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On the Relationship Between Pso and the Mode of Gas Exchange in Tropical Crustaceans! Pacific Science (1982), vol. 36, no. 3 © 1983 by the University of Hawaii Press. All rights reserved On the Relationship between Pso and the Mode of Gas Exchange in Tropical Crustaceans! CHARLOTTE P. MANGUM 2 ABSTRACT: In general, the oxygen affinity of hemocyanin does not decrease when tropical decapod crustaceans carryon gas exchange in air instead ofwater. Other oxygenation properties such as cooperativity and the Bohr shift also change very little, if gt all. The generalization of a higher oxygen affinity in tropical than in temperate zone species appears to be true but has exceptions of unclear origins, emphasizing the crudity of correlations between respiratory properties of the blood and gross features of the environment. THE EXCHANGE OF RESPIRATORY GASES in air tropods (Jones 1972, Mangum and Lykkeboe occurs in a medium far richer in oxygen than 1979, Redmond 1968b, Wells and Wong water. Among the vertebrates (e.g., am­ 1978). One aquatic species actually has a phibians), increasing dependence on air is ac­ lower Hc02 affinity (Brix, Lykkeboe, and companied by profound modifications of the Johansen 1979) than pulmonates. No clear sites and organs of gas exchange, and a clear trend can be discerned among the chelicerates, decrease in the oxygen affinity (Pso ) of the where the comparison is limited by the scar­ blood (Johansen and Lenfant 1972), presum­ city of information as well as a surprising ably in response to higher levels of blood P02' heterogeneity within the terrestrial arachnids However, the taxonomic scope of this gen­ (Mangum 1980). An enormous difference be­ eralization appears to be limited, and the re­ tween Hb02 affinities in larval, water­ lationship may even be reversed. Among breathing chironomids and adult, bubble­ the annelids, hemoglobin-oxygen (Hb02 ) breathing notonectids is related to the unique affinity is uniformly high in the earthworms, function of hemoglobin in the back swim­ in which the gas exchange site is the general mers, viz. buoyancy control, and not to the body wall epithelium, whereas it may become mode of gas exchange (Wells, Hudson, and very low in the aquatic polychaetes, with their Brittain 1981). In a study of water- and air­ frequently elaborate gills (Mangum 1976). breathing fishes, Johansen, Mangum, and Despite morphological adaptations for air Lykkeboe (1978) found no clear relationship breathing, hemocyanin-oxygen (Hc02 ) between Pso at pH 7.4 and the mode of gas affinity under physiological conditions is exchange; only at the physiological pH about the same in pulmonates (Spoek, characteristic ofthe particular species can sig­ Bakker, and Wolvekamp 1964; Wells and nificantly lower oxygen affinity be detected in Shumway 1980) and in several aquatic gas- air breathers. They concluded that the design ofthe gas exchange organs and the cardiovas­ cular system is so different among the various 1 This research was conducted as part of the Alpha groups of air breathers (see also Johansen Helix Cephalopod Expedition to the Republic of the 1970) that physiological determinants of Philippines, supported by National Science Foundation oxygenation such as blood acid-base balance grant PCM 77-16269 to J. Arnold. This study was also may counteract the influence of ambient supported in part by National Science Foundation grant PCM 77-20159 to C. P. Mangum. oxgen availability. Thus, Fyhn et al. (1979; see 2 College of William and Mary, Department of also Table 3 in Riggs 1979), who controlled Biology, Williamsburg, Virginia 23185. PC02 in the equilibration gas and allowed pH 403 • I •• , • .", ,. "~" _ " ,.. " .,. "" .,.. ,... " ,,,. or" ,-....... ",. 404 PACIFIC SCIENCE, Volume 36, July 1982 in the sample to vary with total COz content, been obtained for strictly aquatic and also also found significant differences in several of tropical species. The values for a single tem­ the same species. perate zone air breather (Burnett 1979) do not The relationship between HcO z affinity and differ from those for temperate zone water the mode of gas exchange in crustaceans is breathers (Mangum 1980). uncertain. Redmond (1962, 1968a, 1968b) The Philippines expedition of R/V Alpha found a high oxygen affinity in one terrestrial Helix provided an opportunity to investigate species and a lower oxygen affinity in another, oxygen affinity of the bloods of tropical compared with several aquatic decapods. animals. Although emphasis was placed on Young (1972) concluded that HcOz affinity in water-breathing decapods, the taxonomic crabs decreases with emergence onto land. scope was broadened to include other kinds of However, his comparison includes variables crustaceans, and several air breathers were other than the intrinsic ligand affinity of the studied to ensure against differences due to carrier, viz. blood pH and geographic distri­ technique. bution of the species. When the data are cor­ rected to a common pH of 7.6, the values for the three most terrestrial species differ by less MATERIALS AND METHODS than 1 mm Hg, and the value for an intertidal species that breathes water as well as air sug­ Blood was taken from various sinuses into gests an oxgyen affinity more than 10 mm Hg iced syringes, and expelled into a cell homo­ lower than in the three air breathers. While genizer where serum was expressed from the HcO z affinity in the subtidal water breather clot, if any. It was diluted 2: 1 with an air­ Callinectes sapidus was higher than any ofthe equilibrated suspension of yeast cells in Tris­ others, this comparison is confounded by a maleate buffered seawater (final concentra­ geographic variable; C. sapidus is the only tion 0.05 M). Oxygen equilibrium was then species in the sample that extends throughout determined by the cell respiration method (de­ the temperate zone. Sevilla and Lagarrigue scribed in detail in Johansen et al. 1978), using (1979) found that HcO z affinity decreases in a Yellow Springs Instrument Co. Model 53 Oz isopods with increasing specialization of the monitor and a high-sensitivity (0.0005 in.) organs of gas exchange for breathing air, but Teflon membrane. The pH was also measured all the species in their sample are supratidal air at the end of the experiment, following re­ breathers. The only data available for a water equilibration of the preparation with air. breather are for the giant, deep-sea (and there­ fore cold-water) species Bathyonus giganticus (K. E. Van Holde and M. Brenowitz, personal RESULTS communication). With these additional dif­ ferences in mind, and also with the reserva­ Oxygen Affinity and the Mode ofGas tion that none of the information for isopod Exchange hemocyanins has been obtained under strictly physiological conditions, the comparison also The values for air and water breathers are suggests no difference between Bathyonus and compared below in a physiological pH range several of the air breathers, including one of that is often found at high temperature in the species with a tracheal system. both kinds of species (Mangum 1973, Burg­ A compilation ofdata collected under phys­ gren and McMahon 1981); more detailed iological conditions of inorganic ions and pH effects of pH are shown in Figures 1 and 2. actually suggests that many terrestrial crabs When the Oz affinities of the hemocyanins have hemocyanins with higher oxygen affini­ from all the species listed in Table 1 are com­ ties than those of their aquatic relatives pared according to the mode ofgas exchange, (Mangum 1980). This comparison, however, the trend noted earlier (Mangum 1980) is retains the geographic variable. Most terres­ highly significant (P = 0.015): HcOz affinity is trial crabs live in the tropics, and no data have not lower but rather higher in air and bimodal -~ .", ->'-' - ••~ ..-, '" ,. '" ~'" '",n ,. ~ _ ,, ••• • ., ,_ .,. J:'" 20 E e E e 10 0 U1 8 0. 6 Scylla (~) 4 Portunus and Charybdis (e) 7.2 7.4 7.6 7.8 7.0 7.2 7.4 pH 7.6 7.8 8.0 40 30 20 20 10 ~ - 10 8 :f 8 6 6 Panulirus E GecarcOides (e) a (e) 4 25 e E (~) IGOe (0) 4 Varuna 0 7.0 7.2 7.4 7.6 7.8 U1 pH 0. 30 20 40 Penaeus (~) 0. Thalassina (e) 10 J: 20 E 7.0 7.2 7.4 7.6 E -10 30 Lambrus (e) 0 (~) U1 8 Naxioides 0. 20 6 4 10 7.2 7.4 7.6 7.0 7.2 7.4 7.6 7.8 8.0 ------ pH pH 200 20 Ojontocfac tylus (e) ~ Gonoaactylus (~) E 1 Ol~--L_.L---I.__--I.__--'L--__'--__'--_-j .!; 50 o .040 il. 20 10 8 6 Oratosquilla woodmasoni (e) 4 solicitans (.) 2 6.8 7.0 7.2 7.4 7.6 7.8 pH FIGURE I. The relationship between hemocyanin-oxygen affinity (P,o) and pH in a variety of crustaceans from Bindoy, Philippine Islands, at 25°C; 0.05 M Tris-maleate buffered seawater (33-34%.). , " ",' , ,'.". '''''0 .. , ,. ", , 406 PACIFIC SCIENCE, Volume 36, July 1982 0 4 o~ 3 Scylla (0) and Portunus Charybdis (e) 2t-'"_-...L...------'---L.--L--+-...L.--L.-...,---L--.J--........1.........:~..J,.....j e o • e • 4 e e a e-0>---:;e;:----zt Po nu Ilrus 16 C (0). 25 C (e) 4 Penaeus (e) o I{) e e c e 3 e 3 2 0--0-. o -----o o Lambrus (e) Thalassina (0) 0 --0 Naxioides (0) 7.2 4 Calappa 7.0 7.2 7.4 pH 8r----------------. 7 6 Odontodactylus (e) 5 Gonodactylus (o.) o c'" 6 Orotosquillo 5 woodmasoni (e) solicitans (.) 6.8 7.0 7.2 7.4 7.6 7.8 pH FIGURE 2. The relationship between the cooperativity ofhemocyanin-oxygen binding and pH in crustaceans from Bindoy, Philippine Islands, at 25°C; 0.05 M Tris-maleate buffered seawater (33-34%.).
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