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Role of the Feeding Current in O2 Uptake in Daphnia Magna

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Role of the Feeding Current in O2 Uptake in Daphnia Magna The Journal of Experimental Biology 202, 553–562 (1999) 553 Printed in Great Britain © The Company of Biologists Limited 1999 JEB1669 THE IMPORTANCE OF THE FEEDING CURRENT FOR OXYGEN UPTAKE IN THE WATER FLEA DAPHNIA MAGNA R. PIROW*, F. WOLLINGER AND R. J. PAUL Institut für Zoophysiologie, Westfälische Wilhelms-Universität, Hindenburgplatz 55, D-48143 Münster, Germany *e-mail: [email protected] Accepted 30 November 1998; published on WWW 3 February 1999 Summary In the planktonic crustacean Daphnia magna from 2.3 to 2.7 mm at 20 °C. External PO· measurement (Branchiopoda, Cladocera), different views exist on the revealed oxygen depletion in the ventral body region but mechanism of respiratory gas exchange, ranging from gill essentially no change at posterior, lateral and dorsal breathing to general integumentary respiration. The positions. The PO· difference between the inflow and presumed structures for specialized gas exchange are outflow of the feeding current was 13.0 mmHg (1.73 kPa). located ventrally within the filter chamber, which is The flow rate of the feeding current ranged from 1.2 to continuously perfused with the ambient medium for food 5.2 ml h−1 and showed a close correlation with appendage gathering. To localize respiratory gas exchange in D. beat rate, which varied from 310.4 to 460.7 beats min−1. magna, we determined the contribution of the feeding Model calculations based on the Fick principle suggest that current to total oxygen transport. Combining microscopy oxygen extraction from the feeding current satisfies most with special optical techniques, we used a phosphorescent of the total of oxygen requirement of D. magna. oxygen-sensitive dye for oxygen partial pressure (PO·) measurements and applied fluorescent microspheres for flow-rate analysis. Appendage beat rate was determined by Key words: Crustacea, Daphnia magna, feeding current, flow digital image-processing. All experiments were carried out imaging, oxygen extraction, oxygen phosphorimetry, particle on hypoxia-adapted animals with a body length ranging fluorimetry, zooplankton. Introduction Like other zooplankters, the water flea genus Daphnia epipodites as well as on the ventilatory function of the feeding (Branchiopoda, Cladocera) occupies an important position in current. The epipodites in D. magna have been found to be freshwater food webs by converting phytoplankton food into lined with an epithelium 15–20 µm thick (Kikuchi, 1983; biomass that then becomes available for higher trophic levels. Peters, 1987), which is 4–5 times thicker than over the rest of Specialized thoracic appendages equipped with fine setae the limb. Accordingly, respiratory gas transfer via the so-called enable Daphnia spp. to filter out suspended food particles from branchial sacs would be impeded by a large diffusion barrier. the surrounding water. Encased by the carapace, these Physiological data on D. magna, a species exhibiting a appendages beat rhythmically to pump water through a distinct oxyregulatory behaviour (Heisey and Porter, 1977; virtually closed filtering chamber (see Fig. 121 of Fryer, 1991), Kobayashi and Hoshi, 1984; Paul et al., 1997), have yielded which separates the feeding current into an inflow and outflow no indications to corroborate the ventilatory function of the section. The water current produced by the movements of these feeding current. The beating rate of the thoracic limbs stays thoracic limbs not only serves for feeding but is also thought constant when the oxygen availability decreases (Heisey and to be important in gas exchange (e.g. Gruner, 1993). Possible Porter, 1977; Colmorgen and Paul, 1995). In contrast, other sites for gas exchange are the inner walls of the carapace and oxyregulating water breathers such as fish or crabs increase the epipodites (Gruner, 1993), both structures lying in the their ventilation rate under hypoxic conditions to ensure a ventral region within the filtering chamber. The epipodites are constant rate of oxygen uptake. vesicular protuberances of the thoracic limbs, sometimes These findings suggest that the feeding current in Daphnia termed branchial sacs because of their presumed gill function. magna does not have an important role in respiratory gas The proposed gill function of the epipodites is a typical transport and that the entire body surface is involved in gas characteristic of branchiopod crustaceans (Barnes, 1969; exchange. The surface-to-volume ratio in this millimetre-sized Gruner, 1993). zooplankter is sufficiently large to permit integumentary However, morphological and physiological studies on respiration (Graham, 1988). The aim of the present study is to Daphnia spp. have cast doubt on the respiratory function of the assess the contribution of the feeding current to oxygen uptake 554 R. PIROW, F. WOLLINGER AND R. J. PAUL in the filter-feeder D. magna. We chose this cladoceran species tethered by its apical spine onto a coverslip using a small drop because Daphnia spp. have long been the focus of ecological of wax, allowing a lateral view of the animal. For flow-rate research (see, for example, Lampert, 1987) so that analysis, the apical spine was glued to a glass capillary tube comprehensive information about the biology of this genus is (1 mm o.d.) attached to a plastic cube (8 mm side length), available (e.g. Peters and DeBernardi, 1987). This report is part which allowed lateral, ventral and anterior views of the of a broader study addressing both the external and internal animal. The second antennae were immobilized using a small mechanisms of respiratory gas transport and the importance of drop of wax. This was necessary to prevent any flow currents haemoglobin in D. magna (R. Pirow, F. Wollinger and R. J. from the second antennae that could disturb the PO· Paul, in preparation). We studied ‘hypoxia-adapted’ animals, measurements or the flow-profile acquisition. The second which typically have an increased haemoglobin content antennae are important in locomotion, and the jerky (Kobayashi and Hoshi, 1982; Kobayashi et al., 1990). It has swimming movements they produce are likely to affect the been shown that D. magna, a common inhabitant of ponds and feeding and respiration processes by changing the catchment ditches, is physiologically well adapted to cope with area of fluid surrounding the animal. We did not explore these constraints such as oxygen deficiency (Kobayashi and Hoshi, effects further in this study. Tethered animals in the 1984; Paul et al., 1998), which could occur naturally in experimental chamber were always perfused with medium eutrophic habitats during the summer season. Haemoglobin- from the anterior and were allowed to acclimate to the rich D. magna are able to keep their rate of oxygen experimental conditions for 30 min. consumption constant down to an ambient oxygen tension of The inlet of the experimental chamber was connected using 8 mmHg (1.07 kPa; Kobayashi and Hoshi, 1984). polyvinyl chloride tubing to thermostatted glass vessels filled To clarify the role of the feeding current in oxygen uptake, with normoxic and anoxic culture medium. Two peristaltic we measured the oxygen partial pressure (PO·) within the pumps perfused the chamber at variable PO· by mixing both feeding current and determined the PO· difference between the media at different ratios. The anoxic medium was produced by inflow and outflow. Furthermore, we recorded the flow pattern bubbling with normocapnic nitrogen using gas-mixing pumps of the feeding current and estimated the total rate of flow for (Wösthoff, Bochum, Germany). individual animals. A description of the flow rate was While performing optical PO· measurements, a special O2- necessary for further calculations using a model based on the sensitive dye (see below) was added to medium equilibrated Fick principle. PO· was determined using a phosphorimetric with different normocapnic O2/N2 gas mixtures. Two different method, whereas feeding current profiles were acquired using experiments were performed. In the first experiment, aimed at particle fluorimetry and digital image-processing. assessing qualitatively the sites of respiratory gas exchange in D. magna, PO· was measured at various positions close to the body surface after the perfusion had been stopped. A second Materials and methods experiment was performed to quantify oxygen extraction from Animals the feeding current. For this, the PO· difference between the Water fleas, D. magna Straus, were obtained from the inflow and outflow was measured immediately after the Staatliches Umweltamt, Nordrhein-Westfalen, Münster, perfusion of the chamber had been stopped. Germany. The animals were kept in 1 l glass beakers at approximately 20 °C under a 14 h:10 h L:D photoperiod using Arrangement for optical PO· measurements daylight fluorescent lamps. Experimental animals developed For the optical determination of PO·, we used a special an increased blood haemoglobin content (Kobayashi and palladium–porphyrin compound [albumin-bound palladium- Hoshi, 1982; Kobayashi et al., 1990) induced by moderate meso-tetra (4-carboxyphenyl) porphine; Medical System hypoxia (30–40 % air saturation) resulting from bubbling Corp., Greenvale, NY, USA]. This compound phosphoresces nitrogen through the culture medium. The synthetic culture at 687 nm when excited at 416 or 523 nm (Lo et al., 1996), and medium (see Paul et al., 1997) had a pH of approximately 7.5 the phosphorescence can be quenched by molecular oxygen. and a conductivity of 3300 µScm−1. The animals were fed with This quenching results from collisions between the excited
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