Research Article |
Corresponding author: Kathryn L. Amatangelo ( kamatang@brockport.edu ) Academic editor: Sidinei Magela Thomaz
© 2018 Kathryn L. Amatangelo, Lee Stevens, Douglas A. Wilcox, Stephen T. Jackson, Dov F. Sax.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Amatangelo KL, Stevens L, Wilcox DA, Jackson ST, Sax DF (2018) Provenance of invaders has scale-dependent impacts in a changing wetland ecosystem. NeoBiota 40: 51-72. https://doi.org/10.3897/neobiota.40.28914
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Exotic species are associated with a variety of impacts on biodiversity, but it is unclear whether impacts of exotic species differ from those of native species with similar growth forms or native species invading disturbed sites. We compared presence and abundance of native and exotic invaders with changes in wetland plant species diversity over a 28-year period by re-surveying 22 ponds to identify factors correlated with observed changes. We also compared communities found within dense patches of native and exotic emergent species with similar habits. Within patches, we found no categorical diversity differences between areas dominated by native or exotic emergent species. At the pond scale, the cover of the exotic grass Phragmites australis best predicted change in diversity and evenness over time, likely owing to its significant increase in coverage over the study period. These changes in diversity and evenness were strongest in younger, less successionally-advanced ponds. Changes associated with cover of P. australis in these ponds were not consistent with expected diversity decreases, but instead with a dampening of diversity gains, such that the least-invaded ponds increased in diversity the most over the study period. There were more mixed effects on evenness, ranging from a reduction in evenness gains to actual losses of evenness in the ponds with highest invader cover. In this wetland complex, the habit, origin and invasiveness of species contribute to diversity responses in a scale- and context-dependent fashion. Future efforts to preserve diversity should focus on preventing the arrival and spread of invaders that have the potential to cover large areas at high densities, regardless of their origin. Future studies should also investigate more thoroughly how changes in diversity associated with species invasions are impacted by other ongoing ecosystem changes.
wetland, invasion, exotic, Phragmites , Typha , scale, richness
The impacts of exotic species on native species and plant communities are diverse. In many cases, exotic species have caused or contributed to extinction of native species (
In the first debate,
The second debate involves the expectation that invasions by exotic species typically lead to local biodiversity decline. While this expectation has been contested for some time (
While these two debates (species’ provenances and invader-driven change in local diversity) have often been considered separately, they are, in fact, related. Intrinsic differences between native and exotic invaders could determine whether particular invasions are more likely to lead to decreases or increases in local-scale biodiversity. The answers to both debates are also likely to be influenced by the ways in which changes in biodiversity are measured (
Determining whether native and exotic invaders have categorical differences in how they impact ecological communities and determining whether these impacts cause decreases in some measure of biodiversity is often difficult. The most straightforward comparisons will be possible when both native and exotic invaders have arrived or increased in abundance over similar time-frames, with relatively long periods of study. The Miller Woods section of the Indiana Dunes National Lakeshore is uniquely suited for a long-term comparison of the impacts of native and exotic invaders. This area has an extensive network of over 150 shallow ponds (Suppl. material
In this study, we evaluated how native and exotic invader abundances are related to changes in vegetation richness, evenness and compositional similarity over 28 years. We examined these relationships for five invaders (two exotic, two native and one native-exotic hybrid) individually and in combination. We also considered whether other environmental variables such as pond age (and successional stage) can help explain the changes observed in these communities over the 28 years that have elapsed between surveys. Furthermore, we examined how one native-exotic hybrid, one exotic invader and two native dominants (one of which is an invader) are related to the richness and evenness of plant species at sub-pond spatial scales. These comparisons allowed us to consider the likelihood that the potential influence of native and exotic invaders differs within this wetland complex and to determine whether either set of invaders decreases biodiversity at local scales.
The over 150 shallow ponds in the Miller Woods section of the Indiana Dunes National Lakeshore formed in relatively discrete rows as Lake Michigan receded to its present level (
We conducted resurveys of vascular plants and aquatic macrophytes in 22 ponds originally sampled in 1982 (
We subsampled 2010 and 2011 quadrats down to 20 quadrats per pond to provide equivalent sampling effort to the 1982 dataset for some analyses, including richness and evenness. A total of 20 quadrats were selected to best replicate the
We updated the names of taxa from the 1982 sample to reflect modern taxonomy. Species within some genera (e.g. Persicaria, Nuphar) had been split or joined in the intervening time, so we analysed those taxa at their lowest resolution. Other taxa contained species with variable morphology that were sampled in a vegetative state; those species could not be definitively identified, so we combined those species into morphotaxa.
Digitised GIS layers, created by the National Park Service in 2006, were used to calculate the area and perimeter of each pond. Average pond depth (cm) was calculated by averaging depths from all sampled quadrats. We designated ponds as ‘young’ (Wilcox and Simonin’s row 1 and 2, 300 to < 2,000 years old) or ‘old’ (rows 3–5, 2,000 to 3,000 years old), based on their ages and distance to shore (
We used single classification G-tests and replicated tests for goodness-of-fit to identify taxa that were significantly increasing or decreasing in quadrat frequency of occurrence within and across ponds (
Species were classified as “Invaders” in our study if they both increased significantly in frequency of occurrence over the past 28 years across the wetland complex (Suppl. material
To evaluate whether provenance or habit predicted direction of change over the 28 years as evaluated by Gtests (increasers, decreasers or no change), we performed tests for association using the Fisher Exact test with the Freeman-Halton extension. To evaluate the effect of growth form, we categorised native taxa into emergent and submersed/floating habits, based on where the majority of their foliage is typically found. To evaluate the effect of provenance, we split our data into native or exotic/hybrid species.
Importance values (IV) were calculated for each species in each sampling period and pond. Importance values were calculated on subsampled data by summing relative frequency and relative cover. An NMDS ordination of ponds in both time periods was performed using species with summed importance values of at least 0.05 across the dataset (out of a possible maximum of 2). NMDS was performed using the Sorensen distance matrix in PCORD using the ‘slow and thorough’ option, with random starting coordinates and 50 runs (
We calculated pond-scale species richness and Pielou’s evenness on subsampled data for all taxa in each time period (
We calculated proportional changes in richness and evenness for each pond to serve as response variables in the analyses of community change. We did not calculate a cover-change metric due to differences in sampling months and estimation methods between the 1982 and 2010/2011 surveys. As we were interested in the impact of each invader on community change over 28 years, we performed five mixed-model ANOVAs to evaluate how each invader contributed to richness and evenness change. We used the invaders’ cover values in 2010/2011 for these analyses. In each model, the fixed predictors were the target invader’s cover in 2010/2011, a combined metric summing the cover of the other four invaders, pond age and interactions between those three factors. Interactions were removed if they were not significant (p >0.05). We also modelled the relationship between Phragmites australis and richness and evenness change in young ponds using simple linear regression.
We investigated whether combined invader cover in 2010/2011 was explained by other continuous pond characteristics (shoreline disturbance, average depth or area) using a stepwise regression model. The best model was selected via forward selection and lowest AIC score. We compared pond area covered by each of our invaders in 2010/2011 across the two pond ages via a Wilcoxon test.
Prior to ANOVA and regression analyses, 2010/2011 biotic proportion cover variables and proportion shoreline disturbance were arcsine(sqrt)-transformed and depth and area were log-transformed to approximate normality.
A subset of species in this wetland complex, regardless of their status as invaders, form dense emergent, often clonal patches that may (but do not necessarily) exclude other species. To evaluate the effects of monodominant emergent taxa, we performed additional sampling in 2011 in patches dominated by each of four taxa: three invaders (Typha × glauca, a native-exotic hybrid, Phragmites australis, an exotic and Cephalanthus occidentalis, a native) and one additional native species (Schoenoplectus acutus). We chose Schoenoplectus acutus rather than our other native invader (Persicaria hydropiperoides) because S. acutus has a more similar habit to the invasive grass species (Phragmites australis). Each of the four selected taxa forms monodominant stands, which we define as dense, largely monospecific emergent patches of vegetation, in many shallow ponds in the Miller Woods wetlands. We selected six ponds that each contained at least two of our focal species (Suppl. material
For 0.5-m2 patch quadrat data, we calculated richness and Pielou’s evenness of each quadrat using individuals. Quadrat-level richness and evenness were compared amongst patch types using nested, mixed-model ANOVAs. Pond and transects nested in ponds were included as random variables and patch type (monodominant species) was a fixed variable – we did not have enough replication to consider the patch-by-pond interaction. Variables were log-transformed before analysis to satisfy assumptions of normality. When the overall model was significant (p < 0.05), we used Tukey’s HSD test to evaluate significant differences between patch types.
To evaluate the effect of monodominant species on richness accumulation, we calculated sample-based rarefaction curves for all quadrats sampled in each patch type (Typha × glauca, Phragmites australis, Cephalanthus occidentalis, Schoenoplectus acutus and reference patches) to evaluate study-wide richness. Analytically estimated richness and standard errors from randomisation trials were selected at 37 quadrats - the number of quadrats sampled for Cephalanthus occidentalis. We also calculated richness at an intermediate scale by analytically estimating richness at 12 quadrats for each patch type/pond combination where at least 12 quadrats were sampled. We compared 12-quadrat level richness estimates in a mixed model ANOVA that included patch type as a fixed effect and pond as a random effect.
Three exotic and seven native taxa significantly increased in frequency of occurrence over the 28 years of this study (Suppl. material
Pond-scale richness was significantly predicted by year (p = 0.0287) and the interaction between pond age and year (p = 0.0016, Table
Richness and evenness of pond macrophytes in 1982 (light grey) and 2010/2011 (dark grey). Medians, first and third quartiles, interquartile ranges and outliers are shown. Richness and eveness differences were evaluated via ANOVAs (see Table
Results of mixed-model ANOVAs explaining pond-scale total species richness and species evenness between two time periods (1982, 2010/2011) and two categorical age groups of ponds (young, old). Pond was included as a random effect.
Response | Source | DF | F Ratio | P |
---|---|---|---|---|
Total richness | Age | 1 | 0.720 | 0.4062 |
Year | 1 | 5.559 | 0.0287* | |
Age * Year | 1 | 13.240 | 0.0016* | |
Species evenness | Age | 1 | 0.085 | 0.7734 |
Year | 1 | 1.674 | 0.2104 | |
Age * Year | 1 | 3.122 | 0.0925† |
The final NMDS ordination of 22 sites in each time period, based on species importance values, had a stress of 12.984 after 399 iterations (Figure
NMDS ordination of 22 sites in two time periods (1982 and 2010/2011) based on species’ importance values. Grey symbols and arrows represent “old” ponds, black symbols and arrows indicate “young” ponds. Arrows pair the same site in two time periods, the arrowhead indicates the later (2010/2011) sample. Dashed lines indicate biplots of variables with r >0.300. Species centroids of invader and monodominant taxa are indicated. PHRAUS: Phragmites australis, SCHACU: Schoenoplectus acutus, LYTSAL: Lythrum salicaria, POLHYD: Persicaria hydropiperoides, CEPOCC: Cephalanthus occidentalis, TYPHA: Typha × glauca.
Invaders reached their greatest cover in ponds that were altered by railroads or roads (Suppl. material
Of the five species identified as ‘invaders’ in this system, only Phragmites australis cover was related to changes in richness (Suppl. material
Relationship between Phragmites australis cover (as proportion of area sampled) and the proportional change in richness (A) and evenness (B) in young ponds. The solid line indicates a significant (p <0.05) relationship and dashed line indicates p <0.10.
Conceptual figure illustrating three possible ways invasive species abundance could negatively correlate with changes in diversity. A At high abundance, invaders could cause declines in diversity over time. B At low invader abundance, diversity increases through natural processes, but at high abundance, invaders prevent arrival of new species. C A combined model, where richness increases in the absence of invaders and invader presence above a threshold causes declines in diversity over time. Note that these hypothesised relationships may not be linear but may include threshold processes.
Native species in this system were more likely to decrease or have no change than increase in frequency (7 of 35 species were increasers, while all three exotics were increasers, Suppl. material
The four monodominant taxa (Cephalanthus occidentalis, Schoenoplectus acutus, Phragmites australis, Typha × glauca) altered their abiotic environments similarly. Each covered about 70% of the quadrat area, blocking 73–88% of the light reaching the water surface (Suppl. material
Richness at three scales in patches dominated by Cephalanthus occidentalis (C), Schoenoplectus acutus (S), Typha × glauca (T), Phragmites australis (P) or reference areas (R). A 0.5 m2 quadrats B aggregated pond-level richness (12 quadrats) C Mao-Tau sampling-richness relationships, with the number of ponds each type was sampled in indicated in parentheses. Error bars indicate standard deviation at 37 quadrats. Patch type (monodominant species) was a significant predictor of pond-level richness as evaluated via a mixed-model ANOVA (F = 3.81, p = 0.035, model R2 = 0.58).
This study provides insight into two major unresolved questions in invasion biology. Can species impacts be predicted based on their provenance? Do species invasions, regardless of provenance, decrease biodiversity at local scales? In this wetland complex, monodominant emergent invaders have likely altered the trajectory of pond community change over 28 years but in ways that are not fully consistent with an expectation of biodiversity loss or of categorical variation by provenance. Invader cover is only minimally correlated with changes in evenness over time and, rather than decreasing richness, invader cover (Phragmites australis) is correlated with suppression of richness gains in some ponds. Further, in this study, invaders that entered the community recently (“exotic invaders”) or were present at low levels historically but increased following human disturbance (“native invaders”), do not show strong categorical differences in how they impact these communities with respect to changes in diversity at local, quadrat scales. However, exotic and native invaders altered temporal trajectories of richness in ponds over 28 years.
Cover of Phragmites australis in ponds during the resurveys was negatively correlated with proportional change in species richness in young ponds, but this was not because of a loss of species over time. Indeed, in our study, average net richness of species in ponds increased between surveys. To understand this apparent contradiction, it is useful to consider three qualitative ways that a negative correlation between invader cover and change in biodiversity could manifest in communities that have shown a net increase in richness between surveys (Fig.
Regardless of the mechanism, however, these patterns raise an important challenge for ecological studies of long-term change – namely, determining the relative influence of invaders versus other changes in the environment in driving change in diversity. In the meta-analysis by
This lack of evidence for significant loss of diversity, in spite of pronounced invasions, not just in young ponds but across our broad set of ponds, might be due to several factors – in addition to the possibility of pond succession, described above. Many uncommon taxa are still present in this wetland complex and no ‘common’ taxa were extirpated from the ponds we surveyed during the 28-year period. It is possible that seasonal and between-year variations in water levels may provide opportunities for continued survival or regeneration of species with differing requirements, maintaining some degree of balance between invading emergent stands and diverse sedge meadows, as elsewhere in the Great Lakes (
Native and exotic invaders do not show consistent differences in how they impact these ecosystems across all biodiversity measures or spatial scales. At the scale of entire ponds, the exotic invader Phragmites australis had the greatest impact on change in richness over time. However, Phragmites australis has a pond-scale impact not because of unique within-patch processes, but because of the number and size of patches it had invaded. At the scale of individual habitat patches, there was no evidence that native and exotic monodominant species had categorically different effects on plant diversity. Although neither natives nor exotics showed categorical differences at this scale, species accumulation measures showed that both natives and exotic invaders were associated with reduced diversity relative to uninvaded reference areas. In other studies, both T. × glauca and P. australis are reported to decrease plant richness in freshwater wetlands (
Historical disturbance in this wetland complex may have provided opportunities for invaders to colonise and spread, ultimately leading to different species accumulation trajectories in the recent past. As a consequence, it is difficult to disentangle the extent to which patterns observed are driven by the invaders or instead driven by disturbance, per se, which may have also benefited the invaders, i.e. it is difficult to know if the invaders are ‘drivers’ or ‘passengers’ of observed change. We do know that invader abundance in these ponds is positively correlated with shoreline alterations and hydrological disturbances; this is particularly true in younger ponds, where the large differences in invader cover are apparent between ponds with and without disturbed shorelines. Differences in the responses observed in younger and older ponds are consistent with the important differences these ponds have with respect to their natural history but might also reflect differences in susceptibility to the influences of invasion with successional stage. In both pond types, however, the initial creation of roads and railroads may have altered the environment in a manner known to be favourable for emergent wetland vegetation, including the three exotic invaders studied here (
Given the highly dynamic nature of wetland habitats, it is possible that invader-induced suppressions of increases in richness could have long-term negative impacts on biodiversity in these wetlands, particularly since there can be time lags before some impacts are manifest (
Although our results cannot resolve the debates regarding the importance of species provenance or the impact of exotic species on local diversity, they do provide an important point of reference for these debates and highlight the potential interactions between them. The recent meta-analysis by
We thank Chrissie Bodznick, Stephanie Crook, Maggie Goter, Josh Jacobs, Abby Percifeld, Liz Ryan and Hallie Stallman for assistance in field and laboratory. We appreciate Joy Marburger and the rest of the staff at Indiana Dunes National Lakeshore for providing support, housing and assistance. We thank Noel Pavlovic, Paul Bollinger, Dan Mason and Robin Scribailo for assistance with plant identification. The manuscript benefitted from thoughtful reviews by Jason D. Fridley, Uwe Starfinger, Sidinei M. Thomaz and one anonymous reviewer. Data are available for download at Pangaea Data Publisher. This research was supported by grants DEB-0949525 and DEB-0949308 from the National Science Foundation.
Supplementary tables and figures