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The role of multiple partners in a digestive mutualism with a protocarnivorous plant
Authors:Aline Hiroko Nishi  Jo?o Vasconcellos-Neto  Gustavo Quevedo Romero
Institution:1.Pós-graduação em Biologia Animal, IBILCE, Universidade Estadual Paulista (UNESP), CEP 15054-000, São José do Rio Preto-SP, Brazil;2.Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), CEP 13083-970, CP 6109, Campinas-SP, Brazil
Abstract:

Background and aims

The protocarnivorous plant Paepalanthus bromelioides (Eriocaulaceae) is similar to bromeliads in that this plant has a rosette-like structure that allows rainwater to accumulate in leaf axils (i.e. phytotelmata). Although the rosettes of P. bromelioides are commonly inhabited by predators (e.g. spiders), their roots are wrapped by a cylindrical termite mound that grows beneath the rosette. In this study it is predicted that these plants can derive nutrients from recycling processes carried out by termites and from predation events that take place inside the rosette. It is also predicted that bacteria living in phytotelmata can accelerate nutrient cycling derived from predators.

Methods

The predictions were tested by surveying plants and animals, and also by performing field experiments in rocky fields from Serra do Cipó, Brazil, using natural abundance and enriched isotopes of 15N. Laboratory bioassays were also conducted to test proteolytic activities of bacteria from P. bromelioides rosettes.

Key Results

Analyses of 15N in natural nitrogen abundances showed that the isotopic signature of P. bromelioides is similar to that of carnivorous plants and higher than that of non-carnivorous plants in the study area. Linear mixing models showed that predatory activities on the rosettes (i.e. spider faeces and prey carcass) resulted in overall nitrogen contributions of 26·5 % (a top-down flux). Although nitrogen flux was not detected from termites to plants via decomposition of labelled cardboard, the data on 15N in natural nitrogen abundance indicated that 67 % of nitrogen from P. bromelioides is derived from termites (a bottom-up flux). Bacteria did not affect nutrient cycling or nitrogen uptake from prey carcasses and spider faeces.

Conclusions

The results suggest that P. bromelioides derive nitrogen from associated predators and termites, despite differences in nitrogen cycling velocities, which seem to have been higher in nitrogen derived from predators (leaves) than from termites (roots). This is the first study that demonstrates partitioning effects from multiple partners in a digestion-based mutualism. Despite most of the nitrogen being absorbed through their roots (via termites), P. bromelioides has all the attributes necessary to be considered as a carnivorous plant in the context of digestive mutualism.
Keywords:Animal–  plant interactions  nutrient flux  nitrogen cycling  digestive mutualisms  multiple partners  carnivorous plants  Paepalanthus bromelioides  Latrodectus geometricus  Isoptera  stable isotopes of 15N  rupestrian fields
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