Farming by ants remodels nutrient uptake in epiphytes

Abstract

True agriculturedefined by habitual planting, cultivation, harvesting and dependence of a farmer on a cropis known from fungi farmed by ants, termites or beetles, and plants farmed by humans or ants. Because farmers supply their crops with nutrients, they have the potential to modify crop nutrition over evolutionary time. Here we test this hypothesis in ant/plant farming symbioses.We used field experiments, phylogenetic-comparative analyses and computed-tomography scanning to investigate how the evolution of farming by ants has impacted the nutrition of locally coexisting species in the epiphytic genus Squamellaria (Rubiaceae).Using isotope-labelled mineral and organic nitrogen, we show that specialised ants actively and exclusively fertilise hyperabsorptive warts on the inner walls of plant-formed structures (domatia) where they nest, sharply contrasting with nitrogen provisioning by ants in nonfarming generalist symbioses. Similar hyperabsorptive warts have evolved repeatedly in lineages colonised by farming ants.Our study supports the idea that millions of years of ant agriculture have remodelled plant physiology, shifting from ant-derived nutrients as by-products to active and targeted fertilisation on hyperabsorptive sites. The increased efficiency of ant-derived nutrient provisioning appears to stem from a combination of farming ant behaviour and plant 'crop' traits.

Specialized bacteriome uncovered in the coralloid roots of the epiphytic gymnosperm, Zamia pseudoparasitica

“…However, plant genotype, developmental stage, and habitat also influence the composition of the microbial community found in the rhizobiome (Lundberg et al, 2012). Most plants have relatively easy access to soil nutrients and microbes; however, canopy epiphytes are exposed to a much harsher environment and face several unique constraints regarding nutrient acquisition: They are disconnected from soil nutrients and thus have to rely on nutrients leached by precipitation (rain or mist), nutrient-rich dusts, association with invertebrates (e.g., ants), vertebrates (e.g., treefrogs), and microbes found either epiphytically or endophytically (Chomicki & Renner, 2019;Okin, Mahowald, Chadwick, & Artaxo, 2004;Romero et al, 2010;Stanton, Bateman, Von Fischer, & Hedin, 2019). Three elements that typically limit growth in tropical epiphytes are phosphorus, nitrogen, and molybdenum (Barron et al, 2009;Stanton et al, 2019).…”

Squamellaria: Plants domesticated by ants

“…Hence, the complex nutritional physiology that has evolved in Squamellaria–P. nagasau agriculture might help humankind's own challenge for food security (Chomicki & Renner, ).…”

Tradeoffs in the evolution of plant farming by ants

“…To answer this question, we studied an obligate farming mutualism between the ant Philidris nagasau (Dolichoderinae) and epiphytic plants in the genus Squamellaria (Hydnophytinae, Rubiaceae), occurring in Fijian rainforests on Taveuni and Vanua Levu islands (11). P. nagasau workers cultivate multiplant colonies of Squamellaria epiphytes that can contain 50 or more individuals whose plant-formed cavities in modified stems (domatia) house one queen and ∼250,000 workers (11,18). In this mutualism, the ants control dispersal, fertilization, and defense of the epiphytes.…”

“…They do this by actively collecting Squamellaria seeds, planting them under the branch bark of their host tree, and subsequently protecting both seedlings and adults from herbivory (11,18). The ants also fertilize these nutrient-limited (soilless) epiphytes by defecating on specialized and highly absorptive warts within a plant's tuberous domatium, which is also the ants' obligatory nest site (11,18). In return, the ants feed on sugar-and amino acid-rich food rewards produced by the flowers' nectaries.…”

“…In return, the ants feed on sugar-and amino acid-rich food rewards produced by the flowers' nectaries. The food rewards and the domatia, which contain a complex network of interconnected cavities (11,(18)(19)(20)(21), are key to the ants' survival. Similar to the other "true" agricultures in attine ants, termites, and…”