Hide ‘n seq: direct versus indirect metabarcoding of coral reef cryptic communities

Ecological patterns in biodiversity are primarily based on conspicuous
organisms. Few methods are used to survey the taxonomically
rich cryptobiome, which is made up of inhabitants from
within microhabitats. One way that
cryptic marine biodiversity can be non-invasively
surveyed is by analyzing environmental DNA (eDNA) present in
seawater. Using coral reefs as a model system, here we
compare estimates of cryptic diversity among community
biomass and eDNA metabarcoding sampling methods
with a broad eukaryotic marker (COI). First, contributions to eDNA were
investigated across cryptobiomes through a comparison
of community metabarcoded biomass
from standardized autonomous reef monitoring structures
(ARMS) to eDNA acquired from seawater in which
individual ARMS were soaked. Second, we compared these results
to those from eDNA samples taken from within reef
crevices and the ambient water column. Metabarcoding
of community biomass from ARMS and eDNA
from the two types of water samples revealed
significantly different communities of cryptic coral reef habitat with
little overlap between methods. Taxa that were unique to metabarcoding
of ARMS biomass were predominantly from chitinous and
calcifying groups (polychaetes, palaemonid shrimp, molluscs,
brittle stars, and red algae), which suggests that these taxa are
underrepresented in eDNA surveys. Other than the corals
themselves, sponges and red algae were significant drivers of reef crevice
community differences, while ambient seawater samples detected mostly
planktonic organisms and reef fishes. Our data indicate
that both eDNA and ARMS provide incomplete
accounting of cryptic diversity. Direct sampling of
biomass is best suited for building taxonomies and improving databases,
whereas eDNA methods offer rapid insights into the composition
of cryptobiomes. Because each method likely captures
different taxa, multiple targeted assays can be
used to provide the greatest estimates of
metazoan and macroalgal richness.