Grantee Research Project Results
Final Report: Impact of Invasive Plants on Abundance and Fitness of Salamanders
EPA Grant Number: R828902Title: Impact of Invasive Plants on Abundance and Fitness of Salamanders
Investigators: Blossey, Bernd , Maerz, John C. , Liebherr, James K. , Nuzzo, Victoria
Institution: Cornell University
EPA Project Officer: Packard, Benjamin H
Project Period: August 3, 2001 through August 2, 2004
Project Amount: $446,959
RFA: Exploratory Research to Anticipate Future Environmental Issues (2000) RFA Text | Recipients Lists
Research Category: Ecological Indicators/Assessment/Restoration , Water , Aquatic Ecosystems
Objective:
With increasing numbers of invasive plant species spreading through agricultural and natural areas in North America, economic and natural resource losses grow exponentially. At present, we lack any systematic approach or methodology to assess the impact of the more than 5,000 known naturalized plant species on native ecosystems. The spread of nonindigenous plant species coincides with declining amphibian populations; however, few studies have attempted to link these two phenomena (Brown, et al., 2005; Maerz, et al., 2005a).
The main objective of our project was to test the following three hypotheses regarding nonnative plant invasions of deciduous hardwood forests:
1. Nonnative plant invasions are associated with reduced native plant cover and diversity.
2. Nonnative plant invasions are associated with reduced invertebrate abundance (invertebrates being prey for woodland salamanders).
3. Nonnative plant invasions are associated with reduced fitness and abundance of red-backed salamanders (Plethodon cinereus).
An additional objective of our project was to assess whether plethodontid salamanders are effective bioindicators of invasive species impacts on forest food webs.
The objectives of our study were met by locating 15 mature hardwood forest sites with clearly defined invasion fronts (five sites invaded by each of the focal plant species). The sites were distributed through central New York and eastern Pennsylvania, and logistical and natural constraints created a biased distribution of sites among the three plant types. Sites invaded by garlic mustard (Alliaria petiolata), Japanese barberry (Berberis thunbergii), and Japanese stilt-grass (Microstegium vimineum) were clustered in central New York, northeastern Pennsylvania, and southeastern Pennsylvania, respectively. At each site, we established 30 coverboard monitoring plots, 15 in the invaded habitat and 15 in the noninvaded habitat of each site (monitoring plot specifications, sampling techniques, and data forms are available to download in pdf at http://www.invasiveplants.net Exit ). Vegetation communities were sampled three times annually over the study period, and litter invertebrate communities were sampled three times during one year of the study. Coverboards in plots were used to monitor larger invertebrates (earthworms, spiders, centipedes, millipedes, and ground beetles) and salamander populations. We checked coverboards every 2-3 weeks in Year 1 of the project, and, based on capture rates in Year 1, every 2-3 weeks during the spring and autumn in subsequent years. We used individual mark-recapture techniques to study salamanders to conduct robust analyses of salamander abundance and efficacy of different monitoring approaches.
Summary/Accomplishments (Outputs/Outcomes):
Changes in Native Plant Communities Associated with Nonnative Plant Invasions
We found equivocal support for the hypothesis that nonnative plant invasions were associated with reduced coverage or diversity of native plants. Native cover was lower in invaded habitats at 8 of 15 sites; however, at the 2 sites with the highest native cover, native cover was greater in the invaded habitat, and across all 15 sites, native plant cover in invaded and noninvaded habitats was highly positively correlated (r = 0.776, P < 0.001). This suggests that any potential effects of nonnative plant invasions on native plant cover were small relative to other, larger scale factors driving variation in native plant cover.
The volume of the soil organic layer varied greatly among sites and within sites, was significantly lower in invaded habitats at 13 of 15 sites (Figure 1). Among the Alliaria and Berberis sites, estimates of mean annual active earthworm biomass were greater in invaded habitats at 8 of 10 sites, and organic layer volume was significantly negatively correlated with earthworm biomass (Figure 2).
Figure 1. Organic Layer Volume in Adjacent Habitats Not Invaded and Invaded by Nonnative Plants A. petiolata, B. thunbergii, or M. vimineum. Bars show means, error bars show ± 2 standard error, and stars indicate sites where means between adjacent habitats are significantly different.
Figure 2. Correlations Between Mean Estimated Earthworm Biomass and Mean Soil Organic Layer Volume Among Invaded and Noninvaded Habitats From five A. petiolata and five B. thunbergii Invaded Hardwood Forests. Linear regression lines also are shown.
Principal components analysis using percent cover of nonnative plants and native plant functional groups (graminoids, annual herbs, perennial herbs, ferns, and woody shrubs and seedling trees) indicated three distinct plant communities among our 15 sites: an annual and perennial herb and fern community in the noninvaded habitats of Alliaria sites, a woody community (primarily shrubs in the family Ericaceae) in the noninvaded habitats of Berberis and Microtegium sites, and a native graminoid and invasive plant community. Principal components analysis also showed nonnative plant and native graminoid cover were positively associated with nonnative earthworm biomass, whereas native woody, herb, and fern cover was negatively associated with earthworm biomass (Figure 3).
Figure 3. Principle Components Analysis Projection Graph of Factor 1 and 2 Loadings for Percent Cover of Plant Groups and Nonnative Earthworm Biomass and Mean Factor Scores for Invaded and Noninvaded Habitats. Values in parentheses indicate proportion of variance explained by that factor. Plant groups are inv = nonnative, gram = native graminoids (grasses and sedges), ann = native annual herbs, perr = native perennial herbs, fern = native ferns, and woody = native shrubs (primarily Ericaceae) and seedling trees. Circles are A. petiolata sites, and squares are B. thunbergii sites. White symbols are noninvaded habitats and grey symbols are invaded habitats.
Most northern forests of North America lacked earthworms prior to European settlement of those regions (Bohlen, et al., 2004). Earthworms of European and, more recently, Asian origin are rapidly invading these forests over a wide geographic area and dramatically reducing soil organic layers and affecting nutrient cycling, soil food webs, and understory plant communities (reviewed by Bohlen, et al., 2004). In addition to our study, several other studies have linked the plant invasions of northern forests to the increased biomass of exotic earthworms (Kourtev, et al., 1998; Kourtev, et al., 1999). Earthworm invasions may alter competitive relationships among native plant species and between native and nonnative plant species by altering nutrient availability, disrupting mycorrhizae, and interacting with herbivore pressures.
Changes in Invertebrate Communities Associated with Nonnative Plant Invasions
As we have just presented, one major change in invertebrate communities associated with nonnative plant invasions is an increase in nonnative earthworm biomass. Including earthworms, we identified a diverse array of nonnative invertebrates common across all 15 study sites, some of which were important in salamander diets (Maerz, et al., 2005b). We measured the abundance of native and nonnative insects common in salamander diets from leaf litter samples from four Alliaria site, and found that across sites and habitats, spring and autumn nonearthworm arthropod abundance among habitats and sites declined as organic layer volume declined. This is consistent with other studies showing negative effects of earthworm invasions soil arthropod abundance (Migge, 2001; Scheu, et al., 2003; Migge, et al., in review).
Nonnative Plant Invasions and Salamander Fitness and Abundance
For our analysis of plant invasion impacts on salamander abundance, we used Year 1 mark-recapture abundance estimates for invaded and noninvaded habitats for the five Alliaria and five Berberis sites. We did not use data from multiple years because they are still being analyzed to determine whether mark-recapture activities affect long-term capture rates of animals, and we did not include data from Microstegium sites because Year 1 data for the two sites established late currently are being proofed and analyzed. Within sites, salamander abundance did not differ significantly between plant and noninvaded habitats. Salamander abundance differed significantly between Alliaria sites in central New York and Berberis sites in northeastern Pennsylvania, and within both regions, salamander abundance was not significantly correlated with native or nonnative plant cover but was significantly positively correlated with soil organic layer volume (Figure 4). This indicates that earthworm impacts on the organic layer of forest soils are contributing to declines in salamander abundance.
Figure 4. Relationship Between Mean Salamander Abundance and Autumn Litter Volume Among Hardwood Forest Sites. Shaded symbols indicate habitats invaded by nonnative plants and linear regression lines are shown.
Our results suggest that changes in plant communities, including plant invasions and invertebrate abundance within and among forests, are, at least in part, the result of invasions by nonnative earthworms. Because invasive plants are associated with high earthworm biomass, they tended to be associated with reduced cover of some native plants, organic layers, and arthropods. However, plant invasions appear to have been conspicuous symptoms rather than the root causes of those conditions. The apparent negative impact of earthworm invasions on salamander abundance was surprising given their reported importance in salamander diets (Maerz, et al., 2005b) and demonstrates how complex invasive species effects can be. However, the pattern is consistent with other studies that link salamander declines to reductions in soil organic layers (Pough, et al., 1987; Petranka, et al., 1993). Our study supports the work of others who propose soil organic layers are a positive index of forest ecosystem integrity or health.
Efficacy of Using Plethodontids to Study Invasions and Forest Food Webs
Our study has shown that plethodontid salamander abundance can be affected by exotic species impacts on forest soils and soil food webs. We found that salamander abundance can vary regionally, but regional biases can be controlled for by experimental design and subsequent analyses. The mark-recapture techniques we used were effective but extremely labor (and therefore cost) intensive. In addition to training and time to conduct individual mark-recapture, there is significant time required for data entry and analyses. Because of the time and expertise required, it is necessary to determine whether specific protocols or less intensive monitoring techniques are sufficiently robust to use in monitoring.
Salamander abundance under coverboards was highest and the difference among sites most apparent from mid-April through mid-May and mid-September through late-October. From June through August, when conditions were hotter and drier, numbers of salamanders captured were low and consequently differences among sites were not apparent. Within the first year, the average number of salamanders captured per survey during peak activity (early April-early June and early September-late October) was highly correlated with all abundance estimates requiring mark-recapture (Table 1). Other studies also indicate that count data from cover area searches reasonably index salamander abundance (Smith and Petranka, 2000).
Table 1. Correlation Coefficients Among Different Measurements of Salamander Abundance
Measure |
Avg. no. captured per plot per survey |
First year closed population estimate |
Robust estimate of spring abundance |
Robust estimate of autumn abundance |
Avg. no. marked per plot within first year |
0.984 |
0.981 |
0.917 |
0.915 |
Avg. no. captured per plot per survey |
----- |
0.986 |
0.921 |
0.924 |
First year closed population estimate |
----- |
0.956 |
0.966 |
|
Robust estimate of first year spring abundance |
----- |
0.946 |
||
It appears that less labor-intensive monitoring of salamander populations using count data are adequate for evaluating relationships between salamander abundance and environmental variables. Count surveys will allow for comparative surveys among large numbers of sites and geographic areas; however, count surveys may be insufficient for evaluating mechanisms driving population change. Cross-sectional studies of populations may be sufficient for estimating population structure and life history parameters such as growth or fecundity (Marvin, 2001). We suggest that an ideal design for large scale monitoring studies using plethodontids use count surveys among large numbers of sites and more intense mark-recapture studies among a random subset of sites.
Conclusions
Our study adds substantially to a growing body of empirical evidence showing nonnative earthworm invasions are a major agent of change in northern deciduous forests (Bohlen, et al., 2004). Plant invasions of forest understories appear symptomatic of larger plant community shifts in response to nonnative earthworm invasions, and earthworm invasions appear capable of causing declines in vertebrate populations even when those vertebrates utilize earthworms as prey. Our study shows that when measured at appropriate times, plethodontid abundance can be an effective measure of forest soil health.
References:
Bohlen PJ, et al. Non-native invasive earthworms as agents of change in northern temperate forests. Frontiers in Ecology and The Environment 2004;2:427-435.
Brown CJ, Blossey B, Maerz JC, Joule SJ. Invasive plant and experimental venue affect tadpole performance. Biological Invasions 2006;8(2):327-338.
Kourtev PS, Ehrenfeld JG, Huang WZ. Effects of exotic plant species on soil properties in hardwood forests on New Jersey. Water, Air and Soil Pollution 1998;105:493-501.
Kourtev PS, Huang WZ, Ehrenfeld JG. Differences in earthworm densities and nitrogen dynamics in soils under exotic and native plant species. Biological Invasions 1999;1:237-245.
Maerz JC, Blossey B, Nuzzo V. Green frogs show reduced foraging success in habitats invaded by Japanese knotweed. Biodiversity and Conservation 2005a;14(12):2901-2911.
Maerz JC, Karuzas JM, Madison DM, Blossey B. Introduced invertebrates are important prey for a generalist predator. Diversity and Distributions 2005b;11(1):83-90.
Marvin GA. Age, growth, and long-term site fidelity in the terrestrial plethodontid salamander Plethodon kentucki. Copeia 2001:108-117.
Migge S. The effect of earthworm invasion on nutrient turnover, microorganisms and microarthropods in Canadian aspen forest soil. In: University of Calgary, Calgary, 2001, p 133.
Migge S, McLean MA, Heneghan L, Maerz JC. The influence of invading earthworms on indigenous fauna in ecosystems previously uninhabited by earthworms. Biological Invasions (in review, 2006).
Petranka JW, Eldridge ME, Haley KE. Effects of timber harvesting on southern Appalachian salamanders. Conservation Biology 1993;7:363-370.
Pough FH, Smith EM, Rhodes DH, Collazo A. The abundance of salamanders in forest stands with different histories of disturbance. Forest Ecology and Management 1987;20:1-9.
Scheu S, et al. The soil fauna community in pure and mixed stands of beech and spruce of different age: trophic structure and structuring forces. Oikos 2003;101:225-238.
Smith CK, Petranka JW. Monitoring terrestrial salamanders: repeatability and validity of area-constrained cover object searches. Journal of Herpetology 2000;34:547-557.
Journal Articles on this Report : 1 Displayed | Download in RIS Format
Other project views: | All 1 publications | 1 publications in selected types | All 1 journal articles |
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Type | Citation | ||
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Nuzzo V, Maerz J, Blossey B. Earthworm Invasion as the Driving Force Behind Plant Invasion and Community Change in Northeastern North American Forests. CONSERVATION BIOLOGY 2009;23(4):966-974. |
R828902 (Final) |
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Supplemental Keywords:
earthworm invasions, forests soils, mark-recapture, facilitation, invasional meltdown, invasive species, salamanders, invertebrates,, RFA, Scientific Discipline, Geographic Area, Ecosystem Protection/Environmental Exposure & Risk, amphibians, State, Ecological Risk Assessment, Biology, Exp. Research/future, Futures, emerging environmental problems, bioindicator, biodiversity, forest, biopollution, vegetation, amphibian, salamanders, invasvie species, exploratory research, invasive species, ecological dynamics, invasive plants, amphibian bioindicator, futures researchRelevant Websites:
http://www.invasiveplants.net Exit
Progress and Final Reports:
Original AbstractThe perspectives, information and conclusions conveyed in research project abstracts, progress reports, final reports, journal abstracts and journal publications convey the viewpoints of the principal investigator and may not represent the views and policies of ORD and EPA. Conclusions drawn by the principal investigators have not been reviewed by the Agency.