An Integrative Assessment Combining Deep-Sea Net Sampling, in situ Observations and Environmental DNA Analysis Identifies Cabo Verde as a Cephalopod Biodiversity Hotspot in the Atlantic Ocean

Abstract

The deep sea is among the largest, most biologically diverse, yet least-explored ecosystems on Earth. Baseline information on deep-sea biodiversity is crucial for understanding ecosystem functioning and for detecting community changes. Here, we established a baseline of cephalopod community composition and distribution off Cabo Verde, an archipelago in the eastern tropical Atlantic. This baseline served to test the hypothesis that Cabo Verde is biogeographically separated from other Macaronesian archipelagos and allowed the identification of cephalopod species which may play a role in the Macaronesian carbon cycle and oceanic food web. To investigate cephalopod community composition, this study used 746 individual cephalopods obtained by nets (0–1000 m) and 52 cephalopod encounters during video surveys with either towed camera (0–2500 m) or manned submersible (0–375 m). Additionally, environmental DNA (eDNA) metabarcoding on 105 seawater samples (50–2500 m), using an 18S rRNA universal cephalopod primer pair, and a species-specific primer pair for Taningia danae resulted in the detection of 32 cephalopod taxa. When combined, the three methods detected a total of 87 taxa, including 47 distinct species. Each method contributed between 7 and 54% of taxa that were not detected by the other methods, indicating that multiple methodological approaches are needed for optimal deep-sea cephalopod biodiversity assessments. This study documents the occurrences of six species and three genera for the first time in waters surrounding Cabo Verde. Video surveys and eDNA analysis detected Taningia danae recurrently (100–2500 m). eDNA metabarcoding proved to be a powerful tool for cephalopod biodiversity monitoring and complementary to traditional sampling methods. When also including literature records, Cabo Verde hosts at least 102 cephalopod taxa including 30 families and 64 benthic and pelagic species. The total number and species composition of Cabo Verde cephalopods is similar to the Canary Islands and Azores, two known cephalopod biodiversity hotspots, but the Cabo Verde octopus fauna seems to differ. Due to a range of life history characteristics, we hypothesize that the squids Taningia danae (Octopoteuthidae) and Sthenoteuthis pteropus (Ommastrephidae) are important in the carbon cycle of Macaronesia. As a cephalopod biodiversity hotspot Cabo Verde could function as a model region to investigate cephalopod biology and ecology in a rapidly changing Atlantic Ocean.

First evidence of population genetic structure of the deep-water blackmouth catshark Galeus melastomus Rafinesque, 1810

“…Maximising the monitoring of Mediterranean and Atlantic populations of blackmouth catshark both in its temporal and spatial coverage is advisable and it could be achieved by capitalising established scientific surveys where G. melastomus represents one of the target species (i.e., MEDITS and PNAB; Spedicato et al, 2020;Vieira et al, 2020). In addition, the employment of non-invasive sampling protocols (i.e., environmental DNA; Aglieri et al, 2021) represent a valuable approach to obtain data without sacrificing individuals for research purposes, even though such techniques have not been extensively applied to threatened and deep water species (Dugal et al, 2022;Merten et al, 2021). The improvement of the genotyping approach (i.e., the application of an increased number of polymorphic microsatellite loci or the development of panels of Single Nucleotide Polymorphisms, SNPs) will provide more statistical power for the robust delineation of the genetic structure of the species.…”

Improved biodiversity detection using a large-volume environmental DNA sampler with in situ filtration and implications for marine eDNA sampling strategies

“…Sample volumes used for eDNA filtration typically range between 1 to 5 liters and are limited by bottle size, competing scientific needs for sample water, and filtration capabilities (e.g., how quickly and how many samples can be filtered). Relative to the vastness of midwater habitats, these eDNA sampling volumes are minute (Govindarajan et al, 2021;Merten et al, 2021); and may be insufficient for obtaining representative eDNA snapshots, given that eDNA distributions appear to be patchy (Andruszkiewicz et al, 2017). However, the issue of optimizing sample volume is relatively poorly understood relative to other eDNA sampling and processing parameters, such as filter type and DNA extraction protocol (Dickie et al, 2018).…”

“…DNA sequencing of the trace genetic remains of animals found in bulk environmental samples provides detailed information on the taxonomic makeup of marine communities, and leads to important insights on the diversity, distribution, and ecology of community inhabitants (e.g., Sawaya et al, 2018;Jeunen et al, 2019;Closek et al, 2019;Djurhuus et al, 2020;West et al, 2021;Visser et al, 2021). eDNA analyses are being increasingly applied to mid-and deepwater ocean ecosystems (Canals et al, 2021;Easson et al, 2020;Govindarajan et al, 2021;Laroche et al, 2020;Merten et al, 2021), and advances in robotics and sampling technology could improve sampling strategies to these otherwise difficult to reach regions.…”

Optimization of environmental DNA analysis using pumped deep-sea water for the monitoring of fish biodiversity

“…In the deep sea, eDNA analysis has focused on the sediments to survey the benthic communities (e.g., Guardiola et al, 2016;Sinniger et al, 2016;Laroche et al, 2021). On the other hand, a few surveys of aquatic communities in the deep sea have been conducted (Fraija-Fernańdez et al, 2020;McClenaghan et al, 2020;Merten et al, 2021). Recently, a combination of eDNA with other methodologies (e.g., imaging data) is shown to be a more comprehensive method of monitoring deep-sea biodiversity (Fujiwara et al, 2022;Stefanni et al, 2022).…”