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Life-History Correlates of Plant Endemism in Longleaf Pine Ecosystems
Jennifer M. Fill, Shane M. Welch, Herrick Brown, Jayme L. Waldron, Alan S. Weakley, and Timothy A. Mousseau

Southeastern Naturalist, Volume 13, Issue 3 (2014): 484–492

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Southeastern Naturalist J.M. Fill, S.M. Welch, H. Brown, J.L. Waldron, A.S. Weakley, and T.A. Mousseau 2014 Vol. 13, No. 3 484 2014 SOUTHEASTERN NATURALIST 13(3):484–492 Life-History Correlates of Plant Endemism in Longleaf Pine Ecosystems Jennifer M. Fill1,*, Shane M. Welch2, Herrick Brown3, Jayme L. Waldron2, Alan S. Weakley1, and Timothy A. Mousseau1 Abstract - The herbaceous ground-layer community is a key target of restoration efforts in Pinus palustris (Longleaf Pine) ecosystems (LLPE). Identification of life-history traits that correlate with endemism could shed light on advantages or limitations of restoration strategies. We investigated whether dispersal and longevity (life cycle) correlate with species endemism in the LLPE. We characterized plant species as obligate associates of the LLPE (LLO), strong associates (LLP), or neither (N). We predicted that increased dependency on the LLPE (N < LLP < LLO) would correlate with decreased dispersal and greater longevity (longer life cycle). We failed to detect a significant relationship between LLPE affinity and dispersal ability. However, there was a significant positive relationship between LLPE affinity and longevity. We suggest that if dispersal is not limiting, LLO species restoration may depend on both soil properties and the precise use of fire to enhance their establishment and persistence. Introduction Ecological restoration activities target many different aspects of ecosystem structure and function. The overarching goal of these efforts is restoration of an ecosystem’s “species composition, community structure, ecological function, suitability of the physical environment to support the biota, and connectivity with the surrounding landscape” (Clewell and Aronson 2013). Typically, ecological restoration activities initially focus on vegetation because of the relationship between plants and ecosystem function (Hooper and Vitousek 1997, Tilman et al. 1996). Thus, a fundamental strategy of restoration is the re-establishment or rehabilitation of damaged or lost plant species native to the ecosystem (Bowles and Whelan 1994, Jordan et al. 1987, Palmer et al. 1997). In the southeastern US, Pinus palustris Mill. (Longleaf Pine) ecosystems (LLPE) have experienced widespread decline and are a current focus of restoration activities in the region. In particular, the recovery of the herbaceous ground-layer is a key restoration objective in these communities (Brockway et al. 2005, Walker and Silletti 2006). The LLPE ground-layer community exhibits some of the highest rates of endemism in North America (Sorrie and Weakley 2001). These plant 1Department of Biological Sciences, University of South Carolina Columbia, Sumter Street, Columbia, SC 29208. 2Department of Biological Sciences, Marshall University, 1 John Marshall Drive, Huntington, WV 25755. 3Andrew Charles Moore Herbarium, Department of Biological Sciences, University of South Carolina, Sumter Street, Columbia, SC 29208. 4Department of Biology, University of North Carolina Chapel Hill, 120 South Road, Chapel Hill, NC 27599. *Corresponding author - Manuscript Editor: Alvin R. Diamond, Jr. Southeastern Naturalist 485 J.M. Fill, S.M. Welch, H. Brown, J.L. Waldron, A.S. Weakley, and T.A. Mousseau 2014 Vol. 13, No. 3 species have characteristics conducive to fires that maintain the structure and function of the ecosystem (Beckage et al. 2009, 2011; Platt 1999). Restoration activities, therefore, target increases in species richness and successful establishment of rare species with limited geographic range, habitat specificity, or small population size (Palmer et al. 1997, Spellerburg 1992). There are two general approaches to LLPE groundcover restoration: engineered restoration, and passive restoration or spontaneous succession (Prach et al. 2001). In the former approach, species are actively reintroduced or rehabilitated through protocols such as direct seeding or planting (Bowles and Whelan 1994, Walker and Silletti 2006). The latter approach focuses on the creation or restoration of site conditions and habitat structure (Bakker et al. 2000) with the assumption that the creation of suitable site conditions is sufficient to promote the natural return of the native vegetation to fire-excluded land (the “Field of Dreams” hypothesis; Palmer et al. 1997, Prach et al. 2001, Suding et al. 2004). Restoration techniques include removal of hardwoods through herbicide application, tree felling, reinstatement of fire, or mechanical means (Outcalt and Brockway 2010, Walker and Silletti 2006) with the assumption that increased light and decreased competition will facilitate the repopulation or recovery of the groundcover, resulting in an influx of colonizing LLPE species. Development of these restoration strategies is enhanced by information on the life-history traits of target species. In both cases, the establishment or recovery of target species is used as the measure of success in restoring species composition (Bakker et al. 2000). Therefore, both approaches rely on species’ life-history traits related to establishment and persistence (Bakker et al. 2000, Pywell et al. 2003). For example, the success of the initial step depends on species availability. In spontaneous succession, establishment is controlled by propagule dispersal (dispersal in space) or seedbank persistence (dispersal in time; Bakker et al. 1996, 2000). A species cannot establish and reproduce successfully at a site if it cannot arrive via aboveground dispersal or presence in the seedbank. For engineered restoration, dispersal attributes may be important in cases where only a few individuals are planted in order to repopulate an area. Thus, poor dispersal can be a major limiting factor in ecosystem recovery and self-sustainability (Donath et al. 2003, Holl et al. 2000, White et al. 2004). Finally, the longevity of groundcover species must also be considered in both restoration approaches. Long-lived, or perennial species can serve as a source of species availability, for example, through vegetative reproduction, where remnant populations still exist and have not been extirpated by soil disturbance (Garcia and Zamora 2003). Restoration of groundcover composition in the LLPE, including numerous endemic species, has proven especially difficult (Walker and Silletti 2006). Identification of life-history traits that correlate with endemism could shed light on advantages or limitations of restoration approaches. In this study, we investigated whether dispersal and longevity (using life cycle as a proxy) may be particularly important factors in endemic species restoration in the LLPE. Our objective was to answer the question: Does the specificity of LLPE endemic species correspond to lower dispersal ability and increased longevity? Southeastern Naturalist J.M. Fill, S.M. Welch, H. Brown, J.L. Waldron, A.S. Weakley, and T.A. Mousseau 2014 Vol. 13, No. 3 486 Methods We obtained a reference list of species endemic to the Atlantic and Gulf Coastal Plains Floristic Province—at least 90% of all occurrences are restricted to this province (Sorrie and Weakley 2001; Fig.1). In this analysis, we used only those species (excluding Cyperaceae and Juncaceae) that occurred in at least one of the five ecoregions (out of 8 total ecoregions, subunits, or subregions; Sorrie and Weakley 2006) within the floristic province that most closely matched the historical distribution of the LLPE: the mid-Atlantic coastal plain, south Atlantic coastal plain, temperate central Florida peninsula, east Gulf coastal plain, and west Gulf coastal plain (Sorrie and Weakley 2006). Each species was characterized as an obligate associate of the LLPE (LLO), a strong associate of the LLPE (LLP), or neither (N; see description in Sorrie and Weakley 2006). We collected information on species’ dispersal traits using the following literature sources: Godfrey and Wooten (1981), Isely (1990), Flora of North America (1993+), and Weakley (2011). For dispersal, we rated each species on a scale of 1–3 for increasing dispersal-distance ability (Van der Pijl 1982, Willson and Traveset 2000): 1 = dispersal primarily by gravity, water, or ants; glabrous spikelets or legumes; absence of pappi, or, if present, scale-like or falling; abortive spores; 2 = dispersal primarily by vertebrates (fruits, berries); 3 = dispersal by wind; hairy legumes or spikelets; spores; pappi. If there was no mention in the literature of structures that particularly facilitated dispersal (e.g., black seed), or there was no mention of the propagule at all, we coded the species as no data. We used life cycle as an approximation of longevity (Weiher et al. 1999). Data on species longevity were obtained primarily from the USDA NRCS PLANTS Database (www.plants.usda. gov). We coded species as 1 (perennial) or 0 (annual, biennial, or combinations of annual, biennial, and perennial). Figure 1. The Atlantic and Gulf Coastal Plains Floristic Province. This province includes eight total subregions, five of which were included in the analy ses. Southeastern Naturalist 487 J.M. Fill, S.M. Welch, H. Brown, J.L. Waldron, A.S. Weakley, and T.A. Mousseau 2014 Vol. 13, No. 3 We fit generalized linear mixed models to dispersal and longevity using Proc GLIMMIX in SAS v. 9.3 (SAS Institute 2011). We coded LLP as the reference level in both analyses. Since there is currently no published comprehensive phylogeny for southeastern flora (A. Weakley, unpubl. data), we included family as a random factor. For dispersal, we ran a one-way ANOVA using the default unstructured covariance matrix and the Laplace approximation (Raudenbush et al. 2000) for parameter estimation. Analysis-of-fit statistics indicated that the data were moderately underdispersed (Pearson chi-square/df = 0.56). For longevity, we ran a binomial logistic regression with the logit link, the default unstructured covariance matrix, and the Laplace approximation for parameter estimation. Fit statistics indicated a good model fit to the data (Pearson chi-square/df = 0.7). We predicted that relative to LLP species, dispersal would be lower and longevity higher for LLO species, and that dispersal would be higher and longevity lower for N species. Results We used 129 families in each analysis. Out of 1320 species, we found dispersal information for 645 species and longevity (life cycle) information for 1300 species. Neither N nor LLO species were significantly different from LLP in their dispersal ability (n = 645; df = 2, 580; F = 0.16; P = 0.8512; Table 1). However, status was a significant predictor of longevity (n = 1300; df = 2, 1169; F = 9.96; P < 0.0001). LLO and LLP species are longer-lived than N species (Table 2). Table 2. Parameter estimates from binomial logistic regression (SAS Proc Glimmix) for effect of status on longevity (life cycle) of Longleaf Pine ecosystem groundcover species. We used degree of association with Longleaf Pine as the reference category. LLO = obligate associates of Longleaf Pine ecosystems. N = neither an obligate associates nor strong associates of Longleaf Pine ecosystems. Solutions for fixed effects Effect Estimate Standard error df t value Pr > |t| Intercept 4.9601 0.9245 128 5.37 less than 0.0001 LLO -0.6021 0.4470 1169 -1.35 0.1782 N -1.3943 0.4577 1169 -3.05 0.0024 Table 1. Parameter estimates from one-way ANOVA (SAS Proc GLIMMIX) for effect of status (endemism) on dispersal ability of Longleaf Pine ecosystem groundcover species. We used degree of association with Longleaf Pine as the reference category. LLO = obligate associates of Longleaf Pine ecosystems. N = neither an obligate associates nor strong associates of Longleaf Pine ecosystems. Solutions for fixed effects Effect Estimate Standard error df t value Pr > |t| Intercept 2.1347 0.1326 62 16.10 less than 0.0001 LLO -0.0400 0.1120 580 -0.36 0.7226 N -0.0037 0.1195 580 -0.03 0.9750 Southeastern Naturalist J.M. Fill, S.M. Welch, H. Brown, J.L. Waldron, A.S. Weakley, and T.A. Mousseau 2014 Vol. 13, No. 3 488 Discussion Plant species’ dispersal mode and longevity are important considerations in LLPE restoration and management practices. In this study, we sought to detect a relationship between these two attributes and ecosystem affinity, rather than to obtain an absolute measure of dispersal or longevity. Therefore, it is beyond the scope of this study for us to draw inferences regarding the absolute dispersal or longevity of species based on our results. Although we failed to detect an expected decrease in dispersal ability with increasing LLPE affinity, we cannot conclude that LLO species are necessarily either broad or restricted dispersers. In fact, Kirkman et al. (2004) found that LLPE species associated with non-disturbed Longleaf Pine reference sites displayed restricted absolute dispersal distances (see also Hilton and Boyd 1996). In contrast, our results indicated that dispersal may not be more limiting to endemic species than to those less strongly affiliated with the LLPE. However, we found that stronger affinity corresponded to a longer life cycle. Our results provide a basis for discussion of potential restoration implications. Studies on successful establishment of LLPE species, including Aristida spp. (wiregrass) and several wildflowers, have suggested that ecological similarity of source and destination conditions play a large role in determining success (Noel et al. 2011, Norcini et al. 1998). These studies inform the generally accepted view of specialization in the LLPE ground-layer species to environmental conditions (Carr et al. 2010) and species variation across environmental gradients (Walker and Silletti 2006). Persistence of LLO species (via a longer life cycle) over the widespread geographic range of the LLPE would enhance their modification of the environment (e.g., via allelopathy or other belowground interactions; Bever 2003, Casper and Castelli 2007, Fischer et al. 1994, Stover et al. 2012, Van der Putten 2003), and stabilize the ecosystem (Latham 2003). Indeed, current research points to the important role of vegetation–mycorrhizae relationships in grasslands and the implications of vegetation–soil relationships for restoration and management activities (Casper et al. 2008, Johnston and Crossley 2002, Ohsowski et al. 2012). In particular, there is a growing body of literature on vegetation–soil feedbacks and their role in successional processes, especially in grasslands (Bever 2003, Kardol et al. 2006, Klironomos 2002, van der Putten 2003). Unfortunately, we were unable to measure seedbank longevity as an essential means of dispersal in time, or even as a mode of persistence via fire avoidance or tolerance. Seedbanking is a particularly important consideration for restoration approaches that rely on spontaneous succession. Seedbank longevity has proven extremely difficult to measure reliably, and there are very few data available (Carol Baskin, University of Kentucky, Lexington, KY, pers. comm.). The ability to long-term seedbank may mitigate the negative effects of limited availability of suitable post-dispersal establishment sites by allowing species (particularly shortlived species) to persist locally until more sites become available. It is possible the relative longevity of LLO species would render a seedbank less important if their persistence contributes to stable conditions. However, recent seed-burial studies indicate that LLPE plants in the Asteraceae, Poaceae, and Orobanchaceae may form Southeastern Naturalist 489 J.M. Fill, S.M. Welch, H. Brown, J.L. Waldron, A.S. Weakley, and T.A. Mousseau 2014 Vol. 13, No. 3 at least short-term persistent seedbanks, and some members of the Fabaceae may even form longer-term seedbanks (Coffey and Kirkman 2006, Kaeser and Kirkman 2012). For example, seeds of Erythrina spp. (coral tree) collected in summer and sown in autumn did not emerge until the following autumn (H. Brown, pers. observ.). Thus, we are unsure of the relative importance of seedbanking in affecting restoration success of LLO versus LLP or N species. Furthermore, future studies might also address the role of tradeoffs between relative dispersal ability and viable seed production among LLO, LLP, and N species. Although dispersal ability may not limit the successful establishment of endemic species, seed viability may be a contributing factor to endemism (Lavergne et al. 2004). For this study, we were limited in the number of traits we could include due to a dearth of data and lack of standards in data collection. As more life-history data become available, restoration efforts would greatly benefit from research that extends our efforts to include multiple traits. To this end, we strongly advocate the development of methods for data standards. Much of the information was qualitative, and it was difficult to discern the comparability of quantitative measurements. In an age where technology is rapidly facilitating the accessibility of records, we encourage discussion of data standards that will enhance our ability to conduct rigorous research. 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