Discussion
A variety of human activities can impact coral reefs directly and
indirectly, resulting in their degradation (Pandolfi et al. 2003) and a
decline of fish diversity associated with this habitat (Graham et al.
2011). In particular, the coral cover of Curaçao has been steadily
decreasing over the last decades (Gardner et al. 2005, Jackson et al.
2014) although to a lesser extent than most other islands in the
Caribbean and with variations between different coastal stretches of the
island (Waitt institute 2017). Here, using eDNA, we showed differences
in species functional and phylogenetic compositions between two coastal
areas on the Southern side of the island of Curaçao. By comparing two
reef stretches under different degrees of anthropogenic pressures, we
showed how eDNA combined with species features from associated databases
and advanced modelling approaches can deliver ecological indices that
can inform ecosystem status. Management toward the preservation of coral
reef ecosystems requires monitoring approaches that can be quickly
deployed in the field (Obura et al. 2019), and we demonstrated that eDNA
metabarcoding provides as rich fish assemblage information as UVC in
term of taxa samples, but which requires significantly less sampling
time and resource in the field. Yet, remaining gaps in the reference
database still limit the information provided by eDNA. Building on
increasing evidence of the monitoring capacity of eDNA metabarcoding
(DiBattista et al. 2017, West et al. 2021, Polanco Fernández et al.
2021), our study illustrates how this technique could evolve toward a
general approach for the monitoring of fish communities on coral reefs.
Functional and phylogenetic characteristics are expected to offer higher
dimensions of information to describe and manage ecosystems (Strecker et
al. 2011). Coupling ecological indices with eDNA can provide more
complete ecosystem information for coral reefs (Aglieri et al. 2020,
Marques et al. 2021). As demonstrated previously with UVC (D’agata et
al. 2014), we found that functional and phylogenetic indices better
discriminate between the two inventoried coastal areas than taxonomic
information alone. While the two reefs were similar regarding the fish
species richness recovered from eDNA, we found more marked differences
in their functional and phylogenetic properties. Specifically, the
Valentijnsbaai reef area contained larger species such asAetobatus narinari , more pelagic species (e.g. Thunnus sp,Istiophorus sp.) with higher trophic levels (e.g.Acanthocybium solandri ). In addition, crypto benthic species are
also present such as the mimic cardinalfish (Apogon phenax) or
the pale cardinalfish (Apogon planifrons) increasing the
functional diversity. In contrast, Willemstad presented higher
phylogenetic diversity, mainly driven by a few phylogenetically distinct
species associated with soft bottoms (Albula vulpes , Elops
smithi ) or the water column (Anchoa colonensis ,Opisthonema oglinum ). The higher occupancy of this coastal
stretch by sandy bottom and pelagic species could reflect the higher
state of degradation of the coral reefs near the city. These findings
suggest that environmental filtering under high levels of coastal
development near Willemstad and high levels of sediments is associated
with distinct fish assemblages as previously documented using UVC in
Singapore (Wong et al. 2018). Hence, even if the difference between the
fish assemblages in two coastal areas is subtle, the combination of eDNA
metabarcoding surveys, functional and phylogenetic information allow
their discrimination. Díaz-Pérez et al. (2016) proposed that the
estimation of coral reef health indices should be complemented with fish
community indices, to improve the accuracy of the estimated health
status of coral reefs in the western Caribbean Sea. In future research,
indices such as the Reef Health Index (RHI) could be complemented with
multidimensional information including functional and phylogenetic
indices from eDNA to inform policy makers about reef health status
(Obura et al. 2019).
With the combination of eDNA metabarcoding including all MOTUs and novel
statistical approaches (i.e., HMSC), we reveal a greater power of eDNA
to discern species occupancy across the two coastal stretches in
comparison with traditional UVCs. The application of joint species
distribution models to eDNA was suggested to increase the ecological
interpretation of the molecular signal (Burian et al. 2021). For similar
sampling effort, eDNA metabarcoding outperformed UVCs in its capacity to
identify the contrast between the two coastal areas and detected more
negative responses to the more anthropogenically stressed reef area.
Importantly, some of the strongest responses of MOTUs to the spatial
contrast were assigned to species that are elusive, highly mobile, and
cryptic. In contrast, UVCs could fail to detect the occurrence of those
species, thus increasing uncertainty in their estimated responses to the
environment in the distinct coastal areas. Additionally, eDNA
metabarcoding generates more identifications of taxa as MOTUs than UVCs
does. When we combine this richer data with HMSC, a statistical
framework that reduces parameter uncertainty (via shrinkage) across
similarly responding species, we can obtain greater confidence in
species responses. MOTU response was further associated with a
phylogenetic signal, indicating a strong distinction between clades with
a positive response (Apogonidae, Murenidae) and those with more negative
responses (Labridae) towards more anthropogenic stressed areas. We
expect that, assuming that MOTUs are true diversity units acting as a
species proxy, the generation of more data (MOTUs) to feed statistical
models will lead to more robust indicators of ecological status (with a
higher certainty of responses). That said, key sources of uncertainty
still exist in using eDNA to assign species and a better coverage within
reference databases will yield more information on the taxonomic units
recovered from eDNA (Valdivia‐Carrillo et al. 2021), to the point where
generating MOTUs as a species proxy will become unnecessary if almost
all regionally occurring species are genetically referenced.
Increasing evidence suggests that eDNA metabarcoding offers higher
species detection abilities compared with traditional surveys (Polanco
Fernández et al. 2021, Valdivia‐Carrillo et al. 2021), which was
confirmed in our study with the greater number of MOTUs detected with
eDNA (129 MOTUs) than fish species in UVC (120 species). We found
overlap in species composition between eDNA and UVC, but also
differences. While several species of relatively high abundance and easy
to detect visually such as Bodianus rufus andMicrospathodon chrysurus were detected with both methods, the UVC
detected more shallow reef species (e.g. Acanthurus spp), which
were not detected with eDNA. The shallow reef of Curaçao is
characterized by a very thin stretch averaging 40 m and the eDNA
transects were conducted slightly further away from the coast at
approximately 100 m of distance, which could explain why some of the
reef fish species were not detected. Our results suggest that the eDNA
signal could be spatially localized (e.g. as in West et al. 2021),
stressing the need for careful eDNA sampling to capture the entire
signal of a habitat. Nevertheless, both methods of observation detected
distinct fish composition between the two areas. While eDNA
metabarcoding can provide a rapid inventory of species composition
(Polanco Fernández et al. 2021) and can better detect small and cryptic
species, eDNA surveys cannot entirely replace UVC. In addition to
generating species lists, UVC transects can provide fish ontogenetic
stage, body size structure and abundance information that, at present,
eDNA does not provide at all or not accurately (Rourke et al. 2021).
These sources of information are key ecological indicators so that
future surveys might integrate, when possible, the strengths of both
survey approaches.