Biodynamics of Suspension-Feeding in Adult Bivalve Molluscs: Particle Capture, Processing, and Fate

Abstract

The technique of endoscopic examination and video-image analysis has allowed for in vivo observations of adult, bivalve molluscs and has led to a more accurate understanding of suspension-feeding processes in these animals. Several mechanisms, however, needed to be examined further. For example, the process by which particles are captured by the ctenidia remained unclear, and current models of this process did not adequately explain in vivo observations of capture events. In addition, the kinematics of particle processing by the labial palps and mode of particle ingestion have remained undefined. In this study I use results from endoscopic observations of nine species of bivalves to provide an integrated description of suspension feeding. These observations reveal that particle feeding is accomplished by both mucociliary and hydrodynamic mechanisms that often act simultaneously on the pallial organs. I introduce a model of particle capture that focuses on the ctenidial filament as the capture unit, unlike previous work that emphasized the laterofrontal cilia or cirri. The model is consistent with accepted fluid dynamic principles. In vivo observations in bivalves indicate that the suspension-feeding complex as a whole is, functionally, more than merely the sum of its parts. Additional key words: transport, ingestion, kinematics Suspension-feeding bivalves are a large group of ecologically and economically important aquatic animals. In many habitats they can be dominant infaunal or epibenthic organisms, affecting the surrounding community through processes such as benthic-pelagic coupling, particle depletion, and nutrient cycling (Peterson & Black 1987; Asmus & Asmus 1993; Smaal & Prins 1993). Therefore, many aspects of bivalve biology and ecology have been studied and described (Bayne et al. 1988; Bayne & Hawkins 1992; Bayne 1993; Dame 1993; Grant et al. 1993; Newell & Shumway 1993), including anatomical and physiological aspects of suspension-feeding (J0rgensen 1966, 1990; Owen 1974; Morton 1983). Most of these descriptions of suspension-feeding have been largely based on surgically altered specimens or on feeding structures isolated from the pallial cavity. While valid under certain circumstances, results from most of these studies should be interpreted with caution because surgery and isolation can: (1) cause feeding structures to function abnormally, (2) alter hydrodynamics of flow around the structures, and (3) destroy subtle interactions between adjacent feeding structures (e.g., ctenidia and labial palps). In addition, extrapolation of in vitro results to in vivo mechanisms implicitly assumes that the filaments or structures function as discrete units and that the feeding complex functions merely as the sum of its constituent parts (e.g., Nielsen et al. 1993). This may not be a valid assumption. In fact, previous researchers have suggested that mechanisms of feeding cannot be understood from studies on exposed ctenidia or ctenidial filaments (e.g., J0rgensen 1976). During the past several years, in vivo studies in intact bivalves by means of video endoscopy have provided a better understanding of suspension-feeding processes (Beninger et al. 1992; Ward et al. 1993; Ward et al. 1994). However, the details of many feeding processes, especially as they occur in intact animals, remain unclear. For example, the process by which particles are captured by the ctenidia has been a subject of debate for many years. Some workers have maintained that particles are mechanically trapped by rows of laterofrontal cilia or cirri (Tammes & Dral 1955; Dral 1967; Moore 1971), while others have suggested that particles are retained by hydrodynamic forces that operate at the level of interfilamentar spaces (Owen & McCrae 1976; J0rgensen 1981, 1990). AsThis content downloaded from 207.46.13.129 on Wed, 29 Jun 2016 04:33:02 UTC All use subject to http://about.jstor.org/terms Suspension-feeding biodynamics in bivalves pects of both theories, however, violate some of the physical and biological constraints imposed by the intact feeding system, and neither adequately explains in vivo observations of capture. The goal of this study was to integrate the observations and results obtained by video endoscopy, including previously unpublished data, with those obtained by more invasive techniques, in order describe a more holistic model of suspension-feeding biodynamics. Specifically, data on particle capture and transport by the ctenidia, transfer of particulate matter to the labial palps, processing of material by the palps, and ingestion of food material will be presented. I do not attempt a detailed, exhaustive explanation of feeding processes; rather, I focus on general mechanisms that are common to most suspension-feeding bivalves and that serve to unify this group. Where appropriate, my results are placed in the context of previous descriptions of feeding mechanisms in bivalves.