Oecologia DOI 10.1007/s00442-015-3408-1 COMMUNITY ECOLOGY - ORIGINAL RESEARCH Environmental tolerances of rare and common mangroves along light and salinity gradients Emily M. Dangremond1,2 · Ilka C. Feller2 · Wayne P. Sousa1 Received: 19 November 2014 / Accepted: 21 July 2015 © Springer-Verlag Berlin Heidelberg 2015 Abstract Although mangroves possess a variety of responded less to variation in light and salinity. However, at morphological and physiological adaptations for life in a high salinity, its relative growth rate was low at every light stressful habitat, interspecific differences in survival and level and none of these plants flushed leaves. As predicted, growth under different environmental conditions can shape the rare species, Pelliciera rhizophorae, was the most sen- their local and geographic distributions. Soil salinity and sitive to environmental stressors, suffering especially high light are known to affect mangrove performance, often mortality and reduced growth and quantum yield under the in an interactive fashion. It has also been hypothesized combined conditions of high light and medium–high salin- that mangroves are intrinsically shade intolerant due to ity. That it only thrives under shaded conditions represents the high physiological cost of coping with saline flooded an important exception to the prevailing belief that halo- soils. To evaluate the relationship between stress toler- phytes are intrinsically constrained to be shade intolerant. ance and species distributions, we compared responses of seedlings of three widespread mangrove species and one Keywords Mangrove · Distribution · Rarity · Stress narrow endemic mangrove species in a factorial array tolerance · Pelliciera rhizophorae of light levels and soil salinities in an outdoor laboratory experiment. The more narrowly distributed species was expected to exhibit a lower tolerance of potentially stress- Introduction ful conditions. Two of the widespread species, Avicennia germinans and Lumnitzera racemosa, survived and grew Narrow endemic and widespread potentially invasive spe- well at low–medium salinity, regardless of light level, but cies represent opposite ends of the continuum of species performed poorly at high salinity, particularly under high distribution–abundance patterns, and both present major light. The third widespread species, Rhizophora mangle, challenges to the design of effective environmental man- agement and conservation efforts. How species distribu- tion patterns at different spatial scales are shaped and Communicated by Amy Freestone. maintained by life history, demographic, genetic, and envi- ronmental processes is a fundamental focus of research Electronic supplementary material The online version of this in ecology and evolutionary biology (Rabinowitz 1981; article (doi:10.1007/s00442-015-3408-1) contains supplementary Kruckeberg and Rabinowitz 1985; Gaston 1994, 2003; material, which is available to authorized users. Gaston and Kunin 1997; Rosenzweig and Lomolino 1997). * Emily M. Dangremond Recognizing that assessments of species rarity are scale [email protected] dependent (Harper 1981), Rabinowitz (1981; see also Rabi- nowitz et al. 1986; Gaston 1994) distinguished different 1 Department of Integrative Biology, University of California, 3040 VLSB MC 3140, Berkeley, CA 94720‑3140, USA categories of rare species. These were defined by seven out of the eight combinations of three distribution–abundance 2 Present Address: Smithsonian Environmental Research Center, 647 Contees Wharf Road, Edgewater, MD 21037, characteristics: geographic range (wide or narrow), habi- USA tat specificity (broad or restricted), and local abundance 1 3 Oecologia (somewhere dense or everywhere sparse). Any species that It has previously been proposed that halophytes inhabit- has a narrow geographic range, lives in a restricted number ing the intertidal zone are shade intolerant, which explains of habitats, or typically lives at low density exhibits a form why mangrove forests typically lack an understory layer of of rarity. Common species comprise the eighth combina- plant species that mature and reproduce beneath the closed tion: they have wide geographic ranges and occupy a broad canopy (Janzen 1985; Lugo 1986; Snedaker and Lahmann range of habitats, in which they are generally abundant. 1988). The high metabolic costs of tolerating salt and inun- These eight classifications were presented as simplified, dation are hypothesized to preclude the evolution of mor- heuristic divisions of what is really a continuum of distri- phological and physiological traits that allow growth and bution–abundance patterns. reproduction in a low-light environment. However, the rare Species whose populations are typically sparse and neotropical mangrove Pelliciera rhizophorae (Tetramerista- patchily distributed tend to have narrower geographical ceae) often occurs as a reproducing understory species in ranges than common species (Hanski 1982; Gotelli and forests where Rhizophora mangle (Rhizophoraceae) domi- Simberloff 1987; Collins and Glenn 1990; Gaston and nates the canopy, indicating that Pelliciera may be shade Lawton 1990; Hanski et al. 1993; Boulangeat et al. 2012). tolerant throughout its life. Pelliciera is largely restricted Among the hypothesized explanations for the restricted to sites of low to moderate soil salinity, where it typically distributions of rare endemics compared to common wide- grows in partial shade beneath a mixed-species canopy of spread species is that the former have smaller fundamental adult conspecifics and Rhizophora mangle (Jiménez 1984; niches, possessing more limited ranges of physiological tol- E. Dangremond, pers. obs.). erance or more specialized resource or other habitat require- In this study, we investigated the independent and poten- ments (Kruckeberg and Rabinowitz 1985; Boulangeat et al. tially interacting effects of two environmental factors, 2012; Slatyer et al. 2013). If these requisite conditions and salinity and light, on the establishment, early growth, and resources are of limited spatial extent, or are otherwise diffi- survival of four mangrove species. We compared Pelliciera cult to access, then the distribution and abundance of a spe- rhizophorae to three mangrove species that are common cies that depends on them will be constrained as well. This throughout their native ranges: two neotropical species, study tests the hypothesis that widespread species are more Rhizophora mangle (Rhizophoraceae) and Avicennia ger- stress tolerant than narrow endemics, examining the spe- minans (Acanthaceae), and the Indo-West Pacific species, cific case of mangrove trees, a taxonomically diverse col- Lumnitzera racemosa (Combretaceae). All three have also lection of taxa that have evolved convergently to live under become established, either accidentally or intentionally, as the stressful edaphic conditions at the interface of tropical reproducing populations outside their native ranges (see marine and terrestrial environments. We compared the per- “Discussion”). The study focused on the responses of seed- formances of four species of seedlings establishing across lings in the first 12 weeks of life to the tested environmen- an array of experimental environmental conditions that are tal factors, because variation in seedling demography is a typical of natural mangrove habitats. major driver of forest dynamics and structure (Smith 1992; Mangrove forests offer an excellent system in which to McKee 1995; Krauss et al. 2008). We expected light and investigate the relationship between the stress tolerance salinity to exert a synergistic impact on mangrove seed- of species and their spatial distributions, as these forests ling performance (Ball 2002; López-Hoffman et al. 2006, occupy a habitat that is physically challenging to both plant 2007), with the interactive impact being strongest for the establishment and growth (Ball 1988a; Smith 1992; Krauss rare species Pelliciera rhizophorae. et al. 2008), and component tree species range from rare endemic to common, and may include non-native invasives. The tidally influenced mangrove habitat is characterized by Materials and methods flooded, hypoxic, and saline soils. Adaptations that allow plants to live in such severe edaphic conditions are varied, Study species but have evolved in 16 different plant families (Tomlinson 1986; Hogarth 2007). These adaptations include morpho- As noted above, three of the study species are native to the logical traits such as aerial roots, lenticels, and pneumato- Atlantic–East Pacific (AEP) biogeographic region, and one phores that aerate the rhizosphere in hypoxic soils, and to the Indo-West Pacific (IWP) region (Tomlinson1986 ). regulation of tissue salt concentrations by specialized salt- Rhizophora mangle occurs from northern Florida to south- excreting leaf glands or exclusion of salt at root surfaces. ern Brazil on the Atlantic coast of North America, and Physiological and growth responses to gradients in salin- from Mexico to Peru on the Pacific coast. It also inhab- ity vary among mangrove species and can ultimately affect its the shores of West Africa, from Senegal to Angola. Its their distributions and abundances (Ball 1988a, b, 2002; propagules are large; the average fresh mass ( 1SE) of ± Smith 1992; Ball and Pidsley 1995; Krauss et al. 2008). propagules used in this experiment was 14.5 g ( 0.40) ± 1 3 Oecologia (corresponding to a dry mass of 8.1 g), and were collected 80.31°W). The experiment had a three-way factorial design,