Monday 12 December 2016

How a Plant Evolved to Eat Bat Poo!

Pitcher plant (Nepenthes hemsleyana) with woolly bat (Kerivoula hardwickii)
Why plants eat faeces when they could eat flesh

Mutualism as a result of evolution is a well-known phenomenon to biologists but this example is, by any stretch of the imagination, unusual and even a little counter-intuitive. It has ended up with a carnivorous pitcher plant switching from a diet of captured insects to one consisting of bat faeces.

Examples of mutualism can be found in for example, the production of nectar by flowers which supplies insects with food in return for targeted dispersal of pollen. The insects gets fed and the plant gets its pollen delivered to another flower of the same species without the wastefulness and hit and (mostly) miss nature of wind dispersal. Another example would be the gut microbes in ruminants and termites which digest plant cellulose providing nutrients from an otherwise indigestible resource in return for shelter, warmth and a ready supply of raw materials.

Mutualism is the inevitable result of genes acting 'selfishly' because it is in the interests of all the genes, from two or more species, to form mutually-beneficial alliances from which all of them gain in the long run.

In the case of the coprophageous pitcher plant the mutual benefits for both species are maybe not quite so obvious, but a team of ecologists from Germany, Brunei Darussalam and Australia believe they have the answer.

  1. 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.
  2. 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.
  3. 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.
  4. 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.

The background to pitcher plant evolution, like that of other carnivorous plants is the nitrogen-poor conditions of the bogs in which they invariably grow. Digested arthropods captured in the elaborate traps supply the nitrogen missing in the nutrients otherwise obtained through a plant's root system.

However, several pitcher plants have subsequently abandoned trapping insects and instead provide ideal conditions for bats to roost in and live instead on the partially predigested remains of insects in the faeces of the bats they play host to. So advantageous has this been for the pitcher plant that they have evolved pitchers into which bats fit snugly and even with a parabolic reflector making it easier for bats to find them using echolocation.

Dr Caroline Schöner from the Department Applied Zoology and Nature Conservation, University of Greifswald and co-author of the paper, explains:

Pitcher plants grow on nutrient-poor soils, but whereas N. rafflesiana copes with this lack of nutrients by using fluid-filled pitchers to catch insect prey, N. hemsleyana has abandoned carnivory in favour of a unique and intimate relationship with the woolly bat.

To provide the bat with an ideal roost, the pitchers of N. hemsleyana have evolved to perfectly fit the bat’s body. Unlike other pitcher plants they contain very little fluid. And most striking of all, the backwall of the pitcher forms a parabolic dish that aids the bat’s echolocation. In return for its roost, the bat hunts and pre-digests the insects, depositing them as faeces in the pitcher.

In a simple but elegant experiment, Dr Schöner selected samples of both species of pitcher plant in the wild in Borneo and blocked their pitchers with cotton wool and cling film to prevent insects and bat faeces from entering them. She then fed the plants on bat faeces, insects, or a mixture of both before measuring their growth rate, nitrogen content and photosynthesis. She then replicated the experiment in laboratory glasshouses in Germany.

As the hypothesis suggests, N. hemsleyana fed on bat faeces had the highest rates of growth and photosynthesis, and the highest nitrogen levels, showing that it benefits by efficiently outsourcing prey capture and digestion to its mammal mutualists and strongly benefits from this ecological outsourcing,” explains Schöner.

By interacting with bats N. hemsleyana has access to a wide variety of insects because bats are better hunters than plants. And because the bats have predigested the insects, the nutrients should be easier for the plants to extract.

It's quite easy to imagine how this system evolved. Such was the efficiency in terms of speed of digestion and release of nitrogen for the plant that anything that increased to likelihood of the occasional bat choosing to roost in a pitcher would pay dividends. Enough nutrient was left in the faeces to supply the plant with its needs and any loss of quality was more than made up in quantity and ease of digestion. In competition with other members of the species the evolutionary pressure to accommodate a bat would have been strong as would the evolutionary pressure on the bat to exploit the available and easily-found pitchers for safe roosting, hanging as the pitchers do on the end of a slender stem.

In fact, what may be harder to understand is why the closely-related species of pitcher plant, N. rafflesiana, retained its dependence on captured insects and never went down the bat faeces route. What we can be sure of with this system is that these pitcher plants will not be found before about 50-60 million years ago because there were no bats. This might seem like an obvious point but it illustrates how a change in the environment - in this case the appearance of bats in the pitcher plant's environment - creates a new evolutionary opportunity.

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