Data accessibility statement
The data supporting the results will be archived in the public repository Zenodo (https://zenodo.org/) and the data DOI will be included at the end of this article.
Type of article: Letter.
Abstract word count: 150; Main text word count: 4999.
Number of references: 114; Number of Figures: 6.
Correspondence author: Ángela Martínez-Quintana. Department of Geology. Buffalo, NY 14260-4130 Phone: (716) 536 - 1693. email: am298@buffalo.edu
ABSTRACT
The 3-dimensional structure of habitats is a critical component of species’ niches driving coexistence in species-rich ecosystems. However, its influence on structuring and partitioning recruitment niches has not been widely addressed. We developed a new method to combine Species Distribution Modeling and Structure from Motion and characterized three-dimensional recruitment niches of two ecosystem engineers on Caribbean coral reefs, scleractinian corals and gorgonians. Fine-scale roughness was the most important predictor of suitable habitat for both taxa, and their niches largely overlapped, primarily due to scleractinians broader niche breadth. Crevices and holes at mm-scales on calcareous rock with low coral cover were more suitable for octocorals than for scleractinian recruits, suggesting the decline of scleractinian corals is facilitating the recruitment of octocorals on contemporary Caribbean reefs. However, the relative abundances of the taxa were independent of the amount of suitable habitat on the reef, emphasizing niche-processes solely do not predict recruitment rates.
INTRODUCTION
The 3-dimensional structure of habitats influences biotic interactions, and species distributions and abundances (Ehbrecht et al. 2021; Gámez & Harris 2022). Relevant components of 3D habitat structure can range from scales of kilometers, where geomorphologic features and vertical space are core, to scales down to decimeters, where the roles of ecosystem engineers are particularly evident. The 3D physical structure of the habitat on even finer scales may be critical for sessile organisms that recruit to populations as larvae, spores and seeds. For these taxa, introducing new individuals to a population is a multi-step process in which the initial establishment and subsequent survival of individuals are, in part, mediated by the physical structure of the substratum.
The role of the three-dimensional substratum in the recruitment and population dynamics of sessile taxa may be particularly important in ecosystems that are structurally complex (Lepczyk et al. 2021; Gámez & Harris 2022), such as corals reefs, where biophysical interactions can affect both larval settlement and post-settlement survival. Sessile species compete for the same limited resource, space (Dayton 1971; Porter 1976; Connell 1978), and the nature of the substratum that supports successful settlement and survival defines realized “recruitment niches” (Young et al. 2005). Characterizing recruitment niches is critical to understand the role of environmental filtering, resource partitioning and interspecific competition in the assembly of communities, as well as, in predicting the effects of changing environmental conditions on community composition and dynamics. However, spatially-explicit niche metrics have never been quantified for coral recruits, largely due to the difficulty of quantitatively assessing the topography of complex three-dimensional coral reefs.
Within reef communities, the spatial recruitment niche is strongly influenced by reef topography (Keough & Downes 1982; Lubchenco 1983). Parameters such as water velocity at the water-substratum interface, and the availability of resources such as light and oxygen are modified by reef topography, impacting larval transport, settlement and post-settlement survival (Brakel 1979; Reidenbach et al. 2009, 2021; Hata et al. 2017; Virtanen et al. 2019). Topographic heterogeneity also affects biological interactions, , by providing cryptic surfaces that act as refugia from predators (Carleton & Sammarco 1987; Nozawa 2008; Edmunds et al. 2014; Gallagher & Doropoulos 2017), and variable microhabitats that can support higher diversity (Kovalenko et al. 2012; Graham & Nash 2013; Darlinget al. 2017; Ehbrecht et al. 2021).
Technological advances in remote sensing and benthic habitat mapping enable the study of coral reef topography, providing spatially referenced data that can be used to study recruit distributions. In particular, close range photogrammetry, i.e., Structure-from-Motion (SfM), generates high-resolution digital 3D models or point clouds with X, Y and Z coordinates (i.e. latitude, longitude and height; Westoby et al. 2012). The method has been used to characterize the structural complexity of coral reefs (Burns et al. 2015; Palma et al.2017; Fukunaga et al. 2019; Couch et al. 2021), and to study organism-habitat relationships, distribution patterns, and the effect of diseases and environmental disturbances in coral growth and ecosystem structure (Burns et al. 2016, 2019; Ferrari et al. 2017; Pedersen et al. 2019; Fukunaga et al. 2020; Combs et al. 2021; Olinger et al. 2021). However, the methodologies that have been used to characterize structural complexity simplify the 3D reefscape using orthomosaics or raster gridded 2.5D digital elevation models (DEMs) (Kissling et al. 2017). Recruits are often on cryptic surfaces, and those approaches overlook the biophysical environment along steep slopes or overhanging cliffs not visible from the ‘top-down” perspective, preventing the examination of species distributed in cryptic microhabitats (Figure 1).
We developed an analytical framework to examine organism-habitat relationships in complex three-dimensional ecosystems, and use it to fully represent the three-dimensional nature of the substratum and to characterize recruitment niches. The approach allows fitting and projecting Species Distribution Models (SDMs) on polygon meshes derived from 3D digital reconstructions of the reef (i.e., meshSDM). Species Distribution Models are powerful tools that couple geographically explicit environmental information with species locations to characterize the present and future geographic range of species (Davieset al. 2008; Elith & Leathwick 2009; Yesson et al. 2012; Barbosa et al. 2020). In addition, SDMs can be used to characterize species’ realized niche breadths and their degree of overlap (Warren et al. 2019; Grant & Kalisz 2020). SDMs typically estimate species distributions across large-scale geographic domains with spatial resolutions of tens of meters to tens of kilometers, failing to characterize structural complexity at ecosystem scale. We used fine-grain (sub-cm resolution) three-dimensional habitat structure with a presence-background SDM (Maxent; Phillips et al. 2006) to characterize the realized spatial recruitment niche of two key ecosystem engineers on shallow Caribbean coral reefs, alcyonacean octocorals (hereafter octocorals), and stony corals (hereafter scleractinians) (Kinzie 1973; Jones et al. 1994).
Scleractinians are the primary structure builders of modern coral reefs and octocorals provide three-dimensional structure above the hard substratum. Both taxa are colonial Anthozoans with complex life cycles, that reproduce mainly sexually, depend on lecithotrophic larvae to disperse, and often settle within concealed microhabitats (Lasker & Kim 1996; Nozawa 2008; Edmunds et al. 2014). How much of the substratum is suitable habitat for the recruitment of each taxon, and whether recruits compete for suitable microhabitats have never been analyzed. Such examination is critical, as scleractinian abundances on Caribbean reefs have declined precipitously (Gardner et al. 2003; Roff et al. 2020), while octocorals have increased in many locations throughout the Caribbean (Norström et al. 2009; Ruzickaet al. 2013; Tsounis et al. 2018). As coral cover declines, the newly available space could provide habitat for octocoral recruitment. However, whether this new space is suitable for octocoral recruitment is unknown.
We characterized the realized spatial niche for the recruitment of scleractinians and octocorals and hypothesized that microhabitats suitable for recruitment are limited, and space-based niche partitioning occurs at the recruitment stage between both taxa, which reduces competition and facilitates coexistence. We specifically examined the following hypotheses: H1) the spatial distribution of recruits on the reef is not random, H2) realized niche breadth of the taxa are not identical and thus their niches do not overlap, H3) the amount of suitable habitat available for each taxonomic group is not similar and H4) the amount of suitable habitat is correlated to recruit abundances. Our study provides new insights on niche dynamics and interspecific competition during the early stages of community development on three-dimensional coral reefs.
MATERIALS AND METHODS
We conducted the study at two shallow fringing reefs on the south shore of St. John, US Virgin Islands, Grootpan and Europa Bays (18° 18.360’N, 64° 43.140’W, and 18° 19.016’N, 64° 43.798’W, respectively; Figure 2A). Both sites have been described in detail in previous studies and in those studies, Grootpan Bay, has been called East Cabritte (Tsouniset al. 2018; Lasker et al. 2020; Martínez-Quintana & Lasker 2021). The sessile benthic community consists of scleractinian corals, octocorals, sponges, ascidians, bryozoans, and macroalgae, resembling similar communities of shallow fringing reefs and reef flats up to 15 m depth throughout the Caribbean (Williams et al. 2015; Figure 2B). At each site, eight quadrats of 0.25 m2 were randomly selected along 4 fixed 10 m transects (see Tsounis et al. 2018 for a detailed description of the transects), and surveyed for recruits in July and August of 2017. Within each quadrat, we counted and marked all octocorals ≤ 5 cm height (Figure 2.2C), and scleractinians ≤ 4 cm wide (Figure 2C).