Lumbricus terrestris Prefers to Consume Garlic Mustard (Alliaria petiolata) Seeds

Lumbricus terrestris Prefers to Consume Garlic Mustard (Alliaria petiolata) Seeds Author(s): Patricia M. Quackenbush, RaeLynn A. Butler, Nancy C. Emery, Michael A. Jenkins, Eileen J. Kladivko, and Kevin D. Gibson Source: Invasive Plant Science and Management, 5(2):148-154. Published By: Weed Science Society of America DOI: http://dx.doi.org/10.1614/IPSM-D-11-00057.1 URL: http://www.bioone.org/doi/full/10.1614/IPSM-D-11-00057.1

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Invasive Plant Science and Management 2012 5:148–154

Lumbricus terrestris Prefers to Consume Garlic Mustard (Alliaria petiolata) Seeds Patricia M. Quackenbush, RaeLynn A. Butler, Nancy C. Emery, Michael A. Jenkins, Eileen J. Kladivko, and Kevin D. Gibson* Temperate and boreal forests in Canada and the northeastern United States have been invaded by several exotic species, including European earthworms (family Lumbricidae) and garlic mustard. Earthworms and garlic mustard co-occur and are both known to adversely impact some native plant species. However, relatively little is known about potential interactions between these two invaders. In a series of growth chamber experiments, we determined the palatability of garlic mustard and six native herbaceous forest species (shooting star, columbine, wild geranium, sweet cicely, butterfly milkweed, and yellow jewelweed) to the common nightcrawler. We also assessed the ability of the common nightcrawler to bury and digest garlic mustard and wild geranium. When offered seeds from garlic mustard and a native plant species, the earthworms ingested more garlic mustard seeds than seeds from four of the six native species. In a mesocosm experiment, the common nightcrawlers apparently digested 72 and 27% of garlic mustard and wild geranium seeds, respectively, that were placed on the soil surface. No seeds were observed on the soil surface at the end of the experiment but the majority of recovered seeds for both species were found within the top 10 cm (3.94 in). More seeds were recovered in 0- to 10-cm and 31- to 40-cm sections for wild geranium than for garlic mustard. No difference in seed recovery was detected at the other depths. Garlic mustard seed is readily consumed by common nightcrawlers and appears to be preferred over some native plant species suggesting that common nightcrawlers may reduce the size of the garlic mustard seed bank. Nomenclature: Common nightcrawler, Lumbricus terrestris L.; garlic mustard, Alliaria petiolata (M. Bieb.) Cavara & Grande ALAPE; columbine, Aquilegia canadensis L.; butterfly milkweed, Asclepias tuberosa L. ASCTU; common shooting star, Dodecatheon meadia L.; wild geranium, Geranium maculata L.; yellow jewelweed, Impatiens pallida Nutt; sweet cicely, Osmorhiza claytonia (Michx.) C.B. Clarke. Key words: Native plants, invasive plants, seed predation, invasive earthworm, forest, seed burial.

Invasive species are a major global threat to biodiversity and ecosystem function (Didham et al. 2005; Dukes et al. 1999; Ehrenfeld 2003; MacDougall and Turkington 2005; Sanders et al. 2003; Zavaleta et al. 2001). Most ecosystems have been invaded by multiple species and nonnative species account for 20% or more of the flora in many countries (Mooney and Cleland 2001; Vitousek et al. 1996). There is a growing body of evidence that suggests DOI: 10.1614/IPSM-D-11-00057.1 * First, second, and sixth authors: Graduate Student, Graduate Student, and Associate Professor, respectively, Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907; third author: Assistant Professor, Department of Biological Sciences and Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907; fourth author: Assistant Professor, Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN 47907; fifth author: Professor, Department of Agronomy, Purdue University, West Lafayette, IN 47907. Corresponding author’s E-mail: [email protected]

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that invasion by one species may directly or indirectly facilitate subsequent invasions by other nonnative species (Bohlen et al. 2004; Ehrenfeld 2003; Hale et al. 2008; Kourtev et al. 2002; MacDougal and Turkington 2005). Simberloff and Von Holle (1999) referred to this phenomenon as ‘‘invasional meltdown.’’ Earthworms that are not native to temperate and boreal forests in the northeastern United States and eastern Canada have been linked to declines in native plant diversity (Frelich et al. 2006; Hale et al. 2005, 2008), changes in organic matter decomposition and mineralization rates, and reductions in arbuscular mycorrhizal fungi populations at invaded sites (Bohlen et al. 2004; Frelich et al. 2006; Heneghan et al. 2007; Lawrence 2003). Researchers have also hypothesized that earthworms may facilitate nonnative plant invasions (Frelich et al. 2006; Kalisz 1993; Kourtev et al. 1998; Nuzzo 2009). Nuzzo et al. (2009) measured native vegetation and nonnative earthworm biomass in 15 northeastern hardwood forests and found that earthworm biomass was positively

Interpretive Summary The common nightcrawler is an introduced earthworm species that has been linked to reduced native plant diversity and to altered soil processes in invaded temperate and boreal forests in North America. The common nightcrawler can consume large quantities of seeds but the effect of this invasive species on the seed bank dynamics of native and invasive plants in its invaded range is unknown. In this study, we examined the palatability of garlic mustard, an invasive plant species, and six native species to the common nightcrawler. We also assessed the ability of the common nightcrawler to bury seeds below the soil surface. The earthworm preferred garlic mustard seeds over the seeds of four of the six native plant species and consumed or buried large quantities of garlic mustard seed. Although the net effect of the common nightcrawler on native plant species in invaded forests may be negative, our findings suggest that this earthworm has the potential to reduce the size of the garlic mustard soil seed bank.

associated with nonnative plant cover and negatively associated with the cover of native woody, perennial, and annual herbs, and ferns. The authors suggested that nonnative earthworms rather than nonnative plant species were the ‘‘driving force’’ behind reductions in native plant species in northeastern North American forests and that earthworm invasions appear to facilitate the invasion of those forests by nonnative plant species. However, other researchers have suggested that nonnative plants may drive increases in earthworm populations (Ehrenfeld et al. 2001; Madritch and Lindroth 2007), or that both earthworms and invasive plants co-occur because they respond similarly to disturbed habitat (Heimpel et al. 2010; Kalisz and Dotson 1989). Earthworms are ecosystem engineers and can fundamentally change ecosystem processes in ways that might affect plant invasions (Alban and Berry 1994; Bohlen et al. 2004; Frelich et al. 2006; Kourtev et al. 1998). For example, earthworms can reduce the depth of leaf litter in invaded areas thereby exposing plants to desiccation and temperature extremes, as well as promoting plants adapted to more mineral-rich soil profiles (Frelich et al. 2006; Heneghan et al. 2007). Earthworms can also affect the species composition of communities through seed predation, burial, and inducement or release of seed dormancy (Eisenhauer et al. 2009; Regnier et al. 2008), and seeds are considered an important component of common nightcrawler (Lumbricus terrestris L.) nutrition (Eisenhauer et al. 2010). Controlled experiments to assess the effect of earthworms on plant invasions have had mixed results. Belote and Jones (2009) assessed the impact of earthworms on the ability of tall fescue [Festuca arundinacea Schreb.; 5 Lolium arundinaceum (Schreb.) S.J. Darbyshire] to invade mesocosms containing either native or nonnative plant leaf litter. Earthworms limited the ability of fescue to recruit into

mesocosms with leaf litter from native plants but increased its ability in mesocosms with nonnative plant litter. Eisenhauer et al. (2010) examined the effect of earthworms on plant invasions and seed dispersal in a mesophilic grassland near Thuringia, Germany. They concluded that earthworms had little effect on the ability of exotic plants to colonize plots with either high or low plant diversity. However, the presence of earthworms did increase the invasibility of plots with intermediate levels of biodiversity. Garlic mustard [Alliaria petiolata (M. Bieb.) Cavara & Grande] and the common nightcrawler are two of most important invaders of hardwood forests in eastern North America. Garlic mustard is an herbaceous biennial native to Europe but now common in eastern deciduous forests in North America (Natural Resources Conservation Service 2011) that has been implicated in reductions in native plant diversity and abundance (Meekins and McCarthy 1999). Garlic mustard has no significant natural enemies in its invaded range and appears to suppress the growth of several North American forest plant species either through the release of allelochemicals or by disrupting mutualistic relationships between forest plants and mycorrhizal fungi (Prati and Bossdorf 2004; Stinson et al. 2006). The common nightcrawler is also native to Europe and is the largest of the invasive earthworms in eastern deciduous forests (Hale 2007). The species is known to be an important predator and seed disperser in natural and agricultural systems (Eisenhauer and Scheu 2008; Regnier et al. 2008). It is the only invasive earthworm in North America that establishes a network of vertical burrows (Kladivko 1993). In this paper, we assess the palatability of six native herbaceous forest species and garlic mustard to the common nightcrawler. We also determine the consumption and vertical transport of seeds of garlic mustard and wild geranium (Geranium maculata L.) by the common nightcrawler. Materials and Methods

Seed Ingestion. Two experiments were conducted to assess seed palatability to the common nightcrawler. The first experiment was initiated on June 9, 2008, and repeated on June 12, 2008. The second experiment was initiated on June 16, 2008 and repeated on June 19, 2008. In the first experiment (referred to as the one-choice experiment), a complete randomized design with seven plant species and eight replicates was used to determine seed ingestion when common nightcrawlers were offered a single food source. One invasive species, garlic mustard, and six native plant species(Prairie Moon Nursery, 32115 Prairie Lane, Winona, MN 55987), including yellow jewelweed (Impatiens pallida Nutt.), columbine (Aquilegia canadensis L.), wild geranium, shooting star (Dodecatheon meadia L.), sweet cicely [Osmorhiza claytonii (Michx.) C.B. Quackenbush et al.: Nightcrawler ingestion and burial

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Table 1. Characteristics of garlic mustard and six native herbaceous forest species. Life cycle and blooming dates (earliest to latest month that the species has been reported in bloom in Indiana) are from Yatskievych (2000). Seed length and width data are the means of measurements taken on 25 seeds for each species. Plants are listed in order of increasing seed length. Species

Life cycle

Blooming dates

Seed length (mm)

Seed width (mm)

Shooting star Columbine Wild geranium Garlic mustard Butterfly weed Yellow jewelweed Sweet cicely

Perennial Perennial Perennial Biennial Perennial Annual Perennial

April to June April to July April to July April to July June to September June to September May to June

1.00 1.90 2.05 2.90 4.40 5.65 15.85

1.00 1.00 1.95 1.00 3.05 2.05 1.00

Clarke], and butterfly milkweed (Asclepias tuberosa L.), were used (Table 1). Seed size was estimated by measuring the length and width of 25 seeds for each species. The native species were selected to provide a range of seed sizes and because they are commonly found in Indiana forests. One adult common nightcrawler was placed on moistened filter paper in a 15-cm diam (5.9-in-diam) petri dish with 50 seeds of a single species. Common nightcrawlers used in this and subsequent experiments weighed between 3.0 and 4.0 g (0.11 and 0.14 oz) each and new individuals were used for each run and experiment. The common nightcrawlers were obtained from a commercial vendor (WalMart, 2801 Northwestern Avenue, West Lafayette, IN 47906), kept in small containers filled with moist peat moss, and placed in the petri dishes within a week of purchase. Each dish was covered with aluminum foil and small holes were punched into the foil to provide air to the common nightcrawlers. The dishes were placed into a darkened growth chamber at 18 C (64 F) for 18 h before the common nightcrawlers were removed and the remaining seeds counted (Willems and Hujismans 1994). Missing seeds were assumed to have been ingested. Methods for the second experiment (referred to as the two-choice experiment) were as described above except that the common nightcrawlers were placed in petri dishes containing 25 seeds of garlic mustard and 25 seeds of a single native species. Thus, a split-plot design was used with species as the main plot and seed type (invasive or native) as the subplot. Eight replicates were used.

sand to discourage the common nightcrawlers from burrowing along the sides of tubes. A Gilford series field soil (coarse-loamy, mixed, superactive, mesic Typic Endoaquolls) was sterilized for 3 h a day for 3 d at 240 C at 0.10 MPa (15 psi) and then packed into tubes to create a 40-cm soil column. Soil in the tubes was saturated with water and drained before adding the nightcrawlers. After the worms were introduced, the tubes were bottom-watered, using dish tubs as a water reservoir, so that the soil remained moist but not waterlogged. A single common nightcrawler was placed in each tube. Five hundred garlic mustard or wild geranium seeds were placed on the soil surface 48 h after the worms were introduced. The experiment was conducted in a growth chamber with 14 h of light at 20 C and 10 h of dark at 10 C. Leaf litter was added to each tube 14 d after the seeds were applied in order to provide an alternate food source for the common nightcrawlers. After 30 d, the tubes were removed from the growth chamber and soil was extruded in 10-cm sections (0 to 10 cm, 10 to 20 cm, 20 to 30 cm, and 30 to 40 cm). Each soil section was sieved through 600-mm mesh to collect seeds. For data analyses, we assumed that unrecovered seeds were digested by the common nightcrawlers although it is also possible that seeds germinated and died or simply decomposed during this period. However, no seeds germinated at the soil surface and germinated seed was not recovered in the soil column, which suggests that germination may not have been a major contributor to seed loss.

Seed Transport. The seed transport experiment was initiated on October 1, 2008 and repeated on March 1, 2009. Garlic mustard and wild geranium were chosen to assess seed consumption and transport by the common nightcrawler in a mesocosm experiment because seeds of the two species are of similar size (Table 1). A split-plot design with plant species as the main plot and depth as the subplot was used. Polyvinylchloride tubes (inner diam 15 cm, height 52 cm) were lined at the bottom with 1-mm (0.04-in) aluminum mesh. A polyurethane adhesive was used to coat the inner tube walls with a thin layer of coarse

Seed Digestion. After the burial experiment was completed, a follow-up experiment was conducted to determine if garlic mustard and wild geranium differed in their ability to pass undigested through the gut of the common nightcrawler. Methods were as described for the first seed ingestion experiment except that the common nightcrawlers were placed on moistened filter paper in new petri dishes after the first 18 h and allowed to excrete casts for an additional 48 h. During that period, the common nightcrawlers remained in the darkened growth chamber with the temperature maintained at 18 C. The number of

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Table 2. Number of seeds ingested by the common nightcrawler in 18 h when offered 50 seeds of a single species. Values are means; parentheses enclose standard errors. Species Shooting star Garlic mustard Wild geranium Columbine Butterflyweed Sweet cicely Yellow jewelweed

No. of seeds ingested 23.3 17.5 11.4 11.0 6.3 6.0 1.1

(2.67) (2.77) (1.63) (2.09) (1.20) (1.38) (0.33)

aa ab bc bc cd cd d

error. Regression analysis was used to examine the relationship between seed ingestion and seed size (length and width) in the one-choice experiment. Analyses for all experiments were conducted with the SAS 9.1.3 software package (SAS Institute Inc., Cary, NC). All alpha values 5 0.05 unless specifically stated otherwise. Results and Discussion

a Values with the same letter were not significantly different (P # 0.05).

seeds in the common nightcrawler casts was determined and digestion calculated as the difference between ingested seed and seed recovered in the casts. Statistical Analyses. Data were tested for normality and heterogeneity of variance and square-root or log transformed as necessary to comply with the assumptions of ANOVA. Data were back-transformed for presentation. Mixed models (PROC MIXED), with species as fixed effects and run of the experiment as random effects, were used to analyze data in the one-choice experiment; species and seed type were considered fixed effects and run a random effect in the two-choice experiment. Mixed models were also used to assess the effect of plant species, depth, and run on common nightcrawler consumption and transport of seed. Run was treated as a random effect whereas species and depth were considered to be fixed effects. Finally, a mixed model was used to compare garlic mustard and wild geranium ingestion and digestion by the common nightcrawler. No interaction was detected between run and the fixed effect variables so runs were pooled and the data reanalyzed for all experiments. Means were separated using the DIFF procedure and a TukeyKramer adjustment was applied to control experiment-wise

The common nightcrawler ingested more seeds from shooting star than from any other plant species except garlic mustard (Table 2). More seeds from garlic mustard were ingested than from butterfly milkweed, sweet cicely, and yellow jewelweed (Table 2). Differences in seed ingestion were not detected among wild geranium, columbine, butterfly milkweed, and sweet cicely or among yellow jewelweed, butterfly milkweed, and sweet cicely (Table 2). An interaction was detected between species and seed type in the two-choice experiment, so ingestion of the native species was compared to ingestion of garlic mustard separately for each native species (Table 3). More garlic mustard seeds were ingested than seeds from four of the six native species (Table 3). More shooting star seeds were ingested than garlic mustard seeds; no difference in seed ingestion was detected between columbine and garlic mustard (Table 3). Ingestion of garlic mustard ranged from 15% when offered with sweet cicely to 35% when offered with wild geranium. When offered with garlic mustard, 56% of shooting star seeds were ingested, while less than 20% of seeds for the remaining native species were consumed. Two percent or less of yellow jewelweed and sweet cicely seeds were ingested when offered with garlic mustard. In the first seed ingestion experiment, seed ingestion was negatively associated with seed length and width (Y 5 4.2 2 0.12X1 2 0.47X2 where Y 5 the square root of the number of seeds ingested, X1 5 seed length, and X25 seed width; P , 0.01; adjusted r2 5 0.13). Seed ingestion has been negatively associated with seed length and width in

Table 3. Number of seeds ingested by the common nightcrawler in 18 h when offered 25 seeds of garlic mustard and 25 seeds of a native species in the same petri dish. Values are means; parentheses enclose standard errors. No. of seeds ingested Species

Native species

Shooting star Wild geranium Columbine Butterfly weed Yellow jewelweed Sweet cicely

13.9 4.6 4.9 2.3 0.6 0.4

a

(1.53) (0.75) (1.05) (0.54) (0.27) (0.16)

aa b a b b b

Garlic mustard 8.1 8.7 6.6 7.6 5.5 3.7

(1.76) (1.59) (1.09) (1.11) (1.26) (0.89)

b a a a a a

Values within a row with the same letter were not significantly different (P # 0.05).

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In the seed burial experiment, the nightcrawlers digested 72 and 27% of all garlic mustard and wild geranium seeds, respectively. Interaction between species and soil depth was detected and the percentage of seeds recovered for each species was compared at each soil depth. No seeds were observed on the soil surface at the end of the experiment but the majority of recovered seeds for both species were found within the top 10 cm (Figure 1). More seeds were recovered for wild geranium than for garlic mustard in the 0- to 10-cm and 30- to 40-cm depths (Figure 1). No difference in seed recovery was detected at the other depths (Figure 1). Greater ingestion and digestion of garlic mustard seeds than wild geranium seeds was also detected in the follow-up seed digestion experiment (Table 4). More than half (52%) of garlic mustard seeds ingested were digested whereas only 36% of ingested wild geranium seeds were digested (Table 4). Differential burial depths and digestion rates among plant species by the common nightcrawler can contribute significantly to the species composition and spatial arrangement of plant communities (Milcu et al. 2006; Regnier et al. 2008; Willems and Huijsmans 1994). Garlic mustard was preferentially ingested over most native species in this study (Table 3) and a majority of ingested garlic mustard seeds were digested by the common nightcrawler (Table 4). Wild geranium and garlic mustard seeds were both transported below the soil surface by the common nightcrawler but fewer wild geranium seeds than garlic mustard seed were digested (Figure 1). These results suggest that earthworms might reduce garlic mustard seed banks more than those of four of the six native species examined in this study. However, the relationship between seed transport and predation by the common nightcrawler and plant population dynamics can be complex. Buried seed may be protected from surface seed predators (Eisenhauer et al. 2009; Shumway and Koide 1994) but seedlings that are buried too deeply may not be able to germinate or reach the soil surface after germination. Seed germination may be increased or decreased by passage through the earthworm gut depending on the plant species (Eisenhauer et al. 2009; Lazcano et al. 2010) and high fertility levels in earthworm burrows and middens may provide favorable conditions for germination, recruitment, and growth of large-seeded species (Milcu et al. 2006).

Figure 1. Number of wild geranium and garlic mustard seed recovered from four soil depths in a mesocosm experiment. A single common nightcrawler was placed in soil-filled tubes and seed was recovered after 30 d. Five hundred seeds from either wild geranium or garlic mustard were placed on the soil surface at the start of the experiment. Values are means, with error bars representing standard error. Within each depth, values with the same letter were not significantly different (P # 0.05).

other studies (Eisenhauer et al. 2009; Shumway and Koide 1994). Garlic mustard seeds were longer than those of shooting star, columbine, and wild geranium but shorter than seeds of the remaining species (Table 1). Garlic mustard seed width was less than that of wild geranium but similar to shooting star and columbine. Seed width might explain differences in ingestion between garlic mustard and wild geranium (Table 1). However, seed size explained only 13% of the variation in seed ingestion and the number of wild geranium and columbine seeds ingested were very similar (Tables 2 and 3) even though columbine seed length and width was less than that of wild geranium. This suggests that seed size alone does not explain why more garlic mustard seeds were ingested than wild geranium seeds. It should also be noted that earthworm activity is typically greatest during April and May but butterfly milkweed and yellow jewelweed bloom between June and September. Thus seed consumption of these two species by nightcrawlers might be expected to be low based solely on their phenology.

Table 4. Number of seeds ingested, cast, and digested by common nightcrawlers in 18 h when offered 50 seeds of a single species. Digestion was calculated as the difference between the number of ingested and recovered seeds. Values are means, parentheses enclose standard error. Species Garlic mustard Wild geranium a

No. of seeds ingested

No. of seeds recovered in casts

No. of seeds digested

14.55 (1.72) aa 10.15 (2.09) b

7.05 (1.50) a 6.50 (1.28) a

7.50 (1.23) a 3.65 (0.73) b

Values with the same letter within a column were not significantly different (P # 0.05).

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Even relatively high seed predation rates may have only limited effects on plant population dynamics if sufficient seed remain in the soil seed bank, i.e., garlic mustard may produce enough seeds to satiate earthworms without significantly limiting its own population growth. Thus, additional experiments over longer periods in more natural conditions are necessary to determine the cumulative impact of seed predation and transport by earthworms on garlic mustard and native forest species. Acknowledgments

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