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(American Journal of Botany. 2004;91:285-288.)
© 2004 Botanical Society of America, Inc.

Brief Communications

Allelopathic inhibition of germination by Alliaria petiolata (Brassicaceae)1

Daniel Prati2,4 and Oliver Bossdorf2,3

2UFZ-Centre for Environmental Research Leipzig-Halle, Ltd., Department of Community Ecology, Theodor-Lieser-Strasse 4, D-06120 Halle (Saale), Germany; 3Institut für Umweltwissenschaften, Universität Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland

Received for publication April 25, 2003. Accepted for publication September 12, 2003.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Garlic mustard (Alliaria petiolata, Brassicaceae) is an invasive, nonindigenous species currently invading the understory of North American woodlands where it is a serious threat to the native flora. Part of this success might be due to allelopathic interference by garlic mustard. Two congeneric species, the European Geum urbanum and the North American Geum laciniatum, were tested for allelopathic inhibition of germination by garlic mustard. Seeds were germinated either on substrate contaminated by garlic mustard or on substrate with contamination neutralized by activated carbon. Allelopathic effects of native European and invasive North American garlic mustard populations were also compared. Activated carbon increased germination by 14%, indicating that garlic mustard contaminated the substrate through root exudates. Activated carbon in turn counteracted this effect. The two test species differed in their sensitivity to allelopathic interference. North American G. laciniatum had a much stronger increase in germination when activated carbon was added to the substrate, independent of the origin of garlic mustard. In contrast, the European G. urbanum germinated better in substrate precultivated with North American garlic mustard, whereas activated carbon increased its germination only in substrate precultivated with European garlic mustard.

Key Words: allelopathy • biological invasion • competition • garlic mustard • Geum laciniatum • Geum urbanum


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Allelopathic interference between plant species has often been invoked to explain why some invasive, nonindigenous plants have become extremely dominant, out-compete native species, or even produce monospecific stands (Wardle et al., 1993 ; Dolling et al., 1994 ; Ridenour and Callaway, 2001 ). However, empirical evidence that allelopathic interference plays an important role in plant invasions is still ambiguous. Controlled bioassays to test putative allelochemicals often failed to show allelopathic effects (Choesin and Boerner, 1991 ; Dietz et al., 1996 ; Keay et al., 2000 ; Conway et al., 2002 ) and are generally criticized for their artificial nature (Harper, 1977 , p. 369; Williamson, 1990 ). On the other hand, a number of experiments revealed large differences in the outcome of competition when allelopathic interference was reduced by adding activated carbon to the substrate (Nilsson, 1994 ; Callaway and Aschehoug, 2000 ; Ridenour and Callaway, 2001 ; Siemens et al., 2002 ). Wardle et al. (1998) have argued that allelochemicals may alter plant competition also indirectly through changes in ecosystem properties. For instance, the presence of decomposing leaves of the invasive plant Carduus nutans decreased nitrogen fixation in legume species through a reduction in nodulation.

Allelopathic interference must be species-specific to explain why nonindigenous species dominate an invaded community while they normally do not reach high dominance in their native community. It is possible that co-occurring species adapt to allelochemicals released by competitors; hence, it might be difficult to find pronounced effects in established communities (Harper, 1977 ). Invasive species, however, do not share a coevolutionary history with the community they invade, and one might therefore expect greater allelopathic effects in such systems. However, only a few studies compared the allelopathic effects of an invasive species on competitors from the native and the invaded range. Callaway and Aschehoug (2000) found that the outcome of competition between the invasive Centaurea diffusa and grass species from the new and the old range depended on whether or not activated carbon reduced allelopathic interference among them. To our knowledge, no one has ever tested the possibility that the degree of allelopathy of an invader may change as a result of encountering new competitors.

Garlic mustard [Alliaria petiolata (Bieb.) Cavara & Grande (Brassicaceae)] is a biennial (and sometimes perennial) species native to Europe that was introduced to North America in the middle of the 19th century. In the last few decades it started to expand rapidly its range and has invaded the understory of mesic forests in the northern United States and in southern Canada (Nuzzo, 1999 ). Garlic mustard reduces the abundance of native species and decreases diversity in its new range in North America because of its high competitive ability (McCarthy, 1997 ; Meekins and McCarthy, 1999 ; B. Blossey, Cornell University, personal communication). In addition, a number of putative allelopathic chemicals have been isolated (glucosinolates and their degradation products) that could be responsible for the success of garlic mustard (Vaughn and Berhow, 1999 ; but see also McCarthy and Hanson, 1998 ).

Here, we tested for allelopathic inhibition of germination through the presence of garlic mustard in two congeneric competitor species. Geum urbanum is a native European species that often co-occurs with garlic mustard, whereas Geum laciniatum is a member of the invaded North American communities (McCarthy, 1997 ). In addition to comparing an old with a new competitor, we used plants from native European and invasive North American garlic mustard populations and asked whether their allelopathic potential differed depending on the origin of the plants. In contrast to the laboratory bioassays often used to test for allelopathic effects, our approach was to grow garlic mustard in flower pots and let the species contaminate the substrate with root exudates. Seed germination was then tested in the contaminated substrate and compared with a control where activated carbon was added to neutralize contamination.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Study species
Seeds of garlic mustard were collected from natural populations in North America and Europe. For a better geographic representation, we sampled seeds from three different locations on each continent (Halle, [Germany, 51°28' N, 11°58' E], Copenhagen [Denmark, 55°43' N, 12°34' E], and Soyhières [Switzerland, 47°24' N, 07°22' E] in Europe; Athens [Ohio, 39°19' N, 82°07' W], Ipswich [Massachusetts, 42°41' N, 70°51' W], and Milwaukee [Wisconsin, 43°05' N, 87°53' W] in North America), but no attempt was made to test for population differences. Geum urbanum L. and G. laciniatum Murr. (Rosaceae) are both perennial woodland herbs that co-occur with garlic mustard either in its native and/or invasive range, respectively. Seeds of G. urbanum and G. laciniatum were bought from commercial seed suppliers (Rieger-Hofmann GmbH, Blaufelden-Roldshausen, Germany, and Ernst Conservation Seeds, Meadville, Pennsylvania, USA).

Garlic mustard cultivation
Seeds of garlic mustard were dark-stratified for 3 mo at 5°C. Transplanted seedlings were cultivated in small pots of 125 cm3 for 4 wk. Then 28 seedlings of European and 28 of North American origin were planted into pots containing 0.5 L of a 1 : 1 mixture of sand and compost substrate. To half of the pots, finely ground activated carbon was added at a concentration of 20 mL/L substrate. Activated carbon is often used to reduce interference by allelopathic chemicals in the soil because it has a high affinity to organic compounds and a weak affinity to inorganic nutrients (Callaway and Aschehoug, 2000 ; Ridenour and Callaway, 2001 ). Activated carbon did not have any direct effect on the growth (+6% aboveground biomass, F1,52 = 0.767, P > 0.3) and reproduction (+16% number of pods, F1,52 = 0.774, P > 0.3) of garlic mustard.

From spring 2001 to early summer 2002, the plants were grown in a greenhouse with a 25°/15°C day/night cycle and additional light provided by 500-W lamps. During winter, the plants were vernalized in an unheated greenhouse or in a climate chamber at 5°C when the greenhouse was too cold. Plants were harvested after seed set, and the substrate was carefully separated from the roots.

The germination experiment
Ten petri dishes were filled with the substrate from each flower pot totalling 560 dishes. In half of these, we placed 10 seeds of Geum urbanum, and in the other half of the petri dishes, we placed 10 seeds of G. laciniatum. To test for a direct effect of activated carbon on the germination of either species, 10 control petri dishes were filled with the same 1 : 1 mixture of sand and compost substrate but without precultivation with garlic mustard. Activated carbon was added at the same concentration to half of these dishes. The petri dishes were kept in a refrigerator for 1 wk and transferred to a climate chamber at 15°C with 14 h light. The number of germinated seeds was recorded weekly for 8 wk.

Statistical analysis
The total number of seedlings that germinated after 8 wk was analyzed using a split-plot analysis of deviance with activated carbon and origin of garlic mustard (Europe vs. North America) as plot level treatment and with species (G. urbanum vs. G. laciniatum) and its interactions as within-plot treatment. As seed germination follows a binomial distribution, a likelihood ratio test was used with logit-link function to calculate variance ratios that are approximately F-distributed (McCullagh and Nelder, 1989 , pages 98 and following). The analyses were computed using the program GENSTAT 6 (Payne et al., 1987 ).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Germination between the two test species differed significantly, with G. laciniatum germination more than twice that of G. urbanum during the first 6 wk, and no further germination was observed thereafter (Table 1, Fig. 1). Overall, there was a marginally significant increase by about 14% in germination when activated carbon was added to the substrate, indicating that garlic mustard contaminated the substrate through root exudates and that adding activated carbon in turn counteracted this effect. The control experiment using substrate without a history of garlic mustard showed no direct effect of activated carbon on seed germination (quasi-F = 0.227; df = 1, 16; P > 0.6). Here, activated carbon even reduced germination slightly from 50% to 47%. Thus, the observed increase of germination in the main experiment cannot be a direct effect of activated carbon.


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  		Table 1. Summary of analysis of deviance of the germination success of the two species Geum urbanum and G. laciniatum. Seeds germinated on substrate previously containing garlic mustard of European or North American origin either with or without activated carbon

 


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  		Fig. 1. Germination success (%) over time of two test species, Geum urbanum and G. laciniatum, in substrate previously either contaminated by root exudates of Alliaria petiolata (broken lines) or contamination neutralized with activated carbon (solid lines). Data are weekly means ± 1 SE

 
The two species differed in their reaction to activated carbon, i.e., in their response to allelochemicals. Germination of North American G. laciniatum consistently increased when activated carbon was added to the substrate (Table 1, Fig. 2). This effect was independent from the origin of garlic mustard. For the European G. urbanum, the pattern was more complex. Geum urbanum germinated better in substrate in which North American populations of garlic mustard were previously cultivated. Moreover, activated carbon slightly decreased germination in substrate precultivated by North American garlic mustard. In contrast, activated carbon increased germination when substrate was precultivated with European garlic mustard. This complex pattern for G. urbanum was indicated by a significant two-way interaction between the two test species and the origin of garlic mustard and a significant three-way interaction between species, origin, and activated carbon (Table 1). The difference in the reaction to activated carbon between G. urbanum and G. laciniatum showed that the sensitivity to the presence of allelochemicals in the substrate was species-specific.



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  		Fig. 2. Germination success (%) of two test species, Geum urbanum and G. laciniatum, on substrate previously contaminated by root exudates of garlic mustard (Alliaria petiolata) from either European (EU) or North American (US) origin and either with (hatched bars) or without (open bars) activated carbon added to the substrate. Bars represent means + 1 SE. Asterisks above the bars indicate statistically significant differences between treatments with and without activated carbon

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
This study showed that garlic mustard negatively affected the germination of co-occurring species, but the result depended intricately on the identity of test species and the origin of garlic mustard. The overall effect of allelopathy was rather small: germination increased only by 14% when activated carbon neutralized the adverse effects of either root exudates or decomposing dead roots. However, individual-based models on the role of allelopathy in invasion showed that even moderate sensitivity to allelochemicals might shift the outcome of between-species competition (Goslee et al., 2001 ). Our approach, to grow garlic mustard in flower pots and let the species contaminate the substrate by root exudates, represented a more realistic test of allelopathy than bioassays, at a cost of not being able to quantify dose–response relationships or to identify the chemicals responsible for allelopathy. Although it does not meet all criteria to prove allelopathy outlined by Williamson (1990) , the use of activated carbon could improve our ability to understand allelopathy. Vaughn and Berhow (1999) isolated several phytotoxic chemicals from garlic mustard (mainly allyl isothiocyanate and benzyl isothiocyanate), but we do not know whether these chemicals are involved in our study. Field experiments are now needed to test the effect of allelopathy under more natural conditions and to estimate its magnitude relative to resource competition or other interactions.

We found that the two species of Geum differed in their sensitivity to allelochemicals. When activated carbon was added there was a much greater increase of germination in the American G. laciniatum than in the European G. urbanum. There still was allelopathic inhibition of G. urbanum when growing in substrate precultivated with European garlic mustard, but North American garlic mustard has obviously lost its "nastiness" to a former competitor. This was the most remarkable finding of our experiment: germination of G. urbanum depended on the origin of garlic mustard populations. It is tempting to invoke local adaptation to explain this pattern. However, examination of evolutionary changes in garlic mustard during the colonization of North America was out of the scope of this paper. Our results do suggest that North American garlic mustard behaved differently than European garlic mustard, but whether this resulted from a single introduction of one particular population that then spread in North America or whether the two types of garlic mustard differ consistently must remain open. One would need to have greater information regarding the number of initial populations and the colonization history in North America, but little is available (Cavers et al., 1979 ). Alternatively, one would have to compare a much larger number of European and North American populations of garlic mustard to test the consistency of the difference. Nevertheless, our results suggest that plant material should be carefully selected when testing allelopathy in invasive species.

In conclusion, our data suggest that allelopathy may contribute to the success of garlic mustard as an invader of North American forests, but field trials are needed to examine the relative importance of allelopathy vs. other factors. The use of activated carbon to test for allelopathy is a fruitful approach as compared with laboratory bioassays. Finally, the degree of allelopathic interference is species-specific and can even vary within species. This is particularly important for invasive species that compete with different sets of species in the native and invasive ranges. Target species should be used that co-occur with the allelopathic species in nature to produce meaningful data.


   FOOTNOTES
 
1 The authors thank V. Schmidt and A. Thondorf for help during the experiment; J. Kollmann, J. F. Meekins, and H. Hinz for collecting seeds; and H. Auge, M. A. K. Lodhi, and two anonymous reviewers for comments on the manuscript. Back

4 daniel.prati;caufz.de Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Callaway R. M. E. T. Aschehoug 2000 Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290: 521-523[Abstract/Free Full Text]

Cavers P. B. M. I. Heagy R. F. Kokron 1979 The biology of Canadian weeds. 35. Alliaria petiolata (M. Bieb.) Cavara and Grande. Canadian Journal of Plant Science 59: 217-229[ISI]

Choesin D. N. R. E. J. Boerner 1991 Allyl isothiocyanate release and the allelopathic potential of Brassica napus (Brassicaceae). American Journal of Botany 78: 1083-1090[CrossRef][ISI]

Conway W. C. L. M. Smith J. F. Bergan 2002 Potential allelopathic interference by the exotic Chinese tallow tree (Sapium sebiferum). American Midland Naturalist 148: 43-53[CrossRef][ISI]

Dietz H. T. Steinlein P. Winterhalter I. Ullmann 1996 Role of allelopathy as a possible factor associated with the rising dominance of Bunias orientalis L. (Brassicaceae) in some native plant assemblages. Journal of Chemical Ecology 22: 1797-1811[CrossRef][ISI]

Dolling A. O. Zackrisson M.-C. Nilsson 1994 Seasonal variation in phytotoxicity of Bracken (Pteridium aquilinum L. Kuhn). Journal of Chemical Ecology 20: 3163-3172[CrossRef][ISI]

Goslee S. C. D. P. C. Peters K. G. Beck 2001 Modeling invasive weeds in grasslands: the role of allelopathy in Acroptilon repens invasion. Ecological Modelling 139: 31-45[CrossRef]

Harper J. L. 1977 The population biology of plants. Academic Press, London, UK

Keay J. W. E. Rogers R. Lankau E. Siemann 2000 The role of allelopathy in the invasion of the Chinese tallow tree (Sapium sabiferum). Texas Journal of Science 52: S57-S64

McCarthy B. C. 1997 Response of a forest understory community to experimental removal of an invasive nonindigenous plant (Alliaria petiolata, Brassicaceae). In J. O. Luken and J. W. Thieret [eds.], Assessment and management of plant invasions, 117–130. Springer-Verlag, New York, New York, USA

McCarthy B. C. S. L. Hanson 1998 An assessment of the allelopathic potential of the invasive weed Alliaria petiolata (Brassicacea). Castanea 63: 68-73

McCullagh P. J. A. Nelder 1989 Generalized linear models, 2nd. ed. Chapman & Hall/CRC, Boca Raton, Florida, USA

Meekins J. F. B. C. McCarthy 1999 Competitive ability of Alliaria petiolata (garlic mustard, Brassicaceae), an invasive, nonindigenous herb. International Journal of Plant Sciences 160: 743-752[CrossRef][ISI]

Nilsson M.-C. 1994 Separation of allelopathy and resource competition by the boreal dwarf shrub Empetrum hermaphroditum Hagerup. Oecologia 98: 1-7[CrossRef][ISI]

Nuzzo V. 1999 Invasion pattern of the herb garlic mustard (Alliaria petiolata) in high quality forests. Biological Invasions 1: 169-179[CrossRef]

Payne R. W. P. W. Lane A. E. Ainsley K. E. Bicknell P. G. N. Digby P. Harding K. Leech H. R. Simpson A. D. Todd P. J. Verrier R. P. White 1987 GENSTAT 5 reference manual. Clarendon Press, Oxford, UK

Ridenour W. M. R. M. Callaway 2001 The relative importance of allelopathy in interference: the effects of an invasive weed on a native bunchgrass. Oecologia 126: 444-450[CrossRef][ISI]

Siemens D. H. S. H. Gardbner T. Mitchell-Olds R. M. Callaway 2002 Cost of defense in the context of plant competition: Brassica rapa may grow and defend. Ecology 83: 505-517[ISI]

Vaughn S. F. M. A. Berhow 1999 Allelochemicals isolated from tissues of the invasive weed garlic mustard (Alliaria petiolata). Journal of Chemical Ecology 25: 2495-2504[CrossRef][ISI]

Wardle D. A. K. S. Nicholson A. Rahman 1993 Influence of plant age on the allelopathic potential of nodding thistle (Carduus nutans L.) against pasture grasses and legumes. Weed Research 33: 69-78[CrossRef][ISI]

Wardle D. A. M.-C. Nilsson C. Gallet O. Zackrisson 1998 An ecosystem-level perspective of allelopathy. Biological Reviews 73: 305-319[CrossRef]

Williamson G. B. 1990 Allelopathy, Koch's postulates, and the neck riddle. In J. B. Grace and D. Tilman [eds.], Perspectives in plant competition, 143–162. Academic Press, San Diego, California, USA




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