As part of my research on the nettle family, Urticaceae I became aware of plants growing in the entrance caverns of caves several years ago and for over a year now my collaborators at the Guangxi Institute of Botany, China lead by Professor Yigang Wei and I have been working on documenting the full diversity of this unusual flora. This lead us to think about whether these plants may have become adapted to life in caves, in particular the relatively constant climate and low light. Especially for species which grow amongst the lowest light levels at the back of caverns where they are growing in a fraction of the light they could be expected to receive in a forest. We therefore applied for a grant from the Guangxi Key Laboratory of Plant Conservation and Restoration Ecology in Karst Terrain, and the Foreign Experts Bureau to undertake some preliminary work to document the climate, light and photosynthesis of the plants in the caves.
We selected the Yangtse cave as we know the diversity of plants that grow there (ten species of nettle alone), we have three data-loggers recording temperature and humidity in it and it is close to a town where we can spend the night. It is also a spectacular and beautiful place to spend several days working. The aim of our work was to collect the data necessary to test the hypothesis that the plants growing within the entrance cavern of the Yangtse cave exhibit different photosynthetic performance than the same or congeneric species growing outside of the cave. To do this we randomly selected individuals of three species of nettle in the genus Elatostema, one species of Begonia and a species of fern at four different locations in the cave, the back, midway into the entrance cavern, at the entrance and outside of the cave. We also brought two species of Elatostema from the living collection at the Guangxi Institute of Botany to compare their photosynthesis performance with members of the same species that had grown up within the cave. This was to get some indication as to how plastic their response was.
Each plant was connected to a hand-held PAM chlorophyll fluorometer, an incredibly sensitive device that can measure several key outputs of photosynthetic reactions in the chloroplasts as they take place. By comparing our study plants to those growing outside of the cave and from the scientific literature we hope to see whether cave-dwelling plants differ from non-cave plants in some of those parameters, and whether those differences are dependent upon what kind of plant they are. These parameters include the efficiency of photosynthesis, that is how much of the light energy is harnessed by the photosynthetic reactions, how much is dissipated and how resilient the photosynthetic apparatus is to changing light intensity. If we find a difference between cave and non-cave dwelling plants then taken together these measurements can provide some indication of which group of photosynthetic reactions are leading to these differences.
Thanks to funding from the Bentham Moxon Trust and the Guilin Botanical Garden, myself and colleagues explored five caves for plants in October of this year (2014). There are likely thousands of caves in the limestone karsts of south-east asia which contain plants. Whilst of great interest botanically and for conservation they are also beautiful in their own right and each cave is unique. I thought I would provide a portrait of each one to show how varied they are in their form, where plants grow in them and their size.
The cave above was one of the few that we spotted from the road and then were able to get to. It is also one of the few that had little evidence of human disturbance, very few footprints and areas of pure white travertine that had fallen from the roof had not been walked on or collected. The main plant-bearing cavern of the cave was about 25 m deep and the roof 15 m high and it had a well developed flora, you can see plants from the african-violet family (Gesneriaceae) in the foreground and we collected five species of nettle here.
Xiangshuidong Tian Keng cave in Guizhou was one of the largest caves that we have collected in, but also one of the most impacted by tourism and use by local communities. The main cavern is about 250 m deep with a roof between 45 and 30 m high and it is set within a huge cliff forming the side of a mountain. It also has a waterfall and river running across the back of it. It is in this cave that we found a very rare and unusual form of Elatostema oblongifolium that has its male flowers borne on specialised shoots but overall the plant diversity of the cave was quite low, presumably because of the large numbers of local tourists and associated trampling of much of the ground available for plants
This was the first cave that we encountered on this field trip. We found it after first being taken to a hole in the ground as what must have been a mistranslation from Mandarin into the local dialect. The cave was relatively big and had a trail running inside. The main cavern shelves very steeply meaning that very little light penetrates into the cave. Despite this and the relatively high altitude, 1500 m, we collected seven species of nettle from here.
This cave should have been perfect as it shelved gently meaning that light penetrated quite deep, it also had plenty of places for plants to grow, such as boulders and rocks. We only collected four species of nettle here, probably because the cave was heavily impacted by farmers using it as a barn to keep their water buffalo in at night. Evidenced by lots of hoof prints and dung. This is a very common use of caves and the trampling of buffalo and their herders can have a significant impact on the plants in the caves (see below).
Nettles have unisexual flowers, that is each flower functions only as a male or a female. Counter-intuitively though the flowers still retain the non-functional and often much-reduced organs of the non-functional sex. These are called pistillodes in the case of the rudimentary female organs in male flowers and staminodes in the case of the rudimentary male organs in female flowers. Inpart of the nettle family the staminodes are put to good use: ejecting the seed from the fruit.
This can be best understood by considering that nettles have male flowers which open explosively, pollen being released in tiny clouds (they are also very small). In fact one species, Pilea microphylla, is commonly known as the artillery plant for this reason. The mechanism for the explosive opening of the male flower is that the stalks (filaments) of the pollen sacks (anthers) are folded in on themselves in bud. As they develop these stalks fill with water until they are all pressing against each other within the flower bud and ready to burst. At a certain point the pressure becomes too great for the thin petals of the flower bud and they rip leading to the stalks being able to straighten explosively. This has happens incredibly quickly and although it has not been recorded for nettles, in the closely related mulberry where this also happens, the flower can open in 25 millionths of a second, moving petals to velocities in excess of half the speed of sound.
In one group of nettles which includes seven genera this explosive ability of the pollen sacks has been harnessed to release the seed from the fruit. Below you can see a close-up of the fruit of Pilea japonica showing the staminodes flexed and ready to eject the seeds (dark coloured).
I have just returned from collecting nettles in South West China with my great friend and colleague Professor Wei Yi-Gang and researcher Fu Long-Fei from the Guilin Botanic Gardens. For several years we have been working on documenting the nettle diversity of the limestone karst of this region, focusing on the poorly known cave-associated floras. Karst is a form of limestone which has been weathered by rain for millions of years resulting in finely divided and sharp surfaces and very steeply sided hills, small mountains and gorges. The karst where we have been working form part of a formation which runs from Myanmar, northern Thailand and Vietnam and across into southern China and includes the famous ‘stone forests’ of Yunnan and Guangxi. I am interested in karst because it is where nettles are most diverse, both in terms of genera (species groupings) and species. At a single location it may be possible to encounter eight genera and over a dozen species!
Because the limestone is porous it has resulted in the formation of thousands of caves whose entrances have been colonized by plants from a small group of families: nettles (Urticaceae), african violet family (Gesneriaceae), Begonias (Begoniaceae), ivy family (Araliaceae), the coffee family (Rubiaceae) together with ferns and mosses. The most diverse of these are the nettles, one group of which, Elatostema has about 1/5 of the species from this region known only from caves. As well as having very low light levels, sometimes 1/10 of 1% daylight, the caves have constant humidity and low temperatures which contrast strongly with the cave exterior. The cool air of a cave can be felt up to 20 m from the entrance, often before the cave itself can be seen. We believe that the species associated with caves have likely come from the deep shade of the forests that once dominated this area but which have since been lost to agriculture. It also possible that some of the species are relicts of a previous, cooler climate during the last ice-age. This is something that we have begun to study.
Caves represent a last refuge for several hundred species in SW China and now is a time of great change as caves come under threat from tourism, agriculture, urbanization and cement production. We want to help conserve these caves and the species that they include by first documenting their diversity and distribution across SW China. This information can be disseminated within China in the hope of raising awareness and protecting individual caves. It could also be used to identify a network of protected caves which include all of these species. Professor Wei would also like to develop protocols for cultivating the species outside of caves, something that is very difficult to achieve at the moment and which could represent a vital step for their conservation.
Since 2007 I have been working with colleagues at the Chinese Academy of Sciences Guilin Institute of Botany on documenting the unusual cave flora of SW China and Guangxi. My interest stems from the fact that one of the most common groups of plants in these caves are two particular groups of nettles, members of the succulent herbaceous genera Elatostema and Pilea. It is also heavily influenced by the presence of a very knowledgeable and dedicated botanist at the Guilin Institute of Botany, Professor Wei Yi-Gang.
More recently I have wanted to see whether it is possible to explain how, and when these plants occupied these ancient caves. Possible explanations are that they evolved in the caves, some of which are 15-25 million years old; alternatively that they represent plants which grew outside of the caves when the climate was different, during the last ice-age for example; lastly that they are relics of plants which grew in the forest understory outside of the caves prior to the arrival of agriculture in the area maybe 1,500 years ago. To try and answer these questions I have, together with a Masters student Alfred Gay, used DNA extracted from the leaves of the plants to look for patterns which may point to one of the three possible explanations above. Click here to see a slide show of the preliminary results.
Another interesting line of research would be how these nettles survive in such low light levels. In some cases 1/50th of 1% daylight! For the moment though I am focussing on documenting their diversity and describing the new species we find but in the long-term I am hoping to find collaborators to explore these other areas of research.