Environmental Controls on Corallite Morphology in the Reef Coral Montastraea Annularis

Scleractinian reef-coral species display high phenotypic plasticity in skeletal morphology. Understanding environmental and physiologic controls on this variation is essential to explaining the distribution and abundance of coral species as well as understanding their susceptibility to pollution and global climate change. Here we assess phenotypic plasticity in the corallite morphology of genetically determined colonies of Montastraea annularis s.s. (Ellis and Solander, 1786) by analyzing the three-dimensional morphology of calical surfaces and the two-dimensional corallite morphology represented in transverse thin sections. Samples were collected along gradients of seawater depth and coastal influence on the island of Curaçao, Netherlands Antilles, and additionally compared to M. annularis and two closely related species, M. franksi (Gregory, 1895), and M. faveolata (Ellis and Solander, 1786), collected from Panama. Significant phenotypic plasticity was found between seawater depths and localities of Curaçao, as well as between the two geographic regions. Morphologic characters associated with calical surfaces were significantly more plastic than characters preserved in transverse thin sections. While characters preserved in thin section were more successful at classifying the three closely related species, characters associated with calical surfaces provide a basis for interpreting the adaptive significance of the observed differences between these three species. High variability in skeletal morphology is a well-known characteristic of scleractinian coral species. This includes variation in overall colony growth form (Goreau, 1963; Roos, 1967; Dustan, 1975; Veron and Pichon, 1976; Jaubert, 1977; Graus and Macintyre, 1982; Muko et al., 2000; Kaandorp et al., 2005), as well as corallite architecture observed both within and between coral colonies (Foster, 1979a, 1980, 1983, 1985; Budd, 1993; Budd et al., 1994). These changes in skeletal morphology allow corals to survive in a variety of environmental conditions (Porter, 1976; Lasker, 1981; Lesser et al., 1994; Kaandorp et al., 2005), and can influence the distribution, abundance, and evolutionary success of a species (Foster, 1979b; Jackson, 1979; Johnson and Budd, 1995; Klaus and Budd, 2003). Morphologic variation is caused by the combined effects of genetic polymorphism and phenotypic plasticity. However, separating the individual effects of these two components can be difficult without genetic data distinguishing species and populations within species (Knowlton and Budd, 2001; Budd and Pandolfi, 2004; Fukami et al., 2004). Moreover, taxonomic classifications have historically underestimated the number of species within many common coral genera (Knowlton and Budd, 2001). Given the tendency for closely related taxa to partition themselves along environmental gradients, failure to recognize true species boundaries has led authors to invoke a large degree of phenotypic plasticity to explain observed morphologic variations along ecologically meaningful gradients (e.g., seawater depth). As ongoing molecular and nontraditional systematic studies continue to reveal cryptic species (Weil and Knowlton, 1994; Carlon and BULLETIN OF MARINE SCIENCE, VOL. 80, NO. 1, 2007 234 Budd, 2002), the extent of plasticity interpreted within coral species will likely decline (but see Miller and Benzie, 1997). The highly plastic nature of reef-corals is in part a byproduct of the coral skeletogenic process. Corals calcify a hundred times faster than inorganic calcification on the reef, yet exert little control over the specific shape and organization of their skeletal crystals (Cohen and McConnaughey, 2003). Calcification occurs outside of the coral tissue in the space adjacent to cells of the calicoblastic ectoderm (Barnes and Chalker, 1990). In this space, corals build their skeletons primarily from sclerodermites, three-dimensional fans of aragonite similar to inorganically precipitated spherulitic crystal fibers (Given and Wilkinson, 1985; Cohen and McConnaughey, 2003). These sclerodermites combine to form thickening deposits and centers of rapid accretion (Stolarski, 2003), which form the septa within the individual corallites of a colony. The accretionary growth of corals has been subdivided into two major components, upward linear extension and skeletal thickening (Graus and Macintyre, 1982; Barnes and Lough, 1993; Cohen et al., 2004). Upward growth has been shown to occur primarily at night through the accretion of randomly-oriented fusiform-shaped crystals (Barnes and Crossland, 1980; Gladfelter, 1982, 1983; Vago et al., 1997), while skeletal thickening occurs during the daytime when corals exhibit calcification rates three to five times faster in the presence of light and actively photosynthsizing symbiotic algae (zooxanthellae) (Barnes and Crossland, 1980; Gladfelter, 1983; Le Tissier, 1988). Variations in skeletal growth have been correlated with light-mediated photosynthesis (Goreau, 1959; Vandermuelen et al., 1972; Chalker and Taylor, 1975; Graus and Macintyre, 1982; Marubini and Thake, 1999; Muko et al., 2000; Marubini et al., 2002; Kaandorp et al., 2005), turbidity and sediment load (Foster, 1979b; Carricart-Ganivet and Merino, 2001), seawater nutrients (Edinger et al., 2000; Cook et al., 2002), hydrodynamics (Jokiel, 1978; Bruno and Edmunds, 1998; Kaandorp et al., 2005), and temperature (Dodge and Vaisnys, 1975; Lough and Barnes, 2000); with varying degrees of influence on either vertical extension or skeletal thickening. In the present study we explore the magnitude and nature of phenotypic plasticity in the common reef-building coral Montastraea annularis sensu strictu (Ellis and Solander, 1786) along gradients of seawater depth and coastal influence on the island of Curaçao, Netherlands Antilles. Curaçao is an especially conducive natural laboratory for this study (Fig. 1). The approximately 150,000 people living on Curaçao are concentrated in the capital city of Willemstad, surrounding the natural harbor of St. Annabaai. The large commercial and military harbor of St. Annabaai, and the urban center of Willemstad are a major point source of pollutants such as nutrients, metals, hydrocarbons, and other toxic chemicals (Gast, 1998). Furthermore, the island is surrounded by shallow fringing reefs up to 250 m from shore where a stepped shelf break occurs from 8–10 m to 30–50 m water depth (Van Duyl, 1985). These factors provide a consistent depth and environmental impact gradient to sample along the length of the island. We selected M. annularis because it is one of the most well studied reef-coral species, and it clearly demonstrates the problem of distinguishing genotypic vs phenotypic variation. Historically, M. annularis sensu lato was considered the model ecologic generalist, exhibiting a high degree of phenotypic plasticity. It could be found from intertidal to over 80 m water depths (Goreau and Wells, 1967), with colony morphologies varying dramatically from hemispherical heads to vertical colKLAUS ET AL.: CONTROLS ON CORALLITE MORPHOLOGY IN MONTASTRAEA ANNULARIS 235 umns and horizontal plates. Recent taxonomic studies based on molecular genetics, aggressive behavior, ecology, growth rate, corallite morphometrics, and stable isotopes (Tomascik, 1990; Knowlton et al., 1992; van Veghel and Bak, 1993), show that M. “annularis” is actually a complex of at least three species: (1) M. annularis s.s., which forms smooth columns; (2) M. faveolata (Ellis and Solander, 1786), which forms bumpy or keeled heads and sheets; and (3) M. franksi (Gregory, 1895), which forms bumpy mounds and plates. On the reefs of Curaçao, M. annularis and M. faveolata are most common between 1 m and 20 m, while M. franksi is typically found at depths > 10 m (Van Veghel, 1994a). Previous studies of the three species on Curaçao have characterized significant differences in genetics, as well as reproductive, behavioral, and morphologic aspects (van Veghel and Bak, 1993, 1994; van Veghel, 1994b; van Veghel and Kahmann, 1994; van Veghel and Bosscher, 1995). Here we focus on the corallite morphology of genetically determined colonies of M. annularis s.s., analyzing the three-dimensional morphology of calical surfaces (Budd and Klaus, 2001; Knowlton and Budd, 2001; Fukami et al., 2004) and the twodimensional corallite morphology as represented in transverse thin sections (Budd and Klaus, 2001; Pandolfi et al., 2002; Klaus and Budd, 2003; Budd and Pandolfi, 2004). We assess four different environmental and physiologic factors as possible causes of the observed phenotypic plasticity: (1) light intensity of the seawater environment; (2) seawater pollution; (3) relative photosynthetic activity of zooxanthellae; and (4) the diversity of zooxanthellae communities. Furthermore, we examine the extent to which phenotypic plasticity observed along the sampled environmental gradients obscures species boundaries within the M. “annularis” species complex. Species of M. annularis-like corals have been common in the Caribbean for the past 22 million yrs (Budd, 2000; Knowlton and Budd, Figure 1. Map of Curaçao, Netherlands Antilles, in the southern Caribbean Sea. The five sites chosen for this project are distributed along the leeward coast of the island. St. Annabaai is a major seaport in the urban area of Willemstad. Boca Simon and Water Plant are the most environmentally impacted sites, while Playa Hundu is the least impacted site. BULLETIN OF MARINE SCIENCE, VOL. 80, NO. 1, 2007 236 2001) and preliminary studies indicate a diverse and complex evolutionary history during this time (Budd, 1991; Budd and Klaus, 2001; Klaus and Budd, 2003; Budd and Pandolfi, 2004). Understanding how environmental factors affect species boundaries is essential to accurately interpreting the complex evolutionary history of this group. To determine the extent to which phenotypic plasticity obscures taxonomic identification, corals collected from Curaçao were compared to colonies of M. annularis, M. faveolata, and M. franksi, collected from the San Blas and Bocas del Toro regions of Panama, which were identified based on genetic analyses. Materials and Methods