Pelagic tunicate grazing on marine microbes revealed by integrative approaches

Abstract

Marine microorganisms comprise a large fraction of ocean carbon and are central players in global biogeochemical cycling. Significant gaps remain, however, in our understanding of processes that determine the fate, distribution, and community structure of microbial communities. Protists and viruses are accepted as being part of the microbial loop and a source of microbial mortality. However, pelagic tunicates (salps, doliolods, pyrosomes, and appendicularians), which are abundant in oceanic and coastal environments and consume microorganisms with higher individual grazing rates than other common grazers, remain underappreciated in their role controlling microbial communities, distributions, and flux through ecosystems. In spite of sampling challenges owing to their fragile nature and patchy distributions, recent developments in methodology have deepened understanding of grazing rates and selectivity of these ubiquitous grazers. Next-generation sequencing, quantitative polymerase chain reaction, high-resolution videography, improved microscopy, biomarkers, and in situ approaches are transforming our knowledge on the role of pelagic tunicates in determining the fate and function of microbial communities. Here, we review recent research on pelagic tunicate grazing with a focus on newer methodologies and their application across pelagic tunicate taxa. Synthesis of these studies points to a major role for pelagic tunicates in the control of marine microbial communities. Comparisons between pelagic tunicate taxa indicate important differences in prey selectivity, which will impact how these grazers are incorporated into global models. Application and integration of these methods will produce continued insights with the ultimate goal of illuminating the unique role of pelagic tunicates in the microbial loop and biological pump.

Multi-storm analysis reveals distinct zooplankton communities following freshening of the Gulf of Mexico shelf by Hurricane Harvey

“…Changes in the abundance of larger, soft bodied organisms such as gelatinous zooplankters may alter the available carbon within coastal food web and redirect secondary production through the microbial loop rather than transferring energy to higher trophic levels. Additionally, filter feeding gelatinous zooplankton such as doliolids and salps can process and filter greater volumes of water at increased body sizes 44 , 45 , potentially increasing their ecological success leading to positive feedback of recovering energy from the microbial loop 46 and enhancing vertical carbon flux 47 . Kurtay et al 20 reported an increase in pico- and nanoplankton, prey items that falls within the filtering size of both doliolids and salps 44 , 45 .…”

Laboratory study ofFritillarialifecycle reveals larvacean commonalities and key morphogenetic events leading to genus-specific anatomy

“…Tunicates are a fascinating group of animals with considerable diversity in size, feeding strategy, reproduction, and other fundamental life traits. However, biological studies have been more sustained on sessile tunicates (represented by solitary and colonial ascidians) than on pelagic tunicates, even though the latter are increasingly recognized as key components of the oceanic ecosystems 39 . Some pelagic tunicates are difficult to access and as a matter of fact, the abundant and ubiquitous O. dioica rapidly became one the few species to be established in a continuous laboratory culture 6 .…”

Self-organisation of zooplankton communities produces similar food chain lengths throughout the ocean

“…2e) become more important. Heterotrophic flagellates and ciliates 14,17 , and the much-larger larvaceans and salps 30,32,33 , feed on smaller phytoplankton unavailable to copepods and euphausiids 29 (Fig. 2a,c).…”

“…The ability of low-trophic position filter-feeders 17 to ingest picophytoplankton and bacteria could short-circuit the microbial loop, transferring carbon to larger sizes. However, traditional sampling techniques underestimate their role and almost no food-web models include filterfeeders 33,34,38 . Our findings highlight the unique, yet critical and overlooked role of filter-feeding zooplankton.…”

“…The crustacean-gelatinous shift also has implications for the food quality for fish and nutrient cycling 9,31,33 . Consistent with observations of active carbon flux 41 , the greater importance of crustaceans in eutrophic regions (Fig.…”