Cyclical contributions of the digestive epithelium to faecal pellet formation by the copepod Calanus helgolandicus

Faecal pellet formation within the gut of Stage V and adult females of the copepod Calanus helgolandicus Claus involves (1) cyclical processes of digestion and (2) the contribution of parts of the gut epithelium to the pellets. During an experimental regime in which dim lighting was restricted to day-time and feeding to night-time (17.00 to 09.00 hrs), the copepods responded with cyclical changes in both the quantity of pellets they produced and the fine structure of the contents. During the feeding period, the contents showed changes in the relative amounts of materials originating from disintegrated cells of the digestive epithelium and those derived directly from the ingested food. The vacuolar B-cells of the gut contribute to the content of the pellets and the distal, necrotic N-cells appear to be involved in forming the peritrophic membrane which encloses each pellet. Cells of the gut epithelium which are broken down during feeding are all replaced during the non-feeding period. Other individuals were taken directly from the sea and in these, also, the cells of the gut broke down during feeding and contributed to the faecal pellets. The supply of epithelial cells may limit the duration of the feeding period.     

Trophic diversity in amphipods within a temperate eelgrass ecosystem as determined by gut contents and C and N isotope analysis

A conjoint analysis of gut contents and stable C and N isotopes was applied to determine the main food sources and feeding habits of dominant amphipods in an eelgrass bed (Zostera marina) in Gwangyang Bay, Korea. Gut content observations demonstrated that, while Gammaropsis japonicus and Jassa slatteryi are herbivorous, feeding on epiphytes and detritus, Pontogeneia rostrata and Monocorophium acherusicum are omnivorous, feeding on mesozooplankton fragments and detritus. Stable isotope data confirmed that epiphytes, detritus, and mesozooplankton fragments were major food sources for amphipods in the eelgrass bed. Isotopic mixing model calculations clearly showed an interspecific difference in diet composition. A high isotopic dissimilarity between amphipod taxa demonstrated interspecific trophic diversity, reflecting their herbivorous (G. japonicus and J. slatteryi) and omnivorous (P. rostrata and M. acherusicum) feeding habits and confirmed the detrivorous feeding habits of caprellids. Such trophic diversity at interspecific level of the amphipod species indicates that they use different food resources within their microhabitats and play species-specific functional roles as mediators in trophic pathways from producers to higher-level consumers of the eelgrass ecosystem. Finally, our findings suggest that information on the species-specific trophic ecology of amphipods is needed to better understand their potential role in the trophic dynamics and carbon flow of seagrass bed ecosystems.     

Transport of brine shrimps via the digestive system of migratory waders: dispersal probabilities depend on diet and season

Waterbirds are known to disperse invertebrate propagules that survive gut passage, but there is very little information about how the probability of dispersal changes at different times of the annual cycle when birds move in different directions, or how it is affected by changes in diet. We studied internal transport of brine shrimp Artemia cysts by migratory waders in the Odiel saltworks in south-west Spain. Viable cysts of parthenogenetic Artemia were abundant in the faeces and regurgitated pellets of redshank Tringa totanus, pellets of spotted redshank T. erythropus, and faeces of black-tailed godwit Limosa limosa during spring and/or autumn migrations in 2001–2002, but were not recorded during winter. Godwits did not produce pellets, and spotted redshank faeces were not sampled. Significant correlations between the number of cysts in a pellet or faecal sample and the proportion of that sample constituted by Artemia adults suggested that most cysts were ingested while in the ovisacs of gravid females. The proportion of cysts destroyed during digestion increased when accompanied by harder food items or grit, and when fewer cysts were ingested. The median number of intact cysts was higher in redshank faeces than in their pellets, but cysts extracted from pellets were more likely to hatch. A higher proportion of redshank pellets contained Artemia cysts in spring than in autumn, but more redshank migrated through the area in autumn. Significantly fewer cysts were recorded in redshank pellets in winter than in spring or autumn. Our results confirm that there is potential for long-distance dispersal of Artemia cysts via waders during both northwards (spring) and southwards (autumn) migrations.     

Diet of four species of deep-sea isopods (Crustacea: Malacostraca: Peracarida) in the South Atlantic and the Southern Ocean

The food of four species of asellote isopods (Crustacea, Malacostraca), Haploniscus rostratus, Haploniscus unicornis, Acanthocope galatheae and Betamorpha fusiformis, was evaluated by analysis of their gut contents. The isopods were sampled at several stations on the abyssal plains of Guinea Basin, Angola Basin and Cape Basin (southeast Atlantic), the Weddell Sea abyssal plain and the Antarctic continental slope during the DIVA and ANDEEP expeditions in 2000, 2001 and 2005. While all species had mineral particles in their guts and mucus material was the most frequent food item, the remaining gut contents differed among species. Betamorpha fusiformis fed mostly on phytodetritus, especially in the Southern Ocean basins and ingested along with it whole calcareous foraminifers. Acanthocope galatheae showed some differences in gut contents between basins, but in the Guinea Basin, the contents were to a large extent stercomata, i.e., waste pellets of soft-walled foraminifers, i.e., the Komokiaceae. Indications were that the haploniscids were feeding on detritus and agglutinating foraminifers (stercomata). This indicates spatial differences in food availability for this diverse group of deep-sea isopods and the importance of poorly known foraminiferal groups, like the Komokiaceae, as a food source in the deep sea.     

Selectivity in feeding by the deposit-feeding bivalve Macoma nasuta

Macoma nasuta Conrad is primarily a deposit-feeding bivalve sucking the top millimeter of the sediment surface. Growth experiments show that surface sediment supports growth better than detritus falling from the water column. Gut clearance time is between 1 and 9 h (12°C). Fecal pellets are ejected in a regular rhythm. However, the total amount of feces per unit time shows considerable individual variation. Due to sorting in the mantle cavity, about 97% (dry weight) of the surface material is ejected again as pseudofeces. Selectivity by the bivalve is estimated by comparison of particle size and organic composition of sandy and muddy sediments and compared with feces produced by clams fed these sediments. Fecal pellets are in all cases richer in organic components than the sediment, indicating a high degree of selectivity. Ingestion and digestion of small animals (meiofauna) occur, but many of the ingested specimens survive. It is not possible to estimate the assimilation of organic matter by simple difference between the ingested sediment and the ejected feces. The difficulties in calculating energy budgets which arise from selective feeding and associated bacteria are discussed.     

Trace-metal detoxification in the ventral caeca of Orchestia gammarellus (Crustacea: Amphipoda)

The talitrid amphipod crustacean Orchestia gammarellus (Pallas) was collected from metal-contaminated (Dulas Bay, Gironde) and control (Millport) sites in the UK and France. Irrespective of site of origin, the amphipods showed the same physiological mechanism of trace-metal detoxification, involving the ventral caeca. Copper was always present in lysosomal residual bodies in the ventral caeca. Following laboratory exposure to zinc and cadmium, the lysosomes usually contained both copper and zinc but cadmium was not detectable. The lysosomal copper concentration is positively correlated to that of sulphur, while the concentration of lysosomal zinc is related to that of phosphorus. Results are interpreted in terms of the differential rates of turnover of metallothioneins chelating copper, zinc or cadmium. Received: 9 February 1999 / Accepted: 2 December 1999     

A note on the feeding of Calanus helgolandicus on detritus

Experiments on the feeding of Calanus helgolandicus females on detrital material were carried out. Natural detritus from the ocean was never ingested, whereas dead diatoms were readily eaten. Furthermore, it was shown that C. helgolandicus females ingested large amounts of fecal material produced by the same species in other vessels. These results indicate that the copepod C. helgolandicus feeds not only on living organisms, but also on dead particles.     

Digestive mechanics and gluttonous feeding in the feather starOligometra serripinna (Echinodermata: Crinoidea)

The movement and digestion of food in the gut ofOligometra serripinna (Carpenter) were studied at Lizard Island (14°3842S; 145°2710E) in the austral winter of 1986. Feather stars in the laboratory were fed a brief, small meal of brine shrimp nauplii and killed at increasing time intervals thereafter. Histological reconstructions showed that the ingested nauplii progressed along the digestive tract surprisingly quickly. Some nauplii were found in the mid and hind intestine in only 30 min, and all of the nauplii had reached the hind intestine and rectum in 1 h. Digestion of the nauplii had started at 1 h, and only a few fragments of naupliar exoskeleton remained in the hind intestine and rectum 5 h after the start of feeding. Videotape analysis showed that no fecal pellets were released during this experiment. In the natural environment ofO. serripinna, ingested particles may similarly be transported quickly to the hind part of the gut and digested there — when feather stars were fixed in the field, most of the gut contents were found in the hind intestine and rectum.O. serripinna, which efficiently rejects inert particles before they are ingested, usually defecates infrequently (probably not more than once over a span of many hours) and differs from some other feather stars that ingest numerous inert particles and defecate much more frequently. When specimens ofO. serripinna were fed continuously on brine shrimp nauplii,Artemia sp. (San Francisco strain), in the laboratory, the feather stars fed gluttonously, packing their guts with several hundred nauplii in 1 to 2 h. Thereafter, superfluous feeding began (i.e., further ingestions appeared to force undigested nauplii, some of them still living, out of the anus). These observations suggest thatO. serripinna usually feeds at relatively modest rates in its natural habitat, but can feed gluttonously to take advantage of infrequent patches of highly concentrated, nutritious particles (e.g. copepod swarms, migrating demersal zooplankton, and invertebrate gametes from mass spawnings). It is likely that such patches of nutritious particles are usually small enough to drift out of reach of the feather stars before gluttonous feeding proceeds to superfluous feeding. Opportunities for superfluous feeding in nature are probably very infrequent (e.g. ingestion of coral gametes and embryos after a mass spawning), and the feather stars evidently have no behavior that stops further ingestions after the gut becomes filled to capacity.     

Collembola gut passage shapes microbial communities in faecal pellets but not viability of dietary algal cells

Microarthropods are known as vectors for soil microorganisms, predominantly fungi. This laboratory study uses the widespread unicellular green algae Chlorella vulgaris as model to assess the role of Collembola in algal dispersal and to determine the effects of gut passage on propagation. Living algal cells were observed in 70 % of the faecal pellets of Folsomia candida, Heteromurus nitidus and Protaphorura fimata. Moreover, marker fatty acids for green algae, i.e. 16:2ω6,9 and 16:3ω3,6,9, were consistently detected in the pellets. Compared to the algal diet, the high content of methyl-branched total lipid fatty acid (TLFA) with hydroxyl substitution indicated microbial colonisation during gut passage. The TLFA profile of faeces revealed no species-specific differences but similar changes in microbial communities over the duration of feeding, indicating comparable indigenous bacteria and colonisation mechanisms during gut passage. In sum, faecal pellets of soil microarthropods such as Collembola can act as a vector for both dietary algae and specific gut-associated microorganisms, with the latter likely involved in resource degradation inside and outside the gut habitat.     

In-situ studies on deep-sea amphipods and their intestinal microflora

Amphipods, trapped at depths of 1 410 to 5 330 m and incubated in situ in the presence of a radiolabeled protein as a food source, were fractionated to measure the distribution of label in the major biochemical constituents: low molecular pools, ethanol and base soluble proteins, lipids, polysaccharides and nucleic acids. The results suggest lipid energy storage and enhanced microbial growth within the amphipod guts as compared to growth on the uningested food material. The merits and limitations of this general approach are critically evaluated.     

Multifarious activities of gut epithelium in an appendicularian (Oikopleura dioica: Tunicata)

The functions of the various gut regions of Oikopleura dioica (oesophagus, left and right gastric lobes, vertical intestine, mid-intestine and rectum) were investigated by means of histochemical, histoenzymatic and immunohistochemical techniques at light and electron microscopes. Ciliary food progression is evidenced by the presence of ATPases on cilia, along the entire gut, with the exception of the cardiac valve, a passive device controlling food direction. Absorptive processes (alkaline phosphatase), active transport (ATPases) and nitrogen excretion (D-amino acid oxidase) occur along the entire gut, in both ciliated microvillar and globular cells. The latter, typical of the left gastric lobe and rectum, are also involved in endocytotic processes (exogenous peroxidase as tracer) and intracellular digestion (!-amylase, aminopeptidase M, acid phosphatase, 5'-nucleotidase, non-specific esterase). The giant cells of the gastric band participate in extracellular digestion; they contain secretory granules positive to various hydrolytic enzymes, the activity of which is also recognisable in faecal pellets inside the intestinal lumen. Lipid storage occurs mainly in the right gastric lobe and vertical intestine, whereas protein storage takes place in the rectal granular cells. Epithelial transport and possible osmoregulation occur along the entire gut, especially at the level of diffuse baso-lateral interdigitations, which increase the plasmalemma surface enormously, are often associated with mitochondria and possess numerous ATPase pumps. Data extend previous histological observations and hypotheses on the physiological role of the various gut regions. The remarkable and specific location of enzymatic activities and nutrient storage are in agreement with the high capacity of O. dioica to process a great quantity of food very rapidly and efficiently.     

Zooplankton feeding ecology: contents of fecal pellets of the copepods Temora turbinata and T. stylifera from continental shelf and slope waters near the mouth of the Mississippi River

In-situ feeding habits of the copepods Temora turbinata and T. stylifera were investigated by scanning electron microscope examination of fecal pellets, the contents of which reflected copepod gut contents upon capture. Pellet contents were compared with assemblages of available phytoplankton in the water column at the times of zooplankton sampling. Samples were collected in continental shelf and slope waters of the Gulf of Mexico near the mouth of the Mississippi River. Both species ingested a wide size range and taxonomic array of phytoplankters, and to a lesser extent, other crustaceans. Fecal pellets contained primarily the remains of the phytoplankters that were most abundant in the water at times of collection. There was considerable overlap in the food items ingested by adult females of both copepod species, or two stages of T. turbinata copepodites. Thus, T. turbinata and T. stylifera are omnivores, but primarily opportunistic herbivores.     

Zooplankton grazing on the coccolithophore Emiliania huxleyi and its role in inorganic carbon flux

Grazing and faecal pellet production by the copepods Calanus helgolandicus and Pseudocalanus elongatus, feeding on the coccolithophore Emiliania huxleyi, were measured under defined laboratory conditions, together with the chemical characteristics and sinking rates of the faecal pellets produced. Ingestion rates of both copepods were equivalent at comparable cell concentrations, the relationship between ingestion rate (I, cells copepod^-1 h^-1) and food concentration (C, cells ml^-1), being I=0.558C for both species. P. elongatus produced a larger number of smaller faecal pellets than C. helgolandicus, but egested a larger volume of material per individual. Only between 27 and 50% of the ingested coccolith calcite was egested in the faecal pellets, and it is possible that acid digestion in the copepod gut is responsible for these considerable losses. Average sinking rates of faecal pellets containing E. huxleyi coccoliths, produced by both species, were >100 m d^-1. The implications of the quantitative laboratory estimates for the vertical flux of inorganic carbon are considered using recently studied shelf-break and oceanic E. huxleyi blooms in the N. E. Atlantic as examples.     

Particle size-selection of two deposit feeders: the amphipod Corophium volutator and the prosobranch Hydrobia ulvae

The feeding biology of the deposit-feeding amphipod Corophium volutator is compared to that of the coexisting, deposit-feeding prosobranch Hydrobia ulvae. Regarding ingestion of particles, both forms show size selection which alone can explain their coexistence. Particle size-selection also explains some qualitative differences in the composition of the food of the two forms; thus, diatoms play a relatively larger role in the diet of H. ulvae than in the diet of c. volutator, whereas bacteria are probably relatively more important for the latter. Results of experiments with feeding of C-14 labelled microorganisms are in accordance with the findings on particle size-distribution of the gut contents, and show that (1) C. volutator can only utilize bacteria adsorbed to particles within the size range 4 to 63 (this is why the presence of clay and silt particles in the sediment are necessary for efficient feeding of this amphipod); (2) C. volutator can utilize bacteria suspended in the water pumped through its burrow for respiration if silt and clay particles are present in the sediment. (3) H. ulvae can utilize large particles, and also browses on surfaces, and some evidence is brought forward that it also utilizes mucus for trapping microorganisms. The coexistence of deposit-feeding animals is discussed. It is concluded that the number of coexisting, closely related species is usually small, and that their resource partitioning is probably mainly based on particle-size selectivity. In the case of unrelated forms (e.g. H. ulvae and C. volutator, a number of behavioural, physiological and morphological differences, and also the widespread ability of deposit feeders to utilize alternative feeding mechanisms may also lead to resource partitioning. Thus, there are often several niche dimensions related to feeding allowing a certain diversity of coexisting deposit feeders.     

Diet of calyptopes of the euphausiidEuphausia pacifica in the Yellow Sea

Foregut contents of calyptopes (the first feeding stage) ofEuphausia pacifica Hansen, collected from the Yellow Sea in June 1989, were examined using scanning electron microscopy with the dry-fracturing method. There was no clear evidence of phytoplankton ingestion by calyptopes. The foregut contents consisted entirely of amorphous organic detritus, crustacean remains and inorganic particles. The inorganic particles adhered to amorphous organic detritus, and bacterial populations were found on peritrophic membranes of fecal pellets which enveloped crustacean remains. These materials seemed to have originated from aggregates of organic and inorganic detritus. It is quite possible that the detrital aggregates are utilized extensively as food by calyptopes ofE. pacifica in the Yellow Sea.     

Variations in the content of trypsin and trysinogen in larval herring (Clupea harengus) digesting copepod nauplii

Trypsin and its proform trypsinogen were quantified by radioimmunoassay in herring (Clupea harengus L.) larvae subjected to different prey densities. During the first weeks of larval life, the enzyme content fluctuated in a threephased pattern. Yolk resorption (Phase 1) was characterized by an increase in enzyme. During the first few days after yolk resorption (Phase 2), there was a sharp decline in enzyme. Older larvae (Phase 3) exhibited a second period of intensive enzyme synthesis. Amounts of trypsin in intestines of feeding larvae were analysed. At first feeding, a basal level of gut enzyme of approximately 30ng was recorded, and the amount of additional enzyme secreted from the pancreatic tissue into the intestine appeared to be dependent upon the numbers of prey items ingested. The enzyme-substrate ratio in the intestine was approximately 1 to 4. Prey availability affected amount of trypsinogen. Larvae experiencing a high prey density had an approximately two-fold higher specific enzyme content in Phase 2 compared to larvae exposed to a low prey density. A proposed nutritional strategy for first feeding herring larvae is discussed.     

On the feeding of Branchiostoma senegalense (Acrania: Branchiostomidae)

The feeding biology of Branchiostoma senegalense Webb from the North-West African shelf region off Mauritania was investigated. The hindgut contained almost exclusively seston components, ranging in size from less than 1 m (bacteria size) to 300 m. Numerous chloroplasts of ingested phytoplankton appeared to be undigested. Dunaliella salina was still alive when leaving the anus after 1 to 2 h. Detritus formed the greater part of the gut contents. The authors conclude that the lancelets feed mainly on detritus and thus are indiscriminate suspension feeders.     

Herbivory and detritivory among gammaridean amphipods from a Florida seagrass community

The gammaridean amphipods Cymadusa compta (Smith), Gammarus mucronatus Say, Melita nitida Smith and Grandidierella bonnieroides Stephensen from a seagrass community in the Indian River estuary of Florida (USA) fed variously upon large drift algae, small algae epiphytic on seagrasses and seagrass leaf debris and detritus. Consumption was measured in the laboratory using an index (CI) equivalent to mg ingested mg^-1 amphipod day^-1. Observations revealed that the amphipods fed by macrophagy, an attack upon large algae and seagrass debris, and by microphagy, small particle detritus feeding and scraping of plant surfaces for diatoms and other epiphytic algae. C. compta was a macrophagous feeder with a generalized diet of algae and seagrass debris, preferring epiphytic algae and drift algae at mean rates of 1.10 and 0.87 CI, respectively. Gammarus mucronatus fed upon epiphytes and seagrass debris equally at mean rates of 0.90 and 0.97 CI, respectively. The diet of M. nitida condisted primarily of epiphytes, consumed at an average rate of 1.05 CI. Grandidierella bonnieroides fed in a specialized microphagous manner, grooming plant surfaces for small particle detritus and diatoms at an approximate CI rate of 1.45. Assimilation of plants ingested, as reflected by carbon-14 uptake, varied similarly among the 4 amphipods. Epiphytic algae appeared to be most useful as food, providing means of 41 to 75% carbon-14 uptake as ingesta. Drift algae and seagrass debris were of less value, with means varying between 11 and 24 % of carbon-14 uptake by the amphipods. The data show a pattern of feeding which resembles resource partitioning of food both by size and kind. Other evidence, however, including population limitation by predators and an apparent overabundance of food, indicate that resource partitioning as seen may be an artifact, and one which has no co-evolutionary basis among the present species.Contribution No. 102 of Harbor Branch Foundation, Inc.     

Sedimentation of organic detritus in Lochs Etive and Creran,Argyll, Scotland

The rates of sedimentation of organic detritus were measured at 3 stations in two Scottish sea lochs, Loch Etive and Loch Creran, using sedimentation jars exposed at various depths. Details are given of the seasonal and depth distribution of sedimenting material, and its composition for a 1-year period. Differences in the pattern of sedimenting material collected at different depths and in the seasonal patterns of sedimentation at the different stations suggested that, in each case there were differences in the relative importance of detritus from various sources. At all stations, phytoplankton production made a relatively small contribution to the total detritus collected, either directly as dead cells, or indirectly as the faeces of zooplankton organisms. Near the head of Loch Etive there were contributions by filamentous algae and Enteromorpha sp., but a major source of detritus was terrestrial debris, mainly carried into the loch in the waters of the River Etive. In the lower basin of Loch Etive, terrestrial detritus also contributed to the total sedimenting near the surface, but at greater depths much of the material collected in the sedimentation jars probably resulted from short-term resuspension and re-deposition of bottom material, reflecting a net transport of fine sediment from the shallower to the deeper areas of the loch. Secondarily resuspended material was also a major source of material collected in the jars exposed in Loch Creran.     

Feeding biology and carbon budget of the sediment-burrowing heart urchin Brissopsis lyrifera (Echinoidea: Spatangoida)

This study of the burrowing heart urchin Brissopsis lyrifera includes measurements on feeding and food selection, ingestion rate, absorption efficiency, ventilation and respiration. B. lyrifera regulated feeding depth, ingestion rate and absorption efficiency in relation to food source. When food was added to the top layer of sediment, B. lyrifera burrowed closer to the surface and ingested mainly enriched surface material, whereas it burrowed deeper and ingested deep-seated sediment in the controls. In non-enriched sediment, the feeding rate was 0.04 g sediment DW h^-1 ind.^-1, and, in macro- and microalga-enriched sediment the feeding rate was 0.06 and 0.08 g sediment DW h^-1 ind.^-1, respectively. Absorption efficiency of TOC was about 43% in non-enriched sediment and in microalga-enriched sediment, but was significantly lower (34%) in macroalga-enriched sediment. Absorption efficiency of N varied between 48% and 55%, and was independent of food source. B. lyrifera feed selectively, enriching the gut TOC content about 2-fold and N content about 2.5-fold. The C/N ratio was therefore lower within the gut compared to the surrounding sediment, while the faecal C/N ratio was almost equal to the surrounding sediment. The faeces were, however, slightly richer in TOC and N compared to the surrounding sediment. For 3-5 cm long B. lyrifera, water current rate varied between 4 and 24 ml water h^-1, with a mean of 11 ml h^-1. Mean respiration rate was 205 µl O₂ h^-1 ind.^-1. The water current rate was not sufficient for B. lyrifera to sustain itself by filter feeding only. However, organic-rich particles from the surface are suggested to be an important contribution to the diet. A carbon budget was calculated for B. lyrifera from measured values of consumption, absorption efficiency and respiration, in order to estimate annual production of B. lyrifera. Compared to literature values, growth was overestimated about tenfold in the budget. A large proportion of the absorbed carbon was suggested to leave the animal as dissolved carbon, through mucus production or through anaerobic pathways, either by the heart urchin or by micro-organisms in the gut.