Life stage influences the resistance and resilience of black mangrove forests to winter climate extremes 1, 1 1 2 MICHAEL J. OSLAND, RICHARD H. DAY, ANDREW S. FROM, MEAGAN L. MCCOY, 3 4 JENNIE L. MCLEOD, AND JEFFREY J. KELLEWAY

1U.S. Geological Survey, Lafayette, Louisiana 70506 USA 2McLemore Consulting at U.S. Geological Survey, Lafayette, Louisiana 70506 USA 3McLeod Consulting at U.S. Geological Survey, Lafayette, Louisiana 70506 USA 4Plant Functional Biology and Climate Change Cluster, University of Technology Sydney, Broadway, New South Wales 2007 Australia

Citation: Osland, M. J., R. H. Day, A. S. From, M. L. McCoy, J. L McLeod, and J. J. Kelleway. 2015. Life stage influences the resistance and resilience of black mangrove forests to winter climate extremes. Ecosphere 6(9):160. http://dx.doi.org/ 10.1890/ES15-00042.1

Abstract. In subtropical coastal wetlands on multiple continents, climate change-induced reductions in the frequency and intensity of freezing temperatures are expected to lead to the expansion of woody plants (i.e., mangrove forests) at the expense of tidal grasslands (i.e., salt marshes). Since some ecosystem goods and services would be affected by mangrove range expansion, there is a need to better understand mangrove sensitivity to freezing temperatures as well as the implications of changing winter climate extremes for mangrove-salt marsh interactions. In this study, we investigated the following questions: (1) how does plant life stage (i.e., ontogeny) influence the resistance and resilience of black mangrove (Avicennia germinans) forests to freezing temperatures; and (2) how might differential life stage responses to freeze events affect the rate of mangrove expansion and salt marsh displacement due to climate change? To address these questions, we quantified freeze damage and recovery for different life stages (seedling, short tree, and tall tree) following extreme winter air temperature events that occurred near the northern range limit of A. germinans in North America. We found that life stage affects black mangrove forest resistance and resilience to winter climate extremes in a nonlinear fashion. Resistance to winter climate extremes was high for tall A. germinans trees and seedlings, but lowest for short trees. Resilience was highest for tall A. germinans trees. These results suggest the presence of positive feedbacks and indicate that climate-change induced decreases in the frequency and intensity of extreme minimum air temperatures could lead to a nonlinear increase in mangrove forest resistance and resilience. This feedback could accelerate future mangrove expansion and salt marsh loss at rates beyond what would be predicted from climate change alone. In general terms, our study highlights the importance of accounting for differential life stage responses and positive feedbacks when evaluating the ecological effects of changes in the frequency and magnitude of climate extremes.

Key words: Avicennia germinans; climate change; coastal wetlands; extreme climatic event; freeze damage; mangrove; marsh; ontogeny; plant-climate interactions; positive feedback; range expansion; woody plant encroachment.

Received 23 January 2015; revised 7 April 2015; accepted 1 May 2015; published 28 September 2015. Corresponding Editor: J. A Langley. Copyright: Ó 2015 Osland et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. http://creativecommons.org/licenses/by/3.0/ E-mail: [email protected]

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INTRODUCTION marsh plant dominance. However, small increas- es in extreme minimum winter air temperatures There is a need to better understand and can lead to landscape-scale changes in ecosystem preparefortheecologicalandconservation structure and function as mangrove forests implications of future changes in climate ex- replace salt marshes (Osland et al. 2013, Cav- tremes (Jentsch et al. 2007, Glick et al. 2011, IPCC anaugh et al. 2014; Osland et al., in press). From a 2013, Stein et al. 2014). Potential ecosystem functional perspective, mangrove and salt marsh responses to climate extremes are diverse, rang- plants are both considered foundation species ing from abrupt state changes that produce major because they create habitat, modulate ecosystem alterations in ecosystem structure and function to functions, and support entire ecological commu- minor events with negligible ecological implica- nities (sensu Dayton 1972, Bruno and Bertness tions (Smith 2011). Research that improves our 2001, Ellison et al. 2005, Angelini et al. 2011). understanding of the resistance and resilience of Despite many similarities, there are several ecosystems to climate extremes plays an espe- functional and structural differences between cially important role in helping future-focused mangrove and salt marsh ecosystems (Day et environmental managers better gauge and plan al. 2013). Given the potential for poleward for potential climate change impacts (Lloret et al. mangrove range expansion in response to climate 2012, Hoover et al. 2014, Ruppert et al. 2015). In change and the expected concomitant changes in this study, we examine the life-stage dependent the provision of some goods and services, there is effects of winter climate extremes upon the a need to better understand the resistance and resistance and resilience of an important coastal resilience of mangrove forests to severe freeze wetland foundation species. We define resistance events. as the capacity to withstand change (i.e., not be Ontogeny influences resistance and resilience perturbed or affected by a climate extreme) and in most natural systems. As individuals, popula- resilience as the capacity to recover after pertur- tions, or ecosystems become older, more com- bation (i.e., recover after being affected by a plex, and/or more developed, their ability to climate extreme; sensu Pimm 1984, Tilman and resist and recover from extreme events often Downing 1994, Hoover et al. 2014). changes (Odum 1969, Pimm 1984, Sousa 1984, Across the globe, minimum temperature ex- Tilman and Downing 1994, Boege and Marquis tremes greatly influence the distribution and 2005, Gabler and Siemann 2012). There are some productivity of plant species and ecosystems examples of plants becoming more resistant and (Holdridge 1967, Sakai and Weiser 1973, Wood- resilient to severe freeze events as they develop ward 1987). In tidal saline wetlands, changing and mature (Sakai and Larcher 1987, Larcher climatic conditions, in the form of a decrease in 2003). For example, older citrus trees (Citrus spp.) the frequency and intensity of severe freeze are often more resistant to severe freeze events events, are expected to lead to the poleward than younger trees and transplants (Yelenosky migration of woody plants (i.e., mangrove trees 1996), mature Ohio buckeye trees (Aesculus glabra and shrubs) at the expense of graminoid and Willd.) are often more frost tolerant than saplings succulent plants (i.e., salt marsh plants; Osland et (Augspurger 2013), and adult chaparral shrubs al. 2013, Saintilan et al. 2014, Alongi 2015, are more freeze-tolerant than seedlings (Boorse et Cavanaugh et al. 2015). In coastal wetlands al. 1998). Along the Gulf of Mexico coast, the located near the transition between subtropical black mangrove (Avicennia germinans (L.) L.) is and warm temperate climatic zones, severe the mangrove species that is most resistant and freeze events greatly affect the abundance and resilient to severe freeze events (West 1977, productivity of mangrove trees relative to salt Sherrod and McMillan 1985). Because extreme marsh graminoid and succulent plants (West winter events are rare by definition, field-based 1977, Woodroffe and Grindrod 1991, McKee et al. studies of mangrove sensitivity to freezing are 2012). Low winter air temperature extremes can logistically challenging and dependent upon the damage or kill mangrove trees (Fig. 1; Davis occurrence of fortuitous events and/or opportu- 1940, Sherrod and McMillan 1985, Stuart et al. nistic field experiments. To our knowledge, there 2007, Ross et al. 2009), which can lead to salt has not been a study that has quantified the

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Fig. 1. Photos of: (A–C) freeze damage to black mangrove (Avicennia germinans) individuals near their poleward limit in the northern Gulf of Mexico; and (D) a healthy individual without freeze damage. effects of ontogenetic differences in A. germinans crease as plants develop and grow; in other tree resistance and resilience to severe freeze words, taller and more developed A. germinans events (but see Pickens and Hester 2011 for a individuals would be more resistant and resilient valuable comparison of early life stages: propa- to winter climate extremes than smaller individ- gules vs. seedlings). Although it is possible that uals (i.e., the relationship illustrated in Fig. 2B). A there would be no effect of life stage upon positive ontogenetic effect upon resistance and resistance and resilience (i.e., the relationship resilience in mangrove forests (e.g., the relation- illustrated in Fig. 2A), our hypothesis was that A. ships illustrated in Fig. 2B or C) would imply the germinans resistance and resilience would in- presence of a positive feedback loop that may

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Fig. 2. Three potential relationships between vegetation life stage and the resistance and resilience of black mangrove (A. germinans) forests to winter climate extremes: (A) no effect of life stage upon resistance and resilience; (B) a positive relationship between life stage and resistance and resilience; and (C) a nonlinear relationship where resistance and resilience is highest during the seedling and tall tree life stages. accelerate the rate of mangrove growth and studying the implications of mangrove expan- expansion in a future with a lower frequency sion into salt marsh (e.g., West 1977, Patterson and intensity of severe freeze events. Such and Mendelssohn 1991, McKee and Rooth 2008). information is important because it will improve The salt marshes within this area are dominated future-focused models as well as climate change primarily by smooth cordgrass (Spartina alterni- adaptation planning and restoration efforts. flora Loisel.). To our knowledge, A. germinans is Here we investigated the effects of ontogeny the only species of mangrove found in the study upon the resistance and resilience of A. germinans area and throughout the state of Louisiana. individuals to winter climate extremes. We Although A. germinans has been present in parts specifically investigated the following question: of Louisiana for at least the last century how does life stage influence the resistance and (Penfound and Hathaway 1938, O’Neil 1949, resilience of A. germinans individuals to extreme West 1977) and probably much longer (Wood- low winter air temperatures? To address this roffe and Grindrod 1991, Saintilan and Rogers question and test our hypothesis, we quantified 2015), the abundance, structural complexity, and freeze damage (i.e., resistance) and recovery (i.e., spatial coverage of mangrove forests in the Port resilience) for different vegetation strata (i.e., Fourchon area over the past century have likely seedling, short tree, and tall tree) following expanded and contracted in response to the extreme winter air temperatures that occurred duration, frequency, and intensity of extreme in January 2014 near the poleward range limit of winter events (West 1977, Osland et al. 2013). For A. germinans in the northern Gulf of Mexico. the last several decades (i.e., since the last major freeze event in 1989), the spatial coverage of A. METHODS germinans has increased within Port Fourchon (Perry and Mendelssohn 2009, Giri et al. 2011) Study area and other parts of the northern Gulf of Mexico This research was conducted within a 5-km (Stevens et al. 2006, Montagna et al. 2011) at the stretch of tidal saline wetlands located between expenseofsaltmarshvegetation.Although Port Fourchon and Leeville, Louisiana (USA; severe freeze events in Louisiana can lead to 298100000 N and 908140000 W). This location is in mangrove mortality, moderate freeze events can the Mississippi River deltaic plain and the soils cause aboveground damage that is typically are classified within the Bellpass and Scatlake followed by vigorous resprouting from the stem soil series (Terric Medisaprists and Typic Hydra- and/or base. Damaging freeze events in Louisi- quents, respectively). The study area contains a ana are frequent enough that A. germinans matrix of salt marshes and freeze-affected man- individuals are typically multi-stemmed, shorter, grove forests. Climate-mediated marsh-man- and more shrub-like than their tropical counter- grove interactions in Louisiana are dynamic parts (Osland et al. 2014a). Most A. germinans and have attracted the interest of many ecologists individuals in the Port Fourchon area are

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Table 1. Minimum air temperature and consecutive hours below freezing determined from weather station measurements recorded near the study area for 6–8 January and 28–30 January 2014.

Minimum temperature (8C) Consecutive hours below 08C Distance from Station location study area (km) 6–8 January 28–30 January 6–8 January 28–30 January Port Fourchon 5.3 3.3 1.1 16 10 Galliano 24.9 4.4 3.9 12 9 Cocodrie 42.2 3.9 1.8 18 17 between 0-2.5 m tall; however, there are some ing upon conditions), freeze-damaged leaves fall individuals that are close to 5 m in height (R. H. off of the tree, leaving branches and stems that Day and M. J. Osland, personal observation). remain leafless (Fig. 1B and C) until the growing season when resprouting occurs and new leaves Temperatures during the winter of 2013-2014 are produced. Where tidal inundation is mini- Across much of the eastern United States, air mal, piles of these freeze-damaged leaves can be temperatures during the winter of 2013–2014 observed at the base of the tree. After a moderate were below average. In coastal Louisiana, two freeze, many of the leafless branches and stems extreme winter events (6–8 and 28–30 January will still be visible from a distance at the end of 2014) resulted in minimum air temperatures the first growing season. However, by the end of recorded at nearby weather stations that ranged the second post-freeze growing season, the signs from 3.38 to 4.48 and 1.18 to 3.98C, respec- of freeze damage are less visible and may require tively (Table 1). For each of these two events, the close examination (R. H. Day, personal observa- number of consecutive hours below 08C recorded tion). Because other physiological stressors can at these weather stations ranged from 12 to 18 also result in leafless mangroves (e.g., drought, and 9 to 17 hours, respectively (Table 1). high salinity, excessive flooding), field observa- Although these temperatures were not cold tions made within the first several days and enough in the Port Fourchon area to cause weeks following a freeze event can help to extensive mangrove mortality or damage similar determine that the cause of damage was due to to the freezes of the 1980s, temperatures were freezing temperatures. Initial scouting trips lead- low enough in some areas to cause minor ing to this study were made on 8 January, 16 damage and some mortality worthy of investi- January, 23 January, and 7 March 2014 (i.e., gation (see photos in Fig. 1). approximately 1, 9, 16, and 59 days following the In the two months following these 2014 freeze first 2014 freeze event, respectively). During events, R. H. Day and/or M. J. Osland made four these trips, R. H. Day and/or M. J. Osland made separate trips to the study area to plan this study observations of mangrove freeze damage in and observe the vegetation damage due to the coastal wetlands present in the area between freeze events. For A. germinans, leaf damage due Port Fourchon and Golden Meadow, Louisiana. to freezing occurs quickly and can be easily During these trips, direct field observations were identified in the days following a freeze event. made of the life-stage dependent freeze effects Freeze-damaged A. germinans leaves turn brown quantified in this study. Those initial post-freeze (Fig. 1A) and the color of these leaves contrasts field observations along with similar observa- sharply with any live leaves that may be present. tions made following a freeze event that occurred In moderate cases, only a few leaves may be in the study area in 2010 (R. H. Day, unpublished damaged on each individual, and freeze-damage data), led to the development and implementa- observations require close examination (e.g., tion of this study. Pre- and post-freeze observa- within ;1 m of an individual); however, in more tions are an important component of this study extreme cases, all of the leaves on an individual because they allow the authors to attribute the may already be brown on the day following a damage quantified in June 2014 to the freeze freeze event and the color contrast can be seen events that occurred in January 2014, and also to from a larger distance (e.g., ;100 m). With the recognize remnant dead wood still present from passage of time (i.e., ;weeks to months depend- the 2010 freeze.

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Study design freeze (i.e., the height of the tallest stem or Because the effects of freeze damage were branch tip regardless of damage); (3) the height spatially heterogeneous, we quantified resistance of the plant after the freeze (i.e., the height of the and resilience for multiple vegetation strata in tallest non-freeze damaged stem or branch tip); areas with and without extensive freeze damage. (4) the longest crown diameter of the individual Our study design included two freeze damage priortothefreeze(CD1);(5)thelongest treatments: (1) a ‘‘Damaged’’ treatment consist- secondary crown diameter of the individual ing of sites with visible freeze damage in the prior to the freeze in a direction perpendicular form of mangroves with brown leaves and/or to CD1 (CD2); (6) whether the individual leafless branches; and (2) a ‘‘Not Damaged’’ resprouted from the stem; (7) whether the treatment consisting of sites with little to no individual resprouted from the base; (8) whether visible freeze damage (i.e., a very small number there was indication (i.e., presence of standing of brown leaves and/or leafless branches). The dead stems less than 1 m in height) that the plant study included a total of six sites: three Damaged had suffered damage due to a freeze event in sites and three Not Damaged sites. Each of the 2010 (9–11 January 2010). At these sites, damage three Damaged sites was paired with a Not from that 2010 freeze event was still present in Damaged site using a block design. The distances the form of standing dead stems that were less between paired sites within blocks were 1.6, 1.4, than 1 m in height. A gradual decay and loss of and 3.5 km. At each site, we established one 50- damaged aboveground material following the m2 circular plot (radius ¼ 4 m). Within each 50- 2010 freeze event has been documented (R. H. m2 plot, we established a series of randomly- Day, personal observation and unpublished data). located nested subplots that included three 2-m2 Within the 2-m2 subplots, we also estimated subplots (i.e., 1 3 2 m subplots) and three 0.25-m2 the percent coverage of salt marsh species (i.e., subplots (i.e., 0.5 3 0.5 m subplots) for strata- graminoid and succulent plants). We calculated specific vegetation measurements. A. germinans biomass via allometric equations that utilize plant volume (i.e., a combination of Vegetation crown area and plant height; Osland et al. 2014a). All vegetation measurements were conducted Freeze resistance metrics that were determined in June 2014. Vegetation measurements were include freeze damage (i.e., the percentage of the made within three strata: (1) a tall mangrove plant damaged), freeze-induced height reduction stratum that consisted of individuals with a (i.e., the difference between the pre-freeze and height that was greater than or equal to 140 cm; post-freeze heights), and the freeze-induced (2) a short mangrove stratum that consisted of percent height reduction (i.e., the percentage of individuals with a height that was greater than or the pre-freeze height that was reduced due to the equal to 50 cm but less than 140 cm; and (3) a freeze). Freeze resilience was quantified as the mangrove seedling stratum that consisted of percent of individuals resprouting from the base individuals with a height of less than 50 cm. or stem after freeze damage. The seedling stratum included a mixture of seedlings that became established prior to and Soil and elevation after the 2014 freezes. Strata-specific measure- In order to account for potential edaphic or ments were conducted in density-appropriate hydrologic effects, we measured the elevation plot sizes. The tall mangrove stratum measure- and a basic suite of soil properties present at each ments were conducted across the entire 50-m2 site. We measured elevation because we expect plot. Within each 50-m2 plot, the short mangrove that tidal inundation may affect near-soil surface and the mangrove seedling strata measurements temperatures during freeze events. Elevation was were conducted within the three 2-m2 subplots measured at each 50-m2 plot centroid using a and the three 0.25-m2 subplots, respectively. high-precision Global Navigation Satellite Sys- For each individual in each of the three strata, tem (GNSS; Trimble R8 and TSC3, Trimble, we recorded the following information: (1) the Sunnyvale, California, USA) and the Continu- percentage of the plant that was damaged by ously Operating Reference Stations (CORS) freeze; (2) the height of the plant prior to the contained within Louisiana State University’s

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GULFNet real-time network (RTN). ments. Soil and elevation differences between the Soil samples were collected to 15-cm depth freeze damage treatments were evaluated using using a custom-made stainless steel split-coring Student’s t-tests, and for the freeze resistance- cylinder (diameter: 4.7 cm). At each site, one soil focused response variables (i.e., site-level mean sample was collected within a 1-m buffer of each percent freeze damage, percent height reduction, of the three 2-m2 subplots (i.e., a total of three actual height reduction), we evaluated analysis of samples were collected per site). Samples were covariance (ANCOVA) models that included the stored in a cooler with ice while in the field and freeze damage treatment as a factor and individ- at 48C while in the laboratory. Soil bulk density ual soil or elevation properties (i.e., soil bulk was determined as a simple dry weight to density, soil organic matter, or elevation) as a volume ratio (Blake and Hartge 1986). Soil covariate. The data met the assumptions for organic matter was determined via loss on ANOVA and ANCOVA. All data analyses were ignition (Karam 1993). conducted in R (http://cran.r-project.org; Version 3.0.1). Data analyses For the site-level data analyses, the subplot- RESULTS level data were converted to site-level data (i.e., site-level means were calculated from the sub- Resistance to winter climate extremes plot-level data). Initial models indicated that the For the freeze resistance metrics (i.e., percent block effect was not significant and was therefore freeze damage, percent height reduction, and not included as a variable in subsequent models. actual height reduction), there was a significant To determine the effects of vegetation strata, interaction between the freeze damage treat- freeze damage treatment, and their interaction ments and vegetation strata (Table 2; Figs. 3A– upon mangrove resistance and resilience, we C and 4). Freeze resistance metrics were affected used analysis of variance (ANOVA) models that by vegetation strata within the Damaged treat- included vegetation strata, freeze damage treat- ment, but not in the Not Damaged treatment ment, and their interaction as independent (Figs. 3A–C and 4). Within the Damaged variables. Response variables included site-level treatment, percent freeze damage and percent mean percent freeze damage, percent height height reduction were highest in the short reduction, and actual height reduction. For those mangrove stratum, lower in the tall mangrove individuals that were most damaged by the 2014 stratum, and close to zero in the mangrove freeze events (i.e., all of the data from the tall and seedling stratum (Figs. 3A–B and 4). Within the short strata within the Damaged treatment), we Damaged treatment, actual height reduction was also evaluated ANOVA models that included highest in the short and tall mangrove strata and vegetation strata, resprout location, and their close to zero in the mangrove seedling stratum interaction as independent variables and the (Fig. 3C). Within the Not Damaged treatment, percent resprouting individuals as the dependent percent freeze damage, percent height reduction, variable. To illustrate the height-dependent and actual height reduction were close to zero freeze damage at the Damaged sites, we com- and not different for all three strata (Fig. 3A–C). bined all of the individual-based data within the Damaged sites and calculated the proportion of Resilience to winter climate extremes individuals within 10% freeze damage incre- For the percentage of individuals that re- ments for each the following 50-cm increment sprouted after damage from the 2014 freeze plant height categories: 0–50 cm, 50–100 cm, events (i.e., for those individuals in the tall and 100–150 cm, 150–200 cm, 200–250 cm, and 250– short strata within the Damaged treatment), 300 cm. Post hoc mean comparisons were there was a significant interaction between conducted using Tukey’s Studentized Range vegetation strata and resprouting location (F1,8 (HSD) tests. A Student’s t-test was used to ¼ 22.1, P , 0.01; Fig. 5). For both the tall and compare the percentage of tall stratum individ- short strata, resprouting percentage was higher uals with visible damage remaining from the from the stem than the base (Fig. 5). The winter of 2010 within the freeze damage treat- percentage of individuals resprouting from the

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Table 2. Effect of freeze damage treatment, vegetation strata, and their interaction upon freeze resistance metrics (i.e., percent freeze damage, percent height reduction, and actual height reduction).

Response variable Freeze damage treatment Vegetation strata Interaction Percent freeze damage 78.5*** 27.1*** 26.9*** Percent height reduction 51.9*** 16.8*** 16.8*** Actual height reduction 65.7*** 16.5*** 16.3*** Notes: Numbers shown are ANOVA F values. *** indicates P , 0.001. stem was 100 % for both the tall and short strata atures (i.e., the relationship illustrated in Fig. 2B). (Fig. 5). Basal resprouting, however, was higher There are many examples from other ecosystems in the tall mangrove stratum than in the short of mature plant individuals being more freeze mangrove stratum (Fig. 5). tolerant than juveniles (e.g., Sakai and Larcher Freeze-damage from 2010 was still visible at 1987, Yelenosky 1996, Boorse et al. 1998, Aug- some of the Damaged and Not Damaged sites spurger 2013). In this study, we expected that tall (Fig. 6). The percent of individuals within the Tall mangrove trees would be more resistant to Stratum that still had visible damage from the winter climate extremes than short trees and 2010 freeze event was higher at the Damaged seedlings. Our data indicate that tall A. germinans sites than the Not Damaged sites (P ¼ 0.046; Fig. trees are indeed more freeze-tolerant than short 6). trees. However, we found that freeze damage to seedlings was lower than for tall and short trees Soil and elevation (Figs. 3 and 4). These findings indicate that the The ANCOVA models indicated that elevation relationship between life stage and A. germinans and soil properties did not significantly affect resistance is best illustrated by the pattern in Fig. any of the freeze resistance-focused response 2C. variables (i.e., site-level mean percent freeze The extremely low occurrence of freeze dam- damage, percent height reduction, actual height age (,1%) among all mangrove seedlings pro- reduction). There was no difference in soil bulk vides a strong indication that seedlings which density, soil organic matter, or elevation between established prior to the freeze remained essen- the freeze damage treatments (P ¼ 0.63, P ¼ 0.75, tially undamaged (Fig. 3A–C). Multiple authors P ¼ 0.40, respectively). The mean 6 SE soil bulk have noted cases where mangrove seedlings and density and soil organic matter for all six sites propagules survived freeze events that had were 0.66 6 0.06 g/cm3 and 12.90% 6 1.32%, resulted in the mortality or damage of more respectively. The mean 6 SE elevation for all six mature individuals (Lugo and Patterson-Zucca sites was 0.29 6 0.01 m NAVD88. The similarity 1977, Sherrod and McMillan 1985, Olmsted et al. in elevation at our sites implies that the sites were 1993, Ross et al. 2009, Pickens and Hester 2011). inundated at the same level during the freeze Protection of seedlings, propagules and low events. mangrove individuals (i.e., ,50 cm height) may be due to the presence of a buffering layer of DISCUSSION warmer and more humid air near the soil surface. Ross et al. (2009) noted that leaf mortality Our analyses demonstrate that ontogeny (i.e., following a freeze event was lowest near the soil plant life stage) influences black mangrove surface. Field observations imply that seedling resistance and resilience to winter climate ex- protection and survival under cold temperatures tremes. Following freeze events in January 2014, may be higher beneath and near vegetation (i.e., we quantified A. germinans freeze damage and a mangrove canopy layer or a tall salt marsh recovery as indicators of resistance and resilience, layer such as that produced by S. alterniflora; respectively. Our original hypothesis was that Lugo and Patterson-Zucca 1977, Sherrod and there would be a positive relationship between McMillan 1985, Olmsted et al. 1993, Ross et al. mangrove life stage development and the ability 2009, Pickens and Hester 2011, Guo et al. 2013), to withstand and recover from freezing temper- which can minimize nocturnal radiative cooling

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Fig. 4. Histograms of black mangrove (A. germinans) freeze damage within the freeze-damaged sites for the following 50-cm tree height increment categories: (A) less than 50 cm; (B) 50–100 cm; (C) 100–150 cm; (D) 150–200 cm; (E) 200–250 cm; and (F) 250–300 cm. The horizontal axis indicates freeze damage as the percent of the plant that was damaged.

observed in other cold-prone woodland-to-grass- land transition zones across the globe (D’Odorico et al. 2013). However, vertically-explicit air temperature and vegetation measurements are needed to confirm the presence of these feed- backs in mangrove forests. Experiments focused on the effect of vegetation density upon man- Fig. 3. Black mangrove (A. germinans) resistance to grove freeze survival and facilitation would be winter climate extremes. Freeze damage (A), percent valuable. height reduction (B), and actual height reduction (C) Physiological differences in water transport within freeze damage treatments and across vegetation and vulnerability to xylem cavitation could also strata. Different letters denote significant differences. be responsible for the life-stage dependent results For A, the vertical axis indicates freeze damage as the observed in this study. From a physiological percentage of the plant that was damaged. perspective, woody plants in tidal saline wet- lands have much in common with those in (D’Odorico et al. 2013). Our data along with terrestrial dryland ecosystems. In both ecosys- tems, freshwater limitation and freeze events can these observations indicate that a positive vege- interact to result in bubble formation in the ’ tation-microclimate feedback (sensu D Odorico xylem (i.e., xylem cavitation; xylem embolism), et al. 2013) may affect mangrove resistance and which can alter water transport and lead to plant resilience to winter climate extremes. Similar damage and/or mortality (Pockman and Sperry vegetation-microclimate feedbacks have been 1997, Stuart et al. 2007). In dryland terrestrial

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Fig. 6. Black mangrove (A. germinans) resilience to Fig. 5. Black mangrove (A. germinans) resilience to winter climate extremes. The percentage of tall tree winter climate extremes. The percentage of resprouting stratum individuals that had visible damage remain- individuals for different strata (i.e., tall vs. short) and ing from the 2010 freeze event. These individuals resprouting locations (i.e., stem vs. base). Different resprouted and recovered from damage that resulted letters denote significant differences. in a large loss of aboveground biomass. Different letters denote significant differences. ecosystems, several studies have noted life-stage dependent vulnerability to cavitation (Sperry and mangle L. and Laguncularia racemosa (L.) C.F. Saliendra 1994, Mencuccini and Comstock 1997, Gaertn. (the red and white mangrove, respec- but see Linton et al. 1998, Medeiros and Pockman tively). Whereas shorter R. mangle individuals 2010). Similar physiology-focused studies con- had a higher probability of survival than taller ducted in black mangrove forests would help individuals, the probability of L. racemosa sur- identify and differentiate between the physiolog- vival increased with height (Ross et al. 2009). ical and microclimatic processes responsible for Higher mortality of tall R. mangle individuals the life-stage dependent findings observed in this may be explained by the lack of meristem reserve study. buds in older individuals of this species (Tom- In addition to the significant relationship linson 1986), which results in an inability to between ontogeny and resistance, our results resprout following freeze damage (Olmsted et al. indicate that there is a positive relationship 1993). In contrast, L. racemosa and A. germinans between ontogeny and recovery from freeze both have high densities of meristem reserve damage (i.e., resilience). Although recovery was buds, which can result in vigorous basal and high for both short and tall trees, recovery via stem resprouting following moderate freeze basal resprouting was highest for the tall trees events (Fig. 5; Tomlinson 1986). (Fig. 5). In comparison to short trees, tall trees Aboveground A. germinans biomass at the likely have greater densities of meristem reserve study sites ranged from 9.6 to 19.8 Mg/ha (mean buds and also have greater access to resources 6 SE: 12.1 6 1.6 Mg/ha). At our study area and needed for resprout growth (e.g., greater access other mangrove-marsh ecotones in the northern to carbohydrate reserves, freshwater, and nutri- Gulf of Mexico, A. germinans individuals are ents). To our knowledge, this is the first study to typically freeze-stunted and shrub-like due in quantify an effect of ontogeny upon the resilience part to repeated cycles of freeze-induced above- and resistance of A. germinans trees. In an ground damage followed by vigorous basal and/ experiment focused on the temperature tolerance or stem resprouting. Prior to the freeze of 2014, of early life stages, Pickens and Hester (2011) many (mean 6 SE: 60% 6 9%) of the tall tree found no difference in the survival of A. individuals at our Damaged sites had produced germinans propagules and seedlings. Following new sprouts after losing a portion of their a low-temperature event in south Florida, Ross et aboveground biomass due to a freeze in 2010 al. (2009) found a species-specific effect of (Fig. 6). Some of these tall individuals in 2014 mangrove height upon the survival of Rhizophora may have been in the short strata in 2010 and

v www.esajournals.org 10 September 2015 v Volume 6(9) v Article 160 OSLAND ET AL. grown into the tall strata in the ensuing four thresholds that would cause mortality or damage years. to seedlings, juveniles, and mature mangrove In forests across the globe, microclimatic trees are likely different. Our results also high- gradients greatly influence landscape-level pat- light the need to account for the effects of terns in ecosystem structure and function (Chen vegetation-microclimatic feedbacks that would et al. 1999). For mangrove forests in the northern influence resistance and resilience. A more Gulf of Mexico and near their latitudinal limit, nuanced understanding of ontogeny-based the literature is replete with field observations of thresholds and positive feedbacks would im- spatially heterogeneous effects of freeze damage prove predictions of subtropical coastal wetland due to various interacting factors (e.g., landscape ecological responses to changing climatic condi- position relative to wind, water and vegetation; tions. topography; tidal inundation history; genetic The positive relationship between ontogeny variability; positive feedbacks; e.g., Lugo and and resistance and resilience to winter climate Patterson-Zucca 1977, Olmsted et al. 1993, Ross extremes suggests that a decrease in the frequen- et al. 2009). These observations, in combination cy and intensity of extreme minimum air with the large differences in the extent of freeze temperatures could lead to a nonlinear increase damage between the two freeze damage treat- in mangrove forest resistance and resilience, ments in this study, despite similarity of mea- which would likely affect the rate of future sured elevation and edaphic variables, highlight mangrove expansion in response to climate the complexity of making landscape-scale spatial change. In Fig. 7A, we present a conceptual predictions of mangrove forest damage and model that illustrates a potential climate change- recovery in response to winter climate extremes. induced positive feedback loop. In the model, a In recent years, the identification of tempera- decrease in the frequency and intensity of winter ture-based thresholds that would lead to man- air temperature extremes would lead to an grove forest damage and/or mortality has increase in mangrove forest growth, structural become a productive and interesting research development, and reproduction, which would arena (e.g., Pickens and Hester 2011, Quisthoudt lead to an increase in the resistance and resilience et al. 2012, Osland et al. 2013, Cavanaugh et al. of mangrove forests to subsequent winter climate 2014). At the landscape-scale, the minimum extremes (Fig. 7A). The increases in resistance temperature thresholds that separate mangrove and resilience would then lead to additional forests from salt marsh ecosystems are compar- mangrove forest development, which would atively abrupt and more dramatic than those increase resistance and resilience (Fig. 7A). Due observed in many terrestrial systems (Osland et to this positive feedback loop, we expect that the al. 2013, Cavanaugh et al. 2014). Targeted field relationship between changing winter climate and greenhouse-based experiments are needed to extremes and mangrove forest resistance and refine our understanding of mangrove freeze resilience is probably nonlinear (see the relation- damage and mortality thresholds. There is a need ship illustrated in Fig. 7B), and that small for the identification of species-specific thresh- decreases in the frequency and intensity of winter olds (Cavanaugh et al. 2015; Lovelock et al., in climate extremes could increase mangrove forest press) and for a better understanding of the resistance and resilience, which could accelerate physiological effects of interactions between low the rate of mangrove expansion. temperatures and other stressors including fresh- Although our data provide initial support for water limitation and high salinity (Osland et al. the presence of a positive feedback loop that 2014b). Our research has not directly quantified would affect the rate of mangrove expansion into the relationships between specific temperature salt marsh, additional studies are needed to regimes and mangrove life stage-dependent confirm and better quantify the processes re- damage and recovery, but rather the response sponsible for the proposed positive feedback. In of different mangrove life stages to environmen- particular, more research is needed to test and tal conditions associated with low temperatures. quantify the linkages between life stage-depen- There is a need to identify life stage-specific dent resistance, resilience, and ecological pro- thresholds because the temperature-based cesses that are directly related to mangrove forest

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Fig. 7. A hypothetical positive feedback loop that would be induced by a decrease in the intensity, duration and/or frequency of winter climate extremes (A), and the hypothetical effects of changes in winter climate extremes upon the resistance and resilience of black mangrove forests (B). expansion (e.g., propagule production, dispersal In addition to the climate-change focused distances, and recruitment). Although moderate implications, our results also have important freeze events like those that occurred in 2010 and implications for the restoration of coastal wet- 2014 do not result in widespread A. germinans lands in the northern Gulf of Mexico. Avicennia mortality, we expect that freeze-induced reduc- germinans individuals are occasionally used to tions in aboveground biomass and height likely restore coastal wetland habitats. Our results reduce: (1) the resources available for reproduc- indicate that planted A. germinans individuals tion; and (2) the distances that propagules are likely most vulnerable to freeze-damage in disperse from their source plants. Propagule the short-tree stage (i.e., between 50-150 cm dispersal distances are expected to be larger for height) and that taller trees and seedlings are taller and wider A. germinans individuals com- less vulnerable to freeze damage. Therefore, pared to short and compact individuals. Hence, targeting a diversity of life stages during resto- within these poleward mangrove-marsh eco- ration in freeze-prone areas may minimize the tones, we expect that there is a positive relation- potential for vegetation loss due to freeze ship between the absence of winter temperature damage. Also, salt marsh vegetation and/or extremes and propagule production rates and densely planted mangroves could potentially be dispersal distances. Though logical, additional used to create a buffer layer near the soil surface, data is needed to confirm that these relationships which could decrease radiative cooling and are present. Additional studies are also needed to facilitate the establishment of mangrove trans- determine whether the life-stage dependent plants. Experiments are needed to test the results observed here are also present during validity of these restoration-focused hypotheses more extreme freeze events. and recommendations.

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Ecologists and natural resource managers are temperature, phenology, and frost damage over increasingly challenged to better understand, 124 years: Spring damage risk is increasing. predict, and plan for the ecological effects of Ecology 94:41–50. future changes in the frequency and intensity of Blake, G. R., and K. H. Hartge. 1986. Bulk density. Pages 363–375 in A. Klute, editor. Methods of soil climate extremes (Glick et al. 2011, Stein et al. analysis. Part 1. Physical and mineralogical meth- 2014). Ecological responses are greatly influ- ods. American Society of Agronomy, Madison, enced by stabilizing processes that affect the Wisconsin, USA. capacity of an ecosystem to withstand and Boege, K., and R. J. Marquis. 2005. Facing herbivory as recover from extreme climatic conditions (Smith you grow up: the ontogeny of resistance in plants. 2011, Lloret et al. 2012, Hoover et al. 2014). Our Trends in Ecology and Evolution 20:441–448. results emphasize the importance of considering Boorse, G. C., F. W. Ewers, and S. D. Davis. 1998. ontogeny (i.e., plant life stage) in predictions of Response of chaparral shrubs to below-freezing ecological resistance and resilience to climate temperatures: acclimation, ecotypes, seedlings vs. adults. American Journal of Botany 85:1224–1230. extremes. We found that taller mangrove trees/ Bruno, J. F., and M. D. Bertness. 2001. Habitat shrubs were more resistant and resilient than modification and facilitation in benthic marine short trees/shrubs. These findings could indicate communities. Pages 201–218 in M. D. Bertness, the presence of a positive feedback loop between S. D. Gaines, and M. E. Hay, editors. Marine winter climate extremes and mangrove forest community ecology. Sinauer Associates, Sunder- resistance and resilience. A future decrease in the land, Massachusetts, USA. frequency and intensity of extreme winter min- Cavanaugh, K. C., J. R. Kellner, A. J. Forde, D. S. imum temperatures could lead to an increase in Gruner, J. D. Parker, W. Rodriguez, and I. C. Feller. mangrove forest resistance and resilience and 2014. Poleward expansion of mangroves is a accelerate the rate of poleward mangrove expan- threshold response to decreased frequency of extreme cold events. Proceedings of the National sion at the expense of some salt marshes. Academy of Sciences 111:723–727. Cavanaugh, K. C., J. D. Parker, S. C. Cook-Patton, I. C. ACKNOWLEDGMENTS Feller, A. Park Williams, and J. R. Kellner. 2015. Integrating physiological threshold experiments We thank Rebecca Howard, two anonymous re- with climate modeling to project mangrove species’ viewers, and the subject-matter editor for their helpful range expansion. Global Change Biology 21:1928– comments on a previous version of this manuscript. 1938. This research was supported by the U.S. Geological Chen, J., S. C. Saunders, T. R. Crow, R. J. Naiman, K. D. Survey’s Ecosystems Mission Area and the Department Brosofske, G. D. Mroz, B. L. Brookshire, and J. F. of Interior Southeast Climate Science Center. We thank Franklin. 1999. Microclimate in forest ecosystem the ConocoPhillips Company/Louisiana Land and and landscape ecology variations in local climate Exploration Company LLC for permission to conduct can be used to monitor and compare the effects of research on their land. Any use of trade, firm, or different management regimes. BioScience 49:288– product names is for descriptive purposes only and 297. does not imply endorsement by the U.S. Government. Davis, J. H. 1940. The ecology and geologic role of This manuscript is submitted for publication with the mangroves in Florida. Carnegie Institue of Wash- understanding that the U.S. Government is authorized ington Publications. Papers from Tortugas Labora- to reproduce and distribute reprints for Governmental tory 32:303–412. purposes. Day, J. W., B. C. Crump, W. M. Kemp, and A. Ya´n˜ez- Aranciba. 2013. Estuarine ecology. Wiley-Black- LITERATURE CITED well, Hoboken, New Jersey, USA. Dayton, P. K. 1972. Toward an understanding of Alongi, D. M. 2015. The impact of climate change on community resilience and the potential effects of mangrove forests. Current Climate Change Reports enrichments to the benthos at McMurdo Sound, 1:30–39. Antartica. Pages 81–96 in B. C. Parker, editor. Angelini, C., A. H. Altieri, B. R. Silliman, and M. D. Proceedings of the Colloquium on Conservation Bertness. 2011. Interactions among foundation Problems in Antartica. Allen Press, Lawrence, species and their consequences for community Kansas, USA. organization, biodiversity, and conservation. Bio- D’Odorico, P., Y. He, S. Collins, S. F. De Wekker, V. Science 61:782–789. Engel, and J. D. Fuentes. 2013. Vegetation–micro- Augspurger, C. K. 2013. Reconstructing patterns of climate feedbacks in woodland–grassland eco-

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