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Principles of Pseudofeces Rejection on the Bivalve Mantle: Integration in Particle Processing

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Principles of Pseudofeces Rejection on the Bivalve Mantle: Integration in Particle Processing MARINE ECOLOGY PROGRESS SERIES Published March 17 Mar Ecol Prog Ser Principles of pseudofeces rejection on the bivalve mantle: integration in particle processing Peter G. Beningerll*, Anne veniot2,Yves poussart2 'Laboratoire de Biologie Marine, Faculte des Sciences, Universite de Nantes, F-44322 Nantes Cedex 3, France 2Departement de Biologie, Faculte des Sciences, Universite de Moncton. Moncton, New Brunswick ElA 3E9, Canada ABSTRACT: lvlechanisms of pseudofeces voidance from the mantle were investigated in 3 of the 4 major bivalve particle processing systems using scanning electron microscopy, to determine what mechanisms permit the isolation of pseudofeces transport in bivalves presenting discrete mantle rejec- tlon pathways, and how this contrasts with species which do not possess such pathways. The entire mantle surfaces of Mytilus edulis (homorhabdic filibranch), Mya arenaria and Spisula solidissima (eulamellibranchs), and Placopecten magellanicus (heterorhabdic filibranch) were surveyed and photographed. In both the homorhabdic filibranchs and the eulamellibranchs, the mantle rejection tracts previously located using video endoscopy were characterized by cilia which were extraordinar- ily long compared to the cilia of the general paUial surface. These long cilia were grouped into closely adhering tufts, herein termed composite cilia. In M. edulis and M. arenaria, the general pallial surface presented shorter simple cilia, whereas in S. solidissima the general pallial surface presented simple cilia dorsally, long composite cilia ventrally, and an intermediate band of short composite cilia. These 3 species all possess a gill ventral particle groove; hence the site of pseudofeces production is the labial palp, and a discrete mantle rejection tract is necessary to transport pseudofeces to the inhalent siphon for expulsion. The long composite cilia within this tract may provide vertical isolation of pseudofeces from the general pallial surface; effective mucociliary transport using such long cilia can only be accomplished if they are grouped, as in all 3 species with mantle rejection tracts. In the heterorhabdic filibranch P. magellanicus, no specialized cilia were observed on the mantle; this corresponds to the absence of a mantle rejection tract in this system, which does not possess a gill ventral particle groove and relies on valve adduction to expel pseudofeces. These results suggest that elevation above the sur- rounding mantle cllia is the rule in species relying on mantle rejection tracts for the voidance of pseudo- feces. These results show the usefullness of cilia mapping in the study of bivalve suspension-feeding mechanisms. KEY WORDS: Bivalves . Feeding . Pseudofeces . Rejection INTRODUCTION bivalves, both of these processes culminate in rejec- tion, which results in the formation of pre-ingestive Among the free-living aquatic invertebrates, suspen- rejecta termed pseudofeces. The production and void- sion-feeding is a widespread and successful trophic ance of pseudofeces is thus an important physiological strategy, spanning phyla from the Ponfera to the Chor- function (Owen 1966, Bayne & Newel1 1983, Iglesias data (Jsrgensen 1966). Two of the foremost problems et al. 1992), as well as being a major contributor to faced by organisms which have adopted this mode of bivalve biodeposits in the aquatic ecosystem (Bayne & feeding are (1) the regulation of the volume of material Newel1 1983, Kautsky & Evans 1987, Dame 1993). processed and ingested (ingestion volume regulation), Pseudofeces elimination is the final rejection step in and (2) the sorting of edible seston from that which is the cascade of particle processing events which begin inorganic, of low nutritional value, or even toxic (selec- with capture on the gill. One of the salient conclusions tion) (Sierszen & Frost 1992). In suspension-feeding from the intense research effort in the field of bivalve feeding mechanisms (e.g.Beninger et al. 1992, 1997a, Tankersley & Dlmock 1993, Ward et al. 1993) is that O Inter-Research 1999 Resale of full article not permitted 260 Mar Ecol Prog Ser 178: 259-269, 1999 the type of particle processing, and hence the mode $ of pseudofeces rejection, is initially determined by the 2 3 gill type itself (Beninger & St-Jean 1997a).Endoscopic #m observation of whole specimens has demonstrated that -2 pseudofeces rejection involves well-defined mantle " rejection tracts in bivalves presenting 2 of the 4 gill : types: homorhabdic filibranch and eulamellibranch C a, (Table 1).In the homorhabdic filibranch Mytilus edulis, tn the mantle rejection tract presents an extraordinary O density of acid mucopolysaccharide (AMPS)-secreting $ mucocytes (Ansell 1961, Beninger & St-Jean 199?b). which anchors the pseudofeces to the ciliated epithe- 2 lium and hence enables the transport of pseudofeces ; counter to the prevailing pallial current (Beninger & 0g N St-Jean 1997b). Q: It has long been known that the general pallial sur- E face of the mantle is ciliated, and pseudofecal transport ;"l& has often been observed in dissected specimens (Wal- 2 g lengren 1905, Orton 1912, Kellogg 1915, Elsey 1935, % , D .- Ansell 1961, Foster-Smith 1975). Recent comparisons m 2 with endoscopic observations have shown that pseudo- 3 d feces transport on the mantle appears unaffected by c 2 dissection, validating the simpler technique of ob- <-z servation of inert particles deposited on the mantle + 4 (Beninger & St-Jean 199?b, Beninger et al. 1997a). The 2% transport of pseudofeces along well-defined rejection E ai 2 CL tracts situated on the general ciliated pallial surface ,-E raises the possibility of some form of isolation mecha- 5 g nism which would confine pseudofeces transport to 2 5 these tracts, such as ciliary specialization, in addition or= to the aforementioned specialization of mucocyte types o-;.- o-, D c and densities. Although the presence of cilia is fre- 2 quently documented in studies dealing with the -$ mantle pallial surface (e.g. Morrisson 1993, Reindl & % Haszprunar 19961, no comprehensive survey of mantle X g ciliation has been performed, and hence very little 2 4 information is available concerning the possible spe- $e .-F cialization of cilia (either in type or density) in the 2 mant1.e rejection tracts. Based on histological observa- .$ 2 tions, Ansell (1961) stated that cilia on the mantle 5 rejection tract of several species of Veneridae were 2 z longer than those outside the rejection tract; this poses .gU the problem of functionality, since long cilia have .: inherent limitations to effective mucociliary transport (Sleigh et al. 1988, Sleigh 1989).Given the importance $ of rejection i.n particle processing, we have performed a detailed survey of the ciliation of the bivalve pallial surface, using the technique of ciliary mapping 02 (Beninger et al. 1995).The present study reports on the % ciliary types and distribution on the mantle pallial 3.- surface of Mytilus edulis (homorhabdic filibranch), Placopecten magellanicus (heterorhabdic filibranch), and Mya arenaria and Spisula solidissima (eulamelli- 3 branchs), and relates these data to the rejection mech- 5Q, anisms in these species. c Beninger et al.: Pseudofec:es rejection in bivalves 261 MATERIAL AND METHODS RESULTS Sampling and fixation. The size range of specimens Cilia types was limited to individuals 530 mm (maximum size possible for observation of whole specimens in the Two types of cilia were distinguished, based on SEM specimen chamber). Mya arenaria (size range occurrence as single cilia or as discrete groups of 15.3 to 30.0 mm antero-posterior axis) and Mytilus closely adhering cilia, which we here term 'composite edulis (20.0 to 27.0 mm antero-posterior axis) were cilia' Within these 2 types, categories were established obtained from the intertidal on 24 May and 16 July according to length; these 2 characteristics produced 1996 in Passamaquoddy Bay, New Brunswick, Canada the following classification: (45" 07' N, 67" 05' W). Placopecten magellanicus (size Short simple cilia (SSC): individual cilia <5 pm range 26 to 30 mm antero-posterior axis) were cap- Simple cilia (SC):individual cilia 5 to 15 pm tured via SCUBA from the same site in the subtidal on Long simple cilia (LSC):individual cilia >l5 pm 16 August 1996. Specimens of Spisula solidissima were Composite cilia (CC):group of closely adhering cilia obtained at low tide on 5 June 1996 in Shediac Bay, 10 to 15 pm New Brunswick (46' 13' 64" 29' W), as well as on 16 N, Long composite cilia (LCC):group of closely adher- June 1996 in Passamaquoddy Bay. ing cilia > 15 pm The adductor muscles of each individual of Mya are- naria, Spisula solidissin.~a,and Mytilus edulis were sec- It should be noted that these are lengths measured tioned in the field, and specimens were immediately directly on SEM micrographs, and do not take into fixed in a hypertonic solution of cold 2.5 % glutaralde- account fixation shrinkage (approx. 15 to 20%; H. Sil- hyde-sodium cacodylate buffer according to the proto- verman, Dept of Biological Sciences, Louisiana State col of Beninger et al. (1995).Specimens of Placopecten University, Baton Rouge, Louisiana, unpubl. obs.) and rnagellanicus were transported to the laboratory in the height of the microvillar layer (Beninger et al. insulated coolers containing well-oxygenated sea- 199713). water from the sampling site prior to treatment as None of the cilia observed presented artefactual above. anomalies such as paddle cilia (Beninger et al. 1995), On the sampling dates indicated above, all speci- indicating that fixation and SEM processing did not mens showed intense gametogenic activity, and it was alter surface features. often not possible to avoid small lesions to the mantle during dissection of such small specimens prior to fixa- tion. Mytilus edulis, Mya arenaria, and Spisula soli- Mytilus edulis (Fig. 1) dissima all present gonadic infiltration of the mantle when ripe, and gametes were thus unavoidably shed The mantle ciliation of Mytilus edulis presented uni- onto the mantle in some cases; this does not alter the formly dense SSC approx. 5 pm in length, with a dis- observations of the present study, but does explain the crete antero-posterior band of CC approx.
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