Marine host-associated microbiomes are affected by a combination of species-specific (e.g., host ancestry, genotype) and habitat-specific features (e.g., environmental physiochemistry and microbial biogeography). The stingray epidermis provides a gradient of characteristics from high dermal denticles coverage with low mucus to reduce dermal denticles and high levels of mucus. Here we investigate the effects of host phylogeny and habitat by comparing the epidermal microbiomes of Myliobatis californica (bat rays) with a mucus rich epidermis, and Urobatis halleri (round rays) with a mucus reduced epidermis from two locations, Los Angeles and San Diego, California (a 150 km distance). We found that host microbiomes are species-specific and distinct from the water column, however composition of M. californica microbiomes showed more variability between individuals compared to U. halleri. The variability in the microbiome of M. californica caused the microbial taxa to be similar across locations, while U. halleri microbiomes were distinct across locations. Despite taxonomic differences, Shannon diversity is the same across the two locations in U. halleri microbiomes suggesting the taxonomic composition are locally adapted, but diversity is maintained by the host. Myliobatis californica and U. halleri microbiomes maintain functional similarity across Los Angeles and San Diego and each ray showed several unique functional genes. Myliobatis californica has a greater relative abundance of RNA Polymerase III-like genes in the microbiome than U. halleri, suggesting specific adaptations to a heavy mucus environment. Construction of Metagenome Assembled Genomes (MAGs) identified novel microbial species within Rhodobacteraceae, Moraxellaceae, Caulobacteraceae, Alcanivoracaceae and Gammaproteobacteria. All MAGs had a high abundance of active RNA processing genes, heavy metal, and antibiotic resistant genes, suggesting the stingray mucus supports high microbial growth rates, which may drive high levels of competition within the microbiomes increasing the antimicrobial properties of the microbes.
Although trophic cascades were originally believed to be driven only by predators eating prey, there is mounting evidence that such cascades can be generated in large part via non-consumptive effects. This is especially important in cascades affecting habitat-forming foundation species that in turn, influence associated communities. Here, we use laboratory and field experiments to identify a trait-mediated indirect interaction between predators and an abundant kelp in a marine temperate reef system. Predation risk from a microcarnivorous fish, the señorita, suppressed grazing by the host-specific seaweed limpet, which in turn, influenced frond loss of the habitat-forming feather boa kelp. This trophic cascade was pronounced because minor amounts of limpet grazing decreased the strength required to break kelp fronds. Cues from fish predators mitigated kelp loss by decreasing limpet grazing; we found 86% of this indirect interaction between predator and kelp was attributed to the non-consumptive effect in the laboratory and 56% when applying the same effect size calculations to the field. In field manipulations, the non-consumptive effect of señorita was as strong as the total predator effect and most importantly, as strong as the uncaged, "open" treatment with natural levels of predators. Our findings demonstrate that the mere presence of this fish reduces frond loss of the feather boa kelp through a trait-mediated trophic cascade. Moreover, despite large volumes of water, current flow, and wave energy, we clearly demonstrate a strong non-consumptive effect via an apparent chemical cue from señorita, suggesting that chemically mediated trait-driven cascades may be more prevalent in subtidal marine systems than we are currently aware.
Kelp , Animals , Ecosystem , Fishes , Food Chain , Predatory Behavior
