Influence of environmental temperature and hypoxia on oxygen uptake and transport

4.5.4 Influence of environmental temperature and hypoxia on oxygen uptake and transport

Coping with environmental temperature

Critical temperature thresholds (Tc) have been defined as the transition to an anaerobic mode of mitochondrial metabolism, once temperature reaches low or high extremes, due to insufficient ventilation and/or circulation and aerobic energy provision (Zielinski and Pörtner 1996; Pörtner et al. 1998). The lower Tc is set by insufficient aero- bic capacity of the mitochondria, while the upper Tc is set by a mismatch of excessive oxygen demand by mitochondria and insufficient oxygen uptake and distribution by ventilation and circula- tion (Pörtner et al. 2000a). In the cold, energy de- mand will be met by mitochondrial proliferation, which ultimately will cause an increase in oxygen demand that becomes detrimental at the upper Tc. Oxygen demand is not only related to cellular energy requirements but also to the number of mitochondria and their properties, specifically maintenance of the proton gradient. The relation- ship between this so-called proton leakiness and aerobic capacity appears to be constant. Pörtner et al. (2000a) suggest that metabolic cold adapta- tion may depend upon the extent of diurnal and seasonal temperature fluctuations, leading to higher costs of maintenance in eurythermal than in stenothermal fish. Thus in stenothermal fish aerobic capacity and energy expenditure is mini- mized as far as possible according to environmen- tal and lifestyle requirements.

The haemoglobin polymorphism of Atlantic cod (Gadus morhua), which possesses the pheno- types HbI 11 , HbI 12 and HbI 22 , was described more than 30 years ago (Frydenberg et al. 1965; Sick 1965a,b). The frequency of the two alleles HbI(1) and HbI(2) shows a north–south cline along the Norwegian coast: the frequency of the HbI(1) allele is about 10% in the Barents Sea in Arcto- Norwegian cod, 20–50% along the coast of north-

Physiology of Living in Water

87

88 Chapter 4

10 Depth (m)

6.0 5.5 Anode + 5.0 Cathodic haemoglobins

8 Anodic haemoglobins 4

Expressed haemoglobins

Low n 50 2

Oxygen affinities

K. stewarti R. whero F. malcolmi Fig. 4.7 Structural and functional properties of haemoglobins of nine species of triplefin (Blenniidae) in relation to

B. medius

G. signata

G. capito

F. lapilum

R. decemdigitatus

F. varium

their habitat (preferential depths). The species living in the unstable environment (i.e. rock pools) in the upper layers have a larger number of preferential cathodic haemoglobin components (those migrating towards the negatively charged cathode having isoelectric points, pI, >6.25), with higher oxygen affinities and lower cooperativity (expressed

by the Hill coefficient, n 50 ) as well as a much lower pH sensitivity of oxygen binding (expressed by the Bohr coefficient

D log f= P 50 , D pH

where P 50 is the partial pressure of oxygen at half saturation). Those species living in the deeper water, with less fluctuations in temperature and oxygen availability, had fewer haemoglobins. These were preferentially anodic (pI < 6.25), with a larger potential for allosteric regulation. The genera examined are Bellapiscis (B.), Grahamina (G.), Fosterygion (F.), Ruanoho (R.) and Karalepis (K.). (Source: Brix et al. 1999.)

ern and western Norway, and 70% in the Kattegat and coastal groups as well as between populations (Frydenberg et al. 1965). A similar, though less of coastal cod. Karpov and Novikov (1980) reported

clear, cline can be seen along the North American on the functional properties of the HbI 11 , HbI 12 and east coast (Sick 1965b). According to these publica- HbI 22 components. They suggested that the HbI 22 tions, genetic differences exist between Arctic cod molecule has the highest oxygen affinity and is the

Physiology of Living in Water

most efficient oxygen carrier at low temperatures,

Coping with low oxygen availability

while the HbI 11 molecule has the highest affinity at about 20 °C. Brix et al. (1998a, submitted) and Environmental hypoxia causes a fish to maximize Pörtner et al. (2000b) clearly demonstrate that oxygen transport by cellular adjustments in the

HbI 22 is better fitted to cold temperatures than red blood cells combined with a reduced heart- HbI 11 because it is able to transport more oxygen beat (bradycardia), an increase in cardiac stroke

from the environment to the tissues. This could volume, increased peripheral resistance, and result in a higher growth rate, a suggestion sup- enhanced efficiency of gas exchange linked to ported by length and weight data. However, while increased lamellar recruitment in the gills not excluding this possibility, it could also be a re- (Satchell 1971; Booth 1978). Hypoxia causes the sult of higher oxygen demand in response to cold following: adaptation, compensating for some of the energy

1 reduction of ATP (GTP) production in the cells, loss caused by proton leakage in the mitochondria which in turn changes the Donnan equilibrium, (see above). In both cases the HbI 22 phenotype ap- the passive distribution of solutes over a semiper- pears better fitted for life in cold environments. In meable membrane, causing a decrease in the the temperature range 8–12 °C, where maximal concentration of protons and thus an increase in mean growth rates for all phenotypes have been intracellular pH; reported, there are no differences with respect to

2 increase in ventilation, causing increased oxygen-binding properties. Oxygen binding of all plasma pH and thus intracellular pH; phenotypes is very sensitive to pH. Any tempera-

3 increase in Hb/HbO 2 ratio (chronic hypoxia), ture change would thus greatly affect oxygen causing an increase in intracellular pH. affinities by indirectly changing pH (Brix et al. The reduction in ATP (GTP) and the increase in 1981). Brix et al. (submitted) further showed that intracellular pH increases oxygen affinity, which

the heterozygote, HbI 12 , changed the concentra- thus safeguards oxygen uptake (Weber et al. 1976). tion of haemoglobin components during long- When oxygen availability in water becomes lim- term acclimation to either 4 °C or 12 °C, achieving ited fish have to breathe air.

similar oxygen-binding properties as HbI 11 in the

warmer water and vice versa. This clearly suggest Air breathing Various groups of fish have solved that selection is very important for the evolution the problem of air breathing in different ways, of cod. These results are supported by the work of ranging from simple modification of the gills that Árnason et al. (1998), who found that the stock prevent them from collapsing in air to using the from both the Baltic and Barents Sea are more mouth, special parts of the gut, the swimbladder, related to the North Atlantic stock than with each or even the development of lungs. The role of the other, supporting the hypothesis of a transatlantic gills in oxygen uptake is reduced but they are still flow of genes (Árnason et al. 1992). More detail on the most important site for carbon dioxide elimi- the genetic structure of North Atlantic cod stocks nation. The air-breathing organs in bimodally is given by Ward (Chapter 9, this volume).

breathing fish are well vascularized with an effi-

Temperature not only influences the metabo- cient blood supply. In species using modified gills, lism of fish but also oxygen availability. At high mouth or opercular cavities for air breathing, the temperatures the oxygen concentration in water air-breathing organs are parallel with the gills and will be markedly reduced, which makes it very dif- the blood enters directly into the systemic circula- ficult for fish to meet the extra oxygen demand. We tion. For most other bimodal breathers, blood from refer to this condition as environmental hypoxia, the air-breathing organ passes the gills before and fish have to make significant circulatory and entering the systemic circulation. The lungfish, respiratory adjustments in order to extract suffi- Dipnoi, have separated the pulmonary and cient oxygen from the water.

branchial circulation allowing them, unlike most other air-breathing fishes, to respire with their

90 Chapter 4

lungs and gills simultaneously (Johansen et al. 1990). The ability to triturate, contain, and retain 1968). The tetrapods evolved from this ancient plant material will therefore have a major impact group of fish (see Gill and Mooi, Chapter 2, this on the structure and function of the alimentary volume).

tract, in particular the possible role of gastro-

As water dries up and becomes more and more intestinal microbes in digestion. The material in muddy, the African lungfish (Protopterus) makes a this section is complementary to the chapter bottle-shaped burrow lined by mucus secreted by on growth by Jobling (Chapter 5, this the skin to form a cocoon and the fish becomes tor- volume) and the chapter on the behavioural pid. The nares becomes plugged with mud and the ecology of feeding by Mittelbach (Chapter 11, this fish breathes air through its mouth about once an volume). hour. The lungfish may remain aestivated for more than 6 months and may survive for years in this condition. During aestivation, when ammonia ex-

4.6.2 Carnivorous fish

cretion over the gills is impossible, urea is formed As in other vertebrates the alimentary tract in fish in the liver and accumulates in the blood. Other is divided into the mouth and buccal cavity, the species, like the western Australian Lepidogala- pharynx, the oesophagus, the stomach, the intes- xias salamandroides and the New Zealand mud- tine with the pyloric caeca and related organs minnows (Neochanna), also aestivate during (liver, gallbladder and pancreas), and the rectum periods of drought.

and anus. The alimentary tract is lined by an inner epithelium called the mucosa, underneath which is the submucosa, a layer of circular and longitudi-

4.6 DIGESTION AND

nal muscles called the muscularis, and the serosa.

ABSORPTION

The thickness of the different layers varies in the

4.6.1 Structure and function of the

different parts of the alimentary tract.

alimentary tract Ingested food is sometimes broken down

mechanically in the mouth and pharynx. In the Our knowledge of digestive physiology is based oesophagus, which is highly distensible, the food largely on studies conducted on carnivorous is lubricated by mucus secreted from the mucosa Northern Hemisphere species (Kapoor et al. 1975; before entering the stomach. The stomach in Fänge and Grove 1979; Helpher 1988; Lovell 1989), fishes can be a straight tube, U-shaped, or Y-shaped most of which are freshwater or diadromous taxa with a gastric caecum (Fänge and Grove 1979; such as salmonids (Christiansen and Klungsøyr Helpher 1988; Stevens 1988). Distension of the 1987). Thus, the overall morphology and enzyme stomach activates a cholinergic response, which complement of the alimentary tract appears to be triggers secretion from the gastric mucosa of hy- more or less ‘hard-wired’ to the ‘normal’ diet of the drochloric acid, which decreases pH, and protease fish (Jobling 1998). However, many fish in the trop- enzymes such as pepsin that have a pH optimum of ics and the Southern Hemisphere are herbivorous, 2–4. In the foregut, the caecal tissue or the pancre-

a fact that has been very little considered in the atic tissue, which commonly envelops the caeca, physiological literature (Clements 1997). The low produces a secretion with a pH of 7–9 that contains nutritional value of diets high in fibre requires the trypsin, an enzyme that digests protein at alkaline ingestion and processing of a large volume of food pH. The pancreatic tissue is also the primary site (Stevens 1988). The extra time necessary for for the production of lipase and amylase, which microbial digestion of this refractory material re- digest fat and carbohydrate. Lipase activity has quires the retention of food within the gut for also been found in the caecal tissue and in the extended periods of time, and the ability of herbiv- upper part of the intestine (Chesley 1934). The orous fish to triturate ingested food influences the pyloric caeca may also secrete fluids that serve rate and efficiency of fermentation (Bjorndal et al. to buffer intestinal contents (Montgomery and

Pollak 1988). A muscular valve or sphincter, a fold in the mucous membrane, controls the flow of food into the intestine (Stevens 1988). Assimilation of digested food also takes place in the intestine.

The behaviour and ecology of predatory fish is described in detail in Juanes et al. (Chapter 12, this volume).