Epiphytes are keystone species in tropical rainforests because they provide food and/or habitat resources to different organisms not found elsewhere and because they play a major role in the nutrient cycles in canopy ecosystems. However, epiphytism imposes physiological constraints resulting from the lack of access to the nutrient sources available to ground-rooted plants. Hence, many epiphytes are characterized by morphological and functional adaptations – such as litter-trapping leaf arrangements (i.e. Asplenium ‘trash-baskets’); rainwater retention (e.g. tank-forming bromeliads); absorbent leaf trichomes (i.e. Tillandsia spp. bromeliads); velamen radicum in aerial roots (i.e. Orchidaceae); and slippery, waxy walls (e.g. insectivorous pitfall plants such as Brocchinia reducta and Catopsis berteroniana) – that facilitate access to nutrient acquisition. In addition, many epiphytes are involved in complex associations with animals, particularly ants, that provide them with nutritional benefits. You might expect that multiple associations with animals would result in higher nutrient acquisition compared with those with fewer interactions either through direct (i.e. animal mediated) or indirect (i.e. plant-trait mediated) interactions. This question is highly relevant to broadening our understanding of the mechanisms that foster biological diversity in the species-rich Tropics where plant–animal interactions are common.
Plants of the family Bromeliaceae, possessing both CAM and C3 photosynthetic pathways, dominate the vascular flora in Neotropical forests and most of them (i.e. all of the members of the Bromelioideae and Tillandsioideae subfamilies) absorb water and nutrients through specialized leaf trichomes. Their mechanical roots are used to maintain the plant’s position and do not play a significant role in plant nutrition. A conspicuous adaptation to improve nutrient acquisition by bromeliads is the phytotelm (‘plant-held water’). Bromeliad leaves are often tightly interlocking and form rosettes, creating tanks that collect rainwater and debris. These tanks provide a habitat for specialized aquatic organisms. Most major taxa are involved, including bacteria, algae, prokaryotes, protists, micro- and macro-invertebrates, and vertebrates. The detritus that enter the tank (mostly leaf litter) constitutes the main source of nutrients for the aquatic food web. Invertebrates reduce the incoming litter to fragments. Nitrogen and other nutrients are then made available to the plant through the bacterial decomposition of the small detritus and faecal pellets of aquatic metazoans. In sun-exposed areas, algae can grow in the phytotelm. They may then represent a higher trophic resource than leaf litter while constituting an important food source for filter-feeding invertebrates, algae may also compete with the plant for nitrogen. Other direct interactions with the terrestrial or amphibious animals inhabiting bromeliads may also constitute an important source of nutrients for tank-forming bromeliads. For example, bromeliad-associated spiders and treefrogs release faeces that are washed into the plant’s pools and collect at the leaf bases where they provide a source of nutrients for aquatic decomposers and for the bromeliad itself. In summary, tank-bromeliads can be considered ‘assisted saprophytes’. Mutualistic ants influence the vegetative traits of their associated bromeliads by determining the distribution of seedlings along gradients of incident light, thereby affecting the taxonomic composition and complexity of the aquatic food web contained in the phytotelmata, and, subsequently, the nitrogen flux to the plant’s leaves.
A new paper in Annals of Botany studies eight tank- and one tankless-bromeliad species and finds that leaf nitrogen concentrations are positively correlated with the presence of mutualistic ants, with the scale of the benefit depending on the identity of the associated ant species. A protocarnivorous tank-bromeliad not associated with mutualistic ants appears to obtain nitrogen from ant carcasses, but the results suggest that it is more advantageous for a bromeliad to obtain ant-derived nutrients (e.g. faeces, insect remains) via its roots than to use carnivory via its tank.
This study suggests that the contribution of phytotelm communities to bromeliad nutrition is more complex than previously thought. It also highlights a gap in our knowledge of the reciprocal interactions between bromeliads and the various trophic levels (from bacteria to large metazoan predators) that intervene in reservoir-assisted nutrition.