The contribution of microorganisms and metazoans to mineral nutrition in bromeliads

Aims One critical challenge for plants is to maintain an adequate nutrient supply under fluctuating environmental conditions.This is particularly true for epiphytic species that have limited or no access to the pedosphere and often live in harsh climates.Bromeliads have evolved key innovations such as epiphytism,water-absorbing leaf trichomes,tank habit and Crassulacean acid metabolism(CAM)photosynthesis that enable them to survive under various environmental conditions.Bromeliads encompass diverse ecological types that live on different substrates(they can be terrestrial,epilithic or epiphytic)and vary in their ability to retain water(they can be tank-forming or tankless)and photosynthetic pathway(i.e.C3 or CAM).In this review,we outline the nutritional modes and specializations that enable bromeliads to thrive in a wide range of nutrient-poor(mostly nitrogen-depleted)environments.Important FindingsBromeliads have evolved a great diversity of morphologies and functional adaptations leading to the existence of numerous nutritional modes.Focusing on species that have absorptive foliar trichomes,we review evidence that bromeliads have evolved multi-faceted nutritional strategies to respond to fluctuations in the supply of natural nitrogen(N).These plants have developed mutualistic associations with many different and functionally diverse terrestrial and aquatic microorganisms and metazoans that contribute substantially to their mineral nutrition and,thus,their fitness and survival.Bacterial and fungal microbiota-assisted N provisioning,protocarnivory,digestive mutualisms and myrmecotrophic pathways are the main strategies used by bromeliads to acquire nitrogen.The combination of different nutritional pathways in bromeliads represents an important adaptation enabling them to exploit nutrient-poor habitats.Nonetheless,as has been shown for several other vascular plants,multiple partners are involved in nutrient acquisition indicating that there have been convergent adaptations to nutrient scarcity.Finally,we point out some gaps in the current knowledge of bromeliad nutrition that offer fascinating research opportunities.