Multiple Trophic Tracer Analyses of Subarctic Rhodolith (Lithothamnion glaciale) Bed Trophodynamics Uncover Bottom-Up Forcing and Benthic-Pelagic Coupling

Abstract

We paired a survey of cryptofaunal abundance and rhodolith morphology with lipid, fatty acid, and stable isotope analyses to quantify nutritional patterns and trophic linkages of six dominant echinoderm, bivalve, gastropod, and polychaete species, two macroalgal species, seawater, and underlying sediment in a large (>500 m2) rhodolith (Lithothamnion glaciale) bed in southeastern Newfoundland (Canada). We found high densities of chitons (Tonicella marmorea and T. rubra) and daisy brittle star (Ophiopholis aculeata), and overall species composition, rhodolith morphology (shape and size), and total rhodolith biomass were consistent with other studies of the bed, indicating high temporal stability. Our lipid and fatty acid analyses revealed high levels of phospholipids and unsaturated fatty acids combined with low sterols in all animal species, suggesting adaptation for enhanced cell membrane fluidity in a cold-water environment. They also showed that most taxa sampled feed on a shared resource; diatoms, and that (non-kelp) macroalgal detritus are a key food source within rhodolith communities. Our stable isotope analysis uncovered three distinct trophic levels; producers, suspension/filter feeders and grazers, and predators, and unveiled potential resource partitioning between first- (H. arctica) and second- (O. aculeata and Tonicella spp.) order consumers, whereby differences in feeding strategies enable utilization of specific components of the same organic and inorganic material. The unprecedented analytical resolution enabled by the combined use of three trophic tracers indicate that bottom-up forcing (as a mechanism of trophic control) and benthic-pelagic coupling (as a pathway of nutrient and energy flow) operate simultaneously, at least seasonally, in subarctic rhodolith beds.

Spatiotemporal Variability in Subarctic Lithothamnion glaciale Rhodolith Bed Structural Complexity and Macrofaunal Diversity

“…We also showed that rhodolith shape distribution was similar among pebble-nucleated and non-nucleated rhodoliths, with ~70% of compact shapes, while shell-nucleated rhodoliths were mostly bladed (59%) or elongate (20%) but seldom compact. Our finding that the majority of rhodoliths at both study sites were nonetheless non-nucleated and compact in shape parallels observations in other sections of the St. Philip's bed since 2012 [30,36,50]. Predominantly compact shapes have also been documented in arctic [72,73], temperate [71,74], and tropical [75,76] rhodolith beds.…”

“…We showed that the rhodolith bed at both sites was structurally stable throughout the survey, containing >90% of live and dead rhodoliths and coarse biogenic sediments, as well as similar rhodolith densities (~822 individuals m −2 ) and biomasses (~11.5 kg rhodoliths m −2 ) in any given season. Such rhodolith densities and biomasses within the 15-20 m depth range (1) parallel the ~858 rhodoliths m −2 reported by Gagnon et al [30] for a shallower (8 to 10 m deep) portion of the same bed sampled four years before the present study, and (2) are up to twice lower than the peak 19.5 kg rhodoliths m −2 measured in other portions of the bed within the 8-15 m depth range four years before [30] and four years after [50] the present study. That rhodolith biomass varies spatially within the bed despite a homogenous rhodolith density, indicates that rhodolith size varies across the bed.…”

“…Macrofaunal abundance, however, was dominated by a few species with brittle stars (Ophiopholis aculeata and Ophiura robusta) and chitons (Tonicella marmorea and Stenosemus albus), accounting for >50% of all the specimens identified, and ~70% of total macrofaunal biomass. Studies of other portions of the St. Philip's bed carried out 4 y before [30], as well as 1 y [36] and 4 y [50] after the present study, also highlighted the dominance of these and other abundant taxa, including green sea urchin (Strongylocentrotus droebachiensis), common sea star (Asterias rubens), and wrinkled rock borer (Hiatella arctica), therefore highlighting high temporal stability in the main composition of the macrofaunal community. The present study's finer taxonomic resolution unveiled the important contribution of gastropods (Puncturella noachina and Moelleria costulata) and polychaetes (Sabellidae and Terebellidae) to total macrofaunal abundance and diversity.…”

“…One of these beds, located along the shore of the town of St. Philip's and hereafter termed the "St. Philip's bed", is relatively large (~25,000 m 2 ) and highly biodiverse ( [30] and present study). This bed has since been studied for its sedimentary processes [36], calcium carbonate (CaCO 3 ) production [32], resilience to thermal shifts and eutrophication [33][34][35], and trophodynamics [50]. This knowledge base offers an excellent opportunity to further investigate and explain spatial and temporal variability in macrofaunal biodiversity patterns.…”

Seasonal lipid dynamics of four Arctic bivalves: Implications for their physiological capacities to cope with future changes in coastal ecosystems

“…However, the fatty acid composition of polar lipids observed throughout the year likely reflects the acclimation of organisms to the low temperatures observed in the fjord (temperature < to 0.5°C throughout the year at 17 m, Sejr et al, 2022). The strong relative contributions of PUFAs observed in H. arctica, M. discors, and Mya truncata (i.e., >47%) are similar to those observed in other studies that also found an effect of cold temperature on the lipid composition of cell membranes of Arctic/sub-Arctic bivalve species (Gaillard et al, 2015;Hacker Teper et al, 2022;Thyrring et al, 2017).…”