The Physiology of Living in Water OLE BRIX

4 The Physiology of Living in Water OLE BRIX

4.1 INTRODUCTION

especially the river drainages of Southeast Asia and South America. About 500 marine species

About 25 000 living species, which include more enter fresh water during their life cycle (see Gill than 50% of all living vertebrate species, belong and Mooi, Chapter 2, Mooi and Gill, Chapter 3 and to a very heterogeneous assemblage of aquatic Metcalfe et al., Chapter 8, this volume). animals called fish (Nelson 1994; Gill and Mooi,

The diversity of adaptation to these habitats Chapter 2, this volume). They have been divided is determined by the evolutionary background of into three major groupings that have been the fish and the physical and chemical charac- separated during the last 500 million years of teristics of water. These characteristics set a evolution. The Agnatha, or jawless vertebrates, are number of constraints on the functional design of primitive fish that evolved in sea water about fish, of which high density, low compressibility, 350–500 million years ago. The ostracoderms, also solvent properties and transparency are the most an ancient lineage, are largely found in freshwater important. deposits. This line is today represented by the

1 The high density of water reduces the effects hagfishes (about 43 species) and lampreys (about of gravity and enables fish to remain suspended in

41 species). A major group of fishes includes the the water column using a minimum amount of Chondrichthyes or cartilaginous fishes, with 800 + energy. Fish cope with buoyancy problems by types of rays and sharks and about 50 or so species applying either dynamic or static lift or a combina- of chimeras, and the Osteichthyes, which includes tion of both. the bony or teleost fishes and contains more than

2 The low compressibility of water strongly in-

20 000 species. The cartilaginous fishes evolved fluences the swimming performance of fish, who like the Agnatha in sea water. The teleost fish have to push large volumes of water aside to move evolved in fresh water 50–100 million years ago. through it. For this purpose they have developed They proliferated into a huge number of species different motor systems, reduced the drag forces which today can be found in almost every conceiv- and the cost of locomotion, and increased the effi- able aquatic habitat, ranging from hot soda springs ciency of respiratory and cardiovascular adapta- where temperatures may exceed 40 °C to the polar tions during swimming. regions under the ice sheet with temperatures

3 The most important characteristic of water is below 0 °C. Despite salt water covering about 70% that it is an almost universal solvent, containing of the Earth’s surface and comprising about 97% complex mixtures of salts, organic compounds and of all water (Horn 1972), as many as 10 000 fish gases. Many of these are essential for life and are species (nearly 40%) live in fresh water. The largest taken up by fish using specialized organs in com- numbers of these are found in the tropical regions, plicated processes of ion regulation, osmoregula-

72 Chapter 4

tion, gas exchange and acid–base balance, or via di- mackerel (Scomber scombrus) which has a body gestion of food.

just slightly heavier than sea water (1.02–1.06 g

4 The transparency of water is very poor. In cm -3 ), while the heavier bonito (Sarda sarda), clear water, light can penetrate to a maximum skipjack tuna (Katsuwonus pelamis) and bullet of 1000 m; however, penetration is usually much mackerel (Auxis rochei) (body densities 1.08–1.09 less than this. Since most food production is

g cm -3 ) have swimming speeds of about 2 BL s -1 . within the photic zone, most fish reside in this None of these species have a functional swim- region, where prey capture depends on good bladder (Jobling 1998). Continuous effort to sup- visibility and well-developed eyes. In the dark port the body by muscular effort alone would be zone of the oceans, however, fish communicate energetically costly (Marshall 1966). Therefore, and capture prey by producing their own light most other fish, except benthic species that rest on using photophores.

the bottom and only swim occasionally, use static In the following sections the physiological lift as a solution to the problem of buoyancy. mechanisms that fish use to cope with these four physical and chemical constraints upon life are

4.2.3 Static lift

dealt with in more detail. Fish reduce their specific gravity in a number of ways.

4.2 BUOYANCY, OR

1 The ratio of heavy to light tissue is reduced by

COPING WITH PRESSURE

minimizing elements of the skeleton, which has a specific gravity of about 3 g cm -3 . Compared with

4.2.1 Defining the problem

terrestrial animals the skeletal elements of fish are Most fish have body densities slightly higher than very much reduced. For example, the skull of fish the specific gravity of sea water (1.026 g cm -3 ). may contain up to 30% lipids, whereas that of Without any lift mechanism they will sink to the mammals rarely contains more than 1% lipid by bottom. Neutral buoyancy allows fish to mini- weight. mize the energetic cost of staying at a particular

2 Replacement of heavy ions (Mg 2 + , SO 2 4 - ) with depth, and thus they are able to allocate more light ions (H + , Cl - , NH 4 + ) is not a very efficient energy for other activities such as feeding, growth, solution for adult fish. However, it occurs during reproduction, hiding and migration.

early development in pelagic eggs (Fyhn 1993; Fish achieve neutral buoyancy and float by Terjesen et al. 1998). Elasmobranchs employ urea using one or both of two physical principles: dy- and trimethylamine oxide (TMAO) as organic namic lift and static lift.

osmolytes to reduce their density. During the early larval stages of pelagic marine bony fish, urea is

4.2.2 produced via both the urea cycle and uricolysis Dynamic lift

(Chadwick and Wright 1999; Terjesen et al. 2000). Dynamic lift is widely used by elasmobranchs and Although present at considerably lower concen- active teleosts such as mackerels and tunas, which trations than in elasmobranchs, this urea could have bodies that are heavier than water. Lift is gen- possibly lower the density of the larvae, which erated by the caudal and pectoral fins acting as lift- need to reach the upper photic zone where feeding ing foils at about the centre of gravity of the fish begins. and depends on a minimum cruising speed to pre-

3 A better solution to the problem is the removal vent the fish sinking. In scombrid and thunnid fish of ions from the body fluids to the medium, a species a direct correlation exists between the den- process called hypo-osmotic regulation. In the ab- sity of body tissues and sustained long-term swim- sence of gills, kidneys and gut, which are hypo- ming speed. Swimming speeds of about 1 body osmotic regulatory organs found only in the adult, length (BL) s -1 have been recorded for the Atlantic ionic regulation requires the presence of other ap-

Physiology of Living in Water

propriate structures. In pelagic eggs, fish larvae cholesterol. The liver of these fish contains up to take up water into the rudimentary gut over the 80% squalene and accounts for up to 25% of body opercular pores just before hatching (Mangor- weight. Eggs of these sharks also contain squalene. Jensen and Adoff 1987).

Some sharks use sub-neutral buoyancy: they

Fish obtain static lift by the use of two different maintain a constant lipid content, which provides materials: lipids and gas. Since gases are much some lift but not enough; they therefore have to more efficient than lipids with respect to providing swim to keep buoyant. lift, fish with swimbladders have no problems in supporting their heavy body components. Fish

Gas

using lipids for static lift have to reduce their spe- cific gravity as outlined above.

Gas is the most efficient material for providing lift, and most teleosts possess gas-filled swimbladders. Swimbladders have sizes that provide neutral

Lipids

buoyancy: about 5% of body volume for marine The main advantage of using lipids as a means of fish and about 7% of body volume for freshwater static lift is that the lift provided varies very little fish. Since the volume of gas is inversely propor- with depth. Thus if a fish is neutrally buoyant at tional to the ambient pressure, which increases by the surface of the sea, it will also remain close to 101 kPa (1 atm) for each 10 m of depth (Boyle’s law), neutral buoyancy at considerable depths. This the swimbladder must have mechanisms for effi- allows the fish to perform fast vertical migrations. cient filling and emptying at different depths. The main drawback in the long term is that fat and Volume changes are much larger near the surface oils may also be used as fuel for sustained swim- than at greater depths. A fish at the surface ming or even as substrates for growth and develop- (101 kPa) halves the volume of its swimbladder ment. Where lipid is the only source of static lift, at 10 m depth (202 kPa), while a fish at 200 m fish will also have great problems adjusting buoy- (2020 kPa) has to descend to 400 m (4040 kPa) to ancy in response to short-term density changes halve the volume. Buoyancy control near the due to feeding and parturition. The most impor- surface will thus be very difficult using a swim- tant lipids are:

bladder, and the complete loss of the swimbladder

1 acylglycerol (fatty acid + glycerol, density or at least a reduction in its importance is often 0.90–0.93 g cm -3 );

seen among surface-dwelling pelagic fish. A simi-

2 wax esters (long-chain fatty acids + long-chain lar loss of the swimbladder is found among many fatty alcohols, density ~0.87 g cm -3 );

bottom-dwelling species, where buoyancy control

3 squalene (density ~0.86 g cm -3 ).

is of no importance.

In general, lipid stores may contribute relatively The swimbladder arises during ontogeny from little to buoyancy in the majority of bony fish

a diverticulum in the roof of the foregut. In species. Triglycerides present in the muscles or the physostomatous (Greek physa, bladder; mesenteric fat as a consequence of metabolic lipid stoma , mouth) teleosts the connection between storage may provide some lift for scombrids and the foregut and the swimbladder is maintained, as herring (Clupea harengus). Wax esters in muscles, in elopomorphs and clupeoids, and gas can enter or swimbladder and bones may play some role in

be released via this duct. In the more advanced many families of mesopelagic teleosts. Squalene, physoclistuous (Greek kleistos, closed) teleosts which is an extremely light unsaturated hydrocar- this connection has been lost or, for some species, bon, is very important for providing lift, especially closed during development after allowing the in elasmobranchs and particularly pelagic sharks, larvae to fill the swimbladder for the first time. which have large livers and small pectoral fins.

Three major problems need to be solved Squalene is formed by the condensation of iso- before the swimbladder can be used for buoyancy prene units in the metabolic pathway leading to regulation: (i) release of gas from the swimbladder;

74 Chapter 4

(ii) maintaining gas inside the swimbladder; ( <15 m) to nearly 400 mg cm -2 in deep water (iii) filling the swimbladder with gas. Gas can be ( >1000 m, pressure >10 100 kPa). The oval chamber released by two mechanisms: via the pneumatic can be closed off by nervous control, and gas re- duct into the gut whilst ascending/diving (physo- lease via the circulatory system is regulated in an stomes), or into the circulation via oval chamber advanced countercurrent system called the rete control by nervous stimulation (physostomes/ mirabile (Fig. 4.1). The rete consists of a tight bun- physoclists).

dle of afferent and efferent capillaries surrounding

The walls of the swimbladder are impermeable each other. This system may be diffuse, such as the to gas due to a thin lining of overlapping guanine micro-rete in salmonids, or it may be at some dis- crystals and other purines. The density of purines tance from the gas gland as in physostomes. In varies from about 20 mg cm -2 in shallow waters physoclists the length of the rete is directly corre-

Oval patch

O 2 O 2 Lactate, H +

HCO 3 HCO – 3 HCO – 3 +H +

CO 2 , Triose

Swim Guanine crystals

ROOT ON

HbO 2 O 2 Hb +

Lactate: salting out N 2 N 2

Gas gland

PPS, pentose phosphate shunt TCA, tricarboxylic acid cycle

Fig. 4.1 Summary of the main processes involved in filling the swimbladder with gas. The blood entering the descending rete is acidified with lactate, H + and carbon dioxide from the gas gland. This causes the release of oxygen from haemoglobin via the Root effect (see text). Oxygen and nitrogen, which have been salted out, diffuse into the swimbladder. Multiplication of the solutes in the descending rete is obtained by diffusion from the ascending rete. Oxygen is retained in the rete because the process of binding oxygen is slower than the release of oxygen from haemoglobin (Hb).

lated with the depth at which the fish live and the gas pressure in the swimbladder.

Steen (1971) solved the puzzle of how the swim- bladder of the eel (Anguilla anguilla) is filled with gas against huge pressure gradients. The gas-filling mechanism is linked to the countercurrent struc- ture of the rete, which allows gas pressure, and therefore volume, to ‘multiply’ within the swim- bladder (Fig. 4.1). Lactate and carbon dioxide se- creted from the gas gland near the luminal end of the rete decrease blood pH, which results in a fast unloading of oxygen from a very pH-sensitive haemoglobin component in the blood and thus an increase in the oxygen partial pressure. This so- called Root-off mechanism is accompanied by a salting-out mechanism, which allows more oxygen, but also other gases like nitrogen, to accu- mulate. In this way oxygen, and also nitrogen, dif- fuse into the swimbladder. Since lactate and carbon dioxide diffuse from the efferent capillaries to the afferent capillaries by following a downhill gradient like oxygen, pH again increases in the efferent capillary leaving the rete. Oxygen now binds again to the haemoglobin component and the oxygen partial pressure decreases. However, this process, which is referred to as the Root-on mechanism, is much slower than the root-off mechanism, allowing a fraction of the oxygen content to remain within the system.