Effects of leaf litter on establishment, growth and survival of invasive plant seedlings in a deciduous forest.
Habitat disturbance is often invoked as a causal reason for the invasion of an exotic plant species (Hobbs and Huenneke, 1992). Generally the focus is on large disturbances that cover many tens of square meters, or even hectares, e.g., grazing, fires and human disturbance (Parker et al., 1993; Gentle and Duggin, 1997; Stohlgren et al., 1999) that enhance light and release nutrients to the soil that can decrease competitive interactions between plant species (Davis et al., 2000). Smaller disturbances are more frequent, however (White, 1979); in forests these include single tree falls and leaf litter movement due to animal foraging (Theimer and Gehring, 1999). Small disturbances to leaf litter open bare patches of soil and allow increased light to reach the forest floor. The small openings in the leaf litter may provide an opportunity for invasive species to become established in a new habitat or facilitate the spread of a previously established population (Meekins and McCarthy, 2001). Furthermore, the greater litter depth of old growth forests compared to second growth stands (Bray and Gorham, 1964) may be one explanation for the lower invasibility of those forests (Brothers and Spingarn, 1992).
A meta-analysis of the effects of leaf litter on plant life history stages found that germination was the stage most negatively affected by the presence of leaf litter, although leaf litter had a generally negative effect on all life history stages (Xiong and Nilsson, 1999). Litter can act to reduce establishment through several mechanisms: shading, mechanical impedance, reduced thermal amplitude in the soil and biochemical effects (Facelli and Pickett, 1991). Few studies have investigated the effect of leaf litter on forest invasions. Increased leaf litter reduced the emergence of the invasive Celastrus orbiculatus (Oriental bittersweet) and shifted the allocation of seedling growth to longer hypocotyls and smaller radicles and cotyledons (Ellsworth et al., 2004). In wetlands invaded by Lythrum salicaria (purple loosestrife) small disturbances that reduced leaf litter reduced the ability of the native Typha spp. to compete against the invader (Hager, 2004). The effect of leaf litter is not always negative; McAlpine and Drake (2002) found that leaf litter in tree fall gaps in New Zealand enhanced the growth of one invasive species (Berberis darwinii) and did not inhibit the growth of another (Cytisus scoparius).
We investigated the role of litter disturbance in the invasion of two non-native species prevalent in forests and successional habitats in eastern U.S. and adjacent Canada, Lonicera maackii (Rupr.) Herder (Caprifoliaceae) (Amur honeysuckle) and Alliaria petiolata (M. Bieb.) Cavara and Grande (garlic mustard). The shrub L. maackii is native to northeastern Asia and was introduced into the United States in 1898 as an ornamental plant (Luken and Thieret, 1996). It has since naturalized and become abundant from forest interiors to open disturbed sites (Luken and Thieret, 1996). Its red fruits ripen in the fall and are consumed throughout the winter by several species of birds, some of which disperse the seeds (Bartuszevige and Gorchov, 2006). The seeds of this species do not have dormancy and therefore do not form a seed bank (Hidayati et al., 2000). Lonicera maackii negatively affects growth, fecundity and cover of forest annuals, perennials and tree seedlings (Gould and Gorchov, 2000; Collier et al., 2002; Gorchov and Trisel, 2003; Miller and Gorchov, 2004).
Alliaria petiolata is a fast-growing biennial herb that was introduced to North America from Europe in 1868 (Nuzzo, 1993). Seeds are dispersed in the fall by water (Byers, 1988) or by "hitchhiking" on the feet of mammals (Cavers et al., 1979). Alliaria petiolata forms a persistent seed bank, and seeds are known to be viable in the soil for up to five years (Baskin and Baskin, 1992). Alliaria petiolata has negative effects on forest annuals and tree seedlings (McCarthy, 1997), including Quercus prinus (Meekins and McCarthy, 1999), as well as graminoids and spring perennial forbs (Carlson and Gorchov, 2004).
Leaf litter depth may play a key role in the invasion of both Lonicera maackii and Alliaria petiolata. Hutchinson and Vankat (1997) found L. maackii density correlated negatively with basal area across stands in southwest Ohio, and inferred that greater shade inhibited invasion; however, deeper leaf litter could alternatively or additionally account for the lower invasibility of stands with greater basal area. Hutchinson and Vankat (1997) mention anecdotal evidence that suggests L. maackii invasion is associated with disturbances to the forest floor that decrease leaf litter and the herbaceous layer. Nuzzo (1993) found A. petiolata invasion to be linked to disturbance, with plants commonly invading habitats such as riverbanks, floodplains, trailsides, roadways, forest edges and urban areas. Anderson et al. (1996) proposed that micro-site disturbance facilitates A. petiolata establishment by providing small sites with reduced competition and Nuzzo (1999) found that A. petiolata cover declined in the absence of disturbance. However, experimental removal of leaf litter did not increase A. petiolata germination, growth, or reproduction (Meekins and McCarthy, 2001).
To investigate the effects of small-scale disturbance of leaf litter on these two invasive plant species, we tested whether Lonicera maackii seedlings occur in sites with reduced leaf litter and experimentally removed litter from plots in a second-growth forest. To further test whether greater litter depth is responsible for the low invasibility of old-growth forest, we included a treatment where litter depth was doubled. We predicted that L. maackii and Alliaria petiolata seedling establishment and survival, and L. maackii growth, would be enhanced by leaf litter removal and reduced by leaf litter addition.
DISTRIBUTION OF LONICERA MAACKII AS A FUNCTION OF LITTER
We tested whether Lonicera maackii seedlings were associated with sites of reduced leaf litter in Gregg's Woodlot in Butler County, southwest Ohio (39[degrees]28'30'N, 84[degrees]43'40'W). The canopy was dominated by Carya ovata, Fraxinus spp. and Quercus rubra. A complete description of the site is available in Gould and Gorchov (2000). We sampled leaf litter in May 2003 every 3 m along a 125 m transect by inserting a 5 cm diam circular pipe into the ground, cutting away all leaf litter outside the pipe, and collecting the litter within the pipe. At the same points, we located the nearest (within 1.5 m of transect line) L. maackii seedling [less than or equal to] 6 cm in height and took another litter sample from directly around each seedling.
The seedling was discarded. The 6 cm height threshold helped ensure that the sampled L. maackii was, in fact, a seedling. Litter samples were dried for 48 h at 100 C and massed. A Wilcoxon 2-sample test was used to test if there were significant differences between transect points and seedling points.
LEAF LITTER MANIPULATION EXPERIMENT
This experiment was carried out in a second growth forest at the Miami University Ecology Research Center (39[degrees]30'N, 84[degrees]44'W) in Butler County, southwest Ohio. Density of trees >10 cm dbh was 491/ha. The canopy was dominated by Acer saccharum and Fraxinus americana and the understory by A. saccharum. We cleared Lonicera maackii shrubs in a flat, 20 x 16 m area with uniform canopy cover in Sept. 2003 before fruits ripened and fell. We then established 75 circular plots 0.25 m radius (0.196 [m.sup.2]) in a grid centered within this area with 1 m spacing between plots. Each plot was encircled by plastic bird fencing (mesh size = 2.54 cm to prevent litter movement) attached to bamboo poles and secured to the ground using landscape staples.
In Nov. 2003, after all tree leaves had fallen, plots were randomly assigned to three experimental treatments: litter removed (all leaf litter within the plot removed), control (no manipulation) and litter added (litter from a removal plot added). Mass of litter averaged 26.29 -+ 2.02 (mean [+ or -] SE) g dry weight (range 21.4-34.3 g), based on additional control plots not used in the experiment, so litter added plots would average twice this mass. After litter manipulation, 50 Lonicera maackii seeds that had been removed from the fruit pulp by hand were added to each experimental plot to mimic natural seed dispersal by birds. Most L. maackii seed dispersal in southwest Ohio occurs during the winter months, after leaves have fallen from the trees (Bartuszevige et al., 2006). Alliaria petiolata was not sown, as this herb was common in this stand, and therefore its seeds were present in the soil. While seed density may vary spatially, by randomly assigning plots to treatments we prevented this variation from biasing seedling emergence.
Plots were monitored every 14 d Mar.-Jun. 2004 for establishment and survival of Lonicera maackii and Alliaria petiolata seedlings. Individual seedlings were marked with colored toothpicks or paper clips. We counted the number of leaves on each L. maackii seedling over the same time period to measure growth. We defined establishment as the time when the first set of true leaves was fully expanded. This stage has been called 'germination' in some other studies (e.g., Xiong and Nilsson, 1999).
We tested treatment effects on the number of Lonicera maackii and Alliaria petiolata seedlings established per plot with Kruskal-Wallis tests. We selected the mid-May census date because the number of seedlings of both species peaked on this date. The proportion of seedlings surviving of each species was calculated by dividing the number of plants alive at the end of Jun. by the mid-May count. Late Jun. was selected because after this date we could not distinguish seedlings that died from survivors that abscised leaves during the late summer. Treatment effects on this proportional survival measure were determined by Kruskal-Wallis tests. To analyze L. maackii size we calculated, for each plot, the mean number of leaves on seedlings alive in late Jun., and compared treatments with a Kruskal-Wallis test. For each test resulting in a significant treatment effect, we compared each pair of treatments with a Kruskal-Wallis test with alpha values corrected for multiple comparisons (alpha = 0.05/3 = 0.017).
RESULTS AND DISCUSSION
Significantly less litter mass was present around Lonicera maackii seedlings (mean [+ or -] SE = 4 [+ or -] 1 g/[m.sup.2]) than transect points (8 _+ 1 g/[m.sup.]2, t = 2.743, df = 73, P = 0.004).
We found significantly more Lonicera maackii seedlings established in the control and litter removed treatments than the litter added treatment ([X.sup.2] = 17.68, df = 1, P < 0.0001; [X.sup.2] = 33.71, df = 1, P < 0.0001, respectively, Table 1) and significantly more Alliaria petiolata seedlings established in the litter removed treatment than in either the control or litter added treatments ([X.sup.2] = 9.32, df = 1, P = 0.0023; [X.sup.2] = 16.2, df = 1, P < 0.0001, respectively, Table 1). While we do not know the mechanism by which greater litter reduced seedling establishment, possible causes are lower light levels, physical blockage of growth, change in soil pH or leaching of phytotoxins, all of which are associated with litter (Facelli and Pickett, 1991). Additionally, our placement of L. maackii seeds on the top of the leaf litter may have reduced the number of seeds in contact with soil in the spring. We added L. maackii seeds in this manner to mimic natural seed dispersal by birds which occurs during the winter months; seeds subsequently move passively through the litter with precipitation. Not all studies of the effects of leaf litter on germination take into account the timing of dispersal in their experimental design; frequently seeds are planted, in the field or in the greenhouse, beneath leaf litter (Xiong and Nilsson, 1999; McAlpine and Drake, 2002; Ellsworth et al., 2004). If seeds are unable to reach the soil surface they may be unable to germinate because they lack the proper cues from the soil, or may germinate but die rapidly because the young roots are unable to reach the soil, take root and begin collecting nutrients. We did not inspect for seeds imbedded in the litter as we wished to minimize disturbance to the leaf litter. Peterson and Facelli (1992) tested the effect of leaf litter from deciduous trees on germination of Rhus typhina seeds and found that seeds placed on top of the leaf litter did not germinate.
Even within a forest patch, litter depth may vary due to movement by wind and water (Orndorff and Lang, 1981) and litter is generally deeper in the interior than near edges (Shure and Phillips, 1987). Bartuszevige and Gorchov (2006) found that Lonicera maackii seeds were dispersed preferentially to the edge of woodlots by American Robins. The combination of dispersal to the edge and lower amounts of leaf litter may facilitate invasion of the edges of woodlots. Although we found lower seedling establishment in plots with greater leaf litter, leaf litter itself was unable to prevent germination of these two highly invasive species in southwest Ohio. Meekins and McCarthy (2001) found that Alliaria petiolata rosettes were generally larger and had greater survival and reproduction in lowland areas and in forest edge plots, both of which had less litter than the upland area, although they did not find a significant effect of litter removal on A. petiolata demography.
Contrary to what we predicted however, we found that leaf litter had no effect on Lonicera maackii seedling survival ([X.sup.2] = 1.02, df = 2, P = 0.60) or growth ([X.sup.2] = 0.53, df = 2, P = 0.77). Litter removal actually decreased survival of Alliaria petiolata compared to the control treatment ([X.sup.2] = 6.76, df = 1, P = 0.009) (Table 1). Others have found a significant effect of leaf litter on hypocotyls elongation; hypocotyls are longer in seedlings beneath greater amounts of leaf litter (Peterson and Facelli, 1992; Ellsworth et al., 2004). Although hypocotyl length was not measured in our study, we observed longer hypocotyls in litter added treatment plots than in no litter or control plots, suggesting seedlings allocated more to vertical growth or cell elongation and less to photosynthetic tissues (Peterson and Facelli, 1992).
The greater survivorship of Alliaria petiolata seedlings in the control than in the litter removed treatment was opposite of what we had predicted. This may have been due to the mulching effect of leaf litter. According to Facelli and Pickett (1991) leaf litter maintains soil moisture, moderates soil temperature, provides nutrients during litter decomposition and reduces competition from other plants; these may enhance seedling survival after establishment. The lower survival of A. petiolata seedlings in the absence of litter was modest, however, and did not overcome the positive effect of litter removal on establishment. By the end of Jun., the number of seedlings was still greatest in litter removal plots (n = 63), intermediate (n = 18) in control and least (n = 5) in litter addition plots.
This reduced number of Alliaria petiolata seedlings, as well as the reduced Lonicera maackii establishment, in the litter added treatment compared to the control suggest that litter depth may explain the lower incidence of invasion of old-growth, as compared to second-growth forests (Brothers and Spingarn, 1992), as the former typically, though not always, have greater litter depth (Bray and Gorham, 1964). However, old-growth forests also differ from second-growth forest in other ways e.g., increased competition for nutrients, less available light and greater species or functional group diversity. Change in any one of these factors may facilitate invasion by exotic species. For example, McAlpine and Drake (2002) found that increased light availability from tree fall gaps enhanced germination in one species. Even in old-growth forests, small disturbances to the leaf litter due to mammal activity or abiotic forces can open small patches of bare ground that are colonized by exotic plants. Finally, invasive species are often found at the edges of woodlots and in riparian areas both of which are highly disturbed and have low amounts of leaf litter (Shure and Phillips, 1987). The low level of leaf litter in these habitats may be important in facilitating exotic plant invasion.
Acknowledgments.--We thank the Miami University Ecology Research Center for use of facilities and Dr. Thomas Gregg for use of his woodlot. This manuscript was greatly improved by the comments of two anonymous reviewers. This work was funded by U.S. Department of Agriculture National Research Initiatives, Biology of Invasive and Weedy Plants Program (to DLG #CG00717) and Miami University's Doctoral and Undergraduate Opportunities for Scholarship and Undergraduate Summer Scholars Programs.
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ANNE M. BARTUSZEVIGE, (1) RIKKI L. HRENKO (2) AND DAVID L. GORCHOV, Department of Botany, Miami University, Oxford, Ohio 45056. Submitted 16 September 2005; accepted 21 February 2007.
(1) Corresponding author present address: Eastern Oregon Agricultural Research Center--Union Experiment Station, Oregon State University, P.O. Box E, Union 97883. Telephone: (541)562-5129; FAX (541)562-5348; e-mail: firstname.lastname@example.org
(2) Present address: Eesti Energia AS, Tallinn, Estonia
TABLE 1.--Mean (+ SE) number of Lonicera maackii and Alliaria petiolata seedlings established per 0.25 m radius plot, survival of these seedlings (proportion alive at the end of Jun.) and average number of leaves per L. maackii seedling at this date, for each litter treatment. Means within columns with different letters are significantly different (alpha = 0.05; corrected for multiple comparisons) Lonicera maackii # Seedlings Survival Litter removed 5.7 [+ or -] 0.8 (a) 0.50 [+ or -] 0.06 (a) Control 3.3 [+ or -] 0.7 (a) 0.40 [+ or -] 0.l0 (a) Litter added 1.0 [+ or -] 0.5 (b) 0.50 [+ or -] 0.16 (a) Lonicera maackii # Leaves Litter removed 3.7 [+ or -] 0.13 Control 3.5 [+ or -] 0.17 Litter added 3.6 [+ or -] 0.75 Alliaria petiolata # Seedlings Survival Litter removed 4.2 [+ or -] 1.0 (b) 0.60 [+ or -] 0.09 (a) Control 0.9 [+ or -] 0.3 (a) 0.82 [+ or -] 0.12 (b) Litter added 0.4 [+ or -] 0.1 (a) 0.56 [+ or -] 0.20 (a,b)
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|Title Annotation:||Notes and Discussion|
|Author:||Bartuszevige, Anne M.; Gorchov, Rikki L.; Hrenko David L.|
|Publication:||The American Midland Naturalist|
|Date:||Oct 1, 2007|
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