Widespread herbivory cost in tropical nitrogen-fixing tree species

• Published in: Nature (London) Vol. 612; no. 7940; pp. 483 - 487
• Main Authors: Barker, Will, Comita, Liza S., Wright, S. Joseph, Phillips, Oliver L., Sedio, Brian E., Batterman, Sarah A.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 15.12.2022; Nature Publishing Group
• Subjects: 631/158/47; 704/158/2454; 704/158/47/4112; Animals; Carbon; Carbon - metabolism; Carbon Sequestration; Carbon sinks; Cellulose; Costs; Forests; Herbivores; Herbivory; Humanities and Social Sciences; Hypotheses; Leaves; Metabolism; Metabolites; multidisciplinary; Nitrogen; Nitrogen - metabolism; Nitrogen Fixation; Nitrogenation; Panama; Plant Leaves; Plant species; Science; Science (multidisciplinary); Seedlings; Symbiosis; Trees; Trees - classification; Trees - metabolism; Tropical Climate; Tropical forests; Panama
• ISSN: 0028-0836; 1476-4687; 1476-4687
• DOI: 10.1038/s41586-022-05502-6

Recent observations suggest that the large carbon sink in mature and recovering forests may be strongly limited by nitrogen 1 – 3 . Nitrogen-fixing trees (fixers) in symbiosis with bacteria provide the main natural source of new nitrogen to tropical forests 3 , 4 . However, abundances of fixers are tightly constrained 5 – 7 , highlighting the fundamental unanswered question of what limits new nitrogen entering tropical ecosystems. Here we examine whether herbivory by animals is responsible for limiting symbiotic nitrogen fixation in tropical forests. We evaluate whether nitrogen-fixing trees experience more herbivory than other trees, whether herbivory carries a substantial carbon cost, and whether high herbivory is a result of herbivores targeting the nitrogen-rich leaves of fixers 8 , 9 . We analysed 1,626 leaves from 350 seedlings of 43 tropical tree species in Panama and found that: (1) although herbivory reduces the growth and survival of all seedlings, nitrogen-fixing trees undergo 26% more herbivory than non-fixers; (2) fixers have 34% higher carbon opportunity costs owing to herbivory than non-fixers, exceeding the metabolic cost of fixing nitrogen; and (3) the high herbivory of fixers is not driven by high leaf nitrogen. Our findings reveal that herbivory may be sufficient to limit tropical symbiotic nitrogen fixation and could constrain its role in alleviating nitrogen limitation on the tropical carbon sink. Nitrogen-fixing trees are favoured by herbivorous animals relative to non-fixing trees, increasing their carbon opportunity cost and potentially constraining global nitrogen fixation.