Transmission of fungal partners to incipient Cecropia-tree ant colonies

Abstract

Ascomycete fungi in the nests of ants inhabiting plants (= myrmecophytes) are very often cultivated by the ants in small patches and used as food source. Where these fungi come from is not known yet. Two scenarios of fungus recruitment are possible: (1) random infection through spores or hyphal fragments from the environment, or (2) transmission from mother to daughter colonies by the foundress queen. It is also not known at which stage of the colony life cycle fungiculture is initiated, and whether the- symbiont fungi serve as food for the ant queen. To clarify these questions, we investigated four Azteca ant species inhabiting three different Cecropia species (C. insignis, C. obtusifolia, and C. peltata). We analysed an rRNA gene fragment from 52 fungal patches produced by founding queens and compared them with those from established Azteca colonies (n = 54). The infrabuccal pockets of winged queens were dissected to investigate whether young queens carry fungi from their mother colony. Additionally, 15N labelling experiments were done to verify whether the queen feeds on the patches until she is nourished by her first worker offspring. We infer from the results that the fungi cultivated in hollow plant structures are transferred from the parental colony of the young queen. First, fungal genotypes/OTU diversity was not significantly different between foundress queen patches and established colonies, and second, hyphal parts were discovered in the infrabuccal pockets of female alates. We could show that fungiculture already starts before queens lay their eggs, and that the queens do not feed on fungal patch material but feed it to the larvae. Our findings suggest that fungiculture may be crucial for successful colony founding of arboreal ants in the tropics.

Azteca ants maintain unique microbiomes across functionally distinct nest chambers

“…Additionally, Chaetothyriales has been proposed to be part of a tripartite mutualism between ants and L. africana plants [76]. Our results support previous studies that have documented the prevalence of this fungus within ant dwellings [40,42,76]. Assessing whether this prevalent ant-nest associate benefits ants and/or host plants would be an interesting follow-up study.…”

“…Specifically, the fungal order Chaetothyriales was in high abundance inside A. alfari nests (figure 4c). It has been proposed that founding queens carry Chaetothyriales fungal patches inside their infrabuccal pocket; however, whether these fungi are actively or passively transmitted is yet to be determined [42]. Chaetothyriales plays an important role in helping ants build their carton material and is a food source for the colony pupae and workers in some ant species [42,75].…”

“…It has been proposed that founding queens carry Chaetothyriales fungal patches inside their infrabuccal pocket; however, whether these fungi are actively or passively transmitted is yet to be determined [42]. Chaetothyriales plays an important role in helping ants build their carton material and is a food source for the colony pupae and workers in some ant species [42,75]. Additionally, Chaetothyriales has been proposed to be part of a tripartite mutualism between ants and L. africana plants [76].…”

“…Certain Azteca species further compartmentalize their homes by enlarging the domatium space [39] and through the production of carton, which is composed of macerated plant tissue combined with Chaetothyrialean fungi [40]. These beneficial fungal associates are vertically transmitted through newly colonizing queens [41,42]. We ask whether this compartmentalization and chamber specialization leads to similar patterns of microbial structuring as those seen in human-built environments [5,32,43], and whether ant colonies maintain distinct relationships with their microbial co-inhabitants.…”

Ant-plant sociometry in the Azteca-Cecropia mutualism

“…Ant species that invest in smaller workers may be better at scrutinizing the surface of their host plant and removing small sap sucking insects 27 , but worse at fending off larger insects and vertebrates. In addition to plant dimensions, worker morphology may depend on food resources provided to the colony via food bodies 2 or nutritious pith called parenchyma 28,29 – plants providing more nutrition may produce larger workers. Morphometric analysis of the non- Cecropia -inhabiting congener Azteca trigona revealed that workers were dimorphic 30 , but worker size and allometry and their relation to plant traits have not been formally described in A .…”