Biological Invasions 1: 237–245, 1999. © 1999 Kluwer Academic Publishers. Printed in the Netherlands.

Differences in earthworm densities and nitrogen dynamics in soils under exotic and native plant species P.S. Kourtev* , W.Z. Huang & J.G. Ehrenfeld Rutgers University, Cook College, 14 College Farm Rd., DEENR Bdg., Rm. 164, New Brunswick, NJ 08901, USA; ∗ Author for correspondence (e-mail: [email protected]; fax: +1-732-932-8746) Received 12 March 1999; accepted in revised form 9 September 1999

Key words: ammonium, earthworms, exotic plant species, nitrate, nitrate reductase, nitrification, soil respiration Abstract Previous studies of the invasion of two exotic plants – Berberis thunbergii and Microstegium vimineum – in hardwood forests of New Jersey have shown a significant increase of pH in soils under the invasive plants as compared with soils from under native shrubs (Vaccinium spp). We present a further investigation of soil properties under the exotic plants in question. We measured the densities of earthworms in the soil under the two exotics and the native shrubs in three parks in New Jersey. In the same populations we also measured the extractable ammonium and nitrate in the top 5 cm of the soil, as well as the respiration of the soils and the potential rates of mineralization (aerobic lab incubation). In addition, we measured the nitrate reductase activity in leaves of the two exotic plants and several native shrubs and trees. Although there were differences between parks, we observed significantly higher earthworm densities in the soil under the exotic species. The worms were all European species. Soil pH, available nitrate and net potential nitrification were significantly higher in soils under the two exotic species. In contrast, total soil C and N and net ammonification were significantly higher under native vegetation. Nitrate reductase activities were much higher in the leaves of exotic plants than in the leaves of native shrubs and trees. Changes in soil properties, especially the change in nitrogen cycling, associated with the invasion of these two plant species may permit the invasion of other weedy or exotic species. Our results also suggest that even if the two exotic species were removed, the restoration of the native flora might be inhibited by the high nitrate concentrations in the soil. Introduction Successful plant invaders can have profound effects on many aspects of the invaded ecosystem (Mooney and Drake 1986; Vitousek 1986; Vitousek et al. 1987; Vitousek 1990; Wardle et al. 1995; Holmes and Rice 1996). The effects of invasive plants on soil properties and processes is particularly important. Soil properties develop over a relatively long period of time (Tate 1987), and changes in the soil can therefore last for a prolonged time even if the invasive species is removed. We have studied the invasion of two exotic plant species – Berberis thunbergii and Microstegium vimineum – in New Jersey hardwood forests. Soils

under these exotic species have higher pH than soils under native shrubs and the organic (O) horizon under the exotic plants is missing (Kourtev et al. 1998). In this paper, we present evidence that these plants may significantly alter microbial activity and nitrogen cycling in the soil beneath individual shrubs. Exotic species have been shown to alter the nitrogen status of soils (Vitousek et al. 1987; Asner and Beatty 1996), although the best evidence comes from nitrogen poor volcanic soils in Hawaii. The invasion of Myrica faya (Vitousek 1986) introduced nitrogen fixation in the system which led to a much higher nitrogen content in the invaded soils. In the study by Asner and Beatty (1996) the litter of the invasive species had a very

238 low carbon (C) to nitrogen (N) ratio, compared to the native plants and so rapid decomposition of the invasive plants’ litter led to increases in the nitrogen pools in soil. While the invasion of an N-fixing species into Npoor soils could be expected to alter N dynamics, the invasion of non-N-fixers may be more variable, and may depend on the relative importance of a variety of mechanisms by which plants influence soils (Hooper and Vitousek 1997; Hobbie 1996). While sampling soils for our previous studies (Kourtev et al. 1998), we observed a high density of earthworms in the soil beneath the alien plant species. Earthworms are associated with higher nitrogen mineralization and nitrification rates in the soil (Scheu 1987; Lensi et al. 1992; Steinberg et al. 1997). An increase in earthworm densities, in combination with the observed increase in pH of the soils, could lead to enhanced microbial activity and N cycling, especially nitrification, beneath the exotics compared to soils beneath native shrubs. We report here a study of the possible association of increased earthworm densities, increased microbial activity (indexed by soil respiration rate), and increased N mineralization and nitrification with exotic plant invasions. We measured the numbers of earthworms in soils under the exotic species (B. thunbergii and M. vimineum and native shrubs (Vaccinium spp.) in three parks in New Jersey. We also measured the basal respiration of soils from invaded and uninvaded stands, + the available nitrate (NO− 3 ) and ammonium (NH4 ) in them, and the potential mineralization and nitrification rates. In addition, we measured nitrate reductase (NR) activities in the leaves of the two exotic plants and several native shrubs and trees. NR activity is commonly used as an indicator of the ability of plants to utilize NO− 3 from the soil (Barford and Lajtha 1992); since NR is an inducible enzyme, the presence of high levels of the enzyme in plant tissues implies a high availability in the soil.

Materials and methods Study sites We studied areas in three parks in northern New Jersey – Morristown National Historic Park (MOR), Allamuchy (ALL), and Worthington State Forest (WOR) which have dense thickets (B. thunbergii) and lawns (M. vimineum) of the respective exotic plants and adjoining areas of native understory. In two of the

sites (MOR and WOR), mixed stands of B. thunbergii (common name Japanese barberry) and M. vimineum (common name Wiregrass) are common. In ALL, M. vimineum is only present along trails, and sampling was restricted to thickets of B. thunbergii. Uninvaded stands have an understory composed mostly of Vaccinium spp. (blueberries) and Gaylussaccia spp. (huckleberries). In Morristown, uninvaded stands have no understory, probably due to deer browsing. Soils in the three parks are very similar: MOR – Parker and Edneyville soils (Typic Dystrochrept and Typic Hapludult), respectively; ALL – Rockaway soils (Typic Fragiudult); WOR – Oquaga and Steinsburg soils (both Typic Dystrochrepts). All three soils have a high content of rocks (10–30% fragments > 6 cm) and are reported to be acidic (pH 4.5–5.5) (Fletcher 1975). In our previous work in the three parks we identified several populations (up to seven per park) for each of the exotic plant species, as well as many uninvaded sites. We randomly chose some of these populations for the study presented here. We sampled soils in three populations of barberry, three populations of wiregrass and three uninvaded stands in every park, except ALL where wiregrass is not present. All sampled sites had a closed canopy of mature hardwood trees, including Quercus spp., Carya spp. (hickories), Betula lenta (Black birch), and others, and all were located on flat to moderately sloping upland areas. Earthworm sampling We sampled earthworms in the soil at six randomly chosen points in each site in May 1998, after an abundant rain and over a relatively short period of time, since earthworms are known to change their vertical distribution in the soil depending on soil moisture (Edwards and Bohlen 1996). We used the method described in Gunn (1992), which uses a mustard suspension as a vermifuge, instead of formalin. We prepared fresh mustard suspension of 250 ml of mustard in 8 l of water in the field and poured it on to a rectangular area of known dimensions (20 by 40 cm). We delimited that area by inserting metal sheets in the soil, which also stopped as much as possible superficial outflow of the suspension. Earthworms were collected, counted and released, although a few were preserved in formalin for identification by Dr Patrick Bohlen, Institute for Ecosystem Studies, Milltown, New York. In addition, we collected the litter from the sample area and transported it in coolers to the lab at Rutgers

239 University. The litter was then spread on plastic sheets, and earthworms in it were collected and counted. We dried the litter for 24 h at 70 ◦ C to estimate litter mass on the ground in the different sites. We summed the number of earthworms in the litter and the soil, since it was uncertain whether the earthworms were litter feeders or in the litter due to high moisture content. For that reason we only compared the total number of earthworms found, without separating them into soil and litter dwellers. Soil samples We sampled soil in two of the three sites per plant type per park using a 1.2 cm diameter corer to collect the top 5 cm of the soil after the removal of litter. Three intact cores per site were placed in a prelabeled brown glass vial that were sealed immediately with an airtight cap with a rubber septa in it. The vials were transferred to the laboratory at about 20 ◦ C. After 4 h of incubation we measured the concentration of CO2 in their headspace using a Shimadzu gas chromatograph (GC-14). Several more cores were mixed in a ziploc bag for + analysis of NO− 3 and NH4 extracted with 2 M KCl. Subsamples were used to measure soil pH (1 : 2 solution with deionized water), soil organic matter (loss on ignition method), soil moisture, and total Kjeldahl N. After CO2 was measured soil moisture content was adjusted to 60% and the samples were incubated for + two more weeks, then extracted for NO− 3 and NH4 with 2 M KCl. This allowed us to estimate the potential net mineralization and nitrification rates from each soil sample. Nitrate reductase NR activity was measured only in MOR on freshly collected leaves from the field using the method described by M¨uller and Janiesch (1993). The following species were used: barberry, wiregrass, white oak (Quercus alba), blueberry (Vaccinium pallidum), huckleberry(Gaylussacia baccata), and black birch (Betula lenta). We collected the leaves at the same time of the day (around 9:00 am) and on days with similar weather conditions. For the tree species, we measured NR activity in individuals growing in invaded and noninvaded stands in order to estimate effects of the concentration of different N forms in the soil on leaf NR activity. We collected three leafy twigs from each of three to five individuals of each tree and shrub species.

Leaves were transferred to the lab as soon as possible and their NR activity was measured immediately. Leaves from a twig were cut into small square pieces (about 0.5 cm). One gram of the pieces was then incubated for 10 min under vacuum with buffer containing substrate (nitrate) and n-propanol which facilitates the movement of buffer into the leaves. A separate sample of 1 g was similarly incubated with buffer which did not contain the substrate. The samples were then incubated for an hour at 37 ◦ C in the dark and under a nitrogen atmosphere. These conditions have been shown to yield the highest activity when measuring the NR of leaves (M¨uller and Janiesch 1993). After incubation, the leaf suspensions were filtered and the production of nitrite was measured colorimetrically in the remaining solution using standard methods. −1 −1 g fresh NR activity was expressed as µmol NO− 2 h weight of leaves. Statistical analyses Preliminary studies (Kourtev et al. 1998) indicate that the baseline conditions in noninvaded soils of the three parks are significantly different. For that reason we did not average the data across the three parks but rather used them as a separate factor in our analyses. We used two-way ANOVA to test for differences in the number of earthworms and litter biomass on the ground, with park and vegetation cover as factors. We used two-way MANOVA to test for differences in soil chemical properties (moisture content, pH, N + content, available NO− 3 and NH4 ), soil respiration and soil potential mineralization with the same two factors. We did not average data across the three parks. For the NR activity data, we first compared for every tree species the activity in leaves of individuals from invaded and uninvaded soils, using Student’s t-test. We found no significant differences and therefore pooled the NR activity of all the samples from a given tree species. We then compared the leaf NR activity of barberry and wiregrass with that of all other plant species measured using two-tailed t-tests.

Results Earthworms Earthworm densities were different in the three parks, but the differences among plant cover types were even more striking (Figure 1a; two-way ANOVA

240

Figure 1. Number of worms and amount of litter on the ground. White bars represent noninvaded sites, grey bars represent barberry sites and black bars represent wiregrass sites.

F = 12.922 for sites (P = 0.0005), F = 14.821 (P = 0.0002) for species, and F = 5.436 (P = 0.0015) for their interaction). Densities were highest in MOR, and within that park the densities were much higher under M. vimineum than under the other species. In all three parks worm density was higher under exotics than under native plants. All of the earthworms collected were species native to Europe, and exotic invaders themselves. They included Lumbricus terrestris, Lumbricus rubellus, Dendrobaena octaedra, Aporrectodea limicola, and Eisenia rosea. These are a mixture of endogeic and epigeic species, some of which are responsible for producing a thick, conspicuous layer of casts on the soil. Differences in the depth of the litter layer (Figure 1b) also were highly significant among parks and species (two-way ANOVA F (parks) = 22.298 (P < 0.0001), F (plants) = 11.153 (P = 0.0011), F (interaction) = 3.961 (P = 0.0099)). Litter accumulations were much higher in the uninvaded stands, and tended to be higher under barberry than under wiregrass. Soils MANOVA and the corresponding single ANOVAs showed significant differences in soil under the exotic and native plant species (site: Pillai Trace = 0.793, P < 0.05; Plants: Pillai Trace = 1.163, P < 0.0001; Interaction: Pillai Trace = 0.990, P < 0.05). The effects of park and the interaction between park and plant cover as main factors were not significant, except for pH, extractable NH+ 4 and CO2 evolved per g OM. The effects of plants, however, were significant for

Table 1. Effects of plant cover and site (F -values from the two-way ANOVAs) on the measured soil variables. Variable Soil moisture (%) Soil pH Total C in soil (%) Total N in soil (mg g−1 ) −1 Available NH+ 4 (µg g ) − Available NO3 (µg g−1 ) Net NH+ 4 mineralization (µg g−1 2wk−1 ) Net NO− 3 mineralization (µg g−1 2wk−1 ) CO2 evolved g−1 OM ∗P

Park n.s. 40.468∗∗∗ n.s. n.s. n.s. n.s. n.s. n.s. 6.78∗∗

Plant cover 7.643∗∗∗

108.87∗∗∗ 40.10∗∗∗ 4.97∗∗∗ 31.90∗∗∗ 14.56∗∗∗

Interaction n.s. 7.45∗∗∗ n.s. n.s. 4.26∗ n.s.

15.35∗∗∗

n.s.

9.68∗∗∗ n.s.

n.s. n.s.

< 0.05; ∗∗ P < 0.01; ∗∗∗ P < 0.001.

almost every variable measured (Table 1 and Figures 2–4). The chemical characteristics of invaded soils differed from the uninvaded soil in predictable ways in all three parks. Soil pH was higher under barberry and wiregrass, compared to the noninvaded soils (Figure 2b). As reported for other infested and noninfested areas in these parks (Kourtev et al. 1998), the noninvaded soils had pH values characteristic of oak-dominated forests (approximately 4.0), whereas invaded sites ranged above 6.0. The top 5 cm of mineral soil also had a lower organic matter content, and a lower total N content (except WOR) (Figure 2e). Nitrogen availability, reflected in both the extractable concentrations and the rates of production, similarly varied in uniform ways in the three parks among the plant cover types (Figures 2a,c and Figure 3).

241

Figure 2. Soil characteristics in the invaded and uninvaded sites. White bars represent noninvaded sites, grey bars represent barberry sites and black bars represent wiregrass sites.

Differences in absolute amounts among the parks, which contributed to the few significant interaction terms in the ANOVAS (Table 1), did not mask the patterns of difference among plant types. Both extractable NO− 3 and the nitrification rate were much higher under

both exotics than under the native shrubs, whereas both extractable NH+ 4 and the ammonification rate are higher under native species. Soil respiration also differed significantly (F (plants) = 18.371, P < 0.0001) among the plant

242

Figure 3. Nitrogen dynamics in the soil under barberry and wiregrass and in uninvaded soils. White bars represent noninvaded sites, grey bars represent barberry sites and black bars represent wiregrass sites.

Figure 4. Soil respiration under the exotic plants and under native shrubs. White bars represent noninvaded sites, grey bars represent barberry sites and black bars represent wiregrass sites.

cover types, when respiration was expressed per unit mass of soil (Table 1). Respiration was higher in the control sites in ALL and MOR, but not in WOR (Figure 4a). However, respiration can be expected to

reflect the amount of organic matter present in the soil. Regressions of respiration rate on soil organic matter were significant for barberry (slope = 0.53, r 2 = 0.513, P = 0.0006) and uninvaded soils

243 Table 2. Nitrate reductase activity of leaves from different plant species.a BT (4)b

MV (6)

BL (13)

VP (5)

GB (3)

QA (9)

NR activity Mean SE

394.49 49.49

558.84 113.61

465.68 50.41

123.01 52.41

17.52 9.19

162.35 29.32

t-values Barberry Wiregrass

– n.s.

n.s. –

n.s. n.s.

4.27∗∗∗ 3.83∗∗∗

8.66∗∗∗ 5.21∗∗∗

4.55∗∗∗ 3.69∗∗

a BT

– B. thunbergii, MV – M. vimineum, BL – Betula lenta, VP – Vaccinium pallidum, GB – Gaylussacia baccata, QA – Quercus alba. size. ∗ P < 0.05; ∗∗ P < 0.01; ∗∗∗ P < 0.001. b Sample

(slope = 0.89, r 2 = 0.717, P < 0.0001), but not significant for wiregrass soils. When respiration was recalculated to reflect the organic matter content of the soil, significant differences among plant cover types disappeared (Figure 4b). Nitrate reductase NR activity was much higher for barberry and wiregrass leaves than for oak, blueberry and huckleberry leaves (Table 2). The NR activity of black birch leaves, however, was not different from either barberry or wiregrass leaves.

Discussion These data clearly show that soil associated with B. thunbergii and M. vimineum have strikingly different chemical properties and biological activity. Elevated soil pH, decreased litter thickness, decreased soil organic matter and total N combine with a large increase in nitrification and available NO− 3 and a higher density of exotic earthworms to create profoundly different soil conditions in exotics-infested areas. These data cannot resolve the causality of the exotic plant–exotic earthworm association. Earthworms were eliminated from this region during the Wisconsin glaciation (Reynolds 1995) and did not reoccupy the area during postglacial time. The presence of European worms at very low densities in uninfested soils suggests that the worms may have been introduced by agricultural activities nearby. Land-use histories are available for MOR (Ehrenfeld 1982) and ALL (Vermeule 1900), but only anecdotal, region information is available for WOR. Agriculture occurred in some of the study areas

in MOR during the 1800s, but had ceased by the beginning of the 20th century (Ehrenfeld 1982). There is no record of agriculture in ALL; rather, the area was used as a game preserve for deer and grouse during the latter half of the 1800s; the extremely stony soils throughout our study areas also suggest that plowing and cropping were never practiced on these soils. Similarly, the extremely shallow, stony soils in all study areas of WOR, plus local accounts of human activities (Beck 1983) suggest that although some areas may have been used for pasture and/or the forests may have been used for grazing, no crops were cultivated on these soils. Thus, worms may have moved into these areas slowly from cultivated areas in adjacent regions and may have persisted at low densities as oak-dominated forests matured on the sites during the 1900s (Ehrenfeld 1982; Dibeler and Ehrenfeld 1990). If this is the case, then the exotic plant species invasions may have promoted the growth of worm populations. Alternatively, the known association of earthworms with surface litter incorporation, pH increases and increased nitrification (Basak et al. 1990; Lensi et al. 1992) suggests that the worms have created a soil environment that promotes the growth of the exotic plant species. The high concentrations of NR in the exotics suggests that these species are better able to utilize the NO− 3 supplies than most of the native species, especially the native shrubs. Indeed, both scenarios may occur, creating a positive feedback situation in which exotic plants and exotic worms reinforce each other’s population growth. Soil characteristics were significantly different under the exotic species compared to control sites. The unusually higher pH (mean pH = 6.5 for barberry and wiregrass in MOR), and the lower C and N concentrations in the invaded soil found are in agreement with our

244 previous findings (Kourtev et al. 1998). Earthworms have been shown to incorporate organic matter in the soil in numerous occasions (Edwards and Bohlen 1996). In such cases, the organic matter can still be found mixed into the mineral soil. In the invaded soils that we studied, however, there were no differences in the % organic matter in the mineral soil as shown by Kourtev et al. (1998), where a subset of the populations studied here was described. This suggests that the organic matter is being lost from these soils through microbial respiration. Contrary to our hypothesis, however, we were unable to show higher respiration in soils under exotic species than in soils under native shrubs. The exotic populations that we sampled were very dense and therefore relatively old, and the organic horizon in their soils was missing. If indeed high mineralization rates are the reason for the dissapearing of the organic horizon, it might be that such rates are observed only in the beginning of the invasions and so were not detected in our relatively old sites. Interestingly, the regressions for respiration against OM in the soil showed different slopes (see section Results) for the different plant covers. This suggests that the quality of the organic matter in the soil beneath the invasive plants is different from that of noninvaded soils. High nitrate concentrations imply that N losses due to leaching may be higher in exotics-infested stands, with possible implications for downstream water quality (Vitousek et al. 1997; Carpener et al. 1998). This situation may also favor the invasion of other weedy plants, including invasive exotics, as ruderals generally have a high ability to utilize NO− 3 as an N source (Meltzer and van Dijk 1986; Marchese et al. 1988; Mekki and Leroux 1991). Thus, soils created by the exotic plant–exotic worm combination are likely to promote other invasions. Indeed, extensive recent analyses of the vegetation in MOR (Ehrenfeld 1999) clearly show a high density and diversity of other exotic and weedy species in areas containing barberry and wiregrass, compared to uninfested areas. In other regions, weedy invasions have been shown to be facilitated by native shrubs that create high concentrations of available soil N (Maron and Connors 1996). The differences in soil nitrogen dynamics and earthworm densities associated with barberry and wiregrass invasions might have important implications for the management of invaded parks. First, the high NO− 3 levels in the soil might make these already invaded sites more susceptible to invasion by other weeds. Second,

even if the barberry and wiregrass were eliminated from a site, it is very likely that differences in the soils will persist for a prolonged period after that, which might significantly impede the restoration of native flora in the cleared sites.

Acknowledgements This work was funded by USDA grant no. is 95-371011701. We wish to thank Shana Groeschler, Michelle Hughes and Meglena Kourteva for their help in the field and the laboratory.

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