Peculiar Morphology of Montipora millepora Reveals Interspecific Competition for Space Among Two Other Major Foundation Species in Jeju Waters, South Korea

Abstract

An atypical surface shape was observed in encrusting coral colonies of Montipora millepora. Initial assumptions on their origin focused on the presence of epibiotic intermediate habitat formers, such as coral-dwelling and -boring organisms. However, further investigations revealed their origin to also be substrate shape-related, prompted by overgrowing other foundation species. The unusual bumps stemmed from encrusting over specimens of the coral Alveopora japonica, and the forked, tube-like structures over holdfasts of the brown alga Ecklonia cava. Spatial distribution patterns and interspecific competition are briefly reviewed. Potential effects of morphological changes for Montipora species identification, as well as implications of altered topography in general, are mentioned.

Foundation species are ecosystem-modifying organisms, often spatially dominant, that create a habitat by promoting species co-existence through the reduction in physical stress provided by their biogenic structures [1,2]. In the waters surrounding Jeju Island, the competition for space between these foundation species is evident in regime shifts that have been observed in the past: The original ecosystem was dominated by canopy-forming macroalgae, especially the native kelp species Ecklonia cava Kjellman, 1885 [3,4]. During the last three decades, a first regime shift occurred in the north of the island, from vast E. cava forests to primarily “barren ground”, i.e., areas covered by crustose coralline algae [5]. In addition, most recently, scleractinian hard coral communities have successfully been colonizing the coastal areas [6,7]. In particular, the Korean species of the Alveopora japonica species complex [8] now appears dominant in the northwest of the island, where it tends to form extensive and dense carpets, punctuated only by the occasional stalk of E. cava [9,10]. In the south, A. japonica was reported outcompeting the kelp species for space, despite reported bleaching pressure [11]. Another foundation coral gaining significance in Jeju waters is Montipora millepora Crossland, 1952, which has previously been reported to aggressively compete for space with the soft-coral species Dendronephtea gigantea Verrill, 1864 [7].

Here, we report an unusual morphology for Montipora millepora communities observed along the southern coastline of Jeju Island between 10 and 20 m water depth. Instead of the typical small, nodular mounds covering the otherwise smooth colony surface (i.e., corallum) [6], colonies displayed large humps and forked, elongated bump shapes (i.e., corallum modifications) (Figure 1). We assumed the tube-systems to be caused by coral-dwelling, tube-building epibiotic organisms, similar to the chimney-formation reported from M. millepora colonies infested by sipunculan bristle worms [6], or the finger-like branch-formation induced by gammarid amphipods and chaetopterid polychaetes [12]. However, photographic evidence showed that this peculiar surface shape displayed in our encrusting morphotype (i.e., growing along horizontal axis in a two-dimensional manner, strictly adhering to the substrate) of M. millepora originated from successful spatial competition with other foundation species. The forked tubes were caused by overgrowth of M. millepora over E. cava holdfasts (Figure 1a,b), while the large humps were shown to be colonies of the A. japonica species complex overgrown by aggressively expanding M. millepora (Figure 1c,d,e).

These observations imply a strong spatial competition between coral and kelp foundation species in Jeju waters (Figure 2). While previous studies reported a gradual decline in the E. cava populations to the benefit of A. japonica [9], our observations hint at a more complex interplay between these foundation species. Montipora is rapidly expanding its distribution around Jeju Island. Its first record dates back to 1985, when it was found in the south of the island [13]. More than three decades later, this southern population had expanded significantly [14,15], threatening the local soft-coral gardens by severe spatial competition [7]. Additionally, colonies were found to spread further east and west from their initial location of discovery (i.e., Seogwipo). In 2012, M. millepora colonies were reported from the entire western and southern coastline, as far east as Seongsan [15]. However, the eastern waters around Seongsan are, to date, still dominated by E. cava forests, with M. millepora colonies only occasionally occurring under the kelp [16]. Most recently, colonies were also discovered in the north of the island ([17] Table 4 in Supplementary Materials; Figure 2). It appears that the consequences of global climate change, which are generally considered negative repercussions, such as rising sea water temperatures and the increased frequency and severity of typhoons, are here actually benefitting the population growth of M. millepora by accelerating their expansion. Previous studies on Jeju’s marine environments have reported devastating typhoon-impact-related losses of E. cava and A. japonica coverages [16], and elevated seawater temperature-related severe bleaching incidences in the A. japonica population [11]. However, the colonies of M. millepora have shown a lower sensitivity to typhoon-related changes in the environment [17], as well as generally high spatial competitiveness with other corals, indicating fast recovery and growth rates [7]. However, further studies on in-depth hard coral species-specific growth rates and densities based on environment changes are necessary to confirm M. millepora to be truly competitively dominant.

Alterations in colony topography as consequence of profound morphological changes, either infestation-induced or substrate-generated, can benefit, as well as impede, the affected coral colony, as coral size and structure directly impact feeding, fecundity, survival, and their competitive ability ([12] and references therein). Additionally, the density of Symbiodiniaceae appears morphology-dependent [18], which may have further impacts on their spatial competitiveness. On the other hand, they present habitat modifications that increase the structural heterogeneity of basal habitat formers may potentially lead to an increase in biodiversity through habitat cascades, by subsequently enhancing the settlement of intermediate habitat formers, and therefore attracting more epifaunal focal organisms [19,20].

In addition, the most pressing issue with these corallum modifications, however, is of a taxonomic nature. To date, it is unclear which and how many species of Montipora inhabit the Korean waters around Jeju Island. While some researchers identify the specimens as M. efflorescens Bernard, 1897 [13,21,22], others use the species name M. millepora Crossland, 1952 [6,10,14,15,16,17,23]. In our identification, we followed the description that M. millepora is primarily encrusting, while M. efflorescens tends to exhibit a larger growth form [6]. Overall, species identification within the genus Montipora in the wild is very limited, with the main distinction criterion being the overall shape of the corallum surface. M. efflorescens is described as having higher and wider irregular mounds and globular protuberances when compared to specimens of the species M. millepora [6]. Therefore, corallum modifications caused by substrate, rather than species-specific morphology, are a major contributor to the current confusion in species identification. The observations documented here foster insight into the origin of the irregular surface area of Montipora specimens, enhancing our comprehension of species morphology and, subsequently, taxonomy. Based on these, we propose a revision of the genus Montipora within Jeju waters, including in-depth species identification through a combination of molecular, morphological, and morphometric approaches, as areas for future study.