Leaf litter depth has only a small influence on Ranunculus ficaria (Ranunculaceae) biomass and reproduction.
Invasive plant species are important economic and environmental pests, posing threats to endangered species, altering native habitats, decreasing biodiversity, and facilitating the establishment of other invasive species (Pimentel et al., 2005). Several mechanisms have been proposed to explain invasive plants' success, including an increased vigor and seed production in the invaded habitat that gives a competitive advantage over native species (Blossey and Notzold, 1995; Wolfe, 2002). Other invasive species have unique allelopathic properties that inhibit growth of native species (Callaway and Ridenour, 2004). In many cases anthropogenic disturbance plays a driving role in the establishment of invasive plant species (Lozon and MacIsaac, 1997; Schooler et al., 2010). Anthropogenic disturbance can facilitate invasion directly by eliminating less tolerant species or indirectly by altering resources or habitat traits (Price et al., 2011).
Urbanization and the associated altered hydrology in urban riparian drainages is a major cause of disturbance to natural habitats. Sheet erosion and poor water quality associated with catchment urbanization can greatly reduce populations of native species along riparian areas either by directly washing away plants or by altering the habitat (Walsh et al., 2005). The change in hydrology can also facilitate the establishment of tolerant invasive species which may further alter the riparian habitat (Stromberg et al., 2007).
One aspect of habitat alteration associated with urban stream flooding is the redistribution of leaf litter in the riparian corridor and the expanded flood plain. Flooding in riparian areas creates some areas of very deep leaf litter deposition and other areas with no leaf litter (Nilsson et al., 1999). This affects local community structure because deep leaf litter and flotsam drifts suppress the growth of riparian plant species not adapted to this disturbance, whereas species that are sensitive to cold temperatures or desiccation are inhibited in areas free of leaf litter (Facelli and Pickett, 1991; Xiong et al., 2003; Sayer, 2006). Invasive species that can tolerate different leaf litter depths may have a competitive advantage in these habitats over native species not adapted to varying leaf litter depths (Baker and Murray, 2010).
Ranunculus ficaria is an invasive species in riparian areas of temperate deciduous forests in the northeastern United States. It can be especially dense in urban riparian habitats, and is weakly allelopathic to some species (Cipollini and Schradin, 2011). A perennial species native to Europe and western Asia, it was first reported in the United States in 1867 and was probably introduced as an ornamental (Axtell et al., 2010). Ranunculus ficaria is now present in low-lying wet areas in many temperate deciduous forests. It emerges in fall, overwinters, and then forms thick mats of vegetation and produces an abundance of show) flowers in late winter and spring (Sakai et al., 2001). Invasive populations of R. ficaria have three modes of reproduction: seeds, bulbils, and tubers. Seeds generally show low viability, and population growth mostly depends on vegetative propagation through bulbils and tubers (Marsden-Jones, 1935; Verheyen and Hermy, 2001). Whereas the success of this species in native European populations is positively correlated to the previous year's humidity and rainfall (Tyler, 2001), almost nothing is known about factors influencing North American population success. A better understanding of what makes this species so successful will lead to better control efforts.
Ranunculus ficaria has traits which may make it particularly adapted to severe hydrological disturbance associated with urbanization. During flooding events, waxy cuticles and thick tuber clumps provide R. ficaria with some amount of resistance to high velocity water flow (pers. obs.). Flooding also disperses bulbils, seeds, and loose tubers. Combined with early emergence, these interactions with flooding may allow R. ficaria to dominate the riparian corridor and adjacent areas. Whereas little is known about the ecology of R. ficaria in flood-prone habitats, other invasive plants in urban riparian areas are tolerant of Hooding and effectively disperse via flooding (Johansson and Nilsson, 1993; Thomas et al., 2005).
Effective dispersal is probably the most important result of flooding for R. ficaria, but this disturbance also redistributes leaf litter, exposing overwintering sprouts to cold and dry conditions, or creating a physical barrier by burying sprouts in deep leaf litter. The objective of this study was to examine impacts of varying leaf litter depths on Ranunculus ficaria growth and reproduction in a replicated field experiment. We expect R. ficaria will be tolerant to a wide range of leaf litter depths, partly explaining its success as an invasive in this habitat.
We conducted our study along Beargrass Creek (Middle Fork) in Cherokee Park (latitude 38.243301, longitude -85.698220) and Beargrass Greenway (latitude 38.245939, longitude -85.700499), which are part of the Olmsted Parks and Metro Parks systems in Louisville, Kentucky. The catchment in this area is urbanized and strongly channelized [~33% impervious surface (Beargrass Creek Watershed Council, 2005)] and the study sites are subject to flooding throughout the year. The riparian corridor is heavily invaded with R. ficaria, forming large monoculture patches (>90% ground cover) at both sites. The Greenway site is also heavily invaded by Amur honeysuckle (Lonicera maackii).
In fall 2011 we collected approximately 60 kg of fallen leaf litter from properties near our study site, which was then mixed thoroughly and air-dried. This litter was a mix of oak (Quercus spp.) and maple (Acer sp.) leaves, which represented the two dominant tree genera in our invaded sites. Other common tree species in our study sites included sycamore (Platanus occidentalis) and box elder (Acer negundo).
In Dec. 2011 we constructed 50 1 m x 1 m treatment plots grouped into 10 blocks of five plots each in the R. ficaria monoculture patches along the riparian corridor. Five blocks (25 plots) were located in the Beargrass Greenway site and five blocks (25 plots) were located in the Cherokee park site. All plots in the block were within 3 m of each other. Chicken wire cages (5 cm mesh, approximately 30 cm tall) anchored with rebar stakes and landscaping pins were constructed around and over each plot to keep each litter manipulation in place. The chicken wire cage also limited access by large herbivores such as deer. Each block contained one plot each with the following treatments: deep litter (20 cm), intermediate litter (10 cm), shallow litter (5 cm), no leaf litter with cage in place, and an ambient control with no cage and no litter manipulation. The air-dried mixed-leaf litter was added to each cage loosely by hand to avoid compaction. Ambient litter had a slightly different composition and depth across blocks with the average ambient leaf litter depth being 3 cm. Deep litter treatments approximated extreme litter deposition after a flooding event (pers. obs.), and the removal of all leaf litter in a cage represented scouring effects also associated with flooding events.
We monitored plots weekly to remove litter from the top of the cages, as well as to repair damage from weather, wildlife, and vandalism. We collected data on initial sprouting propagules, final biomass of R. ficaria, and final reproductive output (bulbils, flowers, seeds) from 0.5 m x 0.5 m subplots in the center of each plot to limit edge effects. Initial sprouts were counted in Jan. 2012. Final reproductive output per plant was counted for each propagule in Apr. 2012. Final biomass of R. ficaria in plots was harvested in Apr. 2012 by clipping plants at ground level, drying at 60 C for 48 h and weighing. This species also acts as a perennial plant that dies back each summer, so only above ground biomass was measured for the season. We collected environmental data weekly within each plot without disturbing the sampling subplot. These data included surface soil temperature (2 cm depth), surface soil moisture (2 cm depth using General DSMM500 soil moisture meter), and light penetration through the litter to the top of the emerging plants (Extech EasyView 30 light meter).
We performed general linear model analyses on each response variable to evaluate the effects of litter depth on R. ficaria reproduction, survival, and growth. Block, soil temperature, soil moisture, and light penetration were covariates. Bulbil, flower, and seed data were transformed [ln(x +1)] to meet test normality assumptions. Differences between litter depths were determined post hoc using Tukey's HSD. Spearman's rank correlation was used to determine correlations between biomass and bulbils, and between flowers and seeds. All analyses were performed in SYSTAT v. 12.
Ranunculus ficaria plants in shallow (5 cm) litter produced 63.6% more biomass than plants with no leaf litter cover, and plants in ambient litter conditions produced 38.1 % more biomass than plants with no leaf litter (Fig. 1A, Table 1). No other significant differences in biomass were detected between treatments. There was a trend for decreasing biomass under increasing leaf litter depths with an observable difference in biomass production between deep (20 cm) and shallow (5 cm) leaf litter plots (Fig. 1A). However, this difference was not significant in the full statistical model. Increasing light levels below the litter had a positive effect on biomass (Table 1). Although there was a positive correlation between final R. ficaria biomass and bulbil production ([R.sub.s] = 0.506, P < 0.001), there were no significant differences in bulbil production detected between treatments (Fig. 1B, Table 1). As with biomass, there was a trend showing decreasing bulbil production in deeper litter (Fig. 1B). None of the environmental factors significantly impacted bulbil production, and there were no block effects on biomass or bulbil production (Table 1).
Flower production was very sensitive to deep leaf litter depth, and flower production in deep leaf litter (20 cm) was significantly different than all other depths (Fig. 1C). There were no other significant differences between treatments. There were block effects detected for flower production (Table 1), most likely due to differences in tree canopy coverage in the different sites. Light penetrating the canopy was 22.1% lower in the Greenway plots mostly due to complete honeysuckle cover in two of the Greenway plots. There was a significant correlation between flower and seed production ([R.sub.s] = 0.939, P < 0.001), and the average seeds per flower produced were lower in Greenway plots ([F.sub.1,48] = 5.674, P = 0.022). Significant differences in seed production were detected between deep litter (20 cm) and all other treatments (Fig. 1D, Table 1). There were also block effects on seed production (Table 1).
Despite litter effects propagules were still produced in large numbers across treatments. An estimated 789 bulbils per square meter were produced in the most productive plots (5 cm depth). Although deep litter plots (20 cm) were the least productive for bulbils, there was still an estimated 262 bulbils per square meter (Fig. 1B). Ambient plots produced an average of 686 bulbils per square meter. Seeds were produced in large numbers in all treatments but deep litter. Bare ground, shallow litter (5 cm), and ambient plots were the most productive for seeds, and all produced close to the same average number of seeds (~740 seeds per square meter) (Fig. 1D).
Redistribution of leaf litter by flooding is a regular process for most rivers (Nilsson et al., 1999). This process may be especially profound in urban areas where storm runoff is efficiently channeled into the riparian corridor, causing flash flooding. This redistribution of leaf litter can have varying effects on the riparian plant community which may respond to leaf litter mass and chemical properties (Nilsson et al., 1999). In our study leaf litter was mixed to control for varying decomposition rate and nutrient content of the litter species, and the differences detected between treatments should be due to leaf litter depth acting as a physical barrier to sprouting propagules. Shallow leaf litter depths can aid in seedling establishment (Facelli and Pickett, 1991; Kostel-Hughes et al., 2005; Hovstad and Ohlson, 2008), but frequently any leaf litter has an overall negative effect on sprout and seedling survival (Xiong and Nilsson, 1999; Hovstad and Ohlson, 2008). Plant species that can tolerate a wide spectrum of leaf litter depths are expected to have a competitive advantage over species that are inhibited by leaf litter in areas where depth varies greatly (Facelli and Pickett, 1991; Benitez-Malvido and Kossmann-Ferraz, 1999).
Ranunculus ficaria reproduction was not hindered by leaf litter, except for seed production in very deep litter. The strong correlation between flower and seed production suggests very little pollen limitation in this self-incompatible insect-pollinated species (Metcalfe, 1939; Taylor and Markham, 1978). The average seeds per flower produced were lower in Greenway plots, probably due to interactions with honeysuckle. Shading by honeysuckle can reduce pollinator visitation rates (Goodell et al., 2010). The block effects detected in our flower and seed analysis were likely due to this interaction. Overall, the differences that were observed between treatments were not due to variation in micro-environmental factors we measured (covariates of temperature, moisture, and light) usually influenced by leaf litter. Instead, these differences were likely due to leaf litter acting as a physical barrier to smaller emerging vegetative sprouts and seedlings. Deep litter can inhibit sprouts, especially herbs and other species with small seeds (Facelli and Pickett, 1991; Sayer, 2006; Baker and Murray, 2010). Vegetative reproduction may provide R. ficaria one strategy to deal with the physical barrier of deep litter. Reliance on tubers may give new growth sufficient energy to penetrate deep litter and to tolerate low light conditions when buried. Bulbils may also provide more energy for sprouts than seeds, reducing the impact of deep litter as a physical barrier.
Ranunculus ficaria may have a competitive advantage in being able to penetrate and reproduce effectively across litter depths that many other herbs cannot penetrate. Deep leaf litter generally has a negative effect on native seedling sprouting and survival; however, varying litter depths can create habitat patchiness that could increase plant diversity, even in the presence of aggressive invaders (Facelli and Pickett, 1991; Schramm and Ehrenfeld, 2010). The plots in this study were placed in R. ficaria monocultures that were disturbed by flooding during the study period. No other herb species emerged in any of the treatment plots during the experiment; therefore we were unable to separate the effects of leaf litter depth, R. ficaria density, and disturbance on native species in this study.
Ranunculus ficaria appears to tolerate aspects of Hooding disturbance that other species cannot. Once established, R. ficaria may outcompete other species for light and soil resources, or negatively affect some species through allelopathy (Cipollini and Schradin, 2011). Managing flooding disturbances may prevent this species from establishing and becoming problematic. Current management practices for R. ficaria focus mostly on herbicide use to control populations in early spring (Czarapata, 2005). However, this method has had only partial success. Some management techniques may actually facilitate invasion. For example mowing is shown to increase vegetative spread in Alternanthera philoxeroides (Jia et al., 2009). A similar response to mowing has been suggested from genetic studies on R. ficaria (Reisch and Scheitler, 2009), and control methods for this species should be considered carefully.
High fecundity and dispersal by flooding are likely driving the invasions of R. ficaria. Our results suggest varying leaf litter depths caused by flooding disturbance do not strongly limit R. ficaria, even at depths expected to negatively affect growth and reproduction of other species. In addition flooding associated with urban hydrology is expected to further reduce numbers of native species not adapted to this disturbance. Urban flooding appears to facilitate R. ficaria, while negatively affecting local species, and flood mitigation in urban riparian corridors may be effective in enhancing native diversity. Given the broad tolerance of R. ficaria to leaf litter burial or scouring, land managers interested in controlling this species will want to alter the habitat to encourage native species, perhaps by dechannelizing urban streams or reducing impervious surface cover, rather than hope to directly reduce R. ficaria populations through flood control.
Acknowledgments.--The authors would like to thank Carl Cloyed, Cherise Montgomery, and Tommy Ross for help in cage construction and data collection; Margaret Carreiro for advice; Olmsted Parks and Louisville Metro Parks for use of the study area; and Kentucky Academy of Science, Marcia Athey Grant for funding.
SUBMITTED 21 FEBRUARY 2014
ACCEPTED 27 SEPTEMBER 2014
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JEFFERY A. MASTERS (1) and SARAH M. EMERY
Department of Biology, University of Louisville, Louisville Kentucky 40292
(1) Corresponding author: e-mail: email@example.com
TABLE 1.--Results of GLM for effects of leaf litter depth and environmental factors on biomass, bulbils, flowers, and seeds. Statistically significant results are indicated by an asterisk (* P < 0.10, ** P < 0.05, *** P < 0.01) (error df = 34 for all) Biomass Source df F P Litter Treatment 4 5.042 0.003 *** Block 9 1.405 0.226 Soil Temperature 1 0.734 0.398 Soil Moisture 1 0.590 0.448 Light 1 4.309 0.046 ** Bulbils Source df F P Litter Treatment 4 1.607 0.196 Block 9 1.001 0.459 Soil Temperature 1 0.650 0.426 Soil Moisture 1 1.370 0.250 Light 1 0.005 0.945 Flowers Source df F P Litter Treatment 4 12.315 0.000 *** Block 9 2.557 0.024 ** Soil Temperature 1 0.618 0.438 Soil Moisture 1 0.331 0.569 Light 1 0.541 0.467 Seeds Source df F P Litter Treatment 4 12.586 0.000 *** Block 9 5.420 0.000 *** Soil Temperature 1 0.383 0.541 Soil Moisture 1 0.446 0.509 Light 1 0.346 0.561
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|Author:||Masters, Jeffery A.; Emery, Sarah M.|
|Publication:||The American Midland Naturalist|
|Date:||Jan 1, 2015|
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