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Range Expansion of Aratus pisonii (Mangrove Tree Crab) into Novel Vegetative Habitats
Megan E. Riley, Cora A. Johnston, Ilka C. Feller, and Blaine D. Griffen

Southeastern Naturalist, Volume 13, Issue 4 (2014): N43–N48

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N43 2014 Southeastern Naturalist Notes Vol. 13, No. 4 M.E. Riley, C.A. Johnston, I.C. Feller, and B.D. Griffen Range Expansion of Aratus pisonii (Mangrove Tree Crab) into Novel Vegetative Habitats Megan E. Riley1,*, Cora A. Johnston2, Ilka C. Feller3, and Blaine D. Griffen1, 4 Abstract - As ecological communities migrate northward with climate change, associated species are expected to accompany habitat-forming, foundation species. However, differences in physiological limitations and/or sensitivity to climatic cues can cause spatial or temporal mismatches in the expansion of foundation species and associated inhabitants. Here, we document novel habitat switching by an inhabitant that has outpaced its traditional habitat. We provide the first report of the typically mangrove-associated Aratus pisonii (Mangrove Tree Crab) in temperate salt marsh habitats along Florida’s Atlantic coast. Mangrove Tree Crab is present in salt marshes as far north as Little Satilla Creek, GA (31°5'32''N), substantially further north than the northernmost mangrove (~30°N). Based on historical records of the range limit of Mangrove Tree Crab and its current distribution, we calculate that the species has moved northward at a rate of 62 km per decade over the last century, outpacing the range expansions of the foundation species (13–45 km/decade) with which it has traditionally been associated. The geographic ranges of most species are limited by climatic factors, and changes in global climate trends, particularly warming temperatures, have enabled marine and terrestrial species from a wide array of taxa to shift or expand their distributions northward (Chen et al. 2011, Poloczanska et al. 2013). The responses of habitat-forming organisms to climate change are of particular interest because these foundation species provide habitat for diverse resident species. Northward range expansions have been documented for a number of foundation species (e.g., Kim et al. 2012, Saintilan et al. 2014, Yamano et al. 2011), and some of these range expansions have facilitated the northward movement of taxa that are associated or have obligate relationships with them (e.g., Yamano et al. 2012). However, differences in the type and timing of species’ responses to climate change enable some organisms to expand their ranges more quickly than others, and thus some animal species may expand their ranges faster than the foundation species with which they have traditionally been associated. Here, we provide the first report of the range expansion of Aratus pisonii H. Milne Edwards (Mangrove Tree Crab), a tropical and subtropical mangrove-associated species, whose range expansion has outpaced that of its native associated species and led to its establishment in novel temperate salt marsh habitats. Mangrove Tree Crab is abundant throughout Neotropical mangrove systems from Brazil to Florida, including the Caribbean, and along the eastern Pacific coast from Nicaragua to Peru (Chace and Hobbs 1969, Rathbun 1918). These grapsid crabs are highly adapted to the complexity of Avicennia germinans (L.) L. (Black Mangrove), Laguncularia racemosa (L.) C.F. Gaertn (White Mangrove), and Rhizophora mangle L. (Red Mangrove) habitats. They have a unique arboreal lifestyle and consume large amounts of fresh mangrove leaves, which make up an estimated 84% of their diet (Beever et al. 1979, Erickson et al. 2003). They are the dominant folivore on Red Mangrove in Florida, Belize, and Panama (Feller et al. 2013). Although Mangrove Tree Crabs preferentially feed on leaves 1Department of Biological Sciences, University of South Carolina, Columbia, SC 29208. 2Biological Sciences, University of Maryland, College Park, MD 20742. 3Smithsonian Environmental Research Center, Smithsonian Institution, Edgewater, MD 21037. 4Marine Science Program, University of South Carolina, Columbia, SC 29208. *Corresponding author - riley.megan.e@gmail.com. Manuscript Editor: Arthur Schwarzschild Notes of the Southeastern Naturalist, Issue 13/4, 2014 2014 Southeastern Naturalist Notes Vol. 13, No. 4 N44 M.E. Riley, C.A. Johnston, I.C. Feller, and B.D. Griffen of Red Mangroves, they also feed on Black and White Mangrove leaves in mixed stands throughout Florida (Beever et al. 1979). Previously published reports of Mangrove Tree Crab’s range indicate that their distribution was once limited to that of mangroves (Beever et al. 1979, Chace and Hobbs 1969, Rathbun 1918, Warner et al. 1967) and to docks and pilings adjacent to natural habitats (Beever et al. 1979). Observations of numerous (>50) Mangrove Tree Crabs clinging to Spartina alterniflora Loisel (Smooth Cordgrass) among mixed marsh and mangrove vegetation at Fort Matanzas National Monument (29°43'8''N, 81°14'32''W) in August 2012 prompted us to speculate that like many other marine and terrestrial species, Mangrove Tree Crab is expanding its range northward in response to a warming climate. Mangroves are expanding their ranges northward and encroaching on salt marsh vegetation globally (Saintilan et al. 2014); in Florida, Mangroves have experienced a substantial northward expansion along the Atlantic coast in the last 30 years due to a decrease in the frequency of extreme cold events (Cavanaugh et al. 2014). Recent estimates of their range expansion indicate that White, Red, and Black Mangroves are expanding northward at a rate of 13, 37, and 45 km per decade, respectively (Williams et al. 2014). However, the presence of Mangrove Tree Crab in mixed marsh and mangrove vegetation near the northernmost limit of mangrove habitat suggested that Mangrove Tree Crab might be expanding northward more quickly than the dominant plant species in typical mangrove habitat, leading to the crab’s establishment in salt marshes north of the northernmost mangrove trees. In order to determine whether the Mangrove Tree Crab has expanded its range northward into salt marsh habitats beyond the range limit of mangroves, we conducted a distributional survey in June, July, and August 2013 along the Atlantic coast of Florida and southern Georgia that included the current mangrove–salt marsh ecotone (i.e., transition zone). The ecotone extends from 28°N to 30°N, with the northernmost mangrove occurring just north of St. Augustine, FL (Cavanaugh et al. 2014, Williams et al. 2014). Our survey spanned 27°33'2'' N to 31°5'32''N latitude, and included two pure mangrove sites, 3 mixed sites with marsh and mangrove vegetation, and 5 pure salt marsh sites (Table 1, Fig. 1). Mangrove Tree Crabs, including ovigerous females, were present at 9 of the 10 survey sites (Table1; Figs. 1, 2). Our 2 northernmost survey sites, Little Satilla Creek, GA, and Jekyll Island, GA, were both at approximately 31°N. We found 5 Mangrove Tree Crabs at Little Satilla Creek, and no individuals at Jekyll Island (Table 1), suggesting that the current northernmost limit of Mangrove Tree Crab occurs at ~31°5'N latitude. Here, we provide the first report of Mangrove Tree Crab establishment in mixed mangrove and salt marsh habitats, as well as exclusively salt marsh vegetation as far north as Little Satilla Creek, GA (31°5'32''N). This site is 152, 128, and 109 km north of the northernmost White, Red, and Black Mangrove occurrence, respectively. A historical record from 1918 documents the northernmost limit of Mangrove Tree Crab on the eastern coast of Florida as Miami, FL (25°48'N; Rathbun 1918), suggesting that Mangrove Tree Crab has expanded its range at a rate of 62 km per decade over the last century. This rate of range expansion, which is faster than that of the three mangrove species present in Florida, is consistent with reports of other marine species expanding their ranges at an average rate of 72 km per decade (Poloczanska et al. 2013). Future work is necessary to understand the ecological impact of Mangrove Tree Crab’s establishment in salt marshes, as well as the potential alterations in resource use and life-history strategy associated with the crab’s range expansion. Species-specific responses to climate change that lead to spatial mismatches between animals and foundation species have the potential to create novel community assemblages, N45 2014 Southeastern Naturalist Notes Vol. 13, No. 4 M.E. Riley, C.A. Johnston, I.C. Feller, and B.D. Griffen Table 1. Location of survey sites, including descriptions of habitat type, vegetation present at site, and distribution of Mangrove Tree Crab. Y = yes, N = no. Ovigerous White Red Black Smooth Mangrove Mangrove Survey site Latitude (°N) Longitude (°W) Habitat type Mangrove Mangrove Mangrove Cordgrass Tree Crab Tree Crab Little Satilla Creek 31°5'32'' 81°34'15'' Salt marsh N N N Y Y Y Jekyll Island 31°2'50'' 81°25'9'' Salt marsh N N N Y N N Crooked River State Park 30°50'43'' 81°33'35'' Salt marsh N N N Y Y Y Fernandina Beach 30°40'6'' 81°27'59'' Salt marsh N N N Y Y Y Big Talbot Island State Park 30°30'38'' 81°27'39'' Salt marsh N N N Y Y Y Anastasia State Park 29°52'11'' 81°16'24'' Mixed marsh N N Y Y Y Y Devil’s Elbow 29°45'16'' 81°15'8'' Mixed marsh N N Y Y Y Y Fort Matanzas National Monument 29°43'31'' 81°14'36'' Mixed marsh N Y Y Y Y Y Sebastian Inlet State Park 27°51'3'' 80°27'3'' Mangrove Y Y Y N Y Y Avalon State Park 27°33'2'' 80°19'37'' Mangrove Y Y Y N Y Y 2014 Southeastern Naturalist Notes Vol. 13, No. 4 N46 M.E. Riley, C.A. Johnston, I.C. Feller, and B.D. Griffen such as the one described here. IN both terrestrial and marine systems, novel communities resulting from decoupled species interactions may present serious challenges to policy makers and resource managers, and thus should be of particular interest as climate change advances (Hoegh-Guldberg and Bruno 2010, González-Varo et al. 2014). Acknowledgments. This work was supported by NSF (OCE-1129166 and EF1065821), NASA (NNX-11AO94G), the Link Foundation, Binghamton, NY, and the Slocum-Lunz Foundation, Charleston, SC. This is contribution no. 954 of the Smithsonian Marine Station at Fort Pierce, FL. Figure 1. Sites along the Atlantic coast of southern Georgia and Florida where Mangrove Tree Crab was documented during surveys in June–August 2013. Sites (north to south): Little Satilla Creek, GA; Crooked River State Park, GA; Fernandina Beach, FL; Big Talbot Island State Park, FL; Anastasia State Park, FL; Devil’s Elbow, FL; Fort Matanzas National Monument, FL; Sebastian Inlet State Park, FL; and Avalon State Park, FL. Mangrove distribution data from Osland et al. 2013. N47 2014 Southeastern Naturalist Notes Vol. 13, No. 4 M.E. Riley, C.A. Johnston, I.C. Feller, and B.D. Griffen Figure 2. Mangrove Tree Crab clinging to Smooth Cordgrass at (A) Fort Matanzas National Monument , FL, and (B) Big Talbot Island State Park, FL, in August 2013. 2014 Southeastern Naturalist Notes Vol. 13, No. 4 N48 M.E. Riley, C.A. Johnston, I.C. Feller, and B.D. Griffen Literature Cited Beever, J.W., D. Simberloff, and L.L. King. 1979. Herbivory and predation by the Mangrove Tree Crab, Aratus pisonii. Oecologia 43:317–328. Cavanaugh, K.C., J.R. Kellner, A.J. Forde, D.S Gruner, J.D. Parker, W. Rodriguez, and I.C. Feller. 2014. Poleward expansion of mangroves is a threshold response to decreased frequency of extreme cold events. Proceedings of the National Academy of Sciences 111(2):723–727. Chace, F.A., and H.H. Hobbs. 1969. 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