Evolution and Biodiversity

Category: energy

Fairy lantern rediscovered

Unexpectedly, the cheating plant Thismia kobensis still exists

The rediscoverd Kobe fariry lantern is a cheater

It was discovered in 1992 and believed to be extinct because the site where it had been found was destroyed in 1999. But now, it is rediscovered elsewhere: the Kobe fairy lantern. Kenji Suetsugu and colleagues describe the beautiful but cheating tiny plant.

You would hardly recognize them as plants, the small, splendid ‘fairy lanterns’ on the forest floor, often hidden under fallen tree leaves. Fairy lanterns, Thismia species, are indeed remarkable plants. What you see are the flowers, less than a centimeter in size. The plants have no green leaves, only some scales on the very short stem. Most of the plants lives underground.

There are about 90 species, one of which is Thismia kobensis, the Kobe fairy lantern. Small and inconspicuous as it is, it was only discovered in 1992, in an oak forest near the Japanese city of Kobe. The find was small: it consisted of no more than one specimen. The site was destroyed in 1999 when an industrial complex was constructed, and the newly discovered species went extinct. That was what people thought. But fairy tales exist: in 2021 biologists unexpectedly rediscovered the plant on a conifer plantation in the town of Sanda, 30 kilometers from the original site. And this time the find was larger: almost 20 individuals. Now, Kenji Suetsugu and colleagues provide a scientific description of the species.

The loveliness of its flower is deceptive: Thismia kobensis belongs to a group of cheating plants.

Energy requirement

The cheating has to do with the lack of green leaves.

The green leaves of normal plants contain many chloroplasts. In these cellular organelles, photosynthesis takes place: plants extract carbon dioxide from the atmosphere and with the help of sunlight they fix the carbon in carbohydrates such as sugars and starch. From these carbohydrates, they derive energy. Plants without green leaves cannot make carbohydrates, but they do need energy.

Many of these plants solve this problem by extracting sugars with their roots from fungi in the soil. The scientific term for this is mycoheterotrophy.

Fairy lantern is sugar thief

Most mycoheterotrophic plants target fungi that live in a mutualistic relationship with green plants. The fungi get sugars from these plants. In return, the fungi help the green plants to absorb water and nutrients such as nitrogen and phosphorus from the soil. This collaboration, called mycorrhiza, is mutually beneficial and both parties are honest.

However, when mycoheterotrophic plants such as Thismia make contact with mycorrhizal fungi, they don’t cooperate in this way. They do receive water and nutrients, but they do not return sugars. They can’t. Instead, they take up sugars from the fungus in addition to water and nutrients. In other words: they steal. The fungus had received those sugars from green plants, so mycoheterotrophic plants indirectly parasitize on green plants via mycorrhizal fungi.

Difficult alternative

There are about 500 species of mycoheterotrophic plants. They live on nutrient-poor soils in forests, where little sunlight reaches the soil and the ability for photosynthesis, i.e., sugar production, is limited. Sugar theft is the alternative that these plants developed.

sarcodes sanguinea is a myceheterotrophic plantBut it’s not as easy as it seems. It is difficult for a mycoheterotrophic plant to form a relationship with a mycorrhizal fungus. Where a green plant interacts with many mycorrhizal fungi species simultaneously, a mycoheterotrophic plant can make contact with only one or a few fungal species. That’s probably because most fungi detect the cheaters and hold off on the relationship. Therefore, mycoheterotrophic plants are always rare and never widely distributed.

Mycoheterotrophic species often target a fungus that has many different green partners. With so many suppliers, the sugar supply is always guaranteed.

Dust seeds

The vast majority of land plants live in association with mycorrhizal fungi. The mycoheterotrophic mode of life -which abuses this mutualism – has developed dozens of times. In the case of fairy lanterns, this happened many millions of years ago. That is why they have little resemblance to ordinary plants. Other mycoheterotrophic plants emerged much more recently and have a more normal appearance.

the brid's nest is a mycoheterotrophic orchidSome plants are mycoheterotrophic shortly after germination only; this applies to all orchid species. The seeds are as fine as dust and contain no food. After germination, these plants get their sugars from fungi until they have leaves and can make their own sugars. This could be a first step towards a fully mycoheterotrophic lifestyle. There are also orchid species that stay mycoheterotrophic during their whole life, for example the bird’s nest, Neottia nidus-avis.

Broomrape species (Orobanche) look similar to some mycoheterotrophic plants, but are different: with their roots, they parasitize directly on other plants.

Willy van Strien

Photos:
Large:
Fairy lantern of Kobe, Thismia kobensis ©Kenji Suetsugu
Small:
Snow plant, Sarcodes sanguinea, a mycoheterotrophic plant from North-west America. David῀O (Wikimedia Commons, Creative Commons CC BY 2.0)
Bird’s nest orchid, Neottia nidus-avis. BerndH (Wikimedia Commons, Creative Commons CC BY-SA 3.0)

Sources:
Suetsugu, K., K. Yamana & H. Okada, 2023. Rediscovery of the presumably extinct fairy lantern Thismia kobensis (Thismiaceae) in Hyogo Prefecture, Japan, with discussions on its taxonomy, evolutionary history, and conservation. Phytotaxa 585: 102-112. Doi: 10.11646/phytotaxa.585.2.2
Gomes, S.I.F., M.A. Fortuna, J. Bascompte & V.S.F.T. Merckx, 2022. Mycoheterotrophic plants preferentially target arbuscular mycorrhizal fungi that are highly connected to autotrophic plants. New Phytologist 235: 2034-2045. Doi: 10.1111/nph.18310
Jacquemyn, H. & V.S.F.T. Merckx, 2019. Mycorrhizal symbioses and the evolution of trophic modes in plants. Journal of Ecology 107: 1567-1581. Doi: 10.1111/1365-2745.13165
Gomes, S.I.F., J. Aguirre-Gutiérrez, M.I. Bidartondo & V.S.F.T. Merckx, 2017. Arbuscular mycorrhizal interactions of mycoheterotrophic Thismia are more specialized than in autotrophic plants. New Phytologist 213: 1418-1427. Doi: 10.1111/nph.14249

Saving energy

Venus flytrap controls the trapping process in several ways

Venus flytrap has several mechanisms to save energy

Carnivorous plants should control their energy budget, otherwise the benefits of capturing insects will not compensate for the costs. The Venus flytrap has several mechanisms to limit waste of energy, Andrej Pavlovič and colleagues discovered.

To us, it is almost impossible to catch a fly. But the Venus flytrap has no difficulty. The plant (Dionaea muscipula) occurs in North and South Carolina (United States), where it grows in sunny, wet areas on poor soil; it can grow there by ‘eating’ insects. The catch of a fly yields lots of nutrients, but the process also demands lots of energy, and the balance between yield and costs must be positive, otherwise the plant will not grow. So, it has evolved a number of control mechanisms to minimize waste of energy, as Andrej Pavlovič and colleagues point out.

The leaves of the Venus flytrap end in a two-lobed trapThe leaves are arranged in a rosette, and each leaf has a double-lobed trap at the top with a row of ten to twenty teeth at the edge of each lobe. Glands along the edges secrete a sugary substance that attracts insects. Each lobe has a few trigger hairs that respond when touched by an insect, causing the trap to snap shut rapidly. The central zone of the trap contains glands secreting enzymes that digest a trapped prey and proteins that enable the glands to absorb the nutrients that are released upon digestion.

The Venus flytrap has to invest a lot of energy to keep the traps operational and to produce lures, digestive enzymes and absorption proteins. How does the plant control these costs?

1: Two times

First of all, a trap will not snap shut until trigger hairs are touched at least twice within twenty seconds, when there is a fair chance that an insect has landed. So, a trap will not close when a for instance a wind-blown dust grain touches a trigger hair.

2: Panic

But not every animal that landed turns out to be a nice fat fly. Upon closure, small gaps between the marginal teeth allow little insects that are not worth the effort to digest them to escape. If the trap is empty, it will reopen again after a few hours. But if a large insect is encased, it will struggle in panic, and his movements induce the trap to seal hermetically. After the trigger hairs have been touched at least five times, the secretion of digestive enzymes and absorption proteins starts, and the more movements the prey makes, the more enzymes and proteins will be secreted.

3: Limited reaction

Still, a trap may snap shut, close tightly and secrete digestive enzymes and absorption proteins in vein. This happens when it is damaged. The cause of the error is to be found in the evolution of carnivorous plants, for the habit to capture insects probably evolved from defence mechanisms against herbivorous insects. In ordinary plants, herbivory generates an electrical signal, which in turn stimulates the accumulation of plant hormones, jasmonates. These will induce the plants to synthesize toxins that harm the insects, not only locally on the place of damage, but also elsewhere in the plant, as a precaution. In carnivorous plants, such as the Venus flytrap, things have a bit changed. In these plants, the presence of an insect triggers an electrical signal that induces the accumulation of jasmonates; these hormones stimulate the secretion of digestive enzymes and absorption proteins. The electrical signal also induces the trap to close.

Now, Pavlovič conducted an experiment in which he repeatedly wounded a trap of Venus flytraps by piercing it with a needle to mimic herbivory, and noticed that the trap showed the same response as when the trigger hairs wouldhave been touched by an insect: the trap closed and jasmonates accumulated; if he continued damaging every few minutes, the traps secreted digestive enzymes and absorption proteins – to no end. But the misplaced reaction was limited to the local trap that was damaged and did not occur elsewhere in the plant, in contrast to defence reactions agains herbivores.

4: Process stops

The secretion of digestive enzymes and absorption proteins does not run at full speed from the start. Only when certain substances from an enclosed prey are released, the rate of secretion increases to the highest speed. If there is no prey, the process will stop. So, the plant doesn’t waste much energy when it is misled.

After about ten days the fly is digested and the fall will reopen again.

Willy van Strien

Photos
Large: ©Andrej Pavlovič
Small: Olivier License (via Flickr, Creative Commons CC BY-NC-ND 2.0)

Watch the trapping process

Sources:
Pavlovič, A., J. Jakšová & O. Novák, 2017. Triggering a false alarm: wounding mimics prey capture in the carnivorous Venus flytrap (Dionaea muscipula). New Phytologist 216: 927-938. Doi: 10.1111/nph.14747
Böhm, J., S. Scherzer, E. Krol, I. Kreuzer, K. von Meyer, C. Lorey, T.D. Mueller, L. Shabala, I. Monte, R. Solano, K.A.S. Al-Rasheid, H. Rennenberg, S. Shabala, E. Neher & R. Hedrich, 2016. The Venus flytrap Dionaea muscipula counts prey-induced action potentials to induce sodium uptake. Current Biology 26: 286-295. Doi: 10.1016/j.cub.2015.11.057
Libiaková, M., K. Floková, O. Novák, L. Slováková & A. Pavlovič, 2014. Abundance of cysteine endopeptidase dionain in digestive fluid of Venus flytrap (Dionaea muscipula Ellis) is regulated by different stimuli from prey through jasmonates. PLoS ONE 9: e104424. Doi:10.1371/journal.pone.0104424
Pavlovič, A., V. Demko & J. Hudák, 2010. Trap closure and prey retention in Venus flytrap (Dionaea muscipula) temporarily reduces photosynthesis and stimulates respiration. Annals of Botany 105: 37-44. Doi:10.1093/aob/mcp269

Sweet snack

Wild bees can do without flowers – for a while

Andrena-bee visiting a flowerless shrub

When spring arrives in California, wild bees emerge before flowers appear that offer nectar, providing the animals with energy. To survive, they temporarily use sugary honeydew, as Joan Meiners and colleagues discovered.

It seems weird for bees to visit non-flowering shrubs, because they need flowers to find nectar, which contains sugars, and pollen, which contains protein; these nutrients are necessary for themselves and their larvae. Yet, in the Pinnacles National Park in California, Joan Meiners observed many wild bees of different species visiting shrubs on which no flower was to be found.

Honeydew

With a series of experiments, she and her colleagues found out what the bees were looking for at the non-flowering shrubs: the animals were accessing sugary honeydew, the sweet secretions of sap-feeding scale insects. It appeared that bees visit flowerless shrubs only early in the springtime, when they emerge while there are hardly any flowers blooming, and that all these bees belong to solitary species, not living in colonies where a stockpile of nectar is available. Apparently, in early spring honeydew is an alternative source of energy for these bees, a new discovery.

Now, the question is how the bees are able to find this alternative food source. They are specialists in detecting and distinguishing colours and scents. Flowers depend on bees for pollination, because as bees visit multiple flowers in succession, they transfer pollen from the stamens of one flower to the pistil of the next one, so that this second flower can grow seeds after fertilization. Because bees are indispensable, flowers attract them with showy scents, colours and shapes.

Still, bees manage to find the colourless, odourless honeydew as well.

Looking for food

Are they attracted by the black mold fungus that covers the honeydew? The researchers ruled out this possibility by painting a number of branches black: these branches were not visited by the bees. Do the scale insects form a clue to the honeydew? No, because if the sap-sucking insects were temporarily inactivated with a mild anti-insecticide, no bees were seen nearby; they only came when the scale insects were producing honeydew. But on the other hand, they did detect sticks on which the researchers had sprayed a sugar solution, and they did already within an hour.

The biologists propose that the bees are continuously looking for food, and if one bee locates some honeydew, other bees will notice and visit the food source as well.

Using honeydew as an extra source of energy, the bees can survive a period without nectar. But in the end they do need flowers, because the larvae cannot develop on a diet of sugars alone, but have to ingest a high amount of proteins, and therefore they need pollen. So, every female has to gather pollen for her offspring.

Once plants start flowering, bees lose their interest in honeydew-bearing shrubs and visit flowers instead. The mutual relationship between bees and flowers – where pollination is exchanged for food – is not jeopardized.

Willy van Strien

Photo: ©Paul G. Johnson

Source:
Meiners, J.M, T.L. Griswold, D.J. Harris & S.K.M. Ernest, 2017. Bees without flowers: before peak bloom, diverse native bees find insect-produced honeydew sugars. The American Naturalist, online May 30. Doi: 10.1086/692437