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Respiratory Gas Exchange in Daphnia Magna 3091 a B The Journal of Experimental Biology 202, 3089–3099 (1999) 3089 Printed in Great Britain © The Company of Biologists Limited 1999 JEB2272 THE SITES OF RESPIRATORY GAS EXCHANGE IN THE PLANKTONIC CRUSTACEAN DAPHNIA MAGNA: AN IN VIVO STUDY EMPLOYING BLOOD HAEMOGLOBIN AS AN INTERNAL OXYGEN PROBE R. PIROW*, F. WOLLINGER AND R. J. PAUL Institut für Zoophysiologie, Universität Münster, Hindenburgplatz 55, 48143 Münster, Germany *e-mail: [email protected] Accepted 13 September; published on WWW 28 October 1999 Summary Recent studies on Daphnia magna have revealed that the 6 mmHg (0.8 kPa) for the rostrum. Although not all parts feeding current is important for uptake of oxygen from the of the circulatory system could be analyzed using this ambient medium. Respiratory gas exchange should technique, the data obtained from the accessible regions therefore mainly occur within the filtering chamber, whose suggest that the inner wall of the carapace is a major site boundaries are formed by the trunk and the extended of respiratory gas exchange. Taking the circulatory pattern carapace shell valves. The precise site of gas exchange in and the flow pattern of the medium in the filtering chamber the genus Daphnia is, however, a matter of conjecture. We into consideration, it becomes clear that the haemolymph, have developed a method of imaging the haemoglobin after passing from the limbs to the carapace lacuna, oxygen-saturation in the circulatory system of transparent becomes oxygenated while flowing through the ventral part animals, which provides an opportunity to localize oxygen of the double-walled carapace in a posterior direction. The uptake from the environment and oxygen release to the laterally flattened rostral region, where sensory and central tissues. Experiments were carried out at 20 °C on nervous system structures are located, seems to have direct 2.8–3.0 mm long parthenogenetic females maintained in diffusive access to ambient oxygen, which could be hypoxic culturing conditions, which had resulted in an especially advantageous during severe hypoxia when the increased haemoglobin content in the haemolymph. In convective transport systems fail to supply enough oxygen lateral views of D. magna, the highest values of to that region. haemoglobin oxygen-saturation occurred near the posterior margin of the carapace and, surprisingly, in the rostral part of the head. The ambient oxygen partial Key words: Crustacea, Branchiopoda, Cladocera, Daphnia magna, pressures at which haemoglobin was half-oxygenated were gas exchange, respiratory protein, haemoglobin, oxygen-saturation, 15 mmHg (2.0 kPa) for the posterior carapace region and spectral imaging, zooplankton. Introduction Aerobic energy production depends on the continuous respiratory gas exchange in the water flea Daphnia magna. The exchange of oxygen and carbon dioxide between the cellular literature on crustacean biology (Gerstaecker, 1866–1879; combustion sites of an organism and its environment. With Giesbrecht, 1921; Storch, 1925; Krumbach, 1926–1927; increasing body size, the metazoans of the higher phyla have Flößner, 1972; Villee et al., 1979; Gruner, 1993) presents had to evolve dedicated organs with surface-enlarged thin different views about the sites of respiratory gas exchange in epithelia mediating the transfer of respiratory gases between the genus Daphnia, including suggestions of (i) gill breathing, the ventilatory and the circulatory systems. Such extensively (ii) intestinal respiration and (iii) integumentary respiration. elaborate structures are usually not present in animals smaller Assigned to the class Branchiopoda, the genus Daphnia than a few millimetres in length (Graham, 1988; Rombough possesses vesicle-like epipodites on its thoracic limbs, which and Ure, 1991; Rombough, 1998), which is not particularly have been repeatedly regarded as gills and have sometimes surprising given their larger surface-to-volume ratios (Krogh, been termed branchial sacs (e.g. Claus, 1876). This assumption 1941). Thus, it is sometimes difficult to ascertain precisely is, so far, consistent with the morphological organization of a what the respiratory organ is or, if it is lacking, to determine typical crustacean, in which the gills derive primarily from whether the whole body surface or only parts of it are evaginations of the limb integument (Barnes, 1969; Gruner, employed for integumentary respiration. 1993). In contrast to the gills of the advanced crustaceans, The present study aims to determine the favoured sites of however, the epipodites of the genus Daphnia are in no way 3090 R. PIROW, F. WOLLINGER AND R. J. PAUL elaborated with respect to surface area and epithelial thickness which indicates that oxygen is extracted from the feeding (Bernecker, 1909; Fryer, 1991) to enhance the rate of transfer current. of respiratory gases. Although overlain by a cuticle that is very It has repeatedly been suggested that the inner wall of the thin (0.2–0.5 µm) relative to that of the rest of the leg (1–3 µm), carapace is a major seat of respiratory exchange in the genus the epipodites are lined with an epithelium that is considerably Daphnia (Leydig, 1860; Fryer, 1991). Deriving from an thicker (15–20 µm) than ordinary epithelium (3–5 µm; integumental fold of the maxillary region (Fryer, 1996), the Kikuchi, 1983). The selective stainability of the epipodites by double-walled carapace consists of two shell valves, which silver salts or vital stains (Fischel, 1908; Gicklhorn, 1925; encase the thorax, abdomen and limbs, thus forming the lateral Gicklhorn and Keller, 1925a), formerly misinterpreted as boundaries of the filtering chamber. Taking into consideration characteristic of respiratory epithelia (e.g. Gicklhorn and the water flow within the filtering chamber (Westheide and Süllman, 1931), points in D. magna, as it does in other Rieger, 1996) and the complex circulatory pattern (Hérouard, crustaceans (Panikkar, 1941; Croghan, 1958), to an 1905; Storch, 1925), it seems very likely that the haemolymph osmoregulatory function, which has more recently been enters into intensive gas exchange with the medium when confirmed ultrastructurally (Kikuchi, 1983). The role of the circulating through the spaces between the inner and outer neck or nuchal organ, in D. magna, a morphological feature walls of the carapace shell valves. Utilizing the presence of restricted to the first instar juvenile (Halcrow, 1982), has to be blood haemoglobin (Hb), a respiratory protein with useful seen in the same functional context (Potts and Durning, 1980; oxygen-sensitive spectral characteristics, a newly developed Halcrow, 1982) rather than linked to respiratory gas exchange spectroscopic imaging technique enabled us to test this (Gicklhorn and Keller, 1925b; Dejdar, 1930). hypothesis experimentally. The striking phenomenon of anal water intake prompted Lereboullet (1850) and later Weismann (1877) to assume that intestinal respiration occurred in the daphniids. Anal water Materials and methods uptake, caused by antiperistaltic movements of the hindgut Animals (Hardy and MacDougall, 1895), was later related to turgor Female water fleas Daphnia magna Straus were cultured restoration (Fox, 1952; Fryer, 1970). It is also thought to under the conditions described previously (Pirow et al., 1999). improve the efficiency of food utilization in the intestine To induce an increased blood haemoglobin (Hb) concentration, (Fryer, 1970). parthenogenetic offspring were raised under conditions of General integumentary respiration seems plausible because moderate hypoxia (30–40 % air saturation) produced by of the large surface-to-volume ratio of this millimetre-sized bubbling nitrogen through the culture medium. According to animal and because of its delicate thin-walled integument Kobayashi and Hoshi (1982), such hypoxic conditions result in (Halcrow, 1976; Dahm, 1977). This hypothesis was a sevenfold elevation of blood Hb concentration (basic level −1 −1 supported by the finding that the beating rate of the thoracic 1gl or 0.06 mmol O2 l ) in 2.5 mm long adult females. The limbs stays constant in D. magna (Heisey and Porter, 1977; animals used in our experiments had a body length ranging from Paul et al., 1997) when the ambient oxygen concentration 2.8 to 3.0 mm, measured from the anterior part of the head to decreases. If the limb movements serve for ventilation, then the posterior edge of the carapace at the base of the apical spine. the expected response to hypoxia in a water-breather with oxyregulatory capacities would be an enhanced limb beating Preparation of animals for experiments rate (Randall et al., 1997). In the oxyregulating D. magna, The experiments were carried out at 20 °C in a thermostatted however, systemic responses differ from those of a typical perfusion chamber (see Paul et al., 1997) that allowed water-breather (Paul et al., 1997). The fact that there is no microscopic observation of single animals. To analyze its increase in the limb beating rate need not be regarded as spectral characteristics, the animal was immobilized by glueing negative proof of ventilatory function. In an attempt to filter its apical spine to a 1 cm long synthetic brush-hair (histoacryl out as much food as possible from the ambient medium, when adhesive; B. Braun Melsungen AG, Melsungen, Germany; there is little or no food available, planktonic filter feeders Cowles and Strickler, 1983). The animal was positioned such as D. magna exhibit close to maximum limb beating lateral-side down with the opposite side of the brush-hair and rates
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