Ecological outsourcing: a pitcher plant benefits from transferring pre‐digestion of prey to a bat mutualist

Abstract

Summary Mutualisms are interspecific interactions where each of the species involved gains net benefits from the other(s). The exchange of resources and/or services between mutualistic partners often involves tasks that species originally accomplished themselves but which have been taken over by or transferred to the more efficient partner during the evolution of the mutualism. Such ‘ecological outsourcing’ can be seen, for example, in several carnivorous plants that have transferred prey capture and digestion to animal partners. However, the outcome of this transfer and its fitness relevance has rarely been quantified. Using a digestive mutualism between a carnivorous pitcher plant (Nepenthes hemsleyana) and a bat (Kerivoula hardwickii) as a model, we tested the hypothesis that ecological outsourcing is a profitable strategy for the outsourcing partner. To evaluate the value of this mutualism, we conducted a series of field and glasshouse experiments. We measured the benefits of ecological outsourcing by comparing survival, growth, photosynthesis and nutrient content of N. hemsleyana plants fed with bat faeces to those fed with arthropods. To investigate the costs of such outsourcing processes, we repeated the experiment with the closest relative (Nepenthes rafflesiana) that is not adapted to digest bat faeces. We found that N. hemsleyana plants fed with faeces had increased survival, growth and photosynthesis compared to plants fed with arthropods only. On average, plants covered 95% of their nitrogen demand from faeces under strong nutrient deprivation. Despite N. rafflesiana's higher arthropod capture rate, faeces covered a large part of this species’ nutrient demand as well, suggesting low costs for outsourcing. Synthesis. Outsourcing prey capture and digestion to the mutualism partner seems to be a beneficial strategy for N. hemsleyana. It may explain the evolutionary trend of several carnivorous plants to lose their carnivorous traits while increasing their attractiveness to mutualistic partners. On a much broader scale, we propose that ecological outsourcing could be one of the major drivers for the evolution and maintenance of mutualisms.

Dipteran larvae and microbes facilitate nutrient sequestration in theNepenthes gracilispitcher plant host

“…bugs [10]. With the exception of a unique bat-plant mutualism in N. hemsleyana [11], digestive mutualism remains largely unexamined in pitchers of Nepenthes.…”

Coprophagous features in carnivorous Nepenthes plants: a task for ureases

“…In the mutualism between bats and Nepenthes , the pitcher plant is provided with high amounts of urea 11 , 12 . The urea-derived nitrogen is suggested to enter nitrogen metabolism in Nepenthes to drive growth and development 12 .…”

“…In the mutualism between bats and Nepenthes , the pitcher plant is provided with high amounts of urea 11 , 12 . The urea-derived nitrogen is suggested to enter nitrogen metabolism in Nepenthes to drive growth and development 12 . To test whether or not Nepenthes species are generally able to take up and metabolize urea, 15 N-enriched urea was fed to pitchers of N. alata , a carnivorous relative of N. hemsleyana that derives nitrogen from captured insects.…”

“…The montane species Nepenthes lowii, Nepenthes rajah and Nepenthes macrophylla benefit from fecal nitrogen of small mammals such as the mountain shrew, Tupaia montana that are rewarded with nectar from the pitchers’ lid 10 . Similarly, individuals of the bat species Kerivoula hardwickii defecate into pitchers of Nepenthes hemsleyana while roosting inside 11 , 12 . Thus, the visiting activity of mutualistic mammalian partners significantly increase foliar nitrogen content in the host plants, N. hemsleyana and N. lowii 10 – 12 .…”

“…Similarly, individuals of the bat species Kerivoula hardwickii defecate into pitchers of Nepenthes hemsleyana while roosting inside 11 , 12 . Thus, the visiting activity of mutualistic mammalian partners significantly increase foliar nitrogen content in the host plants, N. hemsleyana and N. lowii 10 – 12 . However, the precise origin of the nitrogen and the biochemical background these plants use to harvest the external nitrogen trapped inside the pitchers remained unclear, so far.…”