castes can evolve only when they do not affect survival or life-time fitness of queens in any significant way.

Queen loss increases worker survival in leaf-cutting ants under paraquat-induced oxidative stress

Longevity is traded off with fecundity in most solitary species, but the two traits are positively linked in social insects. In ants, the most fecund individuals (queens and kings) live longer than the non-reproductive individuals, the workers. In many species, workers may become fertile following queen loss, and recent evidence suggests that worker fecundity extends worker lifespan. We postulated that this effect is in part owing to improved resilience to oxidative stress, and tested this hypothesis in three Myrmicine ants: Temnothorax rugatulus, and the leaf-cutting ants Atta colombica and Acromyrmex echinatior . We removed the queen from colonies to induce worker reproduction and subjected workers to oxidative stress. Oxidative stress drastically reduced survival, but this effect was less pronounced in leaf-cutting ant workers from queenless nests. We also found that, irrespective of oxidative stress, outside workers died earlier than inside workers did, likely because they were older. Since At. colombica workers cannot produce fertile offspring, our results indicate that direct reproduction is not necessary to extend the lives of queenless workers. Our findings suggest that workers are less resilient to oxidative stress in the presence of the queen, and raise questions on the proximate and ultimate mechanisms underlying socially mediated variation in worker lifespan. This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’

Associated pseudoscorpions (Arachnida: Pseudoscorpiones) with waste heaps of Atta colombica (Guérin-Méneville, 1844) (Hymenoptera: Formicidae) in Panama

Waste heaps of Atta are host to an extraordinary diversity of myrmecophiles insects and other arthropods. In this study, the presence of four species of pseudoscorpions is recorded in two Atta colombica waste heaps in the years 2016 and 2017. Two of these species, Cordylochernes scorpioides and Lustrochernes carolinensis are new records in waste heaps and except for the deutonymphs of L.carolinensis, the others all stages of post-embryonic development were present in the studied heaps, which could indicate that these two species carry out their entire life cycle in these waste mounds and live there permanently.

The multidimensional nutritional niche of fungus-cultivar provisioning in free-ranging colonies of a neotropical leafcutter ant

The foraging trails of Atta leafcutter colonies are among the most iconic scenes in Neotropical ecosystems, with thousands of ants carrying freshly cut plant fragments back to their nests where they are used to provision a fungal food crop. We tested a hypothesis that the fungal cultivar’s multidimensional requirements for macronutrients (protein and carbohydrates) and minerals (Al, Ca, Cu, Fe, K, Mg, Mn, Na, P and Zn) govern the foraging breadth of Atta colombica leafcutter ants in a Panamanian rainforest. Analyses of freshly cut plant fragments carried by leafcutter foragers showed that the combination of fruits, flowers, and leaves provide for a broad realized nutritional niche that can maximize cultivar’s performance. And, while the leaves that comprised the most harvested resource also delivered an intake target containing protein in excess of the amounts that can maximize cultivar growth, in vitro experiments showed that the minerals P, Al, and Fe can enhance the cultivar’s tolerance to protein-biased substrates, and potentially expand the ants’ foraging niche. Yet, the cultivar also exhibits narrow margins between mineral limitation and toxicity that may render plant fragments with seemingly optimal blends of macronutrients unsuitable for provisioning. Our approach highlights that optimal foraging is inherently multidimensional and links the foraging behavior of a generalist insect herbivore to the fundamental nutritional niche of its microbial symbiont.Significance StatementColonies of Atta colombica leafcutter ants can contain millions of specialized workers exhibiting large-scale generalist herbivory. Yet, this generalist foraging niche also depends on the poorly understood physiological needs of the ants’ domesticated fungal cultivar. We show the cultivar’s fundamental nutritional niche is broad for carbohydrates but narrower for protein and a suite of minerals, but that the cultivar’s sensitivity to excess protein is also mediated by Al, Fe, and P. More generally, this study decouples the multidimensional foraging strategies that enable a generalist herbivore to navigate a complex nutritional landscape and mix many imbalanced foods to achieve balanced cultivar provisioning.

Leaf-cutter ants engineer large nitrous oxide hot spots in tropical forests

Though tropical forest ecosystems are among the largest natural sources of the potent greenhouse gas nitrous oxide (N 2 O), 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 South America, and influence multiple aspects of forest structure and function. In particular, their foraging creates spatial heterogeneity by concentrating large quantities of organic matter (including nitrogen, N) from the 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 N 2 O production (high microbial biomass, potential denitrification enzyme activity, N content and anoxia) and may represent an unappreciated source of heterogeneity in tropical forest N 2 O emissions. Average instantaneous refuse pile N 2 O fluxes surpassed background emissions by more than three orders of magnitude (in some cases exceeding 80 000 µg N 2 O-N m −2 h −1 ) 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.

Cryptic Diversity in Colombian Edible Leaf-Cutting Ants (Hymenoptera: Formicidae)

Leaf-cutting ants are often considered agricultural pests, but they can also benefit local people and serve important roles in ecosystems. Throughout their distribution, winged reproductive queens of leaf-cutting ants in the genus Atta Fabricius, 1804 are consumed as a protein-rich food source and sometimes used for medical purposes. Little is known, however, about the species identity of collected ants and the accuracy of identification when ants are sold, ambiguities that may impact the conservation status of Atta species as well as the nutritional value that they provide to consumers. Here, 21 samples of fried ants bought in San Gil, Colombia, were identified to species level using Cytochrome Oxidase I (COI) barcoding sequences. DNA was extracted from these fried samples using standard Chelex extraction methods, followed by phylogenetic analyses with an additional 52 new sequences from wild ant colonies collected in Panama and 251 publicly available sequences. Most analysed samples corresponded to Atta laevigata (Smith, 1858), even though one sample was identified as Atta colombica Guérin-Méneville, 1844 and another one formed a distinct branch on its own, more closely related to Atta texana (Buckley, 1860) and Atta mexicana (Smith, 1858). Analyses further confirm paraphyly within Atta sexdens (Linnaeus, 1758) and A. laevigata clades. Further research is needed to assess the nutritional value of the different species.

Patrones comportamentales de fóridos (Diptera: Phoridae) parasitoides de Atta colombica (Hymenoptera: Formicidae)

In ecology, the success of parasitoid-host interactions is determined by the behavior of seeking, recognition, attack and defense deployed by the participants in the interaction. Our study aimed to understand the behavioral patterns between parasitoid phorids and their host Atta colombica from a forest fragment of Córdoba department, Colombia. We observed three nests of Atta colombica, from December 2013 to Januray 2015 (including dry and rainy seasons), for a total effort of 189 hours. We observed Phorids, their attacks to ants and collected their loads; we also considered differences in the way the parasitoids attacked and observed the microhabitat they preferred. A total of 52 individuals of Eibesfeldtphora attae and 54 of Apocephalus colombicus were collected. Apparently there was no preference for the size of the ants that were attacked by phorids, but larger loads were selected to land on them. When the ants responded to the phorid attack, they used individual defenses (adopting positions or increasing their speed) or grupal defenses (closer ants attacking the phorid). Parasitoid phorids have specialized their behavior, in order to ensure a successful attack on their host, who responded by modifying its behavior, according to the attacker (parasitoid).

Two castes sizes of leafcutter ants in task partitioning in foraging activity

ABSTRACT: Task partitioning in eusocial animals is most likely an evolutionary adaptation that optimizes the efficiency of the colony to grow and reproduce. It was investigated indirect task partitioning in two castes sizes; this involves task partitioning in which the material transported is not transferred directly from one individual to another, but where it is dropped by one ant to be picked up by another. In two separate approaches, it was confirmed previous results pertaining to leaf caching activities among Atta colombica with task partitioning activities involving leaf dropping among Atta sexdens rubropilosa , in which there is a correlation between the size of an individual ant and the leaf fragment it transports. It was also suggested that this correlation exists only in individual ants that cut and transport (CaT) the same fragment to the nest. When task partitioning occurs and individual ants transporting (T) leaf fragments cut by other ants, the correlation becomes looser or disappears. We also observed that CaT ants are smaller than T ants.