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).