Abstract
Although the clearance rates of planktotrophic bivalve larvae have been widely reported, post-oral particle processing is less well understood. Using a series of exposures to differently colored fluorescent polystyrene microbeads, we quantify several post-oral process in the larval gut, including gut fullness, gut passage time, and degree of mixing by modeling larval guts as a continuously stirred tank reactor (CSTR), plug flow reactor (PFR) or combinations of the two in series. We also varied several experimental conditions to understand how these affected estimates of gut kinematic parameters. We found the larval guts of M. galloprovincialis aged 2 and 7 days post-fertilization, had gut exchange time >1 h and were best described either as a CSTR or CSTR in series with a PFR. Mixing stomach contents likely aids post-oral particle selection, physical breakdown of ingested material, and accelerates the diffusion of digestive enzymes in the gut volume. Reactor models also provided estimates of ingestion rates, which were compared to those obtained by other authors who measured rates of bead accumulation. In accordance with reactor theory, ingestion rates were negatively and nonlinearly correlated with gut passage times and positively related to maximal gut fullness. Collectively, these studies provide new insight on the digestive strategy of planktotrophic bivalve larvae.
Similar content being viewed by others
References
Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second international symposium on information theory. Akademiai Kiado, Budepest, pp 267–281
Almeda R, Messmer AM, Sampedro N, Gosselin LA (2011) Feeding rates and abundance of marine invertebrate planktonic larvae under harmful algal bloom conditions off Vancouver Island. Harmful Algae 10:194–206. doi:10.1016/j.hal.2010.09.007
Armengol X, Boronat L, Camacho A, Wurtsbaugh WA (2001) Grazing by a dominant rotifer Conochilus unicornis Rousselet in a mountain lake: in situ measurements with synthetic microspheres. Hydrobiologia 446/447:107–114
Baldwin BS (1995) Selective particle ingestion by oyster larvae (Crassostrea virginica) feeding on natural seston and cultured algae. Mar Biol 123:95–107
Baldwin BS, Newell RIE (1991) Omnivorous feeding by planktotrophic larvae of the eastern oyster Crassostrea virginica. Mar Ecol Prog Ser 78:285–301
Baldwin BS, Newell RIE (1995a) Feeding rate responses of oyster larvae (Crassostrea virginica) to seston quantity and composition. J Exp Mar Biol Ecol 189:77–91
Baldwin BS, Newell RIE (1995b) Relative importance of different size food particles in the natural diet of oyster larvae Crassostrea virginica. Mar Ecol Prog Ser 120:135–145
Bayne BL (1965) Growth and the delay of metamorphosis of the larvae of Mytilus edulis (L.). Ophelia 2:1–47
Bayne BL (1972) Some effects of stress in the adult on the larval development Mytilus edulis. Nature 237:459
Bertram DF, Strathmann RR (1998) Effects of maternal and larval nutrition on growth and form of planktotrophic larvae. Ecology 79:315–327. doi:10.2307/176885
Brillant MGS, MacDonald BA (2000) Postingestive selection in the sea scallop, Placopecten magellanicus (Gmelin): the role of particle size and density. J Exp Mar Biol Ecol 253:211–227
Brillant MGS, MacDonald BA (2002) Postingestive selection in the sea scallop (Placopecten magellanicus) on the basis of chemical properties of particles. Mar Biol 141:457–465
Brillant MGS, MacDonald BA (2003) Postingestive sorting of living and heat-killed Chlorella within the sea scallop, Placopecten magellanicus (Gmelin). J Exp Mar Biol Ecol 290:81–91
Chen M, Liu H, Song S, Sun J (2015) Size-fractionated mesozooplankton biomass and grazing impact on phytoplankton in northern South China Sea during four seasons. Deep Sea Res Part II Top Stud Oceanogr. doi:10.1016/j.dsr2.2015.02.026
Cranford PJ, Emerson CW, Hargrave BT, Milligan TG (1998) In situ feeding and absorption responses of sea scallops Placopecten magellanicus (Gmelin) to storm-induced changes in the quantity and composition of the seston. J Exp Mar Biol Ecol 219:45–70
Croxton AN, Wikfors GH, Schulterbrandt-Gragg RD (2012) Immunomodulation in eastern oysters, Crassostrea virginica, exposed to a PAH-contaminated, microphytobenthic diatom. Aquat Toxicol 118–119:27–36. doi:10.1016/j.aquatox.2012.02.023
Dadd RH (1971) Effects of size and concentration of particles on rates of ingestion of latex particulates by mosquito larvae. Ann Entomol Soc Am 64:687–692
Dagg MJ, Walser WE Jr (1987) Ingestion, gut passage, and egestion by the copepod Neocalanus plumchrus in the laboratory and in the subarctic Pacific Ocean. Limnol Oceanogr 32:178–188
Dam HG, Peterson WT (1988) The effect of temperature on the gut clearance rate constant of planktonic copepods. J Exp Mar Biol Ecol 123:1–14
Defossez JM, Hawkins AJS (1997) Selective feeding in shellfish: size-dependent rejection of large particles within pseudofaeces from Mytilus edulis, Ruditapes philippinarum and Tapes decussatus. Mar Biol 129:139–147
DeMott WR (1988) Discrimination between algae and artificial particles by freshwater and marine copepods. Limnol Oceanogr 33:397–408
Gerdes D (1983) The Pacific oyster Crassostrea gigas: part I. Feeding behavior of larvae and adults. Aquaculture 31:195–219. doi:10.1016/0044-8486(83)90313-7
Hart MW (1991) Particle captures and the method of suspension feeding by echinoderm larvae. Biol Bull 180:12–27
Hawkins AJS, Bayne BL, Mantoura RFC et al (1986) Chlorophyll degradation and absorption throughout the digestive system of the blue mussel Mytilus edulis L. J Exp Mar Biol Ecol 96:213–223. doi:10.1016/0022-0981(86)90204-2
Hawkins AJS, Navarro E, Iglesias JIP (1990) Comparative allometries of gut-passage time, gut content and metabolic faecal loss in Mytilus edulis and Cerastoderma edule. Mar Biol 105:197–204. doi:10.1007/BF01344287
Ibarrola I, Larretxea X, Iglesias JIP, Urrutia MB, Navarro E (1998) Seasonal variation of digestive enzyme activities in the digestive gland and the crystalline style of the common cockle Cerastoderma edule. Comp Biochem Physiol A 121:25–34. doi:10.1016/S1095-6433(98)10097-1
Jeong HJ, Song JY, Lee CH, Kim ST (2004) Feeding by larvae of the mussel Mytilus galloprovincialis on red-tide dinoflagellates. J Shellfish Res 23:185–196
Jumars PA (2000) Animal guts as ideal chemical reactors: maximizing absorption rates. Am Nat 155:527–543. doi:10.1086/303333
Jumars PA, Penry DL (1989) Digestion theory applied to deposit feeding. Ecology of marine deposit feeders. Springer, New York, pp 114–128
Jumars PA, Penry DL, Baross JA et al (1989) Closing the microbial loop: dissolved carbon pathway to heterotrophic bacteria from incomplete ingestion, digestion and absorption in animals. Deep Sea Res Part Oceanogr Res Pap 36:483–495
Kaposi KL, Mos B, Kelaher BP, Dworjanyn SA (2014) Ingestion of microplastic has limited impact on a marine larva. Environ Sci Technol 48:1638–1645. doi:10.1021/es404295e
Karasov WH, Martínez del Rio C, Caviedes-Vidal E (2011) Ecological physiology of diet and digestive systems. Annu Rev Physiol 73:69–93. doi:10.1146/annurev-physiol-012110-142152
Kiørboe T, Møhlenberg F, Nicolajsen H (1982) Ingestion rate and gut clearance in the planktonic copepod Centropages hamatus (Lilljeborg) in relation to food concentration and temperature. Ophelia 21:181–194
López-Urrutia Á, Irigoien X, Acuña JL, Harris R (2003) In situ feeding physiology and grazing impact of the appendicularian community in temperate waters. Mar Ecol Prog Ser 252:125–141
Mackintosh NA (1925) Memoirs: the crystalline style in gastropods. Q J Microsc Sci 2:317–342
Mayzaud P, Tirelli V, Bernard JM, Roche-Mayzaud O (1998) The influence of food quality on the nutritional acclimation of the copepod Acartia clausi. J Mar Syst 15:483–493
Milke LM, Ward JE (2003) Influence of diet on pre-ingestive particle processing in bivalves: II. Residence time in the pallial cavity and handling time on the labial palps. J Exp Mar Biol Ecol 293:151–172. doi:10.1016/S0022-0981(03)00217-X
Millar RH (1955) Notes on the mechanism of food movement in the gut of the larval oyster, Ostrea edulis. Q J Microsc Sci 3:539–544
Morton JE (1952) The role of the crystalline style. J Molluscan Stud 29:85–92
Nelson PR, Wludyka PS, Copeland KA (2005) The analysis of means: a graphical method for comparing means, rates, and proportions. Series on statistics and applied probability. SIAM, Philadelphia, PA
Newell RIE, Langdon CJ (1996) Mechanisms and physiology of larval and adult feeding. The eastern oyster. Maryland Seagrant, Maryland
Pace ML, Bailiff MD (1987) Evaluation of a fluorescent microsphere technique for measuring grazing rates of phagotrophic microorganisms. Mar Ecol Prog Ser 40:185–193
Paffenhöfer GA, Van Sant KB (1985) The feeding response of a marine planktonic copepod to quantity and quality of particles. Mar Ecol Prog Ser 27:55–65
Penry DL (2000) Digestive kinematics of suspension-feeding bivalves: modeling and measuring particle-processing in the gut of Potamocorbula amurensis. Mar Ecol Prog Ser 197:181–192
Penry DL, Frost BW (1990) Re-evaluation of the gut-fullness (gut fluorescence) method for inferring ingestion rates of suspension-feeding copepods. Limnol Oceanogr 35:1207–1214
Penry DL, Frost BW (1991) Chlorophyll a degradation by Calanus pacificus: dependence on ingestion rate and digestive acclimation to food resources. Limnol Oceanogr 36:147–158
Penry DL, Jumars PA (1986) Chemical reactor analysis and optimal digestion. Bioscience 36:310–315. doi:10.2307/1310235
Penry DL, Jumars PA (1987) Modeling animal guts as chemical reactors. Am Nat 129:69–96. doi:10.2307/2461965
Phibbs FD (1969) Laboratory hatching and rearing of pacific coast clams and oysters. US Department of Interior; Fish and Wildlife Service
Reinfelder JR, Fisher NS (1994) The assimilation of elements ingested by marine planktonic bivalve larvae. Limnol Oceanogr 39:12–20
Rico-Villa B, Pouvreau S, Robert R (2009) Influence of food density and temperature on ingestion, growth and settlement of Pacific oyster larvae, Crassostrea gigas. Aquaculture 287:395–401
Riisgard HU, Randløv A, Kristensen PS (1980) Rates of water processing, oxygen consumption and efficiency of particle retention in veligers and young post-metamorphic Mytilus edulis. Ophelia 19:37–46
Seebaugh DR, L’Amoreaux WJ, Wallace WG (2011) Digestive toxicity in grass shrimp collected along an impact gradient. Aquat Toxicol 105:609–617. doi:10.1016/j.aquatox.2011.08.015
Solow AR, Gallager SM (1990) Analysis of capture efficiency in suspension feeding: application of nonparametric binary regression. Mar Biol 107:341–344. doi:10.1007/BF01319834
Sprung M (1984) Physiological energetics of mussel larvae (Mytilus edulis). II. Food uptake. Mar Ecol Prog Ser 17:295–305
Sutherland KR, Madin LP, Stocker R (2010) Filtration of submicrometer particles by pelagic tunicates. Proc Natl Acad Sci 107:15129–15134. doi:10.1073/pnas.1003599107
Thompson PA, Montagnes DJ, Shaw BA, Harrison PJ (1994) The influence of three algal filtrates on the grazing rate of larval oysters (Crassostrea gigas), determined by fluorescent microspheres. Aquaculture 119:237–247
Tirelli V, Mayzaud P (2005) Relationship between functional response and gut transit time in the calanoid copepod Acartia clausi: role of food quantity and quality. J Plankton Res 27:557–568. doi:10.1093/plankt/fbi031
Wang R, Conover RJ (1986) Dynamics of gut pigment in the copepod Temora longicornis and the determination of in situ grazing rates. Limnol Oceanogr 31:867–877
Wang W-X, Fisher NS (1996) Assimilation of trace elements and carbon by the mussel Mytilus edulis: effects of food composition. Limnol Oceanogr 41:197–207
Wang W-X, Fisher NS (1999) Assimilation efficiencies of chemical contaminants in aquatic invertebrates: a synthesis. Environ Toxicol Chem 18:2034–2045
Ward JE, Kach DJ (2009) Marine aggregates facilitate ingestion of nanoparticles by suspension-feeding bivalves. Mar Environ Res 68:137–142
Ward JE, Shumway SE (2004) Separating the grain from the chaff: particle selection in suspension- and deposit-feeding bivalves. J Exp Mar Biol Ecol 300:83–130. doi:10.1016/j.jembe.2004.03.002
Widdows J (1991) Physiological ecology of mussel larvae. Aquaculture 94:147–163
Widdows J, Newell R, Mann R (1989) Effects of hypoxia and anoxia on survival, energy metabolism, and feeding of oyster larvae (Crassostrea virginica, Gmelin). Biol Bull 177:154–166
Acknowledgments
The authors wish to thank Thaddaeus Buser for helping to count beads and Javan Bailey and Greg Hutchinson of the Molluscan Broodstock Program, Oregon State University, for supplying technical and infrastructural support during studies. RIE Newell, R Mann, and PA Jumars provided insightful comments that greatly improved the manuscript. Funding of this project was through an award from the Markham Scholarship Fund, Hatfield Marine Science Center, and National Science Foundation Grant OCE CRI-OA 1041267. The authors also gratefully acknowledge travel support funded by a research grant from Norwich University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Disclosure statement
The authors are unaware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this manuscript.
Additional information
Responsible Editor: X. Irigoyen.
Reviewed by P. A. Jumars and R. Mann.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gray, M.W., Kramer, S. & Langdon, C. Particle processing and gut kinematics of planktotrophic bivalve larvae. Mar Biol 162, 2187–2201 (2015). https://doi.org/10.1007/s00227-015-2746-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-015-2746-1