Convergent multispecies interactions in coprophagous pitcher plant species
Evolution and Systematics of Plants and Fungi
Microbial Ecology and Applied Microbiology
Organismic Interactions, Chemical Ecology and Microbiomes of Plant Systems
Final Report Abstract
Multispecies interactions are widespread but are still not well understood, especially those including microbes. The pitchers of Nepenthes pitcher plants are a habitat for various microbes and other inquilines. It is still unknown whether evolution and maintenance of interactions between the microbial communities, coprophagous pitcher plants and mammals depend on the nutrition strategies of the pitcher plants. We investigated similarities and differences in the convergent interactions of coprogphagous pitcher plants and their carnivorous relatives and tried to identify selective pressures as well as the ecological roles of the various interaction partners. In a controlled greenhouse experiment we could show that the coprophagous pitcher plant N. hemsleyana has not reduced costs for enzyme production compared to the closely related carnivorous N. rafflesiana. Moreover, bat faeces activate digestive processes better than arthropods in both species. Thus, enzyme composition and the activation of digestive processes do not reveal adaptations of N. hemsleyana to coprophagy. In another greenhouse experiment we could show that N. hemsleyana and N. rafflesiana host similar microbial families in their pitchers independent of the feeding regime although the food sources have different microbial communities. Fluid properties seem to have a major influence on the composition of microbial communities in Nepenthes pitchers. In the same experiment we could show that both N. rafflesiana and N. hemsleyana pitchers that were fed with arthropods were phosphate deprived which was indicated, e.g., by the presence of alkaline phosphatases. This shows that even without adaptations a coprophagous nutrition can be beneficial. In a feeding and sterilisation experiment performed in the field we found that N. hemsleyana benefits faster from the uptake of prey when microbial inquilines are present in its digestive fluid. This may be due to microbial support in prey digestion or N-fixation and could be crucial when the plant competes with other higher trophic-level inquilines for nutrients. Greenhouse experiments with N. rafflesiana suggested a rather neutral or slightly detrimental effect of microbial inquilines, though evidence was sparse and outcomes under more natural conditions in the field may be different. Furthermore, we found no evidence, that either N. hemsleyana or N. rafflesiana are better adapted to the digestion of either insect prey or faeces. In conclusion, this project shows that a multidisciplinary and multimethodological approach is necessary to get insights into ecological and evolutionary pressures that stabilize or destabilize interspecific interactions especially when multiple partners are involved. Here, we could show that there are no major shifts both in enzyme and microbial composition, neither in response to different feeding treatments within species nor between closely related species. Thus, selective pressures seem to only weakly effect digestive processes of Nepenthes pitcher plants with different nutrition strategies. We also found that interactions with microbial inquilines during the digestive process may accelerate digestion of captured prey in a coprophagous species. This suggests a mutualistic kind of interaction with at least some part of the microbial inquilines, though dynamics remain to be investigated.
Publications
- (2021) Enzyme activities in two sister-species of carnivorous pitcher plants (Nepenthes) with contrasting nutrient sequestration strategies. Plant Physiology and Biochemistry 161:113–121
Kocáb O, Bačovčinová M, Bokor B, et al.
(See online at https://doi.org/10.1016/j.plaphy.2021.01.049) - “With a little help of microbial friends? The ecological role of microbes in the digestive process of Nepenthes hemsleyana & N. rafflesiana” - The Rise and Fall of Mutualism – Ecological and evolutionary dynamics of host-microbe symbioses, Ingelheim, 2021
Bota et al.
