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Review
.2018 May 16;285(1878):20180056.
doi: 10.1098/rspb.2018.0056.

Mammoth grazers on the ocean's minuteness: a review of selective feeding using mucous meshes

Affiliations
Review

Mammoth grazers on the ocean's minuteness: a review of selective feeding using mucous meshes

Keats R Conley et al. Proc Biol Sci..

Abstract

Mucous-mesh grazers (pelagic tunicates and thecosome pteropods) are common in oceanic waters and efficiently capture, consume and repackage particles many orders of magnitude smaller than themselves. They feed using an adhesive mucous mesh to capture prey particles from ambient seawater. Historically, their grazing process has been characterized as non-selective, depending only on the size of the prey particle and the pore dimensions of the mesh. The purpose of this review is to reverse this assumption by reviewing recent evidence that shows mucous-mesh feeding can be selective. We focus on large planktonic microphages as a model of selective mucus feeding because of their important roles in the ocean food web: as bacterivores, prey for higher trophic levels, and exporters of carbon via mucous aggregates, faecal pellets and jelly-falls. We identify important functional variations in the filter mechanics and hydrodynamics of different taxa. We review evidence that shows this feeding strategy depends not only on the particle size and dimensions of the mesh pores, but also on particle shape and surface properties, filter mechanics, hydrodynamics and grazer behaviour. As many of these organisms remain critically understudied, we conclude by suggesting priorities for future research.

Keywords: bentho-pelagic coupling; grazers; pteropods; selective feeding; tunicates.

© 2018 The Author(s).

PubMed Disclaimer

Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
Mucous-mesh grazing: (a) clearance rates of mucous-mesh grazers and other common, non-mucus microphagous grazers versus prey-to-predator length (electronic supplementary material, table S1). (b) Schematic showing location of the mucous mesh for different grazers. The mucous mesh is highlighted according to the mechanism used to drive flow through or across the mesh. (b) IF, inlet filter; FCF, food-concentrating filter; PF, pharyngeal filter; MW, mucous web. Drawings by Caitlyn Webster. (Online version in colour.)
Figure 2.
Figure 2.
Hydrodynamics, mesh morphologies, and flux of mucous-mesh grazers. PF: pharyngeal filter; FCF: food-concentrating filter; IF: inlet filter prior- (top) and post-inflation of the house (bottom); MW: mucous web. Photographs courtesy of: Linda Ianniello forClio sp. andCorolla sp., S. Bush for Peraclidae mucous web, © 2008 MBARI, Ron Gilmer forCavolinia uncinata faecal material [10]. Salpidae flux rates based on the faecal pellets ofPegea confoederata [24]; Oikopleuridae flux rates based onOikopleura dioica faecal pellets [25] and houses [26]; Thecosomata flux rates based on the mucous webs ofLimacinia retroversa [27] and faecal material ofCorolla spectabilis [9]. (Online version in colour.)
Figure 3.
Figure 3.
Contributions of mucous-mesh grazers to the ocean food web. Arrows show common flux pathways (solid line) and pathways unique to a specific group (dashed line), including jelly-falls (Pyrosoma atlanticum, courtesy of S. Marion), appendicularian houses (inset shows fluorescent inclusions in the house rudiment ofOikopleura albicans), mucous webs and pseudofaeces (Corella calceola from Gilmer [12], courtesy of R. Gilmer). Pyrosome and thecosome photographs courtesy of Mike Bartick; appendicularian photograph courtesy of Linda Ianniello. (Online version in colour.)
Figure 4.
Figure 4.
Physical and behavioural particle selection mechanisms of mucous-mesh grazers using the appendicularianOikopleura dioica as a model. The inlet filters (IF) exclude large and spinous prey from entering the house. Small particles, such as the red carmine dye, are more likely to adhere to the food-concentrating filter (FCF). Both of these filtration processes determine what reaches the pharyngeal filter and gut. Surface properties, such as charge, influence particle interactions with the mucous filters (courtesy of A. Karim). Particles rejected by behavioural mechanisms (shown by coloured tracks) can exit the house via the exit spout (ES). (Online version in colour.)
Figure 5.
Figure 5.
Future directions for investigating feeding by mucous-mesh grazers at different spatial scales. Mesh-particle scale techniques: micro-scale particle image velocimetry (μPIV) [127]; atomic force microscopy (AFM) topographic image of two conjointSynechococcus cells surrounded by a gel matrix (courtesy of F. Malfatti [128]); flow cytometry cytogram showing prey particles (Syn:Synechoccocus, Peuks: picoeukaryotes) from pyrosome gut contents (courtesy of A. Thompson). Diver-operated methods: Diver Controlled Observation and Measurement of Plankton (DCOMP) (Weelia cylindrica); VacuSIP (courtesy of A. Dadon-Pilosof). Remotely operated systems: remotely operated vehicles (ROVs) (Pteropod © 2008 MBARI, courtesy of S. Bush;Pyrosoma atlanticum © 2014 MBARI); DeepPIV (Bathochordaeus stygius, courtesy of K. Katija). Towed systems: video plankton recorder (VPR) (Salpa aspera, courtesy of C. Davis [129]); underwater vision profiler (UVP) (appendicularian house, courtesy of L. Stemmann [130]); digital holography (DH) (Thalia democratica, courtesy of N. Loomis [131]);In situ Ichthyoplankton Imaging System (ISIIS) (budding doliolid, courtesy of M. Schmid [132]). (Online version in colour.)
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