Allocation of biomass and net primary productivity of mangrove forests along environmental gradients in the Florida Coastal Everglades, USA

Highlights

• We study patterns of biomass and total NPP of mangrove ecotypes in the Everglades.

• Vegetation patterns of mangroves represent the outcome of environmental gradients.

• Riverine mangroves allocate most of the total NPP to aboveground (69%).

• Scrub mangroves show the highest biomass allocation and production to belowground.

• Production to biomass ratios were lower in riverine relative to scrub mangroves.

Abstract

Vegetation patterns of mangroves in the Florida Coastal Everglades (FCE) result from the interaction of environmental gradients and natural disturbances (i.e., hurricanes), creating an array of distinct riverine and scrub mangroves across the landscape. We investigated how landscape patterns of biomass and total net primary productivity (NPP_T), including allocation in above- and below-ground mangrove components, vary inter-annually (2001–2004) across gradients in soil properties and hydroperiod in two distinct FCE basins: Shark River Estuary and Taylor River Slough. We propose that the allocation of belowground biomass and productivity (NPP_B) relative to aboveground allocation is greater in regions with P limitation and permanent flooding. Porewater sulfide was significantly higher in Taylor River (1.2 ± 0.3 mM) compared to Shark River (0.1 ± 0.03 mM) indicating the lack of a tidal signature and more permanent flooding in this basin. There was a decrease in soil P density and corresponding increase in soil N:P from the mouth (28) to upstream locations (46–105) in Shark River that was consistent with previous results in this region. Taylor River sites showed the highest P limitation (soil N:P > 60). Average NPP_T was double in higher P environments (17.0 ± 1.1 Mg ha⁻¹ yr⁻¹) compared to lower P regions (8.3 ± 0.3 Mg ha⁻¹ yr⁻¹). Root biomass to aboveground wood biomass (BGB:AWB) ratio was 17 times higher in P-limited environments demonstrating the allocation strategies of mangroves under resource limitation. Riverine mangroves allocated most of the NPP_T to aboveground (69%) while scrub mangroves showed the highest allocation to belowground (58%). The total production to biomass (P:B) ratios were lower in Shark River sites (0.11 yr⁻¹); whereas in Taylor River sites P:B ratios were higher and more variable (0.13–0.24 yr⁻¹). Our results suggest that the interaction of lower P availability in Taylor River relative to Shark River basin, along with higher sulfide and permanent flooding account for higher allocation of belowground biomass and production, at expenses of aboveground growth and wood biomass. These distinct patterns of carbon partitioning between riverine and scrub mangroves in response to environmental stress support our hypothesis that belowground allocation is a significant contribution to soil carbon storage in forested wetlands across FCE, particularly in P-limited scrub mangroves. Elucidating these biomass strategies will improve analysis of carbon budgets (storage and production) in neotropical mangroves and understanding what conditions lead to net carbon sinks in the tropical coastal zone.

Introduction

Primary productivity represents the major input of carbon and biological energy into world’s ecosystems and can be considered as an integrative measure of ecosystem functioning (McNaughton et al., 1989, Sala and Austin, 2000). Mangrove forests dominate tropical and subtropical coastlines and are among the most productive marine ecosystems in the world, ranking second in terms of net primary productivity (NPP) only to coral reefs (Duarte and Cebrian, 1996). Mangrove forests produce organic carbon well in excess of ecosystem respiration and are considered important sites for carbon burial (∼10%) and carbon export (∼40%) to adjacent coastal waters, indicating their significant contribution to carbon biogeochemistry in the coastal zone (Twilley et al., 1992, Duarte and Cebrian, 1996, Jennerjahn and Ittekkot, 2002, Bouillon et al., 2008). Global estimates indicate that mangrove coverage is approximately 137,760 km², which represents 0.7% of total tropical forests of the world (Giri et al., 2011); yet these forested wetlands are a significant site of carbon sequestration within the coastal zone (Twilley et al., 1992, Bouillon et al., 2008, Breithaupt et al., 2012).

The productivity of mangroves represents the outcome and interactions of several factors that operate at distinct global, regional, and local scales (Twilley, 1995). Climate and the relative role of regional geophysical processes (river input, tides, and waves) within a coastal landform are the dominant forcing functions that control the basic patterns of mangrove forest structure and function (Thom, 1982, Twilley, 1995). At the local scale, variation in topography and hydrology within a coastal landform influence the distribution of soil resources and abiotic regulators, and along with hydroperiod, produce gradients resulting in the development of distinct ecological types of mangroves such as riverine, fringe, basin, scrub, and overwash forests (Lugo and Snedaker, 1974, Twilley and Rivera-Monroy, 2009). The magnitude and interaction of these environmental gradients including regulators (i.e., soil salinity, sulfide), resources (e.g., light, nutrients), and hydroperiod (e.g., frequency, duration, and depth of flooding) define a constraint envelope that determines mangrove productivity within a coastal setting (Twilley and Rivera-Monroy, 2005).

Mangrove species adjust morphological and physiological traits in response to availability of nutrient resources, concentration of regulators, and hydroperiod conditions along these environmental gradients in the intertidal zone (Twilley and Rivera-Monroy, 2009, Krauss et al., 2008). For example, long-term fertilization studies of Rhizophora mangle found in scrub stands in different neotropical regions suggest that these forests respond positively to P additions increasing aboveground net primary productivity (NPP_A) and shifting resource allocation from roots to shoots (Koch and Snedaker, 1997, Feller et al., 2003a, Feller et al., 2003b, Lovelock et al., 2004, Lovelock et al., 2006). Salinity has also been recognized to control the spatial distribution and productivity of mangrove species, particularly in drier coastal settings (Lugo and Snedaker, 1974, Pool et al., 1977, Cintron et al., 1978, Castañeda-Moya et al., 2006). Moreover, changes in above- and belowground biomass and productivity in mangroves also respond to changes in hydroperiod (Krauss et al., 2008). Higher frequency of inundation can maximize growth and aboveground productivity (Twilley et al., 1986, Krauss et al., 2006), while permanent flooding can stimulate fine root biomass allocation due to more soil reducing conditions and sulfide accumulation (Castañeda-Moya et al., 2011).

Understanding the allocation of carbon to above- and belowground biomass and productivity along these environmental gradients is significant to estimating global carbon budgets of mangrove ecosystems (Bouillon et al., 2008). Current estimates indicate that litterfall (NPP_L), along with wood (NPP_W) and root production (NPP_B), account for ∼31%, 31%, and 38%, respectively, of the total net productivity (NPP_T) on a global basis (Bouillon et al. 2008). These estimates underscore the significant contribution of NPP_W and NPP_B to NPP_T of mangrove forests worldwide. Recent summaries indicate few examples of simultaneous measurements of both the aboveground components of NPP (NPP_A = NPP_L + NPP_W) and belowground components (NPP_B) to accurately estimate NPP_T of neotropical mangroves along natural environmental gradients. There are few long-term studies that test the temporal and spatial variation in carbon allocation to above- and belowground production (NPP_B:NPP_A ratio) of mangrove forests, and/or the production:biomass ratio of these coastal wetland forests. Studies of belowground components are particularly lacking in the neotropics (see Castañeda-Moya et al., 2011, Donato et al., 2011, Rivera-Monroy et al., 2013). Our study will contribute to a better understanding of the landscape patterns of NPP_T and carbon allocation of neotropical mangrove forests responding to distinct gradients in environmental settings.

We present a comprehensive long-term (2001–2004) analysis of community structure, above- and belowground biomass and NPP_T, and soil properties and hydroperiod of mangrove forests across two distinct basins of the Florida Coastal Everglades (FCE) landscape. We focused on Shark River Estuary and Taylor River Slough to test the generality that allocation patterns of biomass and NPP of mangroves respond to the interaction of environmental gradients resulting in distinct productivity trends across the southern Everglades (Ewe et al., 2006, Rivera-Monroy et al., 2011). We hypothesized that the allocation of belowground biomass and NPP_B relative to aboveground allocations is greater in the Taylor River sites compared to the Shark River sites, reflecting mangrove vegetation strategies associated with P limitation and permanent flooding conditions. We addressed the following questions: (1) What is the long-term inter-annual variation in community structure and NPP of mangrove forests across a P-limited landscape as modified by different conditions of hydroperiod? (2) What is the production to biomass (P:B) ratio across mangrove sites in response to different nutrient and hydroperiod gradients? (3) What is the NPP_T in mangrove sites across nutrient and hydroperiod gradients, and what is the relative contribution of NPP_B to NPP_T across these gradients? Estimates of both belowground biomass and productivity for our six mangrove sites were not determined during this study, but were obtained from the literature (Castañeda-Moya et al., 2011). This information is used in the context of this study to estimate the total (above- and belowground) biomass and productivity of mangroves in the FCE.