This work characterized the digestive environment (pH, redox, protease activity, dissolved organic carbon [DOC] and surfactancy) in Nereis succinea, and attempted to identify the dominant mechanisms affecting digestion and absorption of organic matter (OM) and hydrophobic organic contaminants (HOC). Gut pH, redox conditions and protease activity in small individuals were measured optically using fluorescent or colorimetric substrates. Gut pH of juvenile N. succinea and three other polychaete species (Streblospio benedicti, Polydora cornuta, Pygospio sp.) ranged between pH 5.5-7.5, falling within the range of previously published gut pH values. Gut redox conditions of N. succinea, estimated using tetrazolium salts, were more reducing in larger worms, suggestive of greater gut microbial activity. Gut protease activity of N. succinea, quantified by monitoring hydrolysis of fluorescently-tagged casein over time, was pronounced and appeared to encounter substrate limitation within a few minutes after ingestion. The in vivo methods described may be expandable to a broader range of ecophysiological questions concerned with the digestive capabilities of animals and how these may be influenced by ontogenetic and environmental factors.
Gut passage time (GPT) in N. succinea is approximately five to ten times shorter in juveniles than in adults. Since shorter GPT is likely to diminish the efficiency of intestinal digestion and solubilization, one would expect juvenile worms to have significantly diminished absorption efficiencies compared to adults. To test this hypothesis, I compared absorption efficiencies (AE) for radioactively labeled phytoplankton, bulk sediment OM, and three sediment-bound HOCs (tetrachlorobiphenyl [TCBP], hexachlorobenzene [HCB] and benzo(a)pyrene [BaP]) among individuals of 10-100 mm body length. To examine whether small worms might counteract shorter gut passage time (GPT) by possessing more aggressive gut conditions, gut pH and gut fluid surfactancy (contact angle) were measured as well. AEs, measured in pulse-chase experiments, were 55-95 % for fresh phytoplankton, 5-18% for OM, and 55-95 % for TCBP, HCB and BaP. AEs were generally higher in larger worms and linear and exponential regressions of AE onto body size explained more than 60% of the AE variance in any treatment. Gut fluid pH ranged between pH 5.8-7.7 and was slightly higher in larger individuals. Contact angles were greatly diminished relative to seawater in all worms, indicative of strong surfactancy, with greatest differences observed in larger individuals. Body size explained <20% of gut pH and surfactancy variability.
To characterize the mechanism of contaminant uptake, biomimetic desorption experiments were conducted with gut fluids extracted from N. succinea and Pectinaria gouldii. In vitro solubilization of sediment-bound HOCs by gut fluids was significantly higher than by seawater and was an excellent predictor of AE. N. succinea gut fluid desorbed 72-79 % TCBP and HCB in vitro (compared to 73 % AE for both HOCs) while P. gouldii desorbed HCB with 37 % efficiency (AE 37%). Solubilization power of gut fluids was similar to mild (0.25-1.0% by weight) solutions of a synthetic surfactant (sodium dodecyl sulfate). Higher desorption and absorption efficiencies of N. succinea correlated with greater gut fluid surfactancy, higher apparent micelle concentration (determined by drop contact angle) and higher gut fluid DOC compared to P. gouldii. Gut fluids from both worm species desorbed more than two thirds of bioavailable TCBP and HCB within the first minute, suggesting that digestive desorption occurs rapidly, and that gut residence time has only minor influence on the degree of desorption or absorption of sediment-bound HOCs. The findings suggests that digestive surfactants (and perhaps other gut fluid DOC) control the digestive bioavailability of sediment-bound HOCs and compete with sediment OM for HOC sorption. Implications for models of food and contaminant uptake are discussed.