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Botanical buffet - the importance of living collections for plant systematics

Volume 4 Number 1 - January 2007

Tim Entwisle

Botanic gardens have plenty of uses, but I want to talk about just one aspect here: how important are the living collections for systematics and taxonomic research? As the head of a major world botanic garden, I often pontificate on the importance of the collection for science. The link to horticulture (and the development and maintenance of cultivars) is relatively easy to explain. The link to conservation is also relatively straightforward (see Makinson 2006), although often overplayed in terms of the ex situ importance of the living collection seen by most visitors. But do we need the collection for systematics, for discovering how plants have evolved, their relationships, and how they are best classified? Well, yes we do.

Firstly let me narrow the definition down a little. Prompted by Makinson (2006), I will exclude seedbanks and other forms of storing genetic material (e.g. tissue collections), and discuss only the whole plants that populate our botanic gardens. These are what Makinson calls “whole-plant live collections”, and which I will lazily call “living collections”. Systematics science and botanic gardens have had a close association since the time of Linnaeus, but why, and is this link still relevant?

I can think of a dozen, somewhat overlapping, reasons why living collections are important for systematics but have grouped them here into three main areas. These are: the range of material, the value of living material and the access to other information. Hay and Herscovitch (1997) covered some of the same ground in their passionate plea for the responsible sharing of living collections. Like them, I’ve drawn examples from the science programs at the Botanic Gardens Trust to illustrate my points.

Range of material

A botanic garden collects together Plants from many different places and grows them in a relatively contained area (although up to 400 ha in the case of our Mount Annan Botanic Garden, or 900 ha for the Xishuangbanna Tropical Botanical Garden in southern China…). This provides easy access to a wide range of living plants and efficiencies in sampling. So our systematist can observe and sample a great diversity of plants in the one place. This saves the costs of organizing extensive field trips which may or may not be successful.

Our understanding of plant diversity is organised around plant families. Over 80 per cent of the approximately 450 families are easy to recognize and are, for the most part, thought to be monophyletic. The Angiosperm Phylogeny Group has rebuilt the evolutionary tree for flowering plants from molecular data (Chase et al. 1993) which is helping us understand the taxonomy of plant families. Almost half of the 499 species sampled in the 1993 paper, representing about 265 families, were from botanic gardens (in later papers the percentage was even higher, driven partly by Mark Chase’s move to the Royal Botanic Gardens, Kew). It would have taken many more years to complete and we would have a much poorer knowledge of the phylogeny of angiosperms today if the rich living collections held by botanic gardens around the world, including those in Sydney, were not available for this research.

Botanic Gardens Trust scientist Peter Weston and his colleagues have published extensively on the phylogeny and biogeography of the iconic southern hemisphere family Proteaceae. For their paper on South African Proteaceae (Barker et al. 2002), all but a couple of the 50 species sampled were from botanic gardens in South Africa and Australia - many are rare and difficult to sample in the wild.

Botanic gardens also hold unique collections of species or variants which no longer exist in the wild (e.g. Sophora toromiro from Easter Island), or are inaccessible due to political or regulatory constraints.

There is often more variety in botanical material available, particularly at the generic level, in a botanic garden than would be possible to access through even extensive field collecting. A large number of genera can sometimes be sampled in one place. Darren Crayn, a systematist at the Botanic Gardens Trust, made extensive use of the collections held at Marie Selby Botanical Gardens in Florida, when he was working as a post-doc at the Smithsonian Tropical Research Institute in Panama. He identified CAM (crassulacean acid metabolism, usually found in plants living under arid conditions) photosynthesis by measuring C12 to C13 ratios (reflecting the different enzymes used in CAM and C3 photosynthesis, and their different affinities for C13) in 56 of the 57 genera of Bromeliaceae, and 1,873 of the approximately 2,890 species. Crayn found that CAM photosynthesis and the epiphytic habit had evolved several times. At least 90 per cent of the taxa sampled were from living collections (Crayn et al. 2004), so this work was made practically possible by collecting from botanic gardens.

There is also an opportunity cost in not bringing plant material into cultivation. Our systematist can swan along the Amazon or the Roper and collect bits and pieces of intriguing new species, but we don’t know what will be useful in 10 or a 100 years’ time. We don’t know what bit of the plant might provide useful data once back in the laboratory examining our pickings. We add value by collecting propagation material and maintaining that plant in the living collection. There is a cost, of course, in caring for any plant introduced into a botanic garden, but there is often a greater cost in not introducing it when you have the opportunity…

Value of living material

Many characters, e.g. morphology, chemistry (including genetic markers), chromosomes, and so on, are best examined from living material. It is usually easier to sample in a botanic garden than in the natural habitat and a botanic garden may be able to provide more material than is available in the wild.

In a recent treatment of the waratahs (Telopea and its relatives), 14 of the 16 taxa examined were grown in botanic gardens, making it straightforward to assess characters from leaf anatomy and floral development using living material (Weston & Crisp 1994). The results of the analysis supported continental breakup (from Gondwana) and climate change as the key drivers behind the present diversity of waratahs and where they occur in the Southern Hemisphere.

Systematists can observe a plant throughout its life history, seeing features that may not be visible at the time of a field visit (e.g. buds, flowers, fruits…). They can also watch how fruits develop, how a flower opens or even the germination of seed and its early growth. Ken Hill and Lawrie Johnson used seedlings grown at the Royal Botanic Gardens in Sydney to help formulate their incisive views on the classification of Australian eucalypts, including rearrangements to the generic and subgeneric classification (e.g. Hill & Johnson 1995).

Most systematists value living collections as an adjunct to extensive herbarium collections. A plant that is taken directly from the wild and preserved is a true representative of the taxon and will provide information to many generations of taxonomists. However, examination of a living plant helps to avoid misinterpretation and misunderstanding of the morphology. Botanic Gardens Trust Honorary Associate, Alistair Hay, grew and studied extensive collections of aroids as part of his detailed monograph of a genus of the Araceae (e.g. Hay & Yuzammi 2000). The accuracy of the taxonomy relied on detailed observations on developing flowers, including their colour, odour and pollen shed. Inflorescences are difficult to find in the field, and a single herbarium collection will rarely include all stages of development.

It is usually easier to sample in a botanic garden than in the natural habitat, the hard work having been done already by the original collector. Our systematist can choose a day to suit the diary, or work around the flowering time of the plant (which may be well recorded or which can be monitored by a colleague at the botanic garden). The scientists cited here all work in the botanic gardens of the Botanic Gardens Trust in Sydney, and are just part of the expertise available.

A botanic garden may also be able to provide more material than is available in the wild. This can be particularly true of a species that is rare or difficult to sample in its natural habitat. For example, there are fewer than 100 individuals surviving in the natural habitat of the Wollemi Pine (Wollemia nobilis) near Sydney. These relictual populations are protected to stop the introduction of life-threatening fire and disease. For over ten years the collections held by the Botanic Gardens Trust have been used to study not only the pine’s biology and ecology, but also its surprising phylogeny and classification. The Wollemi Pine is the only species in the third living genus (Wollemia) of the conifer family Araucariaceae. It has features in common with the other living genera Agathis and Araucaria as well as with Cretaceous and early Tertiary fossil groups such as Araucarioides. A successful propagation research programme has responded to the great demand from gardens around the world. This research is based on the botanic gardens’ collection.

John Thomson, an Honorary Associate with the Botanic Gardens Trust, needed to repeatedly sample specimens of bracken (Pteridium) to improve his extraction technique for DNA fingerprinting, in order to resolve the complex network of hybrids and polyploids obscuring the species level taxonomy in this genus (Thomson 2000). Herbarium material of bracken is typically very fragmentary – sometimes just a few pinnae from an unspecified part of the frond and a piece of stipe. Professor Thomson used the extensive living collections which he had assembled to look at complete fronds, and all the fronds at all stages of development. He found that the pinnae on each frond form a Mandelbrot series, and that the basal (or near basal) pinnae are the most reliable for comparative morphometric purposes (Thomson et al. 2005). It can be difficult to accurately locate the position of a pinna on a frond from the dried fragments held in herbaria.

By growing a wide range of closely related species together, botanic gardens can provide “standard conditions”, allowing the morphology and chemistry of plants to be compared without local variations in the environment. Conditions can be controlled even more strongly in glasshouses for experimental studies. For example, key diagnostic characters such as the morphology of the indumentum are known to be environmentally variable in many fern genera. John Thomson (see above) used a “standardised environment” to help him define morphological groups of bracken that matched the results of his extensive molecular sequencing work. He has also been able to use these standard conditions to test the use of chemicals such as ptaquilosides for their use as characters in taxonomy (Smith et al. 1994).

Mycologists from the Botanic Gardens Trust Sydney in Australia, and the University of Stellenbosch in South Africa (Crous et al. 2000) made good use of the living collections of four botanic gardens in Tasmania and New South Wales to make a first cut of the fungal diversity on the leaves of Australian Proteaceae. Brett Summerell, from the Trust, notes that what would have taken many months and considerable resources to sample from natural habitats, was completed in less than a week, and examining living material was quicker than examining dried material. Their research gives us a snapshot of the fungal species likely to occur in the natural habitats of the host species.

Importantly, the botanic gardens collection is a potentially sustainable source of scientific material and takes the pressure off wild material. A collection can also be part of an educational or horticultural display; the continued growing of the individuals and/or their offspring should be relatively economical as well.

Access to other information

Botanic gardens are institutions dedicated to research into plant diversity. Their facilities and staff underpin systematic research.

By checking the database (whether on computer, on cards, or in the heads of experts, or any combination of these), our systematist can find out quickly whether a plant is held in a given Botanic Garden or not, and if it has reached a stage when it displays critical features (such as flowers or fruits). Additional information, such as what other scientific information may exist (e.g. herbarium collections, DNA extractions, photographs), may also be available. All papers cited here have used data from the various living collections databases to help locate the plant material they have utilised - its origins as well as its location in a botanic garden.

Taxonomists need access to collections of preserved plants (herbarium and spirit collections) and a good botanical library if they are to supply good species descriptions and distribution information, identification tools and sound nomenclature. At the Botanic Gardens Trust, our three key scientific assets are the living collections on all our estates, the specimens in the National Herbarium of New South Wales, and the books, archives and other materials held in the Royal Botanic Gardens Library. While efforts are being made to make label information and images of preserved specimens available on the web, and an increasing amount of scientific literature is available on-line means that some of these data may be available in the field, it’s not quite the same - at least not yet.

Much of the best information is held in the minds of our scientists, horticulturalists, teachers and other staff and associates. Together they are perhaps the fourth great scientific asset of the Botanic Gardens Trust. Botanic gardens around the world will either have their own experts in particular plant groups or can locate someone close by.

Conclusion

So this “botanical buffet” is a wonderful thing. Is there a chance that it is an expensive indulgence? It is important to have a focused collections policy so there is a wide range of species (not only those that by chance are maintained in our botanic gardens collections), be aware that the collection might be a limited genetic subset grown in gardens, be aware of possible errors in record keeping translated into our thinking, and so on. But on balance, the convenience and potential of the living collections in our botanic gardens are too important to ignore, or indeed take for granted. Systematics is all the better for having these collections at its disposal. The crux of this relationship is good record keeping that allows the systematist to relate his or her findings back to the natural world - the botanic garden is a great surrogate as long as the primary data is accurate. And the better the systematics, the better decisions we can make about the wise use and management of our natural world (but that’s another story).

References

  • Barker, N. P., Weston, P. H., Rourke,J. P. & Reeves, G. 2002. The relationships of the southern African Proteaceae as elucidated by internal transcribed spacer (ITS) DNA sequence data. Kew Bulletin 57: 867-883.
  • Chase M. W., Soltis D. E., Olmstead R. G. et al. 1993. Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Annals of the Missouri Botanical Garden 80: 528-580.
  • Crayn, D., Winter, K. & Smith, J. A.C. 2004. Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. Proceedings of the National Academy of Sciences of the United States of America 101: 3703-3708.
  • Crous, P. W., Summerell, B. A., Taylor, J. E. & Bullock, S. 2000. Fungi occurring on Proteaceae in Australia: selected foliicolous species. Australasian Plant Pathology 29: 267-278.
  • Hay, A. & Herscovitch, C. 1997. Living collections and taxonomy of Malesian Araceae: a basis for conservation. Conservation into the 21st Century - Proceedings of the 4th International Botanic Gardens Conservation Congress (Eds. Touchell, D. H., Dixon, K. W., George, A. S. & Wills, R. T.) pp. 301- 307. (BGCI, London.)
  • Hay, A. & Yuzammi 2000. Schismatoglottideae (Araceae) in Malesia I - Schismatoglottis. Telopea 9: 1-177.
  • Hill, K. D. & Johnson, L. A. S. 1995. Systematic studies in the eucalypts, 7. A revision of the bloodwoods, genus Corymbia (Myrtaceae). Telopea 6: 185-504.
  • Makinson, R. O. 2006. Botanic Gardens and Conservation. In Plant Conservation Genetics, ed. R. J. Henry, pp. 75-90, The Haworth Press, New York.
  • Smith, B. L., Seawright, A. A, Ng, J.C., Hertle, A. T., Thomson, J. A. & Bostock, P. D. 1994. Concentration of ptaquiloside, a major carcinogen in bracken fern (Pteridium spp.), from eastern Australia and from a cultivated worldwide collection held in Sydney, Australia. Natural Toxins 2: 347-353.
  • Thomson, J. A. 2000. Morphological and genomic diversity in the genus Pteridium (Dennstaedtiaceae). Annals of Botany 85 (Suppl. B): 77-99.
  • Thomson, J. A., Chikuni, A. C. & McMaster, C. S. (2005). The taxonomic status and relationships of bracken ferns (Pteridium: Dennstaedtiaceae) from sub- Saharan Africa. Botanical Journal of the Linnean Society 148: 311-321.
  • Weston, P. H. & Crisp, M. D. 1994. Cladistic biogeography of waratahs (Proteaceae: Embothrieae) and their allies across the Pacific. Australian Systematic Botany 7: 225-249.
Tim Entwisle E-mail: tim.entwisle@rbgsyd.nsw.gov.au
Postal address: Botanic GardensTrust (including Royal Botanic Gardens, Domain, Mount Tomah Botanic Garden and Mount Annan Botanic Garden)
Mrs Macquaries Road, Sydney NSW 2000, Australia
Tel: +61-2-9231 8112
Fax: +61-2-9251 4403
Internet: www.rbgsyd.nsw.gov.au