Southeastern Naturalist A.Williams, S. Eastman, W. Eash-Loucks, M. Kimball, M. Lehmann, and J. Parker 2014 Vol. 13, No. 1 56 2014 SOUTHEASTERN NATURALIST 13(1):56–63 Record Northernmost Endemic Mangroves on the United States Atlantic Coast with a Note on Latitudinal Migration Asher A. Williams1,2,3,*, Scott F. Eastman1,2, Wendy E. Eash-Loucks1,4, Matthew E. Kimball1,2,5, Michael L. Lehmann6, and John D. Parker7 Abstract - The northern limits of three mangrove species—Avicennia germinans (Black Mangrove), Rhizophora mangle (Red Mangrove), Laguncularia racemosa (White Mangrove)— on the United States Atlantic coast are vouchered and described in comparison to previous boundaries defined in literature and herbarium collections. The location and general status of individual trees were used to delineate northern maxima and show that present ranges extend beyond historic records. The gradient structure of the ecotone within an area of uniform climate is interpreted as ongoing latitudinal movement. Introduction Mangroves represent multiple taxa of tropical macrophytes that occupy coastal margins and reproduce viviparously. Unique among wetland trees, mangroves facultatively resist toxic osmotic gradients in saline soils by excluding and or excreting excess salts (Snedaker and Snedaker 1984). Mangroves are further adaptive in aquatic environments by dispersing viviparous propagules, rather than seeds, via surface waters (e.g., tides, wind, currents) (Odum and McIvor 1990). Hydrologic conditions (wave energy, freshwater influx, tidal prism, etc.) limit local habitat viability (Odum and McIvor 1990), although thermal requirements generally restrict mangroves to tropical and subtropical zones (Waisel 1972). Two biogeographic patterns reflect fundamental ecology and adaptation in these organisms: decreased abundance along latitudinal axes (Ellison et al. 1999), and lower species richness in the Americas as compared with the Indo-Pacific (Macnae 1968). Productivity in mangrove swamps, poised at the interface of the ocean, plays a disproportionately large role in global carbon budgets (Bouillon et al. 2008). Furthermore, mangrove shorelines decrease nutrient efflux from estuaries (Rivera-Monroy et al. 1999), stimulate food webs, and provide habitat that enhances fisheries (Barbier 2000). Mangroves also form a physical barrier that dampens wave energy, directly benefitting human coastal development (Vermaat and Thampanya 2006, Zhang et al. 2012). 1Guana Tolomato Matanzas National Estuarine Research Reserve, 505 Guana River Road, Ponte Vedra Beach, FL 32082. 2Department of Biological Sciences, University of North Florida, 1 UNF Drive, Jacksonville, FL 32224. 3Department of Oceanography and Coastal Sciences, Louisiana State University, Baton Rouge, LA 70803. 4King County Department of Natural Resources and Parks, 201 S Jackson Street, Seattle, WA 98104. 5Baruch Marine Field Laboratory, University of South Carolina, PO Box 1630, Georgetown, SC 29442. 6Smithsonian Marine Station, 701 Seaway Drive, Fort Pierce, FL 34949. 7Smithsonian Environmental Research Center, PO Box 28, Edgewater, MD 21037. *Corresponding author - awil336@tigers.lsu.edu. Manuscript Editor: Joey Shaw Southeastern Naturalist 57 A.Williams, S. Eastman, W. Eash-Loucks, M. Kimball, M. Lehmann, and J. Parker 2014 Vol. 13, No. 1 Three true mangrove species (Tomlinson 1995) are endemic to the United States Atlantic coast: Avicennia germinans Jacq. (Black Mangrove), Rhizophora mangle L. (Red Mangrove), and Laguncularia racemosa Gaertn. (White Mangrove). In south Florida, mangrove swamps or “mangals” are classified within the riverinebasin- fringe continuum (Lugo and Snedaker 1974) where dense tree assemblages dominate intertidal habitat. Disparate freeze resilience causes an uneven latitudinal boundary among the Florida endemics. For instance, by resprouting from roots, Black Mangroves are less inhibited by occassional freezes compared to other species (Odum and McIvor 1990). Morphologic development is impeded by cold stress in the shrubby northern inhabitants, compared to the fully formed trees in south Florida estuaries (Saenger and Snedaker 1993). Precise northern boundary locations for each of the endemic species have proven difficult to determine because of their transient nature, and ecologists have typically delineated mangrove northern ranges along the Atlantic coast in general terms. For instance, Savage (1972) limited Black Mangroves to no further than 30º N, and Teas (1977) noted Reds and Whites do not extend beyond Ponce de Leon Inlet, FL (29.10º N). The University of South Florida Institute of Systematic Botany (hereafter USF), based on voucher specimens, lists the northernmost samples of Black and White Mangroves at St. Augustine Inlet and Volusia County, FL, on the United States Atlantic coast. The 1.5-m Black Mangrove specimen was vouchered at 29º53.39'N, 81º17.41'W in early summer 2007 (Hansen 9825, USF; Wunderlin and Hansen 2008). A less specific account of a White Mangrove at Daytona Beach Shores, FL was discovered in an interdunal swale in 1962 (Ray 11136, USF; Wunderlin and Hansen 2008). Zomlefer et al. (2006) represents the only published account of a northernmost Red Mangrove, documented at Matanzas Inlet, FL (29º42.94'N, 81º14.35'W) in a Spartina alterniflora Loisel (Smooth Cordgrass) marsh with seven other individuals of the same species. Community composition at climatic ecotones change in coincidence with thermal regime (Buchner and Neuner 2011, D’Odorico et al. 2013), and one of the primary distinguishing factors among biomes is climate. Mangrove transgression into temperate salt marshes is a phenomenon that has been globally interpreted as a result of changing climate, including studies in southeastern Australia (Saintilan and Williams 1999), the northeastern Gulf of Mexico (Comeaux et al. 2012), and Florida’s west coast (Raabe et al. 2012). Evaluation of the Atlantic ecotone is ongoing, although most accounts of a migration remain anecdotal, and only the location of an outlying Red Mangrove has been formally vouchered (Zomlefer et al. 2006). Provided here are the record locations and general morphology of the northernmost Black, Red, and White Mangroves on the United States Atlantic coast and comparison with previous northern distributions, verified in specimen collections and literature. Methods The Guana Tolomato Matanzas (GTM) estuary (Fig. 1) is located at the temperate to subtropic climactic transition, in northeast Florida. The GTM estuary is a narrow (east–west) and relatively shallow (average depth 2.7 m) tide-dominated lagoon with two inlets (St. Augustine and Matanzas) connecting it to the Atlantic Ocean (ValleSoutheastern Naturalist A.Williams, S. Eastman, W. Eash-Loucks, M. Kimball, M. Lehmann, and J. Parker 2014 Vol. 13, No. 1 58 Levinson et al. 2009). Sediments are distributed in the channelized-estuary relative to tidal forcing and maintenance dredging for navigation. Tides propagate through the St. Augustine and Matanzas inlets, and flow direction is regulated by ebb and Figure 1. Map of the Guana Tolomato Matanzas estuary in northeast Florida showing locations of the northernmost recorded Avicennia germinans (Black Mangrove), Rhizophora mangle (Red Mangrove), and Laguncularia racemosa (White Mangrove) specimens on the United States Atlantic coast. Southeastern Naturalist 59 A.Williams, S. Eastman, W. Eash-Loucks, M. Kimball, M. Lehmann, and J. Parker 2014 Vol. 13, No. 1 flood. A water-control structure on the Guana River, in the upper estuary, and tidal flux (e.g., hydrologic turnover) make GTM a marine-dominated system in which water is transiently diluted by precipitation (Phlips et al. 2004). Mesotidal flow is conserved in the system’s primary channel and does not form an extensive network of tidal creeks. Laterally compressed geomorphology at GTM is noteworthy in two regards: adjacent intertidal areas are all saline and they can be inspected almost entirely from a boat. The Guana Tolomato Matanzas National Estuarine Research Reserve (GTMNERR) includes the GTM, and as a result, the system is well monitored. Seasonal sampling and surveys by GTMNERR personnel in the emergent intertidal zone revealed that mangroves transitioned from absence to dominance along a north-to-south gradient within a 35-km stretch of the estuary. The gradual structure of an ecocline is applicable to mangrove latitudinal limits; however, the reference to an ecotone made here is in recognition of a steep climactic scale. Observations of northernmost individuals from all three endemic mangrove species were made in 2012 and early 2013, and each was evaluated in March 2013. We verified potential outliers by walking transects oriented to the north and conducted at a vantage point such that the entire marsh was visible. Travelling on foot, we scrutinized wetlands 5 km north of record locations, followed by verification and spot-checking by boat of 17, 37, and 61 km north of the Black, Red, and White records, respectively. Because Black Mangroves were abundant at the site of the northernmost Red and White trees, we individually inspected plots of adjacent trees. We collected data on height, diameter at 10 cm (hereafter D10), and canopy dimensions (long axis, perpendicular short axis) for each plant. We made visual assessments of leaf chlorosis (yellowing or browning) to determine plant status as healthy (0–33%), intermediate (33–66%), or stressed (67–100%). We used a GPS unit, with 3-m accuracy, to collect the coordinates of each record (provided as degrees and decimal minutes), and took photographs for confirmation (Fig. 2). We described the vegetation in the vicinity of each record mangrove for context. Hypothetical migration (km yr-1) was calculated by the difference between previous and current observation locations and year. The historic White Mangrove is approximated to 29º9.55'N, 80º58.28'W, derived from the specimen description that included only the municipality. We provided vouchers of each record tree to the USF Herbarium. Results Avicennia germinans We recorded the northernmost Black Mangrove (Williams and Eastman s.n., USF) (Fig. 2) at 30º6.618'N, 81º22.303'W. The shrub was 86 cm in height, 3.5 D10, with 145 x 93 cm canopy dimensions. Chlorosis was absent from leaf tissue, and thus the plant was categorized as healthy. Another Black Mangrove was present in the S. alterniflora marsh where the precisely northernmost individual was discovered, 10 m south of the record. The nearby shrub was also healthy in appearance as yellow and browning were absent from leaves. The two trees were documented in a marsh adjacent to the main channel of the GTM estuary in the Tolomato River (Fig. 1). We collected data on 27 March 2013. However, the initial observations of Southeastern Naturalist A.Williams, S. Eastman, W. Eash-Loucks, M. Kimball, M. Lehmann, and J. Parker 2014 Vol. 13, No. 1 60 Figure 2. Photographs of the northernmost Avicennia germinans (Black Mangrove; top), Rhizophora mangle (Red Mangrove; center), and Laguncularia racemosa (White Mangrove; bottom) specimens on the United States Atlantic coast. Southeastern Naturalist 61 A.Williams, S. Eastman, W. Eash-Loucks, M. Kimball, M. Lehmann, and J. Parker 2014 Vol. 13, No. 1 the tree were made in 2012. Black Mangroves were documented 27 km south of the current location in 2007; therefore, hypothetical migration was 4.5 km yr-1. Rhizophora mangle We found the northernmost Red Mangrove (Williams and Eastman s.n., USF) (Fig. 2) at 29º56.363'N, 81º18.928'W. The shrub was 137 cm in height, 3.6 D10, with 103 x 88 cm canopy dimensions. Chlorosis on the plant was low and thus we categorized it as healthy. Adjacent to the assessed individual, a small juvenile Red Mangrove was present as well as multiple seedlings. We made the observations along a subtidal tributary 300 m west of the Tolomato River main channel (Fig. 1). The abutting vegetation was S. alterniflora; however, the majority (>50%) of the marsh north of the two Red Mangrove trees was inhabited by Black Mangroves. During on-site authentication efforts, we located the remnants of a Red Mangrove (1.8 m in height) at 29º58.774'N, 81º19.541'W, on a marsh 4.5 km north of the present record. We made the initial observation of the northernmost Red Mangrove 19 March 2013 and comprehensively verified 27 March 2013. The prior outlying Red Mangrove record (Zomlefer et al. 2006) is located 26 km south of the current location, and hypothetical migration was thus 3.7 km yr-1. Laguncularia racemosa We found the northernmost White Mangrove (Williams and Eastman s.n., USF) (Fig. 2) at 29º43.510'N, 81º14.662'W. The juvenile shrub was 76 cm in height, 2.6 D10, with 95 x 69 cm canopy dimensions. Leaf coloration on the plant was 50% yellow, and so we categorized it as intermediately stressed. The location of the northernmost White Mangrove on a subtidal creek bank was 200 m east of the Matanzas River channel in the GTM estuary (Fig. 1). Similar to the other records, S. alterniflora surrounded the individual, although Black and Red Mangroves greater than 2 m in height were dominant in 20- to 30-m-long swaths in the surrounding riparian zone. We encountered the White Mangrove on 25 January 2013, and collected data on 1 March 2013. Examination of the surrounding intertidal zone showed that no other White Mangroves were present. The specimen collections at the USF Herbarium have not verified White Mangrove distribution north of Volusia County. Based on crude mapping and site details, the current observation in the GTM estuary is 67 km north of historic observations, and hypothetical White Mangrove migration was thus 1.3 km yr-1. Discussion All record mangroves were present as morphological scrubs which had been growing for 12–18 months prior to evaluation. Observations were made during late winter, when cold stress is presumably at an annual peak. The northernmost White Mangrove appeared mildly affected by recent cold but was likely to recover in spring and summer. At each site, vegetation appeared similar to descriptions in Perry and Mendelssohn (2009) from Louisiana, in which mangroves were increasingly dominant in S. alterniflora marshes. Hypothetical spread rate was high for all three species. These individual trees may have been unnoticed in the GTM intertidal; Southeastern Naturalist A.Williams, S. Eastman, W. Eash-Loucks, M. Kimball, M. Lehmann, and J. Parker 2014 Vol. 13, No. 1 62 however, the “exhaustive surveys” described by Zomlefer et al. (2006) and the timeframe since previous vouchers (Ray 11136, USF; Wunderlin and Hansen 2008) suggest otherwise. Semidiurnal north-to-south tides may enhance propagule dispersal within the estuary during occasions in which thermal conditions are more appropriate for expansion. As evidenced by the dead Red Mangrove north of the record, conditions unfavorable to mangrove survival have recently occurred as well. More importantly, the mangrove and saltmarsh interface at GTM is gradual. The sequential or gradient structure of the ecotone suggests altered thermal conditions. Black Mangrove cold tolerance is greater than Reds and Whites (Odum and McIvor 1990), which may explain why that species is more widely represented in the estuary, and it appears to pioneer new habitat. While climate transitions are not geographically precise, thermal conditions within the 40 km examined here do not vary enough to explain the recorded gradient in mangrove presence. The conditions found in the southern estuary are similar to those in the north, and the abundance of mangroves in the south and absence in the north is interpreted as an expansion, rather than the effect of declining habitat suitability. Because the conditions are similar throughout the GTM estuary, these northernmost mangroves are not fortuitous waifs; they are likely the initial occupants of recently available habitat. This report is the first evidence of northern migration of the mangrove ecotone on the United States Atlantic coast. Such observations do not necessarily support that mangrove range expansion on the Atlantic coast will extend into the future, but provide insight into a recent migration wherein conditions, including climate, necessary for the establishment of these species were consistent for several years preceding the study. This pattern may also represent habitat oscillation due to an optimized local climate; however, the healthy condition of each record tree suggests otherwise. These records are specific benchmarks for future evaluation of the northern limits of endemic mangroves on the United States Atlantic coast and extend all current distributions beyond historic records. Acknowledgments Bruce Hansen expediently vouchered plant samples into the USF Herbarium. Tom Harding observed potential northernmost mangroves, which was part of the impetus to formalize the locations. Critical insights were provided by two anonymous reviewers. 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