Beyond the visual: using metabarcoding to characterize the hidden reef cryptobiome

Abstract

In an era of coral reef degradation, our knowledge of ecological patterns in reefs is biased towards large conspicuous organisms. The majority of biodiversity, however, inhabits small cryptic spaces within the framework of the reef. To assess this biodiverse community, which we term the ‘reef cryptobiome’, we deployed 87 autonomous reef monitoring structures (ARMS), on 22 reefs across 16 degrees latitude of the Red Sea. Combining ARMS with metabarcoding of the mitochondrial cytochrome oxidase I gene, we reveal a rich community, including the identification of 14 metazoan phyla within 10 416 operational taxonomic units (OTUs). While mobile and sessile subsets were similarly structured along the basin, the main environmental driver was different (particulate organic matter and sea surface temperature, respectively). Distribution patterns of OTUs showed that only 1.5% were present in all reefs, while over half were present in a single reef. On both local and regional scales, the majority of OTUs were rare. The high heterogeneity in community patterns of the reef cryptobiome has implications for reef conservation. Understanding the biodiversity patterns of this critical component of reef functioning will enable a sound knowledge of how coral reefs will respond to future anthropogenic impacts.

Disentangling the complex microbial community of coral reefs using standardized Autonomous Reef Monitoring Structures (ARMS)

“…The Red Sea presents a unique combination of environmental variables that have previously been shown to shape the planktonic community (Kürten et al, , ; Ngugi, Antunes, Brune, & Stingl, ; Pearman et al, ; Pearman, Kurten, Sarma, Jones, & Carvalho, ) and the metazoan component of the reef cryptobiome (Carvalho et al, ). However, knowledge of the factors structuring the composition and function of bacterial communities within coral reefs remains limited (Roik et al, ; Neave et al, ).…”

“…Since standard protocols were developed, covering steps from deployment to sample collection and processing, the ARMS standardized framework ensures the samples obtained are comparable across various spatial scales. ARMS is now a validated tool to describe the biodiversity of the eukaryotic cryptic fauna associated with coral reefs (Al‐Rshaidat et al, ; Carvalho et al, ; Leray & Knowlton, ; Pearman, Anlauf, Irigoien, & Carvalho, ; Pearman et al, ; Plaisance, Caley, Brainard, & Knowlton, ; Ransome et al, ). More widely, ARMS have been applied to study the biodiversity in hard bottom marine habitats of the Atlantic, Indian and Pacific Oceans, as well as in the Black, Mediterranean and Red Seas (David et al, ).…”

Patterns, Drivers, and Ecological Implications of Upwelling in Coral Reef Habitats of the Southern Red Sea

“…Plankton blooms in the Farasan Banks region may also be important for sustaining local populations of planktivorous megafauna known to reside seasonally in the northern Farasan Banks such as whale sharks (Rhincodon typus) (Cochran et al, 2019) and reef mantas (Mobula alfredi) (Braun et al, 2014(Braun et al, , 2015. Although beneficial to some taxa, the higher nutrients in the southern Red Sea, particularly nearshore, have been correlated with reductions in the diversity of benthic and planktonic communities (Ellis et al, 2017;Pearman et al, 2017;Carvalho et al, 2019). However, since the low-diversity communities of bacteria and eukaryotes in the nutrient-rich regions of the southern Red Sea are unique (Carvalho et al, 2019), they still contribute to the overall diversity of the Red Sea (i.e.,  diversity).…”

“…Although beneficial to some taxa, the higher nutrients in the southern Red Sea, particularly nearshore, have been correlated with reductions in the diversity of benthic and planktonic communities (Ellis et al, 2017;Pearman et al, 2017;Carvalho et al, 2019). However, since the low-diversity communities of bacteria and eukaryotes in the nutrient-rich regions of the southern Red Sea are unique (Carvalho et al, 2019), they still contribute to the overall diversity of the Red Sea (i.e.,  diversity). Therefore, the effects of upwelling on biodiversity appear to be complex.…”

Filling in the Gaps: Adopting Ultraconserved Elements Alongside COI to Strengthen Metabarcoding Studies

“…Researchers are increasingly using metabarcoding to address questions across a wide range of scientific fields. For example, metabarcoding has been used in recent studies to assess parasitism in an invasive species (Kitson et al, 2018), characterize hidden cryptic diversity in a reef ecosystem (Carvalho et al, 2019), and identify dietary choices of a prairie bird (Sullins et al, 2018), to name just a few. Over recent years, studies evaluating the performance of these methods have consistently demonstrated that metabarcoding can match, and in many cases exceed, the performance of traditional morphology-based methods (Ji et al, 2013;Deiner et al, 2017;Bush et al, 2019).…”