Research Article |
Corresponding author: Samantha J. Worthy ( sjworthy@ucdavis.edu ) Academic editor: Moritz von der Lippe
© 2022 Samantha J. Worthy, Travis D. Marsico, Rima D. Lucardi, Lauren E. Whitehurst, Kevin S. Burgess.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Worthy SJ, Marsico TD, Lucardi RD, Whitehurst LE, Burgess KS (2022) Variation in plant traits and phylogenetic structure associated with native and nonnative species in an industrialized flora. NeoBiota 77: 101-123. https://doi.org/10.3897/neobiota.77.87307
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Industrialized sites are hotspots for nonnative species because of continuous anthropogenic disturbance and nonnative propagule rain resulting from hitchhikers exchanged through global trade. Investigating plant traits and the phylogenetic structure of species at initial ports of entry can contribute to our understanding of how species are introduced to, assembled into, and survive at industrialized sites, which can also inform how susceptible these sites are to nonnative plant invasions. To compare native and nonnative species, we asked three questions: 1) Are plant traits differentially associated with species nativity (native versus nonnative)? (2) Do these traits have phylogenetic signals? and (3) What is the phylogenetic structure of each trait for native and nonnative species? We collected, identified, and vouchered 170 angiosperm species within the Garden City Terminal at the Port of Savannah, Georgia, USA, the largest container terminal in North America. Species nativity was derived from the literature, as were traits of pollination syndrome, dispersal syndrome, duration, and growth habit. Pearson’s Chi-squared tests were used to determine if traits were differentially associated with species nativity. Phylogenetic signal, along with mean pairwise distance (MPD) and mean nearest taxon distance (MNTD), were used to assess the degree of phylogenetic relatedness of native and nonnative species with each trait. Nonnative species showed a significant association with multiple pollination syndromes. Native species were significantly associated with perennial duration and zoophily pollination syndrome. All traits possessed a phylogenetic signal, and the anemophily pollination syndrome was significantly clustered for both native and nonnative species. Still, most other traits differed in their phylogenetic structure pattern based on the nativity. Overall, findings suggest that the environment is filtering for native and nonnative species that possess traits promoting introduction and survival at this industrialized point-of-entry. They also suggest that nonnative species trait differences partition available niches that promote their introduction to the site. More research is needed at industrialized sites to inventory and monitor the floristic community, investigate the establishment and spread probabilities of nonnative species, and prevent and mitigate nonnative species risks and impacts.
global trade, industrialized flora, phylogenetic structure, species nativity, trait associations
Approximately 13% (47,840) of all vascular plant species have the potential to become nonnative species in new environments (
Industrialized sites experience extraordinarily high levels of human activity and disturbance, creating environmental constraints that limit plant occupancy (
In an industrialized flora (
Uncertainty surrounding which traits are linked to species’ success in new environs limits understanding of how invasion happens and how to predict it (
Analyses of phylogenetic signal and structure can be used to understand which traits facilitate the assembly of native and nonnative species in industrialized communities. For instance, the presence of phylogenetic signals would indicate the degree to which phylogenetic similarity predicts trait similarity in the community (
Industrialized sites, such as the Garden City Terminal, the primary container handling facility of the Port of Savannah, present an ideal laboratory to investigate traits and phylogenetic distributions of native and nonnative species under continuous, active disturbance. At the Garden City Terminal’s green spaces,
This study was conducted at the Port of Savannah, Georgia, USA (32°07.3'N, 81°08.4'W). At the port, we specifically focused on the Garden City Terminal (GCT), the main container-handling terminal that spans 485.6 hectares and is primarily composed of impervious surfaces (i.e., asphalt) interspersed with small green spaces for water run-off (
The flora was sampled from six green spaces (4.51 ha, ~1% of the GCT) on four separate occasions between August 2015 and February 2017 to capture seasonal changes in the flora (see
Information on traits was gathered from the literature (Fig.
The proportion of all species in the dataset in each category of each trait investigated. The flora consists of 170 species comprised of 110 native and 60 nonnative species. Black bars represent the proportion of native species and gray bars represent the proportion of nonnative species in all figure panels.
Pearson’s Chi-squared tests were used to determine if traits were differentially associated with species nativity, with the null hypothesis assuming independence of traits and nativity. For analyses exhibiting significant differences, we performed post hoc analyses considering all combinations of trait categories and species nativity using the chisq.posthoc.test package (
DNA barcoding of the flora was performed to build a phylogenetic tree for analyses and for confirmation of species identifications (
Sequences of the rbcL and matK gene regions were aligned separately using multiple alignment and fast Fourier transform (MAFFT v 7.471) with the FFT-NS-2 algorithm (
We quantified phylogenetic signals in the four traits to determine the degree to which the phylogenetic tree estimates the similarity of species traits. Phylogenetic signals were determined by quantifying the parsimony Sankoff score calculated from the distribution of trait categories on the phylogeny (
We also calculated the mean pairwise distance (MPD) and mean nearest taxon distance (MNTD) using the “picante” package (
For MPD and MNTD, observed values were compared to null distributions generated by randomizing the names of the taxa on the phylogenetic distance matrices 999 times to calculate standardized effect sizes (SES) and P-values (quantiles). Negative SES values (obs.z < 0) and low quantiles (obs.p < 0.05) for both MPD and MNTD indicated species in a group are phylogenetically clustered, with smaller phylogenetic distances among the species in the group than expected (Swenson, 2014). Positive SES values (obs.z > 0) and high quantiles (obs.p > 0.95) indicated species in a group are phylogenetically over-dispersed, with greater phylogenetic distances among species in the group than expected (
Of the 170 species in this study flora, 110 were native to the southeastern region of the USA, and 60 were nonnative (Appendices S1 and S3). Significant differences in association were found between two of the four traits and species nativity (Fig.
Representation of association found between traits and species nativity (native and nonnative). Significant associations (bolded) were determined from Pearson’s Chi-squared tests with post hoc analyses. The sign of association between each trait category and nativity are given, negative (–) and positive (+). Trait categories with significant phylogenetic structure are also displayed. Trait categories with significant phylogenetic clustering are denoted by ^. Trait categories with significant phylogenetic over-dispersion are denoted by *.
Trait | Trait Category | Native | Nonnative |
---|---|---|---|
Dispersal Syndrome | Anemochory | + ^ | – |
Autochory | + | – ^ | |
Polychory | – * | + * | |
Pollination Syndrome | Anemophily | + ^ | – ^ |
Multiple | – | + | |
Selfing | – | + * | |
Zoophily | + ^ | – | |
Duration | Multiple | – ^ | + |
Perennial | + ^ | – | |
Growth Habit | Forb | + ^ | – ^ |
Graminoid | – ^ | + ^ | |
Multiple | – ^ | + |
Dispersal syndrome was not significantly associated with species nativity (χ2 = 3.29, df = 4, P = 0.51). However, there were still differences in the signs of association between trait categories and species nativity. Native species had positive associations with anemochory and hydrochory dispersal syndromes but negative associations with polychory and zoochory dispersal syndromes. Nonnative species had opposite associations with the dispersal syndrome categories as native species. Overall, polychory (native: 17%; nonnative: 29%) contributed the most to the total χ2 score. There was also no significant association between growth habit and species nativity (χ2 = 0.59, df = 3, P = 0.90). The graminoid category contributed the most (native = 18%, nonnative = 32%) to the overall χ2 score.
We quantified the observed parsimony Sankoff score for each trait and compared it to a null distribution of parsimony scores to determine significance. We found significant phylogenetic signals for all four traits (pollination and dispersal syndromes, growth habit, and duration), with close relatives generally sharing more similar traits than expected by chance (Table
Phylogenetic signals using parsimony Sankoff scores. All P-values were significant (< 0.05).
Traits | Sankoff | n | P |
---|---|---|---|
Dispersal Syndrome | 84 | 139 | <0.01 |
Pollination Syndrome | 69 | 142 | <0.01 |
Duration | 81 | 159 | <0.01 |
Growth Habit | 60 | 158 | <0.01 |
Phylogenetic structure within each of the categories of each of the four traits. MPD.obs.z is the standardized effect size of the mean pairwise distance measurement. MNTD.obs.z is the standardized effect size of the mean nearest taxon distance measurement. Standardized effect sizes were calculated from comparisons of observed values to null distributions generated by randomizing the names of the taxa in the phylogenetic distance matrices 999 times. P-values in bold are significant. Significant phylogenetic clustering is denoted by ^ (P < 0.05). Significant phylogenetic over-dispersion is denoted by * (P > 0.95).
Trait | ntaxa | MPD.obs.z | P | MNTD.obs.z | P |
---|---|---|---|---|---|
Dispersal Syndrome | |||||
Anemochory | 24 | -7.19 | 0.001^ | -2.40 | 0.012^ |
Anemochory.NN | 14 | 0.27 | 0.572 | -0.92 | 0.178 |
Autochory | 11 | -0.73 | 0.226 | 0.46 | 0.679 |
Autochory.NN | 6 | -1.95 | 0.049^ | -1.88 | 0.034^ |
Hydrochory | 12 | 0.98 | 0.855 | -0.84 | 0.199 |
Hydrochory.NN | 4 | 0.52 | 0.660 | -0.79 | 0.767 |
Polychory | 18 | 0.93 | 0.812 | 1.99 | 0.972* |
Polychory.NN | 15 | 2.23 | 0.997* | -0.38 | 0.365 |
Zoochory | 22 | -1.47 | 0.080 | -1.24 | 0.110 |
Zoochory.NN | 13 | 0.80 | 0.788 | -0.99 | 0.169 |
Pollination Syndrome | |||||
Anemophily | 18 | 0.51 | 0.683 | -2.72 | 0.004^ |
Anemophily.NN | 9 | -4.25 | 0.001^ | -2.19 | 0.016^ |
Multiple | 18 | -0.41 | 0.322 | 0.66 | 0.746 |
Multiple.NN | 24 | 0.22 | 0.542 | -1.14 | 0.130 |
Selfing | 4 | 0.70 | 0.721 | 1.23 | 0.883 |
Selfing.NN | 9 | 2.04 | 0.994* | 0.49 | 0.676 |
Zoophily | 47 | -5.47 | 0.001^ | -1.98 | 0.024^ |
Zoophily.NN | 13 | -1.71 | 0.057 | 0.43 | 0.657 |
Duration | |||||
Annual | 27 | -1.23 | 0.124 | -1.57 | 0.060 |
Annual.NN | 25 | 1.18 | 0.885 | -1.27 | 0.115 |
Multiple | 22 | -3.72 | 0.002^ | 0.20 | 0.576 |
Multiple.NN | 16 | 1.30 | 0.927 | -0.41 | 0.334 |
Perennial | 52 | -0.23 | 0.383 | -1.95 | 0.025^ |
Perennial.NN | 17 | -0.201 | 0.377 | 0.16 | 0.556 |
Growth Habit | |||||
Forb | 56 | -7.34 | 0.001^ | -2.34 | 0.009^ |
Forb.NN | 29 | -2.00 | 0.035^ | -1.15 | 0.131 |
Graminoid | 18 | -4.69 | 0.001^ | -4.75 | 0.001^ |
Graminoid.NN | 15 | -6.87 | 0.001^ | -3.85 | 0.001^ |
Multiple | 20 | -2.95 | 0.007^ | -1.23 | 0.112 |
Multiple.NN | 10 | -0.64 | 0.253 | -0.12 | 0.446 |
Tree | 5 | -1.77 | 0.052 | -0.37 | 0.360 |
Tree.NN | 2 | -0.57 | 0.268 | -0.64 | 0.246 |
Vine | 2 | -1.27 | 0.101 | -1.23 | 0.106 |
Vine.NN | 1 | NA | NA | NA | NA |
This research is part of an ongoing, innovative research initiative to quantify and assess plant communities within industrialized initial points-of-entry sites (
Native species in the flora at the Garden City Terminal of the Port of Savannah showed significant, positive associations with perennial duration and zoophily pollination syndrome (Table
Nonnative species only showed a significant, positive association to multiple pollination syndromes (Table
As highlighted above, we found differences in the traits associated with native versus nonnative species, notably, significant differences in associations of nativity with pollination syndrome and duration (Table
We also found phylogenetic signals for all four traits assessed in this study. In other words, closely related species shared more similar traits more often than expected by chance in the industrialized flora at the Garden City Terminal at the Port of Savannah (Table
Overall, the categories of traits showing a significant phylogenetic structure in the flora, for the most part, differed from those that had significant relationships with species nativity (Table
Determining what makes communities invasion-prone has been elusive. There are intuitive arguments for environmental filtering, whereby nonnative plants should have traits similar to native ones, and empty niche or niche partitioning, whereby nonnative plants should have different traits from native ones (
Despite the small amount of green space at the Garden City Terminal (~1% of the land area at the industrialized site), this industrialized flora is unique with a large number and proportion of nonnative species (
This research highlights differences in duration along with pollination and dispersal syndromes associated with species nativity that deserve consideration and further investigation in future studies of industrialized floras. It also highlights, through phylogenetic analyses, how highly disturbed sites may filter for species with traits such as anemophily pollination syndrome, regardless of species nativity. Finally, this research suggests the influence of environmental filtering and niche partitioning on the similarity and dissimilarity, respectively, of nonnative and native species traits that may have allowed their introduction and survival at this site. More research, cooperation, and coordination are needed at industrialized and urbanized sites to more adequately investigate nonnative species’ establishment and spread probabilities (
The GenBank accession numbers for all successfully sequenced rbcL and matK DNA barcodes can be found in Suppl. material
The authors thank those who have assisted with collections and cooperated with us to conduct this research: Milton A. King, Rebecca Y. Rhinehart, Lynne F. Brennan, and Lisa Beth M. Brown (USCBP), Dr. William Kauffman (retired), Calvin Schuler (USDA, APHIS), Charles “Chip” Bates (retired) and Chris Barnes (Georgia Forestry Commission), Steven C. Hughes (University of Georgia Herbarium [GA]), Jarron K. Gravesande (University of Georgia and Arkansas State University), Jennifer N. Reed (Arkansas State University), Derek Robertson (USDA FS), Captain Guy Buck and the GPA Police Department, and Mr. Gordon Hammer (retired) and the staff of the Client Relations Center of GPA. We are grateful to Moritz von der Lippe, who was our managing editor for this manuscript, along with Estibaliz Palma and one anonymous reviewer whose comments greatly improved our contribution. This research was supported by the USDA Forest Service, Southern Research Station to Arkansas State University (15JV11330129032 to TDM) and to Columbus State University (15JV11330129031 to KSB).
Author contributions
SJW, TDM, RDL, and KSB were involved in the conception of the idea. SJW, LEW, RDL, and KSB collected data. TDM identified the species morphologically. LEW prepared specimens for DNA barcode analysis, SJW analyzed data, and SJW wrote the original draft with edits, comments, and approvals from all authors.
Species included in this study, listed alphabetically, along with their traits
Data type: docx file
Explanation note: Species included in this study, listed alphabetically, along with their traits. All species are represented by vouchers stored at Arkansas State University Herbarium (
Sequencing and collection information for the species in this study
Data type: docx file
Explanation note: Sequencing and collection information for the species in this study, listed alphabetically. The collection number and GenBank accession number for each sequence are presented below. Sequences downloaded from Barcode of Life Data Systems (BOLD;
Phylogenetic tree depicting genetic relationships among 159 species of the flora at the Port of Savannah, Savannah, Georgia, USA, with available sequences
Data type: docx file
Explanation note: Phylogenetic tree depicting genetic relationships among 159 species of the flora at the Port of Savannah, Savannah, Georgia, USA, with available sequences. The phylogeny was generated using maximum likelihood methods in the “phangorn” package (