Stony coral (Milleporidae and Scleractinia) communities in the eastern Gulf of Mexico: a synopsis with insights from the Hourglass collections

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1 FastTrack publication Bull Mar Sci. 91(2): coral reef paper Stony coral (Milleporidae and Scleractinia) communities in the eastern Gulf of Mexico: a synopsis with insights from the Hourglass collections Lithophyte Research Team W, 273 Catalan Blvd. NE, Saint Petersburg, Florida <wjaap@tampabay. rr.com>, telephone: (727) , mobile (727) Date Submitted: 3 July, Date Accepted: 3 February, Available Online: 19 March, Walter C Jaap ABSTRACT. The eastern Gulf of Mexico is a complex mosaic of coral reefs and epibenthic communities. Although it is a large area of approximately 225,000 km 2, only a small portion sustains viable coral reefs. In the lower margins of the eastern Gulf of Mexico (Key West to Dry Tortugas, N), the coral reef communities are speciose and very similar to Caribbean coral reefs. Controlling factors influencing the distribution of the hydrozoan Millepora and Scleractinian species include climate, the lack of a consistent current system to support larval transport, and stochastic disturbances, such as red tide harmful algal blooms, hurricanes, and winter frontal passages. In the eastern Gulf of Mexico region north of 26 N (Naples), the fauna is more eurytopic; characteristic species inhabiting the rocky hard bottom include Cladocora arbuscula (Lesueur, 1820), Siderastrea radians (Pallas, 1766), Solenastrea hyades (Dana, 1846), Manicina areolata (Linnaeus, 1758), and Isophyllia sinuosa (Ellis and Solander, 1786). Isolated locations, such as the Florida Middle Grounds and Pulley Ridge, sustain the more reef-dwelling-stenotopic species: Leptoseris cuccullata (Ellis and Solander, 1786); Dichocoenia stokesi Milne-Edwards and Haime, 1848; and Meandrina meandrites (Linnaeus, 1758). The present study focuses on the Hourglass collection of Scleractinian coral samples collected from August 1965 through November 1967 in the eastern Gulf of Mexico offshore of Tampa Bay (27 35 N) and Sanibel Island (26 24 N), from 6 to 73 m depths. The zooxanthellate Milleporidae and Scleractinia are important foundations for biodiversity in the eastern Gulf of Mexico. Their ability to construct limestone edifices makes them ecologically significant; they provide multiple ecological services, such as habitat for concentrated populations of organisms, micro-niche habitats with unique flora and fauna, and support fisheries and recreational tourism. Coral reef habitat off Florida takes many forms over a broad area from Stuart or St. Lucie inlet (27 10 N) on the east coast (Monte 2008) to the Florida Middle Grounds (28 35 N) on the west coast (Jaap and Hallock 1990, Moyer et al. 2003, Banks et al. 2007, 2008, Hine et al. 2008, Jaap 2008, Jaap et al. 2008). The broad-shallow continental shelf off the west coast of Florida provides a large potential area for coral reef development. Rohmann et al. (2005) estimated that Florida shallow-water, coral reef habitat includes 30,801 km 2, the majority of which is situated in the Gulf of Mexico. Bulletin of Marine Science 2015 Rosenstiel School of Marine & Atmospheric Science of the University of Miami 1

2 2 Bulletin of Marine Science. Vol 91, No Conversely, a compiled estimate for Palm Beach, Broward, Miami-Dade, and Monroe counties off the east coast of Florida is only 1450 km 2. Hine et al. (2008) estimated that the west Florida shelf includes 225,000 km 2 ; potentially 13% (29,250 km 2 ) of the seafloor may be occupied by coral-sponge communities based on Rohmann s et al. (2005) projections. The Florida coral reef area estimate dwarfs other US reef areas; for example, the reef area for Guam is 16 km 2 ; Main Hawaiian Islands, 1231 km 2 ; and Puerto Rico, 2208 km 2 (Rohmann et al. 2005), plus Mexican estimates in the southern Gulf of Mexico of 384 km 2 [Tuxpan 3 km 2, north Veracruz 10 km 2, South Veracruz 36 km 2, Alacrán 325 km 2, and Campeche Bank 10 km 2 (Tunnell 2007)]. The present study synthesizes research conducted from 1959 through 2005 using multiple sampling methods ranging from dredge and trawl, diving, and high technology (submersibles and ROVs). Fundamental understanding of the area s biological richness is important in the context of natural (harmful algal blooms, hurricanes, extreme thermal stress) and anthropogenic [oil spills, nutrient enrichment, ocean chemistry (ph), and global climate changes] disturbances. Climate change has a potential to radically alter the environment. Warming trends, greater numbers of hurricanes, changes in ocean chemistry, rising sea level, and storm surges could bring major changes to the community structure of the eastern Gulf of Mexico reef communities. This area is strongly dependent upon a healthy environment for tourism, education (multiple marine science education and research institutions), and fishing. Corals are a proxy for the health of the entire ecosystem; we may look at them as our oceangoing canary in the coal mine. A detailed species account of the Hourglass Milleporidae and Scleractinia is provided as an online appendix to augment this report. Milleporidae Species in the family Milleporidae: Hydrozoa: Cnidaria are common in western Atlantic coral reef communities. Their endodermic tissues contain zooxanthellae, exhibiting a color range of gold to chocolate brown (Fig. 1). Colonies are composed of upstanding plates or branches or are encrusting (Boschma 1956). There are three species of Millepora in the Gulf of Mexico: Millepora alcicornis, Millepora complanata, and Millepora squarosa; M. alcicornis is the most ubiquitous species and is found throughout the gulf in 1 55 m depths (Calder and Cairns 2009). See Table 1 for coral species authorities and dates. Scleractinia Species in the order Scleractinia are sedentary and either colonial or solitary, exclusively polypoid hexacorallian Anthozoa: Cnidaria. Scleractinian polyps are supported by an aragonitic calcium carbonate skeleton called a corallum (descriptions are compiled from Vaughan and Wells 1943, Wells 1956, Veron 2000, Cairns et al. 2009). Each polyp bears six or a multiple of six pairs of mesenteries; each pair encloses a calcareous radial aragonite partition called a septum. Scleractinian corals have 12, 24, 48, or 96 or more septa arranged in a radial, hexameral plan. Common names applied to the order Scleractinia include: stony corals and hard corals. The taxonomy employed throughout the manuscript follows Cairns et al. (2009); revision of Montastraea annularis to the genus Orbicella is not followed here; this paper was far advanced in its process when Budd et al. s revision was published.

3 Jaap: Stony corals of the eastern Gulf of Mexico 3 Figure 1. Millepora alcicornis. Photo from Florida Middle Grounds, ridge top, 21 m, May Photo credit: G Schmahl. Physiologically/ecologically (and, to some degree, phylogenetically), Scleractinia can be divided into two groups: those that contain zooxanthellae in their tissues (zooxanthellate species, ZS) and those that do not (azooxanthellate species, AS). Worldwide, both groups have approximately the same number of species (Cairns et al. 1999). Zooxanthellate species contain dinoflagellate alga of the genus Symbiodinium; colors range from iridescent blue to maroon-red; however, gold to brown are more common. The ZS are typically found in tropical-subtropical regions in depths that rarely exceed 70 m (however, in localities with very clear water, some species such as Leptoseris cucullata may occur as deep as 90 m). The ZS include massive species attaining sizes exceeding 3 m in diameter and height (Colpophyllia natans and M. annularis), as well as inconspicuous species such as Cladocora arbuscula and Favia fragum that are <10 cm in diameter. The ZS species are virtually all colonial (multiple polyps, an exception is the genus Scolymia, it is a solitary ZS, which occasionally has fused multiple polyps); their outward morphology includes branching, columnar, encrusting, foliaceous, and massive skeletal structures (Fig. 2). The azooxanthellate corals are ubiquitous but most common in cooler, deeper water (down to 6300 m) or cryptic shallow-water environments, such as caves. The AS are common throughout the Gulf of Mexico; for details on species and distribution, refer to Cairns et al. (1991, 2002, 2009). Within a ZS species, morphology varies greatly, reflecting local environmental conditions and genetic heritage; depth (ambient light), water movement, sedimentation, and temperature are important contributing factors (Wells 1957). Some deep water AS colonial corals, such as Lophelia pertusa (Linnaeus, 1758), may form extensive reef systems at 200 to 400 m depths (Wilson 1979, Cairns and Stanley 1982,

4 4 Bulletin of Marine Science. Vol 91, No Figure 2. Examples of eastern Gulf of Mexico zooxanthellate Scleractinia: (A) Siderastrea radians photo from Smith Shoal, 6 m, July (B) Acropora cervicornis, photo from Western Sambo, 4 m, July (C) Agaricia agaricites, photo from Western Sambo, 4 m, July (D) Leptoseris cuccullata, photo from Pulley Ridge, Deep Worker submersible, 23 m, July Photo credits: WC Jaap. Cairns et al. 2009); Lophelia reefs off Norway are 5 to 31 m high and greater than 50 m wide at their base (Hovland et al. 2001). There are a few species (e.g., Astrangia poculata and Madracis pharensis) that may or may not have zooxanthellae in their endodermic tissues (Wells 1973, Peters et al. 1988). Solenastrea hyades is reported to expel and regain zooxanthellae on a seasonal basis in Onslow Bay, North Carolina (M Wells, pers comm). The majority of species in the present study are ZS; however, there are a few AS colonial species in the assemblages (Madracis asperula, Oculina tenella, Cladocora debilis, A. poculata, Phyllangia americana). Classification, distribution, morphology, biology, and paleontology of the Scleractinia have been described by Vaughan and Wells (1943), Wells (1956), Veron (2000), and Cairns et al. (2009). The ZS found in the Gulf of Mexico were first reported and described in the pioneering studies of Louis and Alexander Agassiz (1852, 1869, 1880, 1882, 1885), Pourtalès (1880), Heilprin (1890), Vaughan (1901a,b, 1909), and Verrill (1902). Smith (1948, 1954) suggested incorrectly that Gulf of Mexico Scleractinia did not build extensive reefs. Understanding ZS in the Gulf of Mexico area benefited greatly from work off The Bahamas and Florida that refined the descriptions, photo-documented species in their natural habitat, and established bathymetric ranges, ecological relationships, and paleontology (Table 2, Online Appendix 1).

5 Jaap: Stony corals of the eastern Gulf of Mexico 5 Table 1. List of eastern Gulf of Mexico Milleporidae and Scleractinia (Cairns et al and personal observations). Phylum Cnidaria Class Hydrozoa, Owen, 1843 Order Anthoathecata Family Milleporidae Fleming, 1828 Millepora alcicornis Linnaeus, 1758 Millepora complanata Lamarck, 1816 Class Anthozoa Ehrenberg, 1834 Order Scleractinia Bourne, 1900 Family Astrocoeniidae Koby, 1890 Stephanocenia intersepta Milne-Edwards and Haime, 1848 Family Pocillopridae Gray, 1842 Madracis asperula (Milne-Edwards and Haime, 1949) Madracis decactis (Lyman, 1859) Madracis pharensis (Heller, 1868) Madracis mirabilis (sensu Wells, 1973 Madracis formosa Wells, 1973 Family Acroporidae Verrill, 1902 Acropora cervicornis (Lamarck, 1816) Acropora palmata (Lamarck, 1816) Acropora prolifera (Lamarck, 1816) 1 Family Agariciidae Gray, 1847 Agaricia agaricites (Linnaeus, 1758) Agaricia forma agaricites (Linnaeus, 1758) Agaricia forma purpurea (LeSeuer, 1821) Agaricia forma carinata Wells, 1973 Agaricia humilis Verrill, 1901 Agaricia lamarcki Milne-Edwards and Haime, 1851 Agaricia fragilis (Dana, 1846) Leptoseris cucullata (Ellis and Solander, 1786) Family Siderastreidae Vaughan and Wells, 1943 Siderastrea radians (Pallas, 1766) Siderastrea siderea (Ellis and Solander, 1786) Family Poritidae Gray, 1842 Porites astreoides Lamarck, 1816 Porites branneri Rathbun, 1887 Porites porites (Pallas, 1766) Porites forma porites (Pallas, 1766) Porites forma clavaria Lamarck, 1816 Porites forma furcata Lamarck, 1816 Porites forma divaricata LeSueur, 1821 Family Faviidae Gregory, 1900 Favia fragum (Esper, 1795) Favia gravida Verrill, 1868 Diploria labyrithiformis (Linnaeus, 1758) Diploria clivosa (Ellis and Solander, 1786) Diploria strigosa (Dana, 1846)

6 6 Bulletin of Marine Science. Vol 91, No Table 1. Continued. Family Faviidae Gregory, 1900 Manicina areolata (Linnaeus, 1758) Manicina forma areolata (Linnaeus, 1758) Manicina forma mayori Wells, 1936 Colpophyllia natans (Houttuyn, 1772) Montastraea annularis (Ellis and Solander, 1786) Montastraea forma annularis (Ellis and Solander, 1786) Montastraea forma faveolata (Ellis and Solander, 1786) Montastraea forma franksi (Gregory, 1895) Montastraea cavernosa (Linnaeus, 1767) Solenastrea hyades (Dana, 1846) Solenastrea bournoni (Milne-Edwards and Haime, 1849) Family Rhizangiidae D Orbigny, 1851 Astrangia solitaria (LeSueur, 1817) Astrangia poculata (Milne-Edwards and Haime, 1848) Family Oculinidae Gray, 1847 Oculina diffusa Lamarck, 1816 Oculina robusta Pourtalès, 1871 Oculina tenella Pourtalès, 1871 Family Meandrinidae Meandrina meandrites (Linnaeus, 1758) Meandrina forma meandrites (Linnaeus, 1758) Meandrina forma danai Milne-Edwards and Haime, 1848 Dichocoenia stokesi Milne-Edwards and Haime, 1848 Dendrogyra cylindrus Ehrenberg, 1834 Family Mussidae Ortmann, 1890 Mussa angulosa (Pallas, 1766) Scolymia lacera (Pallas, 1766) Scolymia cubensis (Milne-Edwards and Haime, 1849) Isophyllia sinuosa (Ellis and Solander, 1786) Isophyllastrea rigida (Dana, 1846) Mycetophyllia lamarckiana (Milne-Edwards and Haime, 1849) Mycetophyllia danaana (Milne-Edwards and Haime, 1849) Mycetophyllia ferox Wells, 1973 Mycetophyllia aliciae Wells, 1973 Family Caryophylliidae Cladocoral arbuscula (LeSueur, 1821) Cladocora debilis Milne-Edwards and Haime, 1849 Phyllangia americana Milne-Edwards, 1850) Eusmilia fastigiata (Pallas, 1766) 1 Designated an F1 hybrid (Vollmer and Palumbi 2002) Geography The Gulf of Mexico (GOM) is a marginal sea, 1500 km 2, with no major islands, open to the south (Straits of Florida and Yucatán), and surrounded by continental land masses (North and Central America). Distance east west (Tampa Bay Tampico) is 1983 km and north south (Galveston Mérida) is 1195 km. Sandy barrier islands

7 Jaap: Stony corals of the eastern Gulf of Mexico 7 parallel the west coast of Florida as far north as Tarpon Springs (28 10 N). Salt marshes and coastal swamps replace mangroves north of Tarpon Springs along Alabama, Mississippi, and Louisiana to Texas. Barrier islands are again prominent off Texas to the Mexico border. Coral cays (solitary islands and archipelagos formed principally by coral reef strata) are a unique feature off the Yucatán Peninsula, east coast of Mexico, and the Florida Keys. The continental shelf is broad and relatively shallow on both the eastern and western margins of the Gulf of Mexico. The shelf terminates in steep escarpments off the west coast of Florida, the Campeche Escarpment to the south, and the Sierra Madre Oriental on the east coast of Mexico; the basin is up to 3700 m deep. The Gulf of Mexico has its origin in the Triassic Period, following separation of the African, North American, and South American plates (Liddell 2007). Galtsoff (1954) defined the southern boundaries of the Gulf of Mexico to include a portion of the Straits of Florida and Yucatán as follows: Cabo Catoche, Quintana Roo, Mexico (21 33 N, W), those in waters north of a line from Cabo Catoche, Mexico, to Cabo de San Antonio, Cuba (21 51 N, W), those from coastal waters and tidal wetlands between Cabo de San Antonio and Punta Hicacos, Cuba (23 12 N, W), and those from waters and tidal wetlands of the Florida Straits and Florida Keys on or west of a line from Punta Hicacos, Cuba to the vicinity (along the coast) of Key Largo, Florida (25 06 N, W). This delineation thus includes all waters and tidal wetlands extending to the eastern extreme of Florida Bay. It excludes Cay Sal Bank as well as the extensive system of islands and estuaries east of Punta Hicacos, Cuba (Galtsoff 1954, introduction). The Key Largo coordinate is a position near South Sound Creek in John Pennekamp Coral Reef State Park. These geographic boundaries were used in an extensive review of the Gulf of Mexico Scleractinia (Cairns et al. 2009). Eastern Gulf of Mexico boundaries in the present study include the Florida Middle Grounds, Hourglass region, and Pulley Ridge, southeast to Dry Tortugas and the Content Keys, to reefs south of Key West, including Western Sambo to Sand Key (Fig. 3). Methods Data were compiled from multiple studies (Table 3). Field sampling methods included diver quadrat and transect inventories, video transects, dredge, and trawl collections. Samples were classified as Florida Middle Grounds (FMG), central-eastern Gulf of Mexico (CE), Florida Bay (FB), Pulley Ridge (PR), southeast Gulf of Mexico (SE), and Dry Tortugas (DT). The following section is a narrative describing the sampling areas: FMG, CE, FB, PR, SE, and DT. Sampling Details Florida Middle Grounds. The Florida Middle Grounds (FMG) reef complex is located between and N and and W (Fig. 3A). Individual carbonate banks are 12 to 15 m in height and crest at approximately 25 to 30 m below sea level. Brooks (1962, 1966) suggested that the FMG are Holocene or late Pleistocene in age. Reich et al. (2013) discovered that the FMG eastern ridge was an unconsolidated mass of muddy sand, overlain by a 3.6 m thick carbonate cover, mostly constructed by a vermetid gastropod mollusk, Petaloconchus sp. Uncorrected carbon dating was 8225 (SE 30) to 8910 (SE 25) YBP, a period of relatively stable, low stands for sea level.

8 Figure 3. Sampling locations, eastern Gulf of Mexico, west Florida shelf. (A) Florida Middle Grounds (FMG) and Bay Point Ledge (BP); (B) Hourglass (HG) and Tampa Bay ledge (TB); (C) Dry Tortugas (BK, PS, TPR, TR, WSH), Tortugas Banks (BCR), and Pulley Ridge (PR); (D) Florida Bay (SS, CK) and Lower Keys (SK, RK, WH, WSA). 8 Bulletin of Marine Science. Vol 91, No

9 Jaap: Stony corals of the eastern Gulf of Mexico 9 Table 2. Supporting historically important studies from Florida, Caribbean, The Bahamas, and Gulf of Mexico. Area Publication Location The Bahamas Newell et al Andros Island The Bahamas Squires 1958 Bimini The Bahamas Storr 1964 Abaco The Bahamas Chiappone et al Exuma Cays The Bahamas Jaap and Olson 2000 Grand Bahama Barbados Lewis 1960a,b Barbados Barbados Ott 1975 Barbados Barbados James et al Barbados Cayman Islands Roberts 1977 Grand Cayman Colombia Pfaff 1969 Islas del Rosario Colombia Antonius 1972 Santa Marta Colombia Geister 1973 Isla de San Andrés Eastern Gulf of Mexico Godcharles and Jaap 1973 Eastern Gulf Eastern Gulf of Mexico Lyons and Collard 1974 Eastern Gulf Eastern Gulf of Mexico Grimm and Hopkins 1977 Florida Middle Grounds Eastern Gulf of Mexico Cairns 1977 Hourglass Eastern Gulf of Mexico Coleman et al Florida Middle Grounds Eastern Gulf of Mexico Halley et al Pulley Ridge Eastern Gulf of Mexico Hine et al Eastern Gulf Eastern Gulf of Mexico Davis 1982 Dry Tortugas Eastern Gulf of Mexico Shinn and Jaap 2005 Dry Tortugas Eastern Gulf of Mexico Jaap et al. 1989, 2008 Dry Tortugas Northern Gulf of Mexico Parker 1960 Flower Garden Banks Northern Gulf of Mexico Edwards 1971 Flower Garden Banks Northern Gulf of Mexico Bright et al Stetson Bank Northern Gulf of Mexico Tresslar 1974 Flower Garden Banks Northern Gulf of Mexico Bright 1977 Flower Garden Banks Northern Gulf of Mexico Rezak et al Flower Garden Banks Northern Gulf of Mexico Bright et al Flower Garden Banks Northern Gulf of Mexico Schmahl et al Flower Garden Banks Western Gulf of Mexico Kornicker and Boyd 1962 Alcran Reef Western Gulf of Mexico Moore 1958 Blanquilla Reef Western Gulf of Mexico Santiago-Fandiño 1977 Blanquilla Reef Western Gulf of Mexico Horta-Puga and Carricart-Ganivet 1989 Blanquilla Reef Western Gulf of Mexico Carricart-Ganivet and Beltrán-Torres 1997 Campechee Bank Western Gulf of Mexico Farrell et al Cayo Arcas Western Gulf of Mexico Busby 1966 Cayo Arenas Western Gulf of Mexico Rannefeld 1972 Isla Enmedio Reef Western Gulf of Mexico Horta-Puga and Carricart-Ganivet 1985 Isla Enmedio Reef Western Gulf of Mexico Lehman and Tunnell 1992 Isla Enmedio Reef Western Gulf of Mexico Rigby and McIntire 1966 Isla de Lobos Western Gulf of Mexico Villalobos 1971 Veracruz Western Gulf of Mexico Horta-Puga and Vargas-Hernandez 2003 Veracruz Western Gulf of Mexico Ganivet 1998 Veracruz Western Gulf of Mexico Beltrán-Torres and Carricart-Ganivet 1999 Compilation Gulf and Atlantic Western Gulf of Mexico Logan 1969 Yucatán shelf Western Gulf of Mexico Horta-Puga et al Compilation of SW Gulf

10 10 Bulletin of Marine Science. Vol 91, No Table 2. Continued. Area Publication Location Cuba Zlatarski and Estalella 1982 Cuba Jamaica Goreau 1959 Discovery Bay Jamaica Goreau and Wells 1967 Discovery Bay Martinique Adey et al. 1977a Caribbean Netherlands Antilles Roos 1964, 1971 Curaçao Netherlands Antilles Scatterday 1974 Bonaire Netherlands Antilles Bak 1975 Caribbean Panama Porter 1972 Caribbean Puerto Rico Almy and Carrión-Torres 1963 Caribbean Saint Lucia Roberts 1972 Caribbean US Virgin Islands Adey et al. 1977b Caribbean The interpretation is that the eastern FMG ridges developed as sandbars that were preserved by the colonization of Petaloconchus sp. (Reich et al. 2013). Benchmark studies have documented 103 species of algae, 40 sponges, 16 Scleractinian corals, 75 mollusks, 56 decapod crustaceans, 41 polycheates, 23 echinoderms, and 170 species of fishes (Smith et al. 1975, Grimm and Hopkins 1977, Hopkins et al. 1977). The FMG is the northernmost reef in the Gulf of Mexico with extensive ZS coral communities. A section of the FMG was designated a Habitat Area of Particular Concern (HAPC) in the Coral and Coral Reefs Fishery Management Plan under the Magnuson Act (Gulf of Mexico and South Atlantic Fishery Management Councils 1982). The FMG HAPC includes 119,349.6 ha (347.5 nmi 2, 294,908.9 acres). Sampling from this area includes Grimm and Hopkins (1977); two sites from a 1981 expedition: , , 24 m; , , 27 m; and Coleman et al. (2005) revisiting the Grimm and Hopkins sites. Additionally, multiple submersible dives were conducted at the FMG in May 2001 during the Sustainable Seas Expedition ( N and W, m); submersible dives provided observations, video and still photos, all used for coral identification. Central Eastern Gulf. The eastern Gulf of Mexico data sets (Fig. 3B) include the Hourglass Cruise collections (Joyce and Williams 1969), for which dredge and trawl samples were taken at 10 locations over a 28-mo period ( ). The Hourglass data are presented here for the first time. Species frequency of occurrence includes 30 samples (dredge and trawl samples were pooled). Hourglass stations A E were located off Anna Maria Island, Tampa Bay (27 37 N); Hourglass sampling stations I M were situated off Sanibel Island, Ft. Myers (26 24 N). Stations A, B, C, J, K, and L (6, 18, 37 m) were investigated in a qualitative manner by scuba divers, and sediments were collected for grain size analysis. Cairns (1977) published on the solitary corals, Caryophyllina and Dendrophylliina (Scleractinia Suborders); he reported six species and described two new species: Flabellum floridanum (Cairns, 1991) and Carophyllia horologium (Cairns, 1977). Each station was sampled with a rectangular box dredge ( cm) for 15 min and an otter trawl (6.1-m mouth opening, 5.1 cm mesh) for 15 or 30 min at a speed of approximately 1.03 m s 1 (2 kts) (Joyce and Williams 1969). Hourglass station characterizations compiled from Joyce and Williams (1969) follow.

11 Jaap: Stony corals of the eastern Gulf of Mexico 11 Figure 4. Ordination by non-metric multidimensional scaling (MDS) of Scleractinian assemblages; 29 locations in the eastern Gulf of Mexico based on abundance data that were square-root transformed prior to computing the Bray Curtis resemblance matrix. Uppercase letters in the plot identify sampling stations: FMG (Florida Middle Grounds), HG (Hourglass), BK, PS, TR, TPR, WS (Dry Tortugas), BCR (Tortugas Banks), PR (Pulley Ridge), CK, SS (Florida Bay), SK, RK, WH, WSA (Lower Keys). Symbols in right panel identify the sampling areas, polygons encircling multiple sampling stations identify sites that are strongly associated based on the similarity profile procedure (SIMPRO). The MDS plot is a good representation of the Bray-Curtis similarity matrix in that the stress (0.09) is very low. Stations A and I, 6 m. These stations were located directly west of Tampa and San Carlos Bays and are influenced by these large estuaries. The benthic habitat was characterized as quartz sand, crushed shell, and larger mollusk shells (Busycon and Atrina). Stations B and J, 18 m. Samples showed limestone outcroppings/ledges with topographic relief approaching one meter. Epibenthic communities on the ledges included algae, sponges, octocorals, scleractinian corals, and bryozoans. Sedimentary expanse between limestone edifices encompassed quartz sand and shell fragments; Caulerpa alga and Halophila sea grass were common in some sedimentary areas. Stations C and K, 37 m. These were situated on low-relief limestone hard bottom separated by sediments dominated by carbonate skeletal fragments. Loggerhead sponges, Spheciospongia vesparium (Lamarck, 1815), up to 1 m in diameter were common. The alga Sporochnus was ubiquitous, covering much of the bottom during diving observations. Stations D and L, 55 m. Mostly comprised of skeletal shell fragments, foraminiferal shells and silt were common in dredge samples. Fathometer tracings documented a smooth-flat bottom. A few loggerhead sponges, smaller sponge species, Lithothaminan alga. Steganoporella magnilabris (Busle, 1854), Hippopetraliella marginata (Canu and Bassier, 1928) (bryozoans) were the characteristic sessile organisms collected at these stations. Stations E and M, 73 m. Samples were mostly composed of mollusk, bryozoan, and calcareous algal fragments. Biological components in the dredge and trawls included calcareous algae, foraminiferal shells, small sponges, and bryozoans.

12 12 Bulletin of Marine Science. Vol 91, No Figure 5. Shade plot, visual representation of the species abundance matrix and sampling sites. Samples are in the x-axis, species in the y-axis. White spaces indicate absence of the species at that site; intensity of the grey scale is linearly proportional to square-root transformation of the relative abundance. Species dendrogram similarity based on standardized transformation and the coefficient of association. Clustering used group averages. Upper case letters in the x-axis identify sampling sites, left to right: PR (Pulley Ridge), WSA (Western Sambo), RK (Rock Key), SK (Sand Key), PS (Pulaski Shoal), WH (Western Head), WS (White Shoal), TPR (Temptation Rock), BCR (Black Coral Rock), TR (Texas Rock), BK (Bird Key), CK (Content Keys), FMG + number (Florida Middle Grounds stations), HG + letter (Hourglass stations), TBL (Tampa Bay ledge), BPL (Bay Point ledge). Species distribution contrasts are distinct; note the upper cluster from PR to CK includes the more tropical Caribbean species and from FMG 77 to HGA more temperate with more overlap for species such as Stephanocenia intersepta, Manicina areolata, and Oculina diffusa. Non-Hourglass samples in the central eastern Gulf, included ledges off Tampa Bay ( N, W, 17 m) and off Bayport ( N, W, 10.7 m) (see Figs. 4, 5). Pulley Ridge. Pulley Ridge (Fig. 3D) is remote and deep (approximately m); video from ROV and Sustainable Seas submersible investigations revealed a lowrelief, bottom topography with occasional karst-like depressions. The southern portion of the ridge is a drowned barrier island (Halley et al. 2005, Hine et al. 2008). The biota is dominated by a leafy green alga Anadyomene menziesii (J. E. Gray) J. Agardh, 1887 and large frondose plates of Leptoseris cucullata and Agaricia spp., including Agaricia lamarcki, Agaricia fragilis, and Agaricia undata. Other ZS species include Montastraea cavernosa and Madracis spp. The area also supports Antipatharia, Hexactinella, azooxanthellate octocorals, and comatulid crinoids. Southeast Gulf and Florida Bay. The Southeast data sets (Fig. 3C) include six sampling sites (Fig. 6) from the US EPA Water Quality Coral Reef Monitoring program (Porter et al. 2002, Somerfield et al. 2008). Western Sambo, Rock Key, and Sand Key are bank reefs with spur and groove formations. Western Head is a patch reef adjacent to the Key West shipping channel and inshore (north) of Sand Key. Smith Shoal is a patch reef complex located northwest of Key West. Content Keys is a hardbottom community located west of Big Pine Key. Smith Shoal and Content Keys are

13 Jaap: Stony corals of the eastern Gulf of Mexico 13 Figure 6. (A) Confidence funnels for taxonomic distinction and (B) variation in taxonomic distinction, randomized TADTEST. Funnel boundaries describe the upper and lower 95% confidence limits using 1000 permutations of selecting species randomly from a comprehensive master species list (compiled from Cairns et al. 2009) for the null distribution. Upper case letters identify sampling sites, PR (Pulley Ridge), WSA (Western Sambo), RK (Rock Key), SK (Sand Key), PS (Pulaski Shoal), WH (Western Head), WS (White Shoal), TPR (Temptation Rock), BCR (Black Coral Rock), TR (Texas Rock), BK (Bird Key), CK (Content Keys), FMG + number (Florida Middle Grounds stations), HG + letter (Hourglass stations), TBL (Tampa Bay ledge), BPL (Bay Point ledge). located at the margin of Florida Bay, a shallow estuary-lagoon. Data on relative species cover used here was derived from point count of video images from 2003 sampling (Somerfield et al. 2008). Dry Tortugas. Dry Tortugas (Fig. 3D) is a complex of islands, shoals, and coral reefs, situated km (60 70 mi) west of Key West, Florida, the westernmost extension of the Florida Reef Tract. Garden Key, occupied by Fort Jefferson, is the prominent upland feature. The seafloor is approximately 5% coral reef/hard bottom and 95% sedimentary/sea grasses within Dry Tortugas National Park, 25,899.9 hectares (100 mi 2 ) (Davis 1982, Shinn and Jaap 2005). Four reef types are found in the shallow areas: patch, bank, monotypic thickets of Acropora cervicornis (staghorn), and a single thicket of Acropora palmata (elkhorn). Patch reefs are most abundant south and west of Loggerhead Key; a chain of bank reefs extends south and east of Garden Key. The best examples of staghorn reefs, a predominant feature of Dry

14 14 Bulletin of Marine Science. Vol 91, No Tortugas in the 1970s, are found south of Garden Key harbor and on White Shoal. Acropora palmata is found in the breach leading into Garden Key harbor. Resident Dry Tortugas flora and fauna are typical of Caribbean reefs. Dry Tortugas coral fauna includes 63 taxa [species and forma (sensu Wells 1973)] of stony corals (Jaap et al. 1989); octocoral fauna includes more than 29 species (Jaap et al. 2008). Bird Key Reef, Dry Tortugas (BK, Fig. 3D) is approximately 2150 m long, 400 m wide from the reef crest to the terminus of the reef at 23 m; at that point it grades into sediments. Sampling included multiple line transects in 1975 and 1976 (Jaap et al. 1989). Pulaski Shoal, Dry Tortugas (PS, Fig. 3D) is approximately 12.8 km NE of Garden Key and just east of the navigation marker (light tower). Sampling quadrants were established in 8 to 11 m depths along a north south azimuth. The reef includes a low relief, horizontal limestone platform with sedimentary channels and a relatively steep escarpment that slopes to around 22 m and then grades into sediments. Octocorals dominate the horizontal upper platform; larger stony corals, sponges, and moderately abundant octocorals occupy the escarpment slope. Texas Rock, Dry Tortugas (TR, Fig. 3D), approximately 5.4 km NNW of Garden Key, is a patch reef, approximately 2 km in diameter. Surrounding depths are 20 m and the top of the reef platform is about 8 m deep. Massive buttresses, pinnacles, and canyons define the western margin of the reef. Large colonies of C. natans, M. annularis, and M. cavernosa are conspicuous on the pinnacles. Sampling quadrants were located in the western pinnacle area. Temptation Rock, Dry Tortugas, is approximately 2.9 km, 320 from Loggerhead Key. This is a high relief patch reef; many old and partially dead Montastraea colonies provide structural complexity. White Shoal, Dry Tortugas (WSH, Fig. 3D) is located 2.6 km NW of Garden Key. It is a sedimentary and rock-rubble shoal, with north-south orientation, 1 2 m deep on top with a steep escarpment on the east that descends to m. Sampling was on the upper slope in A. cervicornis rubble with a few larger colonies of M. annularis and C. natans. Southwest of the sixty-foot contour and outside the Dry Tortugas National Park boundaries, deep reefs (Tortugas Bank, N, W, and Riley s Hump, N, W) are common. Tortugas Bank is a complex carbonate structure approximately 20 km in length by 10 km wide at depths of m below sea level. Deep reef communities on Tortugas Banks are extensive with a complex structure dominated by moderate-sized, plate- and cone-shaped M. cavernosa colonies. Black coral (Antipatharia) and comattulid crinoids were observed at Black Coral Rock and Sherwood Forest. Data Processing To better understand eastern Gulf of Mexico reef communities a multivariate approach was used. The goals were to document community structure, dominant species, salient features that differentiate different areas, and to better understand the driving environmental factors that structure these communities. Data were drawn from the sources listed in Table 3, compiled in Excel, and imported into PRIMER versions 6 and 7 software (Clarke and Gorley 2006, Clarke et al. 2014a). The PRIMER data matrix was square-root transformed, based on shade plot analysis, so that the multivariate analyses would draw on species from across

15 Jaap: Stony corals of the eastern Gulf of Mexico 15 Table 3. Eastern Gulf of Mexico sampling sites used in the present study, supplemented with observations made during various expeditions from of 1970 to Location Site Latitude (N) Longitude (W) Depth (m) Reference Florida Middle Ground FMG-81-A Grimm and Hopkins 1977, Coleman et al Florida Middle Ground FMG81-B Grimm and Hopkins 1977, Coleman et al Florida Middle Ground FMG Grimm and Hopkins 1977, Coleman et al Florida Middle Ground FMG Grimm and Hopkins 1977, Coleman et al Florida Middle Ground FMG Grimm and Hopkins 1977, Coleman et al Florida Middle Ground FMG Grimm and Hopkins 1977, Coleman et al Florida Middle Ground FMG Grimm and Hopkins 1977, Coleman et al Eastern Gulf of Mexico Bay Port Ledge (BPL) Jaap unpublished Eastern Gulf of Mexico TB Ledge (TBL) Jaap unpublished Hourglass North A (HGA) Present study Hourglass North B (HGB) Present study Hourglass North C (HGC) Present study Hourglass North D (HGD) Present study Hourglass North E (HGE) Present study Hourglass South I (HGI) Present study Hourglass South J (HGJ) Present study Hourglass South K (HGK) Present study Hourglass South L (HGL) Present study Hourglass South M (HGM) Present study Pulley Ridge (PR) Hine et al Florida Bay Content Keys (CK) Somerfield et al Florida Bay Smith Shoal (SS) Somerfield et al SE Gulf of Mexico Western Sambo (WSA) Somerfield et al SE Gulf of Mexico Rock Key (RK) Somerfield et al SE Gulf of Mexico Sand Key (SK) Somerfield et al SE Gulf of Mexico Western Head (WH) Somerfield et al. 2008

16 16 Bulletin of Marine Science. Vol 91, No Table 3. Continued. Location Site Latitude (N) Longitude (W) Depth (m) Reference Dry Tortugas Pulaski Shoal (PS) Somerfield et al Dry Tortugas Texas Rock (TR) Somerfield et al Dry Tortugas Temptation Rock (TPR) Somerfield et al Dry Tortugas White Shoal (WSH) Somerfield et al Dry Tortugas Bird Key Reef (BK) Somerfield et al Tortugas Banks Black Coral Rock (BCR) Somerfield et al. 2008

17 Jaap: Stony corals of the eastern Gulf of Mexico 17 the whole assemblage rather than being either dominated only by a few species with great abundance or overly influenced by rare species (Clarke and Green 1988, Clarke et al. 2014b). Bray Curtis similarity coefficients were computed to compare and contrast samples (Bray and Curtis 1957, Bloom 1981, Clarke et al. 2006). Triangular Bray Curtis matrices were input to non-metric multidimensional scaling ordination (MDS) (Kruskal 1964); MDS provides a graphic representation of the ranks in the Bray Curtis similarity matrix, 100 random permutations of the Bray Curtis matrix were imposed for the MDS computation. The similarity profile (SIMPROF) test was employed with clustering to detect evidence of multivariate structure between samples and identify groups of species within samples (Clarke et al. 2014a). A one-way analysis of similarity (ANOSIM) rank test for establishing differences groups (Clarke and Green 1988, Clarke 1993) was computed. The similarity percentage (SIMPER) procedure (Clarke 1993) was used to identify species responsible for observed differences in assemblage structure. Cluster patterns of species and samples were examined using the shade plot (Clarke et al. 2014a,b), also known as heat maps (Sneath 1957). Coherent species curves (Clarke et al. 2014a) documented the relative species abundances based on Similarity profile groups. TADTEST was employed to evaluate the taxonomic distinctness of the species assemblages (Clarke and Warwick 1998, Warwick and Clarke 1998, 2001). The procedure evaluates taxonomic distinctness (TD, Δ+) of the sample, compares it to a regional pool of all species (including higher taxonomic levels: genus, subfamily, family, suborder, and order), and to the variation in taxonomic distinctness (VarTD, λ+). The method is robust and independent of sampling effort (Clarke and Warwick 1998, Warwick and Clarke 2001). Data were exhibited in confidence funnel graphics. The regional Scleractinia master list was compiled from Cairns et al. (2002, 2009) and included all ZS and AS Scleractinia and Milleporidae for the western Atlantic- Caribbean region. Systematics for orders, suborders, families, subfamilies, genera, species, and forma are based on Wells (1956), Veron (2000), and Cairns et al. (2009). Taxonomic distinctness (Δ+) and variation in taxonomic distinctness (λ+) analyses are unique ways to evaluate biological assemblages. These methods have the advantage that the analyses are not influenced by sampling effort and that the taxonomic relationship of each species in the sample is considered (Harper and Hawksworth 1994). Warwick and Clarke (1998) reported that chronically disturbed locations will exhibit greater variation and reduced taxonomic distinctness. Results The eastern Gulf of Mexico Scleractinia in the sampling area includes 52 species and 14 forma, encompassing virtually all of the nominal Caribbean shallow water fauna (Table 1). Dry Tortugas shows the richest assemblage (Table 4); Bird Key results are found in Table 5. Content Key and the shallow (A, I) and deeper (D, E, L, M, 55 and 73 m) Hourglass stations had the fewest species. There is a latitudinal loss in species richness with the exception of the Florida Middle Grounds stations, which were richer in species than Hourglass stations. SE Gulf was the second most speciose area. Species reported for southeast Gulf of Mexico were based on video transect data and are conservative; cryptic species are not captured with birds-eye view video.

18 18 Bulletin of Marine Science. Vol 91, No Table 4. Number of species, colonies, Margalef s index [d = (S 1)/log e N], Pielou s J evenness index [J = H /H max], Shannon-Wiener diversity index [H = i p i log e (p i )], and Simpson s equitability index [1 λ = 1 ( P i2 )]. Pulley Ridge not included, sampling was non-quantitative. Sampling effort Species Colonies d J H (log e ) 1 λ Florida Middle Grounds FMG, Grimm and Hopkins FMG-1, FMG-2, FMG, Coleman et al Mean Standard deviation Hourglass-north Hourglass A Hourglass B , Hourglass C Hourglass D Hourglass E Hourglass ledge BP Ledge, Mean Standard deviation Hourglass-south Hourglass I Hourglass J Hourglass K Hourglass L Hourglass M Mean Standard deviation Southeastern Gulf of Mexico 2002 Smith Shoal Content Keys Rock Key Sand Key Western Head Western Sambo Mean Standard deviation Dry Tortugas Bird Key White Shoal Pulaski Shoal Texas Rock Mean Standard deviation

19 Jaap: Stony corals of the eastern Gulf of Mexico 19 Table 5. Bird Key Reef, Dry Tortugas, rank order of species by cover and depth (m). Species Freq Cover (cm) % cover % Mean SD Max <7 m Diploria clivosa Acropora cervicornis Porites astreoides Siderastrea siderea Millepora alcicornis m Siderastrea siderea Porites porites Montastraea annularis Porites astreoides Dichocoenia stokesi m Montastraea annularis , Acropora cervicornis Siderastrea siderea Colopophyllia natans Montastraea cavernosa m Montastraea annularis , Montastraea cavernosa Siderastrea siderea Stephanocenia intersepta Colopophyllia natans m Agaricia lamarcki Montastraea annularis Montastraea cavernosa Siderastrea siderea Stephanocenia intersepta The Hourglass species (with the exception of the suborders Caryophyllina and Dendrophyllina) are provided in greater detail because they are presently unpublished (more detailed Hourglass species accounts are provided in Online Appendix 1). Hourglass collections yielded 4493 colonies and/or fragments of Milleporidae, Astrocoeniina, Fungiina, and Faviina corals belonging to 18 species. An additional 1448 incertae sedis fragments (too small or crushed to accurately identify) were recovered. Sampling methods (dredge and trawl) bias the relative abundance of the species. Branching species, such as C. arbuscula and Oculina robusta, were typically recovered as fragments, confounding the number of individuals. Frequency of occurrence was employed to better understand abundance and rarity of species (Table 6). The 6 m depth (A, I) stations had two inconspicuous species; both were attached to mollusk shells. Astrangia poculata was more abundant than P. americana. At 18 m depth, stations B and J, there were 13 species, principally C. arbuscula, Solenastrea hyades, and Siderastrea radians (Table 6).

20 20 Bulletin of Marine Science. Vol 91, No Table 6. Frequency of occurrence (percentage of samples containing said species) ranked high to low. Stations A and I are 6 m, B and J are 18 m, C and K are 37 m, D and L are 55 m, E and M are 73 m. Each station was sampled 30 times. See text for additional information on stations. Stations Species A I B J C K D L E M Cladocora arbuscula Phyllangia americana Siderastrea radians Solenastrea hyades Astrangia poculata Oculina tenella Madracis asperula Oculina robusta Stephanocenia intercepta Balanophyllia floridana Scolynia lacera Manicina areolata Isophyllia sinuosa Porites porites divaricata 6.67 Millepora alcicornis 6.67 Cladocora debilis Madracis decactis 3.33 The 37 m stations (C and K) were similar to the 18 m stations in terms of principal species; there were 14 species. Oculina robusta fragments were very abundant in a few samples (Table 6). At the 55 m stations (D and L), the number of species was reduced by half relative to the 37 m stations; ZS were mostly absent; O. tenella and M. asperula were the principal species. At the northern station (D), O. robusta and C. arbuscula were moderately common. At the 73 m station (E and M), the situation was similar to the 55 m sites with reduced species richness and AS species as the most common components in the community. Madracis asperula was more common than O. tenella. Both of these species occurred more commonly and frequently at the southern 55 and 73 m depth stations (Table 6). The non-metric MDS ordination, two dimensional analysis (Fig. 4) and SIMPROF test identified samples having multivariate structure: (A) Pulley Ridge; (B) Florida Middle Ground; (C) Content Keys; (D) Bird Key Reef; (E) Dry Tortugas and Southeast Gulf sites; (F) Hourglass 6 m sites; (G) Hourglass 18, 37 m and ledge sites; (H) Hourglass 55 and 73 m sites. Minimum stress level of 0.09 occurred in 94 of 100 MDS iterations, indicating excellent mapping of Bray Curtis rank orders; 0.05 to 0.1 stress values are considered excellent (Clarke and Gorley 2006). Polygons in the MDF plot identify the Similarity Profile Groups (a h) showing 6 m Hourglass stations (top right), Pulley Ridge upper right, Hourglass 18 and 37 m stations (center), the Dry Tortugas and southeast Gulf clustered together right-center, and 55 and 73 m deep Hourglass stations lower-left-center. Bird Key is situated outside the e group as is Content Keys.

21 Jaap: Stony corals of the eastern Gulf of Mexico 21 Table 7. Average Bray Curtis Dissimilarity Coefficient values for eastern Gulf of Mexico samples. CEG = central eastern Gulf of Mexico, FMG = Florida Middle Grounds, HGN = Hourglass north, HGS = Hourglass south, SEG = Southeastern Gulf of Mexico, PR = Pulley Ridge, DT = Dry Tortugas, TB = Tortugas Banks. FMG CEG HG-N HG-S Fla Bay SEG PR DT CEG HG-N HG-S Fla Bay SEG PR DT TB The SIMPROF polygons match the a priori designations moderately well. The southeast Gulf of Mexico and Dry Tortugas sites are quite similar, with exception of Bird Key, which, due to its more diverse and rich fauna, is isolated outside the centerright polygon. Similarly, Pulley Ridge and Content Keys are unique in their faunal elements and are not grouped within a SIMPROF polygon. Species relatively more abundant in the FMG: M. alcicornis, Dichocoenia stokesi, and Madracis decactis are situated in the upper center. The Caribbean-like locations of the Dry Tortugas and southeast Gulf are seen in Figure 4 as a polygon in the right center of the plot; the three dominating species are M. annularis, Porites astreoides, and Siderastrea siderea. The Hourglass 6 m deep stations A and I are isolated on the far left of the plot; Astrangia poculata and Phyllangia americana are the defining species. The Hourglass 18 and 37 m deep plus the ledge sampling sites are in the middle polygon: C. arbuscula, S. radians, Solenastrea hyades define this group. Deep Hourglass stations (D, E, L, M, 55 and 73 m) are defined by greater abundance for M. asperula, C. debilis, and O. tenella (all AS species); they are in a polygon situated to the lower left of the plot. The shade plot (Fig. 5) provides a perspective of species relative abundance compared to the sampling sites. The darker the shade the more abundant the species is at a site. More species are found at Bird Key than at other sampling locations. Pulley Ridge and Florida Bay locations have fewer species, while the species in the central Gulf show moderately different abundances than Dry Tortugas and southeastern Gulf sites. Cladocora arbuscula is highly abundant in the central Gulf; M. decactis is a dominant in the Middle Grounds. The ANOSIM test rejected that there was no difference between the a priori groups; Global R: 0.583, significance level statistic: 0.01%, 9999 random permuted iterations, number of permuted statistics greater than or equal to Global R: 0. The R value (0.583) is unambiguous: there is meaningful difference between the sites, the null distribution range is approximately 0.2 to 0.2, for the ANOSIM test to support no difference between sites, the R value would need to be within the null distribution range. Average dissimilarity between groups was high (Table 7). Similarity within groups (with two exceptions) was consistently greater than between groups. The exceptions were: White Shoal was most similar to Western Head (SE Gulf) and Rock Key (SE Gulf) was most similar to Smith Shoal (Florida Bay). Hourglass sites were linked by bathymetry more than by latitude (Fig. 4).

22 22 Bulletin of Marine Science. Vol 91, No Table 8. Species most responsible for the dissimilarity between locations (similarity profile analysis). FMG = Florida Middle Grounds, CEG = central eastern Gulf of Mexico, SEG = southeast Gulf of Mexico. Area Primary species Secondary species Tertiary species Quantiary species FMG Millepora alcicornis Dichocoenia stokesi Madracis decactis Oculina diffusa CEG Cladocora arbuscula Siderastrea radians Manicina areolata Oculina robusta Hourglass north Cladocora arbuscula Oculina robusta Oculina tenella Siderastrea radians Hourglass south Cladocora arbuscula Oculina tenella Madracis asperula Solenastrea hyades Florida Bay Porites astreoides Siderastrea radians Solenastrea bournoni N/A Pulley Ridge Leptoseris cuccullata Montastraea cavernosa N/A N/A SEG Montastraea annularis Porites astreoides Siderastrea siderea Millepora alcicornis Dry Tortugas Millepora alcicornis Montastraea annularis Montastraea cavernosa Siderastrea siderea Tortugas Banks Montastraea annularis Millepora alcicornis Siderastrea siderea Montastraea cavernosa SIMPER analysis (Table 8) indicated that the three most important structuring species in each area were different and, within areas, they were responsible for 59% 100% of the dissimilarities. How do these assemblages compare-contrast using a six-step phylogenetic linkage: species-genus-family-suborder-order-class? The sampling sites were compared using taxonomic distinctness (TD) (Fig. 6A) and variation in taxonomic distinctness (Var TD) (Clarke and Warwick 1998). The assumption is that the assemblages at sampling sites are different, and their taxonomic distinctness based on hierarchal phylogeny helps to explain the biodiversity and spatial relatedness of the sampling sites. Areas sampled have different TD; however, unless there has been a meaningful disturbance, the TD should be enclosed within the 95% probability based on a null distribution of 1000 permutations of the regional pool of all eligible species. Two sites (BK and BCR) are far more specious than other sites (Fig. 6). The eastern Gulf of Mexico sites exhibit lower TD than the sites in Florida Middle Grounds, Dry Tortugas, and southeast Gulf of Mexico. All of the sites are within the 95% probability funnel boundaries. High values in VAR TD are often caused by lack of certain types of habitats at some locations. For example, A. undata and A. lamarcki require near vertical surfaces for long-term success. The Var TD plot (Fig. 6B) has a broader probability funnel. The sites with higher Var TD were Smith Shoal, Rock Key, Western Sambo, in Florida Bay, and southeast Gulf of Mexico areas. A few sites are slightly greater and on the border of the Var TD 95% probability limits. The Var TD (range 0 to about 900) corroborates habitat and species distribution heterogeneity in the region. Multivariate analyses document that the eastern Gulf of Mexico stony coral community structure includes a Caribbean tropical assemblage in the southeast, Key West to Dry Tortugas. The species are typical of tropical western Atlantic coral reefs occurring in The Bahamas, Cuba, Mexico, and other locations. To the north there is a rapid loss of tropical fauna, especially in the region of Florida Bay. The Hourglass samples include three assemblages, the very shallowest at 6 m had only two ephemeral species; the intermediate depth samples (18 and 37 m) had a relatively rich assemblage that included a few of the tropical species, such as Manicina areolata and Isophyllia sinuosa; however, the distinguishing species were C. abuscula, S. hyades, and O. diffusa, species that have wide geographic distribution. Deeper Hourglass samples (55 and 72 m) had a suite of colonial and solitary AS species, defining a transition from mixotrophic (autotrophy and heterotrophy) to total heterotrophy. Conversely, the Florida Middle Grounds has a mixture of a few more tropical species

23 Jaap: Stony corals of the eastern Gulf of Mexico 23 (D. stokesi and Meandrina meandrites); however, M. alcicornis and M. decactis are the abundant signature species. Hourglass 18 and 37 m species are common in the FMG. Pulley Ridge is similar to the deep escarpment reef communities in The Bahamas and Caribbean; species have adapted to lower light through morphologic adaptation. The family Agariciidae plays an important role here; large, thin plates of Agaricia and Leptoseris are plentiful, forming mounds of living coral atop a ridge. Controlling influences and why the Scleractinia species distributions are very dissimilar over four degrees of latitude (478 km, 297 mi) and three degrees of longitude (363 km, 226 mi) will be the focus of the discussion. Discussion Geologic Setting The Florida continental shelf in the Gulf of Mexico can be partitioned into a siliciclastic-dominated component off the Florida Panhandle and carbonate-dominated component off peninsular Florida to the south (Hine and Locker 2011). The Florida peninsula (151,670 km 2 ) is a large carbonate plateau that projects south from the continental land mass of North America into the Atlantic Ocean and Gulf of Mexico. The expansive west Florida shelf is a mosaic of carbonate ledges, outcrops, and surficial biogenic and clastic sediments (Gould and Stewart 1956, Holmes 1981). Hine et al. (2008, p. 127) describe the central-west Florida continental shelf as a distallysteepened, carbonate ramp platform; lacking a ridge of reefs, shoals, and islands that define a rimmed platform, such as found off Belize or south of the Florida Keys. In the southern area (Key West to Dry Tortugas), a rimmed platform margin terminates west of Dry Tortugas (Hine and Neumann 1977, Shinn and Jaap 2005). The west Florida shelf is approximately 900 km north-south and 250 km east west (225,000 km 2 ), making it one of the largest carbonate-dominated platforms on earth; carbonate accumulation dates to the Jurassic Period (Hine et al. 2008). Radical changes in sea level during Holocene glacial and inter-glacial ice ages resulted in reefs either keeping pace with sea level rises or becoming inactive carbonate structures with no upward accretion from coral growth (Neumann and MacIntyre 1985, Hine et al. 2008). Limestone ledges and outcrops are a common feature of the eastern Gulf of Mexico seafloor. Some were created or modified by wave action during lower sea level. Linear structures are typically oriented northwest to southeast, with up to 1 m of relief above the seabed. In some situations, the rock structures are covered with a few cm of sediments; sponges, octocorals, and stony corals protrude through the sediments, indicating recent sediment movement due to storm activity. Physical and biological erosion often results in ledges and caves being created that become refuge areas for invertebrates and fish. Hine et al. (2008) recognized five types of hard bottom in the eastern Gulf of Mexico: (1) undulating/scalloped edges, not having any discernable spatial (organized) pattern; (2) long, parallel features; (3) circular depressions with central structure (patch reefs); (4) isolated hard bottom outcrops; and (5) parallel ridges, trending northwest-southeast (paleo-shorelines?). Grady (1971) and Woodward Clyde and Continental Shelf Associates (1983) reported that limestone outcrop exposure in depths <40 m is more prevalent north of 25 latitude (north of Florida Bay and the Ten Thousand Islands). The region between Cape Romano and Big Pine Key is the boundary region for Florida Bay and the Gulf

24 24 Bulletin of Marine Science. Vol 91, No of Mexico. Florida Bay seabed is mostly sedimentary and has the most unpredictable environment of the eastern Gulf of Mexico due to its shallow depths and Everglades runoff (Schomer and Drew 1982). The central portion of the eastern Gulf of Mexico presently does not support highly diverse, Caribbean-like coral reefs; however, they exist in the southern boundary area (Key West to Dry Tortugas) (Jaap et al. 1989, 2008, Shinn and Jaap 2005). Scleractinian and milleporian corals are common on rocky outcrops throughout the eastern Gulf of Mexico. These epibenthic communities include a wide variety of Caribbean/ West Indian reef biota: the algae Halimeda, Caulerpa, Sargassum; sponges such as Cliona celata (Grant, 1826), Spheciospongia vesparium, and Callyspongia vaginalis (Lamarck, 1814); octocoral genera such as Eunicea, Plexaurella, Pseudoplexaura, and Muricea; and echinoderms including the sea urchin, Diadema antillarum (Phillippi, 1845), basket starfish, Astrophyton muricatum (Lamarck, 1816), the reticulated starfish, Oreaster reticulatus (Linnaeus, 1758), and the five-hole sand dollar, Mellita quinquiesperforata (Leske, 1778). Reef Development During the Holocene Holocene or modern-day reef development followed the Wisconsin Glacial Epoch (in North America), which ended approximately YBP. Sea level fell as much as 135 m during the last glacial advances, the current continental shelves were dry land and Gulf Stream circulation was pushed far away from its modern course (Veron 1995). Reefs began their resurgence 9 to YBP; sea level rose at rates of approximately 12 m 1000 yrs 1 ; corals were able to colonize areas along the coast and islands and to form refuge communities that followed changing sea level. According to Veron, The greatest environmental perturbation on the reefs of the Gulf of Mexico and (perhaps) the Caribbean, for example, has been one of low salinity from greatly increased flow of post-glacial melt-water from the Mississippi River (Veron 1995). The vast volume of glacier-derived water in the upper Great Lakes region (Lakes Agassiz and Duluth) filled the Mississippi river basin (Ojakangas and Matsch 1982) and debouched with debris into the Gulf of Mexico. With weakened circulation, the salinity-temperature perturbation was long-lasting and may have extirpated the shallow benthic communities through much of the Gulf of Mexico. The oldest studied Holocene coral reefs in the eastern Gulf of Mexico are located on the Tortugas Banks (Mallinson et al. 2003), where Holocene growth was dated to approximately YBP. Tortugas Banks reefs failed to keep pace with rising sea levels; however, Bird Key Reef within Dry Tortugas National Park did (Shinn et al. 1977). Mallinson et al. (2003) suggested that the Wisconsin glacial meltwater flowing across the Tortugas Banks lowered salinity and temperature and increased turbidity, inhibiting reef growth. It is an enigma why the reefs on Tortugas Banks did not keep pace with rising sea level, while those within Dry Tortugas National Park did. Perhaps, conditions were more favorable around Dry Tortugas National Park because the islands acted as a barrier for water movement? Recent coral diversity and distribution is related to ancestral genera. One genus has origins in the Cretaceous (Table 9); nine genera are known from the Eocene, nine are also known from the Oligocene, and eight date from the Miocene. Average age of the ancestral genera is 32 million yrs with a high degree of variability. These genera came from multiple families and suborders (Table 9); most genera are in the Faviina suborder (12) and fewest are in the suborders Caryophylliana and Fungiina (three

25 Jaap: Stony corals of the eastern Gulf of Mexico 25 Table 9. Genera origins, Scleractinia, with geologic time record. *Dubious Cretaceous record, ** Dubious Eocene record, *** Dubious Oligocene record. YBP = years before present. Genus Family Sub-order Earliest fossil record YBP (million) Location(s) Siderastrea Siderastreidae Fungiina Cretaceous 120 Tethys Sea Acropora Acroporidae Archaeocoeniina Eocene 45 Caribbean and Pacific Cladocora Caryophyllidae Carophylliina Eocene 45 Tethys Sea Colpophyllia Favidae Faviina Eocene 45 Caribbean and Tethy Sea Diploria Favidae Faviina Eocene 45 Tethys Sea Favia Favidae Faviina Eocene * 45 Tethys Sea Millepora Milleporidae Filifera Eocene 45 Caribbean and Pacific Montastraea Favidae Faviina Eocene * 45 Caribbean Porites Poritidae Poritiina Eocene 45 Caribbean and Tethys Sea Stephanocenia Astrocoeiidae Archaeocoeniina Eocene * 45 Caribbean and Tethys Sea Isophyllastraea Mussidae Faviina Oligocene 24 Tethys Sea Isophyllia Mussidae Faviina Oligocene 24 Tethys Sea Leptoseris Agariciidae Fungiina Oligocene 24 Caribbean and Tethys Sea Manicina Favidae Faviina Oligocene 24 Caribbean Meandrina Meandrinidae Meandriina Oligocene *** 24 Tethys Sea Mycetophyllia Mussidae Faviina Oligocene 24 Caribbean Oculina Oculinidae Meandriina Oligocene 24 Tethys Sea Scolymia Mussidae Faviina Oligocene 24 Tethys Sea Solenastrea Favidae Faviina Oligocene 24 Caribbean Agaricia Agariciidae Fungiina Miocene 15 Caribbean Astrangia Rhizangiidae Faviina Miocene 15 Eastern North America Dendrogyra Meandrinidae Meandriina Miocene 15 Tethys Sea Dichocoenia Meandrinidae Meandriina Miocene 15 Tethys Sea Eusmilia Caryophyllidae Carophylliina Miocene ** 15 Caribbean Madracis Pocilloporidae Archaeocoeniina Miocene *** 15 Tethys Sea Mussa Mussidae Faviina Miocene 15 Caribbean Phyllangia Caryophyllidae Carophylliina Miocene 15 Caribbean Mean Median each). Twelve genera have Tethys Sea origins, 8 Caribbean, 4 are known from both Tethys Sea and Caribbean, 2 from Caribbean and Pacific, and 1 from eastern North America. One of the features of the shallow and mostly ZS corals in the Caribbeanwestern Atlantic is that many genera only include one or two species; in contrast to the Indo-West Pacific ZS fauna, where genera typically include multiple species. For example, in the western Atlantic Acropora includes two species and a hybrid (Vollmer and Palumbi 2002, Boulon et al. 2005, Cairns et al. 2009), whereas in the Indo-Pacific region, there are 65 species (Wallace 1999, Veron 2000). Similarly, there are four species of Porites in the western Atlantic Ocean and 47 in the Indo-Pacific region (Veron 2000). Recent Caribbean ZS genera average 2.22 (SD 1.53) species genera 1. Environmental Conditions Climate. South Florida is a unique enclave of the Caribbean Sea resulting from the nexus of geography, geology, and environmental factors. Tropical mangrove, sea grass, and coral reef communities are common from Stuart (27 10 N) on the east

26 26 Bulletin of Marine Science. Vol 91, No coast to Tarpon Springs (28 10 N) on the west coast. The maritime influence of the Caribbean Sea and the Gulf of Mexico transforms Florida s climate (Chen and Gerber 1990, p. 11). Seawater Temperature. Seawater temperatures for the eastern Gulf of Mexico using the Dry Tortugas (Iowa Rock) monitoring station ( N, W) for a 10 yr period range from an extreme low of 9 (March) to 32 C in August; average seasonal temperature is C. Seawater temperature annual range at the monitoring buoy near FMG ( N, W) was C, average range C. Seawater temperature data were assessed using NOAA Buoy network, the data set included 1992 through Minimum seawater temperatures occur in March and maximum in late August to early September. Hourglass station minimum bottom temperatures between August 1965 and November 1967 were 11 C at the northern 6 m deep station and 17.5 C at the 73 m deep station; southern Hourglass stations experienced 17.9 C for the 6 m deep station and 17.2 C for the 73 m deep station. Maximum temperatures were 31.5 and 31.0 C for the northern and southern 6 m deep stations, respectively. Seawater temperature is less predictable from late October until mid-april. The cooling associated with polar frontal passages results in rapid and extreme cooling of shallow bays and nearshore waters. Reef distribution is influenced by the inimical waters generated in Florida Bay (Ginsburg and Shinn 1964). In general, there is poor reef development in those areas where there is unrestricted water movement from Florida Bay into the Atlantic Ocean. Florida Bay water is cooled and transported via winds and tides to the areas south and west, and, in extreme situations, causes coral stress and mortalities (Davis 1982, Roberts et al. 1982, Lirman et al. 2011, Colella et al. 2012). Conversely, during summer doldrums, seawater in shallow bays may become heated and cause hyperthermic as well as hypersaline stress. Threshold seawater temperature inducing stress (zooxanthellae expulsion is: >31 32 C (Jaap 1979, 1985). Seawater temperatures are not ideal for coral reef development in the eastern Gulf of Mexico, but many Scleractinia manage to survive and thrive in spite of thermal disparity (Wells 1956) (Table 10). Mayer (1918) concluded that tropical and subtropical animals are more at risk from hyperthermia than from hypothermia. Smith (1954) attributed the absence of active coral reef building in the greater part of the Gulf of Mexico to unfavorable temperatures. Smith (1954) and Glynn (1973) cited Fuglister s (1947) atlas of oceanic temperatures, arguing that the 21 C isotherm in January represented the northern limits of coral reef development in the Gulf of Mexico. Minimum seawater temperatures of 9 and 14 C have been recorded at Dry Tortugas (Davis 1982, NOAA National Ocean Data Buoy Center). Temperature influences biological communities in the eastern Gulf of Mexico region in a synergistic manner, operating with other physical, chemical, geological, and biological factors such that structural coral reef development is marginal; however hard bottom communities with ZS are common in the eastern Gulf of Mexico. Coral reefs are typically considered the natural habitat for corals; however, for most of their geological history, corals have existed in epibenthic communities that did not build structural reefs (Veron 1995, 2000). Salinity. Salinities (away from shores and estuaries) in the eastern Gulf of Mexico are typically oceanic (34 37), since only a few moderate size rivers empty into the

27 Jaap: Stony corals of the eastern Gulf of Mexico 27 Table 10. Scleractinia thermal tolerances compiled from Mayer (1914, 1918). LST = lowest survival temperature, LLT = lethal low temperature, HST = highest survival temperature, LHT = lethal high temperature. All temperatures reported in degrees celcius. Species LST LLT HST LHT Acropora cervicornis No data Acropora palmata No data No data Agaricia sp. No data No data No data 36.0 Siderastrea radians Siderastrea siderea Porites astreoides No data Porites clavaria 2 No data Porites furcata No data Favia fragum No data No data Montastraea annularis Montastraea cavernosa 5 No data >8.4 No data <37.3 Diploria clivosa No data Diploria strigosa 7 No data No data Manicina areolata No data Oculina diffusa 15.6 No data Isophyllia sinuosa 9 No data No data No data 36.7 Isophyllastraea rigida 10 No data No data No data 36.0 Eusmillia fastigiata 11 No data Reported in Mayer (1914) as Madrepora (Acropora) muricata 2 Also known as Porites porites clavaria 3 Also known as Porites porites furcata 4 Reported in Mayer (1914) as Orbicella annularis 5 Reported in Mayer (1914) as Orbicella cavernosa 6 Reported in Mayer (1914) as Meandra clivosa 7 Reported in Mayer (1914) as Manicina gyrosa 8 Reported in Mayer (1914) as Meandra areolata 9 Reported in Mayer (1914) as Mussa (Isophyllia) dipeacea 10 Reported in Mayer (1914) as Mussa (Isophyllia) rigida 11 Reported in Mayer (1914) as Eusmillia aspera, knorri eastern Gulf of Mexico: Suwannee, Withlacoochee, Anclote, Hillsboro, Peace, Myakka, and Caloosahatchee. Their discharge does not modify salinity over wide areas or transport significant volumes of sediment, with the exception of massive outflows of water prior to and following hurricanes. Large discharges from Lake Okeechobee via the Caloosahatchee influence the area off San Carlos Bay, near Ft. Myers. On occasion, in April and May, winter snow melt from the Mississippi River drainage basin is entrained in the Loop Current and effects salinity (records of 32) and light transmission through the water column. In the area between Key West and Dry Tortugas, density sinking, the result of evaporation, produces very saline (>40) waters during late summer doldrums. Highly saline and hot water causes zooxanthellae expulsions (Mayer 1914, 1918, Jaap 1979, 1985). Inshore Hourglass stations A and I exhibited lower salinities and more variability; salinities were more stable and averaged slightly higher at the m deep stations (Fig. 7A).

28 28 Bulletin of Marine Science. Vol 91, No Figure 7. (A) Bottom salinities at Hourglass stations (Joyce and Williams 1969); Stations A and I = 6 m, B and J = 18 m, C and K = 37 m, D and L = 55 m, E and M = 73 m. (B) Maximum Secchi disk visibility at Hourglass stations (Joyce and Williams 1969). Light transmission through the water column is controlled by time of day, season, cloud cover, plankton, and suspended sediments. Kanwisher and Wainwright (1967) reported that ZS required 200 to 700 foot candles (2153 to 7535 lux) for true autotrophic self-reliance; this is possible in reasonably clear water up to 30 m. Hourglass Secchi disk data indicate that water clarity is generally superior offshore (Fig.7B); average Secchi visibility was greater for northern stations than for comparable depths at southern stations with the exception of the 18 and 73 m deep stations. There was sufficient light at Pulley Ridge at m to support Anadyomene menziesii (Gray) (green alga) and multiple ZS. At this depth, approximately 1% of surface illumination is detectable based on an instrument attached to Deep Worker submersible vehicle (Halley et al. 2005). The ZS in the eastern Gulf of Mexico are generally not in ideal conditions for autotrophy. Autotrophy combined with heterotrophy sustains those populations that have acclimated themselves to low light conditions (Porter 1976). Hard bottoms alternate with large beds of sediments supporting secondary production of interstitial