Fungi as mutualistic partners in ant-plant interactions

Abstract

Associations between fungi and ants living in mutualistic relationship with plants ("plant-ants") have been known for a long time. However, only in recent years has the mutualistic nature, frequency, and geographical extent of associations between tropical arboreal ants with fungi of the ascomycete order Chaetothyriales and Capnodiales (belonging to the so-called "Black Fungi") become clear. Two groups of arboreal ants displaying different nesting strategies are associated with ascomycete fungi: carton-building ants that construct nest walls and galleries on stems, branches or below leaves which are overgrown by fungal hyphae, and plant-ants that make their nests inside living plants (myrmecophytes) in plant provided cavities (domatia) where ants cultivate fungi in small delimited "patches". In this review we summarize the current knowledge about these unsuspected plant-ant-fungus interactions. The data suggest, that at least some of these ant-associated fungi seem to have coevolved with ants over a long period of time and have developed specific adaptations to this lifestyle.

Keywords: Capnodiales; Chaetothyriales; ants; evolutionary history; function; specificity; transmission.

Figure 1

Nest walls, galleries and carton in arboreal ant nests with fungi from “Functional group 1”. (A–C) Fungi from Capnodiales, (D–O) fungi from Chaetothyriales. (A, B) Crematogaster ant carton nest from Cameroon (sample BN-Lon33), (B) Capnodiales hyphae from this carton sample germinating on 2% MEA. (C) Capnodiales hyphae with dark brown globose monilioid cells from a nest in Malaysia inhabited parabiotically by Crematogaster sp. and Camponotus sp. (sample M-Camp2). (D) Chaetothyriales hyphae germinating on 2% MEA from a Crematogaster sp. ant carton (sample CN-Cre-BO3) and (E) elongated monilioid cells with coarsely verrucose walls of a Pheidole carton nest (sample CN-Phe1), both from Cameroon. (F) Monomorium ant nest from Malaysia (sample M-Mo) built of loosely interwoven plant trichomes stabilized with Chaetothyriales hyphae. (G) Hyphae of two Chaetothyriales strains from the Monomorium ant nest shown in (F). (H) Nest of Technomyrmex sp. found in Borneo on a lower leaf surface and stabilized with hyphae. (I) Dark-brown runway gallery of Azteca brevis on a branch of Tetrathylacium macrophyllum in Costa Rica. (J) The scanning electron microscope picture shows that the carton of the galleries consists of plant material with densely intertwined chaetothyrialean hyphae. (K, L) Strains with different morphology were found. (M) Carton gallery of Allomerus decemarticulatus on Hirtella physophora from French Guiana built from plant trichomes which the ants obtained by clearing a path and stabilized with chaetothyrialean hyphae. During the construction process, holes are left which are guarded by Allomerus workers throughout the day. (N, O) The construction and stability of the galleries built by Allomerus ants allow a peculiar ambush tactic to capture prey. (N) Allomerus workers had taken up positions beneath the holes with their mandibles wide open grasping the legs or antennae of other arthropods. (O) The prey is immobilised by stretching its legs, antennae or wings against the gallery so that the workers can kill it. Bars, (E, G, K, L) 10 µm, (B–D) 20 µm, (J) 100µm, (A) 3mm, (I, F) 5mm, (M) 1mm. (H) with courtesy of F. Etl. MEA, malt extract agar.

Figure 2

Domatia of ant-plants (myrmecophytes) with patches that contain chaetothyrialean fungi. (A) Opened branch of Barteria fistulosa (Passifloraceae) from Cameroon with Tetraponera aethiops and a black patch with Chaetothyrialeas. (B) The fungal symbiont (CBS 134920) of T. aethiops growing on 2% MEA showing conidiophores with conidia. (C, D) Cordia alliodora (Boraginaceae) from Costa Rica with swollen hollow nodes which are inhabited by Azteca sp. (D) The domatium cavity is structured into compartments with a carton (arrow). (E) Opened Cecropia obtusifolia stem inhabited with Azteca constructor. The black round patches are containing Chaetothyriales. (F) A squash mount of fresh patches from C obtusifolia inhabited by A. constructor made in the field. Numerous hyphae (stained with calcofluor white) pervade the organic matter (blurry parts) of the patches. (G) Hyphae of a pure culture (CBS 132003) of the Azteca/Cecropia association growing on 2% MEA with spores and conidiophorous cells (arrow). (H-J) Carton made of scratched parenchyma tissue from the inner domatium wall (H) of the same Cecropia individual as in (E) with eggs and larvae (white dots) on the carton surface. (I) Numerous needle-like black conidiophores (arrows) were found on this carton. (J) Close-up of a needle like conidiophore from (I). (K) Triplaris americana (Polygonaceae) branch with an entrance hole from outside, (L) opened showing a domatium inhabited with Pseudomyrmex sp. and a black fungal patch. (M) Conidiophores (arrow) with conidia (asterisk) from a patch in a Triplaris americana domatium. (N) Opened leaf petiole of Tachigali paniculata inhabited by Pseudomyrmex penetrator ants, showing blackish fungal patches in some places covered with masses of nematodes (white parts). (O) Conidiophores from the patch shown in (N). Bars, (A, E, K–M) 2cm, (C, D, H) 1cm, (B, G, I, M) 10µm, (F, O) 20µm. MEA, maltose extract agar.

Figure 3

Geographical distribution of Chaetothyriales growing in ant nests in hollow plant structures (domatia). The bars indicate the number of plant (green) and ant (brown) genera that are known to house ant-associated fungi. The numbers are based on Table 1 in Mayer et al., 2014. While fungi growing in domatia are restricted to the tropics, carton fungi can also be found in temperate regions.

Figure 4

Overview on the two major groups of tropical ant-associated melanized fungi, the substrate and environmental conditions they are exposed to.