Meiofauna Life on Loggerhead Sea Turtles-Diversely Structured Abundance and Biodiversity Hotspots That Challenge the Meiofauna Paradox

Abstract

Sea turtles migrate thousands of miles annually between foraging and breeding areas, carrying dozens of epibiont species with them on their journeys. Most sea turtle epibiont studies have focused on large-sized organisms, those visible to the naked eye. Here, we report previously undocumented levels of epibiont abundance and biodiversity for loggerhead sea turtles (Caretta caretta), by focusing on the microscopic meiofauna. During the peak of the 2018 loggerhead nesting season at St. George Island, Florida, USA, we sampled all epibionts from 24 carapaces. From the subsamples, we identified 38,874 meiofauna individuals belonging to 20 higher taxa. This means 810,753 individuals were recovered in our survey, with an average of 33,781 individuals per carapace. Of 6992 identified nematodes, 111 different genera were observed. To our knowledge, such levels of sea turtle epibiont abundance and diversity have never been recorded. Loggerhead carapaces are without doubt hotspots of meiofaunal and nematode diversity, especially compared to other non-sedimentary substrates. The posterior carapace sections harbored higher diversity and evenness compared to the anterior and middle sections, suggesting increased colonization and potentially facilitation favoring posterior carapace epibiosis, or increased disturbance on the anterior and middle carapace sections. Our findings also shed new light on the meiofauna paradox: “How do small, benthic meiofauna organisms become cosmopolitan over large geographic ranges?” Considering high loggerhead epibiont colonization, the large distances loggerheads migrate for reproduction and feeding, and the evolutionary age and sheer numbers of sea turtles worldwide, potentially large-scale exchange and dispersal for meiofauna through phoresis is implied. We distinguished different groups of loggerhead carapaces based on divergent epibiont communities, suggesting distinct epibiont colonization processes. These epibiont observations hold potential for investigating loggerhead movements and, hence, their conservation.

The ability to get everywhere: dispersal modes of free-living, aquatic nematodes

“…Another mode of dispersal is via turtle shells, as the backs of marine turtles are colonized by a diverse array of micro-, meio-, and macrobenthic organisms, all of which are associated with food webs and energy flows (Corrêa et al, 2014;dos Santos et al, 2018;Ingels et al, 2020). In contrast to all other dispersal modes discussed herein, apart from rafting, turtle shells allow the reproduction of the transferred organisms.…”

“…Although the meiobenthic community on turtle shells resembles that occurring in reef environments, turtle shells represent hotspots of nematode diversity. Moreover, because millions of turtles, with their standing stock of meiobenthic organisms, traveling thousands of kilometers between foraging grounds and nesting beaches (Luschi et al, 2003;Ingels et al, 2020), they must be considered as one of the most important epizoochoric dispersal vectors in marine environments.…”

Nematode epibionts on skin of the Florida manatee, Trichechus manatus latirostris

“…In addition to T. manatus , there are two other Trichechus species in the world, i.e., the Amazonian manatee, T. inunguis and the African manatee, T. senegalensis Link. It would be interesting to examine these two congeners to test the commonality of the origins of their nematode epibionts (if present), and the co-evolution and/or host switching patterns 20 .…”

“…Also, further survey work is needed for nematodes in biofouling layers or epidermal substrates of other aquatic animals to confirm the uniqueness of the nematodes reported herein and to search for other interesting symbiotic associations involving the amazing world of roundworms. For example, a recent study of the epibiont meiofauna of loggerhead turtles, Caretta caretta L. in Florida found heretofore unreported marine nematode diversity from the carapaces of these seafaring vertebrates and implied a potential phoretic mechanism for large scale movement of benthic meiofauna 20 .…”

Colonization of macroalgal deposits by estuarine nematodes through air and potential for rafting inside algal structures

“…Nematodes are usually by far the numerically dominant meiofaunal taxon in soft sediments, and among the most abundant on algae, seagrasses and salt marsh vegetation [ 12 , 13 ]. Their dispersal is considered to be mostly passive, mediated by bedload transport, by drifting in sea water after erosion from sediments or phytal substrata, or through ‘rafting’ on vectors such as drifting macroalgae or sea turtles [ 7 , 10 , 14 – 18 ]. Nevertheless, some nematodes may actively enter the water column, thus facilitating their dispersal through water currents and bedload transport [ 7 , 19 – 21 ], and they appear capable of choosing sites where they will settle again [ 21 , 22 ].…”