Dynamics and drivers of fungal communities in a multipartite ant-plant association.

BACKGROUND: Fungi and ants belong to the most important organisms in terrestrial ecosystems on Earth. In nutrient-poor niches of tropical rainforests, they have developed steady ecological relationships as a successful survival strategy. In tropical ant-plant mutualisms worldwide, where resident ants provide the host plants with defense and nutrients in exchange for shelter and food, fungi are regularly found in the ant nesting space, inhabiting ant-made dark-colored piles ("patches"). Unlike the extensively investigated fungus-growing insects, where the fungi serve as the primary food source, the purpose of this ant-fungi association is less clear. To decipher the roles of fungi in these structures within ant nests, it is crucial to first understand the dynamics and drivers that influence fungal patch communities during ant colony development. RESULTS: In this study, we investigated how the ant colony age and the ant-plant species affect the fungal community in the patches. As model we selected one of the most common mutualisms in the Tropics of America, the Azteca-Cecropia complex. By amplicon sequencing of the internal transcribed spacer 2 (ITS2) region, we analyzed the patch fungal communities of 93 Azteca spp. colonies inhabiting Cecropia spp. trees. Our study demonstrates that the fungal diversity in patches increases as the ant colony grows and that a change in the prevalent fungal taxa occurs between initial and established patches. In addition, the ant species significantly influences the composition of the fungal community in established ant colonies, rather than the host plant species. CONCLUSIONS: The fungal patch communities become more complex as the ant colony develops, due to an acquisition of fungi from the environment and a substrate diversification. Our results suggest a successional progression of the fungal communities in the patches during ant colony growth and place the ant colony as the main driver shaping such communities. The findings of this study demonstrate the unexpectedly complex nature of ant-plant mutualisms in tropical regions at a micro scale.

Evolutionary déjà vu? A case of convergent evolution in an ant-plant association.

Obligatory ant-plant symbioses often appear to be single evolutionary shifts within particular ant lineages; however, convergence can be revealed once natural history observations are complemented with molecular phylogenetics. Here, we describe a remarkable example of convergent evolution in an ant-plant symbiotic system. Exclusively arboreal, Myrmelachista species can be generalized opportunists nesting in several plant species or obligately symbiotic, live-stem nesters of a narrow set of plant species. Instances of specialization within Myrmelachista are known from northern South America and throughout Middle America. In Middle America, a diverse radiation of specialists occupies understory treelets of lowland rainforests. The morphological and behavioural uniformity of specialists suggests that they form a monophyletic assemblage, diversifying after a single origin of specialization. Using ultraconserved element phylogenomics and ancestral state reconstructions, we show that shifts from opportunistic to obligately symbiotic evolved independently in South and Middle America. Furthermore, our analyses support a remarkable case of convergence within the Middle American radiation, with two independently evolved specialist clades, arising nearly simultaneously from putative opportunistic ancestors during the late Pliocene. This repeated evolution of a complex phenotype suggests similar mechanisms behind trait shifts from opportunists to specialists, generating further questions about the selective forces driving specialization.

Exploring the evolutionary dynamics of myrmecophytism: Perspectives from the Southeast Asian Macaranga ant-plant symbiosis.

Myrmecophytic plants utilise defensive services offered by obligate ant partners nesting in their domatia in a novel means of survival in tropical habitats. Although much is known about the ecology of myrmecophytism, there aren't enough empirical examples to demonstrate whether it substantially influences evolutionary patterns in host plant lineages. In this study, we make use of the species-rich Macaranga (Euphorbiaceae) ant-plant symbiosis distributed in the Southeast Asian Sundaland to delve into the evolutionary dynamics of myrmecophytism in host plants. We generated the most comprehensive dated phylogeny of myrmecophytic Macaranga till date using genotyping-by-sequencing (GBS). With this in hand, we traced the evolutionary history of myrmecophytism in Macaranga using parametric biogeography and ancestral state reconstruction. Diversification rate analysis methods were employed to determine if myrmecophytism enhanced diversification rates in the genus. Our results demonstrate that myrmecophytism is labile and easily lost. Ancestral state reconstruction supported a single origin of myrmecophytism in Macaranga âˆ¼18 mya on Borneo followed by multiple losses. Diversification rate analysis methods did not yield sufficient evidence to support the hypothesis that myrmecophytism enhanced diversification rates in Macaranga; we found that topographical features on Borneo may have played a more direct role in the divergence of clades instead. Our study provides evidence that while the acquisition of domatia clearly functions as a key innovation that has enabled host plants to exploit the environment in novel ways, it may not necessarily enhance diversification rates. In fact, we hypothesise that overly specialised cases of myrmecophytism may even be an evolutionary dead end.

Imprints of indirect interactions on a resource-mediated ant-plant network across different levels of network organization.

Indirect interactions are pivotal in the evolution of interacting species and the assembly of populations and communities. Nevertheless, despite recently being investigated in plant-animal mutualism at the community level, indirect interactions have not been studied in resource-mediated mutualisms involving plant individuals that share different animal species as partners within a population (i.e., individual-based networks). Here, we analyzed an individual-based ant-plant network to evaluate how resource properties affect indirect interaction patterns and how changes in indirect links leave imprints in the network across multiple levels of network organization. Using complementary analytical approaches, we described the patterns of indirect interactions at the micro-, meso-, and macro-scale. We predicted that plants offering intermediate levels of nectar quantity and quality interact with more diverse ant assemblages. The increased number of ant species would cause a higher potential for indirect interactions in all scales evaluated. We found that nectar properties modified patterns of indirect interactions of plant individuals that share mutualistic partners, leaving imprints across different network scales. To our knowledge, this is the first study tracking indirect interactions in multiple scales within an individual-based network. We show that functional traits of interacting species, such as nectar properties, may lead to changes in indirect interactions, which could be tracked across different levels of the network organization evaluated.

Urbanization drives partner switching and loss of mutualism in an ant-plant symbiosis.

Mutualistic interactions between species underpin biodiversity and ecosystem function, but may be lost when partners respond differently to abiotic conditions. Except for a few prominent examples, effects of global anthropogenic change on mutualisms are poorly understood. Here we assess the effects of urbanization on a symbiosis in which the plant Cordia nodosa house ants in hollow structures (domatia) in exchange for defense against herbivores. We expected to find that mutualist ants would be replaced in the city by heat-tolerant opportunists, leaving urban plants vulnerable to herbivory. In five protected forest sites and five urban forest fragments in southeast Perú, we recorded the identity and heat tolerance (CTmax) of ant residents of C. nodosa. We also assayed their plant-defensive behaviors and their effects on herbivory. We characterized the urban heat-island effect in ambient temperatures and within domatia. Forest plants housed a consistent ant community dominated by three specialized plant ants, whereas urban plants housed a suite of 10 opportunistic taxa that were, collectively, about 13 times less likely than forest ants to respond defensively to plant disturbance. In the forest, ant exclusion had the expected effect of increasing herbivory, but in urban sites, exclusion reduced herbivory. Despite poor ant defense in urban sites, we detected no difference in total standing herbivory, perhaps because herbivores themselves also declined in the city. Urban sites were warmer than forest sites (daily maxima in urban domatia averaged 1.6°C hotter), and the urban ant community as a whole was slightly more heat tolerant. These results illustrate a case of mutualism loss associated with anthropogenic disturbance. If urbanization is representative of increasing anthropogenic stressors more broadly, we might expect to see destabilization of myrmecophytic mutualisms in forest ecosystems in the future.

Las relaciones de mutualismo entre especies sustentan la biodiversidad y la función de los ecosistemas, pero pueden ser perturbadas si las especies que interactúan responden de manera diferente a los cambios en los factores abióticos. Sin embargo, los efectos del cambio antropogénico global sobre los mutualismos no son bien conocidos. Evaluamos los efectos de la urbanización en la simbiosis entre la planta tropical Cordia nodosa que alberga colonias de hormigas, en estructuras específicas en las plantas (domacios), a cambio de defensa contra herbívoros. Esperábamos encontrar que las hormigas oportunistas, no defensoras, y tolerantes al calor urbano reemplazarían a las mutualistas. En cinco sitios de bosque protegido y cinco fragmentos de bosque urbano en el sureste de Perú, registramos la identidad y la tolerancia al calor (CTmax) de las hormigas residentes en C. nodosa. Analizamos sus comportamientos defensivos y sus efectos sobre la herbivoría. Medimos el efecto de isla de calor urbano en la temperatura del ambiente y dentro de los domacios. Las plantas del bosque albergaban una comunidad estable de hormigas, dominada por tres taxones de hormigas especializadas, mientras que las plantas urbanas albergaban diez taxones, mayormente con especies oportunistas. En general, fue 13 veces más probable que las hormigas del bosque respondan a la perturbación de las plantas, y lo hacían más rápidamente que las hormigas urbanas. La exclusión de las hormigas del bosque tuvo el efecto anticipado de aumentar la herbivoría, contrariamente en los sitios urbanos, la exclusión redujo la herbivoría. Aún con hormigas menos defensivas, no detectamos diferencias en la herbivoría total en sitios urbanos, tal vez porque los herbívoros también fueron impactados en la ciudad. Los sitios urbanos eran más cálidos que los sitios forestales, y las hormigas urbanas eran ligeramente más tolerantes al calor. Si la urbanización es representativa de los factores estresantes creados por el cambio global antropogénico, anticiparíamos ver una desestabilización de los mutualismos mirmecofíticos en los ecosistemas forestales en el futuro.

Long-term strict ant-plant mutualism identity characterises growth rate and leaf shearing resistance of an Amazonian myrmecophyte.

Over 125 million years of ant-plant interactions have culminated in one of the most intriguing evolutionary outcomes in life history. The myrmecophyte Duroia hirsuta (Rubiaceae) is known for its mutualistic association with the ant Myrmelachista schumanni and several other species, mainly Azteca, in the north-western Amazon. While both ants provide indirect defences to plants, only M. schumanni nests in plant domatia and has the unique behaviour of clearing the surroundings of its host tree from heterospecific plants, potentially increasing resource availability to its host. Using a 12-year survey, we asked how the continuous presence of either only M. schumanni or only Azteca spp. benefits the growth and defence traits of host trees. We found that the continuous presence of M. schumanni improved relative growth rates and leaf shearing resistance of Duroia better than trees with Azteca. However, leaf herbivory, dry matter content, trichome density, and secondary metabolite production were the same in all trees. Survival depended directly on ant association (> 94% of trees died when ants were absent). This study extends our understanding of the long-term effects of strict ant-plant mutualism on host plant traits in the field and reinforces the use of D. hirsuta-M. schumanni as a model system suitable for eco-co-evolutionary research on plant-animal interactions.

Disruption of an ant-plant mutualism shapes interactions between lions and their primary prey.

Mutualisms often define ecosystems, but they are susceptible to human activities. Combining experiments, animal tracking, and mortality investigations, we show that the invasive big-headed ant (Pheidole megacephala) makes lions (Panthera leo) less effective at killing their primary prey, plains zebra (Equus quagga). Big-headed ants disrupted the mutualism between native ants (Crematogaster spp.) and the dominant whistling-thorn tree (Vachellia drepanolobium), rendering trees vulnerable to elephant (Loxodonta africana) browsing and resulting in landscapes with higher visibility. Although zebra kills were significantly less likely to occur in higher-visibility, invaded areas, lion numbers did not decline since the onset of the invasion, likely because of prey-switching to African buffalo (Syncerus caffer). We show that by controlling biophysical structure across landscapes, a tiny invader reconfigured predator-prey dynamics among iconic species.