Article

Peritrophic membrane and faecal pellets of Gammarus lacustris limnaeus Smith

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Abstract

Gammarus lacustris limnaeus Smith was fed decomposed autumnshed leaves of maple (Acer saccharum Marsh.) and poplar (Populus tremuloides Michx.). Faecal pellets were collected at various time intervals after egestion and examined under a light and a scanning electron microscope. Nearly all the faecal pellets collected up to a period of about 7 h after egestion possessed a thin, tightly-fitting peritrophic membrane while those that had been outside the gut of the animal for a longer time lacked a peritrophic membrane. Presumably, after egestion faecal pellets swell because of absorption of water leading to eventual rupture and loss of the membrane. The surface of newly extruded pellets is devoid of microbes and microbes seem to play a very insignificant role in the loss of peritrophic membrane from the pellets.

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... Interestingly, we observed large accumulations of PET particles in the cephalic, thoracic or pleonic section of the gut in five out of 60 individuals (Fig. S2) comparable in shape to typical fecal pellets of Gammarus (Lautenschlager et al., 1978). However, this observation was unrelated to age or exposure concentration. ...
... Another potential explanation for the null effects of MP observed in this study is related to the crustacean gut morphology. As detritivorous shredders, amphipods are evolutionary adapted to process non-digestible food components: The chitinous peritrophic membrane is secreted in the midgut where it encloses the food to protect the digestive system against particle-induced injuries (Forster, 1953;Lautenschlager et al., 1978). In the digestive tract of G. pulex PET MP particles are densely packaged (Fig. S2) implying that they are covered in the peritrophic membrane and processed like other non-digestible particles. ...
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Over the past decade, microscopic plastic debris, known as microplastics, emerged as a contaminant of concern in marine and freshwater ecosystems. Although regularly detected in aquatic environments, the toxicity of those synthetic particles is not well understood. To address this, we investigated whether the exposure to microplastics adversely affects the amphipod Gammarus pulex, a key freshwater invertebrate. Juvenile (6-9 mm) and adult (12-17 mm) individuals were exposed to irregular, fluorescent polyethylene terephthalate fragments (PET, 10-150 μm; 0.8-4,000 particles mL-1) for 24 h. Results show that body burden after 24 h depends on the dose and age of G. pulex with juveniles ingesting more microplastics than adults. After chronic exposure over 48 d, microplastics did not significantly affect survival, development (molting), metabolism (glycogen, lipid storage) and feeding activity of G. pulex. This demonstrates that even high concentrations of PET particles did not negatively interfere with the analyzed endpoints. These results contradict previous research on marine crustaceans. Differences may result from variations in the exposure regimes (e.g., duration, particle concentrations), plastic characteristics (e.g., type, size, shape, additives) as well as the species-specific morphological, physiological and behavioral traits. As a detritivorous shredder G. pulex is adapted to feed on non-digestible materials and might, therefore, be less sensitive towards exposure to synthetic particles. Accordingly, we argue that the autecology needs to be taken into account and that research should focus on identifying traits that render species susceptible to microplastic exposure.
... In addition, significant differences were determined for juveniles (p < 0.01) and adults (p < 0.01) between the test groups 40 p mL À1 and 4,000 p mL À1. Interestingly, we observed large accumulations of PET particles in the cephalic, thoracic or pleonic section of the gut in five out of 60 individuals ( Fig. S2) comparable in shape to typical fecal pellets of Gammarus ( Lautenschlager et al., 1978). However, this observation was unrelated to age or exposure concentration. ...
... Another potential explanation for the null effects of MP observed in this study is related to the crustacean gut morphology. As detritivorous shredders, amphipods are evolutionary adapted to process non-digestible food components: The chitinous peritrophic membrane is secreted in the midgut where it encloses the food to protect the digestive system against particle-induced injuries (Forster , 1953;Lautenschlager et al., 1978). In the digestive tract of G. pulex PET MP particles are densely packaged ( Fig. S2) implying that they are covered in the peritrophic membrane and processed like other non-digestible particles. ...
Chapter
Endocrine-disrupting chemicals (EDCs) are man-made compounds interfering with hormone signaling. Omnipresent in the environment, they can cause adverse effects in a wide range of wildlife. Accordingly, Endocrine Disruption is one focal area of ecotoxicology. Because EDCs induce complex response patterns in vivo via a wide range of mechanisms of action, in vitro techniques have been developed to reduce and understand endocrine toxicity. In this review we revisit the evidence for endocrine disruption in diverse species and the underlying molecular mechanisms. Based on this, we examine the battery of in vitro bioassays currently in use in ecotoxicological research and discuss the following key questions. Why do we use in vitro techniques? What endpoints are we looking at? Which applications are we using in vitro bioassays for? How can we put in vitro data into a broader context? And finally, what is the practical relevance of in vitro data? In critically examining these questions, we review the current state-of-the-art of in vitro (eco)toxicology, highlight important limitations and challenges, and discuss emerging trends and future research needs.
... Planktonic crustaceans have a peritrophic membrane, which is a thin tubular sheet secreted in the midgut as a means of preventing abrasion of the gut wall. This acts as a distinct wrapper for feces (Lautenschlager et al. 1978, Lampitt et al. 1990, Gonzalez 1992. The feces of vertebrates and most invertebrates do not have such an external covering and are bound together with mucus, often remaining as discrete entities for days or weeks. ...
... Skin friction drag and hydrodynamic forces that resist sinking then become of greater importance. The pellets of Gammarus egested into fresh water are surrounded by a peritrophic membrane for up to 7 h, after which time the membrane becomes broken off, probably by swelling of the pellets (Lautenschlager et al. 1978), and they then become diffuse. Pellets of invertebrates, like those of protists, are components of marine, lake, and river "snow" (aggregates of mucus, microorganisms, protists, detritus, and algal cells). ...
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... The release of both Fe and C from fecal matter is slower when the physical integrity of the fecal particles, that is, the fecal pellets, is maintained. The presence of a peritrophic membrane that maintains the integrity of the fecal pellets and favors their export to depth is likely limiting exchanges with the environment (Frangoulis et al. 2004), when it is not degraded (Lautenschlager et al. 1978) or eaten by organisms (Lampitt et al. 1990). Without any perturbations, Hutchins et al. (1995) showed that the copepod fecal pellets retained most of their Fe (> 80%) over 30 days and similarly, Cabanes et al. (2017) showed that Fe in salp fecal pellets was highly refractory. ...
Article
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... Although some fecal pellets are very resistant (Ferrante & Parker 1977), Marshall & Orr (1955) observed that others disintegrate immediately after defecation. Lautenschlager et al. (1978) observed that the peritrophic membrane of Gammarus disappears in 7-24 h at 10°C and Turner (1977) believes that the fecal pellets of some marine calanoids lack peritrophic Feeding, Grazing and Assimilation by Zooplankton 359 membranes altogether. Conover (1966a) has observed that calanoids may tear open and then discard fecal pellets. ...
... The funnel and PM are thus different entities in Gammarus oceanicus, as they also appear to be in the amphipods Corophium volutator and Parathemisto gaudichaudi (see Icely and Nott, 1975; Sheader and Evans, 1975) but possibly not in Caprella equilibra and Cyamus boopis, in which species the funnel is suggested to be continuous with PM (Keith, 1974). Several amphipod species have been reported to egest faecal pellets in which a compacted mass of waste particles is enveloped by a tube of PM (Peters, 1968; Georgi, 1969; Lautenschlager et al., 1978; Hansen and Peters, 1997/98); some of these reports identify the presence of chitin in PM. Peritrophic membrane synthesis in these species clearly occurs much more frequently than molt-related synthesis of new cuticle, a situation that is compatible with funnel and PM being separate entities. ...
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The funnel of Gammarus oceanicus extends as a fold of the foregut wall into the midgut lumen. It comprises an anterior segment, to which both foregut epithelium and cuticle contribute, and a posterior segment that lacks the epithelium. The latter segment consists of two layers of foregut cuticle that are in close contact and extend distally beyond the point where the foregut epithelium turns back on itself; contact between the two cuticular layers develops as the epithelium retracts from between them, in postmolt. Light microscopy does not consistently distinguish between the funnel's posterior segment and the peritrophic membrane found within mid- and hindguts; however, their ultrastructural organizations are distinctly different, and an origin of peritrophic membrane from the funnel of some amphipods, as suggested in the literature, is not the case for Gammarus oceanicus. Scattered within the posterior segment cuticle are clusters of short, highly curved, electron-lucent rods. Such features have not been described from other crustacean cuticles. However, rather than being novel structures, they are interpreted as artifacts produced by sectioning of the abundant chitin macrofibrils of the cuticle.
... In 50 thin slices of a freshly egested copepod pellet (,16 h) we found hardly any bacteria ( 1 bacteria 1000 mm 22 thin section area) on the peritrophic membrane but quite a few (,25 bacteria 1000 mm 22 thin section area) within the pellet (Fig. 5). Several authors (Lautenschlager et al., 1978;Gowing and Silver, 1983) also reported that the surfaces of freshly ejected (age ,7 h) crustacean pellets ( planktonic copepods and gammarids, respectively) are devoid of bacteria. With ongoing degradation, copepod fecal pellets were densely colonized by bacteria ('bacterial lawn') as also has been observed by other investigators (cf. ...
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The goal of this study was to determine the morphology and ultrastructure of doliolid pellets using light, epifluorescence and transmission electron microscopy and compare the results to observations of calanoid copepod pellets. For (ultra)structural analyses, pellets of gonozooids of Dolioletta gegenbauri and females of the copepod Eucalanus pileatus were produced in feeding experiments at close to environmental food concentrations. Thin sections of a representative doliolid pellet revealed that these pellets were mainly composed of intact diatom valves, a few fragmented valves and intact flagellates. While the larger diatoms, Rhizosolenia alata, were completely digested (empty valves), the smaller diatoms, Thalassiosira weissflogii, were partly, or not digested at all. The phytoflagellate, Isochrysis galbana, appeared to be hardly digested. Aggregations of bacteria occurred mostly inside pellets associated closely with intact I. galbana flagellates and partly digested T. weissflogii cells; some scattered bacteria were found among fragmented valves. No, or little, bacterial colonization was associated with empty R. alata valves, and hardly digested T. weissflogii cells. Whereas doliolid fecal pellets were loosely packed and composed of fully, incompletely and/or hardly digested food particles, pellets of the copepod E. pileatus were densely packed and consisted mainly of fragmented diatom valves. Pellets of doliolids and calanoid copepods can represent a high percentage of the particulate organic carbon in the water-column on subtropical continental shelves.
... Although it is difficult to account for the mechanisms with which the three faecal types are produced, two factors may have played a role in their production. While it possible that Type 3 faeces may have been a product of Type 1 and 2 feces that had been physically broken up and mixed with pedal mucous as the abalone moved around the aquaria; the production of periotrophic mucosal membranes found around the fecal pellets of invertebrates (Forester, 1953;Lautenschlager et al., 1978) may have also played a role. Periotrophic membranes form around faecal pellets as they pass along the intestine, and it is possible that differential production of this membrane may account for production of the three faecal types. ...
Article
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"December 1999." Thesis (Ph. D.)--Rhodes University, 1999. Includes bibliographical references.
... However, the physiological significance of PTMs deserves further attention (Richards and Richards, 1977). Most crustaceans, but perhaps not all (see Komura and Yamamoto, 1968; Miyawaki and Taketomi, 1984; To et al., 2004), produce a PTM in the midgut trunk (MGT; also called intestine) and possibly in the digestive gland as well (Forster, 1953; Gauld, 1957; Pillai, 1960; Dall, 1967; Talbot et al., 1972; Quaglia et al., 1976; Lautenschlager et al., 1978; Mykles, 1979; Holliday et al., 1980; Johnson, 1980; Avtsyn and Petrova, 1986; Lovett and Felder, 1990b; Tsuda and Nemoto, 1990; Hansen and Peters, 1997/98; HerreraA ´ lvarez et al., 2000; De Jong-Moreau et al., 2000; Halcrow, 2001). These PTMs are simple fibrillar layers formed by delamination from the brush border of the epithelial cells (Georgi, 1969). ...
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Peritrophic membranes (PTMs) are secreted acellular layers that separate ingested materials from the gut epithelium in a variety of invertebrates. In insects and crustaceans, PTMs are produced in the midgut trunk (MGT, or intestine), but the MGT in decapod crustaceans, unlike that of insects, is not involved with digestion or absorption of food. We demonstrate that the PTM in the penaeid shrimp Sicyonia ingentis is similar to that in other crustaceans that have been studied and is primarily composed of chitin. The lectin WGA binds only to the PTM and glycocalyx along the microvilli of the midgut cells, which is consistent with the suggestion that the chitin is synthesized along the microvilli. The PTM is only permeable to inert particles smaller than 20 nm. We also describe the secretion of granules, which fill the apices of the epithelial cells, into the ectoperitrophic space. Although their function is not clear, they do not contribute to the PTM.
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Zooplankton fecal pellets expelled near the surface of lakes provide a mechanism for removal of diatoms to deeper water. Scanning electron micrographs show that copepod fecal pellets, collected from Lake Michigan, contained fractured specimens of 21 species of diatoms. Few intact diatoms were observed and many frustules were reduced to small fragments during ingestion by the copepods. The peritrophic membrane surrounding the pellets is composed of polysaccharides, one of which is chitin. This membrane is broken down by bacterial decomposition in 6 to 14 days as the pellets settle at an average velocity of 4.7 m d⁻¹. As a result, pellets released near the surface in water more than 70 m deep do not transport diatom fragments directly to the sediment. In a large proportion of Lake Michigan the transport of diatoms to the sediments via pellets originating near the surface is unlikely, since about 60 percent of the lake is >70 m deep.
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A thin membrane surrounding the faeces of many of the Caridea has proved to be chitinous. The membrane is not secreted by the fore-gut, but almost certainly by the anterior part of the intestine, and is therefore a peritrophic membrane sensu stricto.
Article
A radiotracer technique involving 51Cr was used to monitor the egestion rates of A. fluviatilis and P. contortus. When snails were starved, either before or after exposure to labelled food, gut emptying rate reduced. Examination of faecal components suggested that this was due to reductions in the rate of passage of food through the hepatopancreas. Since the latter is the major site of digestion and absorption in the Gastropoda this strategy was explained as an attempt by the snails to extract more nutrient from the disturbed food supply. Other factors affecting egestion rate were, temperature, food quality and snail size. Weight for weight egestion was more rapid in P. contortus than in A. fluviatilis and this difference is typical between detrivores and herbivores. Information on defaecation strategy enabled an estimation of field absorption and ingestion rates in A. fluviatilis. There was good agreement between the latter and estimates predicted on the basis of laboratory observation. However, field determined absorption efficiencies were more constant and generally higher than those predicted on the basis of laboratory measurements.
Article
Fecal pellets voided by 70 invertebrate species are described, 66 of these for the first time. Pellet size is related to size of animals, and linear regressions are given for two species. Pellet characteristics described are cross-sectional shape, sculpture, differentiation, composition, and shape. The morphology is specific for many animals. However, certain species void feces which are 1) diffuse, 2) morphologically inconsistent, or 3) lack differentiating characteristics.
Article
In the White Shoal area of the James River, Virginia, recognizable faccal pellets formed an average of 0.42% by weight of the total suspended solids at 1 m above the bottom and 0.14% by weight at 1 m below the surface during a 24-hour sampling period. Pellets retained on soil analysis sieves (mesh sizes 125 and 44 μ), however, formed an average of 26.6% and 19.26% by weight, respectively, of the materials retained on the screens at the same depths. The pellets were apparently being transported in suspension. Although quantities in suspension were small, it is suggested that sorting during transportation and deposition could result in accumulation in areas of the estuary where fine sediments would not settle out. Such accumulations on the bottom could alter the textural and chemical characteristics of the existing sediments because of the fine size and chemical properties of the component particles of the pellets.
Article
Four aspects of the ecology of running water are discussed in relation to the management of watersheds. They are temperature, substratum, the sources of food for invertebrates, and the breeding requirements of fish. It is shown how each may be altered almost inadvertently by man with far-reaching biological effects.
Article
Membrane-enclosed fecal pellets of planktonic herbivores were sampled at several depths in the Baltic Sea (459 meters deep) and off Portugal (4000 meters deep) by means of a Simonsen multinet. Pellets contained mainly empty shells of planktonic diatoms and silicoflagellates. Two kinds of fecal pellets were found, those with the remains of one species (for example, Thalassiosira baltica) and those with the remains of several species (for example, Chaetoceros, Achnanthes, and Thalassiosira). Siliceous skeletons were protected from dissolution during settling by a membrane around the pellet.
A review of present knowledge of faecal pellets
  • H B Moore
  • P Kruse
Consumption of autumnshed leaves by Gammarus and decomposition of leaf-derived fecal pellets
  • K P Lautenschlager
  • Moore H.B.
  • Reeve M.R.