Short note
Dispersal of the non-native invasive species Crassula helmsii (Crassulaceae) may involve seeds and endozoochorous transport by birds L. Denys*, J. Packet, W. Jambon, K. Scheers Research Institute for Nature and Forest, Brussels, Belgium Reproductive abilities are essential to assess pathways of introduction, modes of dispersal, and possibilities for effective on-site remediation of invasive species, as well as to identify areas at risk and develop adequate biosafety protocols. Crassula helmsii (Kirk) Cockayne, an amphibious plant from New Zealand and Australia, was introduced in Great Britain in the early 1900s (Swale & Belcher, 1982) and now occurs throughout most of the British Isles. It was not recorded in continental Atlantic Europe until the 1980s (Margot, 1983) and it is still spreading rapidly there, especially in the Low Countries. Due to its proliferous growth and ensuing negative consequences (Robert et al., 2013), control of this highly invasive species is drawing considerable attention; efforts have so far met with little success. Dispersal of C. helmsii in Europe is believed to depend exclusively on the distribution of vegetative propagules (stem fragments or turion-like apical parts) by water, man, or animals. Overwintering also occurs in a vegetative state. As with many aquatic plants, minute fragments with a single node allow regrowth. Vaughan (1978) mentioned that the species ‘seems to set good fruit’ in Britain, but Dawson & Warman (1987) considered it likely that seeds from British plants are unviable, reporting that some were retrieved from soil samples but that these did not germinate. Germination experiments with UK material at CEH Dorset were unsuccessful (Brunet, 2002), whilst Delbart (2011) recovered only aborted seeds from three populations in southern Belgium. Recent reviews reiterate dependence on vegetative parts for dispersal, overwintering, and regrowth after management, noting uncertainty about seed viability in Europe (e.g. EPPO, 2007; Lansdown, 2012; Minchin, 2008; Willby, 2008) and current management strategies are entirely based on this presumption (Delbart et al., 2011). The rapid regrowth after sod-cutting at sites in Flanders, Belgium, where care was taken to *Corresponding author:
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remove even the smallest fragments, and observations of water birds grazing on stands of Crassula, led us to (re)consider (1) reproduction by means of seeds, and (2) the possibility of endozoochorous transport of vegetative propagules. Dense tufts of flowering C. helmsii were collected from the coastal dune nature reserve at D’Heye, Bredene, Belgium (51u149540N, 2u599190E) in October 2013. Plants were put into plastic bags and transferred to dark storage at 4uC for eight weeks, after which, wilted flowers with seemingly well-developed brown fruits (follicles) were removed by cutting the pedicel just below their base. Dissection of one hundred follicles yielded 30 mature seeds with a maximum of two per follicle. According to the literature, a single flower may produce two to five seeds, each c.500 mm long (EPPO, 2007). The elliptical seeds in our case were slightly smaller, 385–425 mm, and presented a characteristic rugulate surface texture (Fig. 1). 300 flowers were sown in a shallow tray with fine sand and covered with 2–3 mm of sand. Another 1000 were distributed in a similar tray but mixed with the substrate to a depth of 3–4 cm. The trays were placed in a growing chamber with 14 hours of fluorescent illumination at 18uC and 10 hours of darkness at 12uC. The substrate was kept moist by allowing demineralised water to be soaked up from below. The first seedling appeared on the twenty-fifth day in both trays. Emergence ceased completely after 43 days. Overall, 21 plants developed, 86% emerging within 32 days after sowing. The germination percentage was approximately ten times higher (18%) when seeds were at or very close to the surface than when distributed to a depth of a few centimetres; germination was epigeal. Given the small size of seeds and abundant flowering from early summer up to late autumn, we conclude that reproduction from seeds should not be dismissed as a means for site colonisation by C. helmsii or in its reestablishment after control in continental
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Figure 1 Scanning electron micrographs of Crassula helmsii seeds collected from plants growing at Bredene, Belgium: (a) entire seed; (b) characteristic rugulate surface texture.
Europe. Conditions influencing germination and seed longevity remain to be examined further. In its native range, Nicol & Ward (2010) observed germination from sampled aquatic seed banks after 16 weeks in outdoor submerged conditions but only in fresh water (,1000 mS cm21). This period appears considerably longer than the four to five weeks we observed, but the authors noted that germinants may have remained undetected for some time due to their small size. Some data suggest that the species may be an obligate seeder in dry conditions (Penman et al., 2008). Even though the possibility of ectozoochorous transport of fragments by wading birds (Dawson & Warman, 1987) or other animals, e.g. wild boar, remains to be proven (EPPO, 2007), it is a likely explanation for the establishment of Crassula at more remote or isolated sites that are closed to the public and accessible only with considerable difficulty. We examined whether herbivory by water birds provides an opportunity for endozoochorous dispersal. After being kept without food for two days, four barnacle geese (Branta leucopsis Bechstein, 1803), four Egyptian geese (Alopochen aegyptiaca Linnaeus, 1766), and four Canada geese (Branta canadensis Linnaeus, 1758) were placed in separate cages and offered a dense sod of 1 m2 of non-flowering Crassula to eat. After 24 hours, the birds were checked closely for any adhering fragments (none was found) and transferred to individual cages with a meshed floor. Droppings, some of which contained macroscopic plant remains, were collected after one hour and placed in their entirety on a surface of wet fine sand in trays. The trays were placed in a growing chamber in similar conditions as described above. After 47 days, a single Crassula plant grew from one of the barnacle goose droppings. Its initial leaves were morphologically
similar to those of mature plants and not to the cotyledons of germinants; hence, we consider it more likely that it developed from a fragment than from an ingested seed. The experiment was repeated, but with the droppings dispersed more evenly over the surface. Even after five months, they yielded no plants. These observations suggest that, albeit occasionally, ingested parts of Crassula can survive transit through the digestive tract of larger water birds, allowing regrowth from defecated material. Although endozoochorous dispersal by water fowl is common for fruits and seeds and can outweigh external transport (Brochet et al., 2010), it is probably infrequent for vegetative parts lacking the protection offered by a seed coat. In the case of C. helmsii, the thick cuticle typical of Crassulaceae and the ability to regenerate from a single node are likely to be instrumental. Notably, potential endozoochory by water birds was also demonstrated for a variety of small invertebrates (e.g. van Leeuwen et al., 2012). In addition, however, the possibility of seed transport by birds should not be dismissed either. Distances that may be covered by endozoochorous transport will depend on propagule viability in relation to bird species, their diet, and regional behaviour (e.g. Green et al., 2002). Nevertheless, it appears possible that especially heavily infested sites visited by large numbers of herbivorous birds could serve as hubs for the spread of C. helmsii.
Acknowledgements This work was carried out within the EU co-funded Interreg 2Seas project RINSE (Reducing the Impact of Non-Native Species in Europe; http://www.rinse-europe.eu), which seeks to improve awareness of the threats posed by INNS, and the methods to address them. The Agency of Nature and Forest (ANB)
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authorized INBO and RATO to work with Canada geese in exemption of game regulations. We thank F. Hugh Dawson and Jonathan Newman for information on their work with Crassula at CEH. Koen Deforce (Flanders Heritage Agency) is thanked for help with electron microscopy. Wim Pauwels and Hans Vansteenbrugge (ANB) enabled us to harvest Crassula in D’Heye. Karel Van Moer and Johan Vanhooren (RATO) provided facilities, assistance, and animals for the feeding experiment. Tim Adriaens is acknowledged for support and Lon Lommaert (INBO) for arousing our suspicion.
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