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The reasons for exotic plant invasions and why botanic gardens are particularly vulnerable

Volume 8 Number 2 - July 2011
Quentin J. Groom, Anne Ronse and Ivan Hoste

Introduction

Botanic Gardens need to be constantly alert to the possibility of introducing new invasive species. Even gardens with a high awareness of the problem may have conditions that make them prone to losing control of the plants they grow. Many of mankind’s activities can result in invasive plants, yet there are good ecological and evolutionary reasons why botanic gardens are particularly liable to causing new invasions.  Facon et al., (2006) wrote a simple synthesis of the primary reasons for biological invasions. In their paper they reduce the causes of invasions to three basic scenarios: migration change, environmental change and evolutionary change. Here we show, with reference to the National Botanic Garden of Belgium (NBGB) and other northern European gardens, how botanic gardens can actively contribute to each of these scenarios.

Migration

The range of some species is only restricted by their ability to disperse. Such species will survive in new areas, but they are unable to reach such areas by natural spread (Sax and Brown, 2000). Botanic gardens are skilful at growing introduced species, yet not all these species escape cultivation. One explanation is the hypothesis of propagule pressure (Simberloff, 2009). This hypothesis suggests that a minimum rate of propagule import is required to ensure that founder populations of aliens can establish in a novel location. Below this minimum, alien species are unlikely to find suitable habitat and will have insufficient genetic diversity to survive. This acts as a barrier to potentially invasive species, favouring those species that are more frequently imported.

“A minimum rate of propagule import may be necessary for an alien to establish”

It is clearly not only botanic gardens that import alien plants. Plant propagules are imported for all sorts of reasons, particularly for food. Today it is no doubt the horticultural industry that imports the largest range of species, either specifically for propagation and sale, or as stowaways.  By piggybacking on the activities of mankind, plants can easily breach once insurmountable barriers to dispersal.

 While the removal of dispersal barriers by human activity can explain the migration of invasive species, it does not explain why invasive plants are often more successful than native species. The enemy release hypothesis suggests that one of the reasons for the success of invasive plants is that they are released from the stress of pests and diseases that occur in their native ranges (Keane & Crawley, 2002). One of the observations consistent with this hypothesis is that:

invasive alien species have fewer pests and diseases in their invasive ranges”.

This is certainly consistent with our observations at NBGB. Although there are only about 350 wild native species compared to 7,000 cultivated taxa growing outdoors in the garden, of 100 pests and diseases recorded in the garden, only 10 occur only on alien species (Groom, 2011). While enemy release is unlikely to be the sole reason for the success of invasive species, it seems likely that it is a contributing factor in some cases.

Environment

A large number of invasive species occur in places disturbed by human activity, such as in urban environments, on agricultural land and by roadsides (Lozon, 1997). This may, in part, be explained by the creation of novel habitats. The proximity of botanic gardens to large urban areas, full of novel, unexploited habitats, certainly raises the risk of new invasions being initiated by garden escapes.

The now classical tale of how Senecio squalidus spread in Britain from Oxford University Botanic Garden along the railways in the late 19th century, usually does not tell that it was already “very plentiful on almost every wall in Oxford” at the end of the 18th century (Kent, 1956, 1960). Furthermore, it was naturalized in other distant towns, well before Oxford was connected by railway. In at least three cases it had escaped from gardens where the seed had originally been taken from Oxford as a botanical novelty (Kent, 1956). One can see the same influences of botanic gardens, novel habitats, disturbance and horticultural novelty in the introduction histories of many species (Hulme, 2011).

It will come as no surprise that species which escape into the neighbourhood of botanic gardens are those that thrive in the habitats of that area. Thus a garden surrounded by wall, as in the case of Oxford Botanic Garden, exports S. squalidus that grows on walls. Likewise, a forest garden is likely to export shade-loving species and a desert garden will export xerophytes (Marco et al., 2009). In the NBGB we have found that many of the most persistent and invasive escapes are woodland plants whose seeds are spread by birds. This is inevitable, since nearly half of the area of the garden consists of woodland.

Evolution

It has been argued that a species, when liberated from the competition, environmental stress and pests and diseases of its native habitats, can evolve to reallocate its resources from protective mechanisms into traits which confer greater invasive potential (Blossey & Notzold, 1995). While such evolution is generally suggested to occur in wild populations there is certainly also unconscious selection occurring in botanic gardens (Enßlin, Sandnera & Matthiesa, 2011). It is likely that unconscious selection for improved survival in a garden may also mean selection for traits that encourage weediness.

Selecting individuals that grow well may result in selecting for weediness”

A recent example is the case of Poa annua f. purpurea M. L. Grant (Grant, 2003).  Hand-weeding in gardens has apparently selected for this purple-leaved form of a practically ubiquitous weed. Its dark cryptic colouration makes it more difficult to see against dark coloured soil than the normal green P. annua.

Though unconscious selection will predominantly act on annual and other short-lived species, there is also a filtering process in the acquisition of plants. Dead plants are continually replaced until a species or variety is found that persists. In our own garden an accession of Oenanthe pimpinelloides, originally from Bulgaria, has escaped cultivation even though O. pimpinelloides is usually considered too cold sensitive to develop persistent populations in Belgium (Ronse, 2011).

In addition, the pool of introductions to a garden is not unbiased. Botanic gardens often produce a list of seeds for exchange with other gardens, know as an index seminum. A random survey of these lists showed that several invasive species were listed, presumably because of their high rate of seed production (Aplin & Heywood, 2008). All these processes combine to favour invasive species in gardens, indeed the result can be seen in the inventories of many gardens. Hybridisation has been implicated in the evolution of invasive plants (Ellstrand & Schierenbeck, 2000). Examples are Casuarina ssp. in Florida (Gaskin et al., 2009); Fallopia ssp. in Belgium (Tiébré et al., 2011); Senecio squalidus in the UK (Abbott et al., 2000) and Spartina anglica across Europe (Thompson, 1991). While horticulture was not the cause of hybridisation in all of these taxa, the close proximity of closely related taxa in gardens undoubtedly presents an opportunity. In the NBGB we have witnessed the in situ generation of the potentially invasive hybrid Oenothera x fallax from its two parents O. biennis and O. glazioviana. Similarly seedlings of Hyacinthoides x massartiana are increasingly found within the park, both in the collections and in semi-wild areas. This is the hybrid between the native H. non-scripta and introduced H. hispanica which have both been cultivated in the garden for more than forty years.

Despite there being little research on this subject, it seems likely that a combination of unconscious selection, hybridization between genotypes and the filtering out of feeble taxa may all contribute to the evolution of invasiveness in gardens.

Conclusion

There are many hypotheses for why we have an alien invasive plant problem. However, for each hypothesis, the cause relates either directly or indirectly from the activities of humankind. We have created a small, interconnected world, and botanists, horticulturists, and botanic gardens have eagerly cooperated in the process. We need to continually assess how we can benefit from this, while avoiding the drawbacks.
Botanic gardens are a small but significant part of the invasive plant problem. Yet botanic gardens are also leaders in good practice for horticulture and conservation and can play an important role in educating the public. While significant steps have been made to address the problem of invasive plants in botanic gardens, there is still work to be done and a clearer understanding of the mechanisms that result in problem situations is important.

References

Abbott, R.J., James, J.K., Irwin, J.A. & Comes, H.P. 2000. Hybrid origin of the Oxford Ragwort, Senecio squalidus L. Watsonia 23: 123 - 138.

Aplin, D. & Heywood, V. 2008. Do Seed Lists have a future? Taxon 57(3): 1-3.

Blossey, B. & Notzold, R. 1995. Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J. Ecol. 83: 887-889.

Braithwaite, M. 1991. New Zealand Bittercress, Cardamine uniflora. B.S.B.I. News 58: 38-39.

Ellstrand, N.C. & Schierenbeck, K.A. 2000. Hybridization as a stimulus for the evolution of invasiveness in plants? Proc. Natl. Acad. Sci. U.S.A. 97(13): 7043-7050.

Enßlin, A., Sandnera, T.M. & Matthiesa, D. 2011. Consequences of ex situ cultivation of plants: Genetic diversity, fitness and adaptation of the monocarpic Cynoglossum officinale L. in botanic gardens. Biol. Conserv. 144(1): 272-278.

Facon, B., Genton, B.J., Shykoff, J., Jarne, P., Estoup, A. & David, P. 2006. A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol. Evol. 21(3): 130-5.

Grant, M.L. 2003. A new, purple-leaved form of Poa annua L. (Poaceae) is a cryptic weed. Watsonia 24: 525–526.

Groom, Q.J. 2011. Gall causing organisms in the National Botanic Garden of Belgium. Scripta Botanica Belgica 47: in press.

Gaskin, J.F., Wheeler, G.S., Purcell, M.F. & Taylor, G.S. 2009. Molecular evidence of hybridization in Florida’s sheoak (Casuarina spp.) invasion. Mol. Ecol. 18(15): 3216–3226.

Hoste, I., van Moorsel, R. & Barendse, R. 2008. Een nieuwkomer in sierteeltbedrijven en tuinen: Cardamine corymbosa in Nederland en België. Dumortiera 93: 15-24.

Hulme, P.E. 2011. Addressing the threat to biodiversity from botanic gardens. Trends Ecol. Evol. 26: 168-174.

Keane, R.M. & Crawley, M.J. 2002. Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol. 7: 164–170.

Kent, D.H. 1956. Senecio squalidus L. in the British Isles. 1. Early records (to 1877). Proc. Bot. Soc. Br. Isl. 2: 115–118.

Kent, D.H. 1960. Senecio squalidus L. in the British Isles. 2. The spread from Oxford (1879–1939). Proc. Bot. Soc. Br. Isl. 3: 375–379.

Lozon, J.D. & MacIsaac, H.J. 1997. Biological invasions: are they dependent on disturbance? Environ. Rev. 5: 131–144.

Marco, A., Lavergne, S., Dutoit, T. & Bertaudiere-Montes, V. 2009. From the backyard to the backcountry: how ecological and biological traits explain the escape of garden plants into Mediterranean old fields. Biol. Invasions 12(4): 761-779.

Ronse, A. 2011. ‘Botanical garden escapes’ in the National Botanic Garden of Belgium. Scripta Botanica Belgica 47 in press.

Sax, D.F. & Brown, J.H. 2000. The Paradox of Invasion. Global Ecology & Biogeography 9: 363-372.

Simberloff, D. 2009. The role of propagule pressure in biological invasions. Ann. Rev. Ecol. Evol. Syst. 40(1):  81-102.

Thompson, J.D. 1991. The biology of an invasive plant: what makes Spartina anglica so successful? Bioscience 41: 393–401.

Tiébré, M-S., Vanderhoeven, S.,  Saad, L.  & Mahy, G. 2011. Hybridization and sexual reproduction in the invasive alien Fallopia (Polygonaceae) complex in Belgium. Ann. Bot. 99: 193-203.


Quentin J. Groom, Anne Ronse and Ivan Hoste
National Botanic Garden of Belgium,
 Domein van Bouchout, Nieuwelaan 38,
 1860, Meise, Belgium

 
Botanic gardens and alien invasive species
BGjournal Vol 8(2), July 2012. Download the complete issue as a pdf document here