LENGTH–WEIGHT RELATIONSHIPS, AND INDICES OF CONDITION AND GROWTH

5.6 LENGTH–WEIGHT RELATIONSHIPS, AND INDICES OF CONDITION AND GROWTH

The length of a fish can be measured more easily and accurately than weight under field conditions, so length measurements are the most convenient method of growth expression. Frequently, infor- mation about fish weight may be required and this may be estimated from length if the length–weight relationship is known for the fish population under study. The length–weight relationship is generally expressed by the equation:

W = cL m (5.9) or log W = log c + m log L

(5.10) where W is weight, L is length, and c and m are con-

stants. The numerical value of m is nearly always between 2.5 and 3.5, and is often close to 3 (Bagenal

Rates of Development and Growth

107

Chapter 5

and Tesch 1978; Weatherley and Gill 1987; relationship is close to 3, the condition index is Anderson and Neumann 1996; Sutton et al. 2000). usually calculated as Fulton’s condition factor (K): When m = 3, the body is increasing in all dimen- sions in the same proportions as it grows. How-

(5.12) ever, the relationships of the different body dimensions often change with respect to each In most cases K will be satisfactory for analysing other as the fish grows, so body shape changes as differences in condition related to sex or season the fish increases in length. This means that m will when the fish used for comparison are of approxi-

K = IW IL 3 [ ] ¥ 100

be greater than 3 when a fish becomes more rotund mately the same length; however, if the length as it increases in length, and less than 3 if the fish range is large, spurious results will be generated if becomes ‘slimmer’ as it increases in body length.

m differs from 3.

As a fish grows, changes in weight are relatively Changes in growth rate and condition are ac- greater than changes in length, due to the approxi- companied by changes in the biochemical com- mately cubic relationship between length and position of the body tissues; the most marked weight. Thus, measurement of change in weight changes occur in percentages of lipids and body may provide a more precise measure of growth moisture, whereas the relative proportion of pro- over short periods of time. However, a change in tein tends to vary to a lesser extent (Weatherley weight may be a very transient indicator of growth, and Gill 1987; Love 1988; Hislop et al. 1991; because weight can be both gained and lost. Thus, Shearer 1994; Brett 1995; Couture et al. 1998; when fish are feeding and growing well, an individ- Dutil et al. 1998; Sogard and Olla 2000; Sutton ual may have a greater than usual weight at a par- et al. 2000). As a consequence of this, there is a ticular length. On the other hand, when feeding strong negative correlation between the percent- conditions are poor, the fish may lose weight and ages of body lipids and body moisture (Fig. 5.5), and

be light for their length. Thus although length is this relationship seems to hold under different the primary determinant of the weight of a fish, conditions of feeding, growth and gonad develop- there can be wide variations in weight between ment (Weatherley and Gill 1987; Love 1988; fish of the same length both within and between Hislop et al. 1991; Sogard and Olla 2000; Sæther populations. Thus, length–weight relationships and Jobling 2001). Thus, temporal changes in the can be used to assess the ‘well-being’ of individual condition of the fish, related to the deposition and fish. Since it is not particularly easy to interpret mobilization of energy reserves, will be reflected and directly compare the constants in the by movements up and down the lipid–moisture (or length–weight relationship, a series of indices of fat–water) regression line. condition have been developed in an attempt to

Attempts have been made to use a range of circumvent some of the problems.

metabolic variables to obtain an assessment of

The length–weight relationship given by the condition and recent growth history of wild equation 5.9 can be rearranged to give an index of fish (Busacker et al. 1990; Houlihan et al. 1993; condition, or condition factor (CF):

Couture et al. 1998; Dutil et al. 1998). The meta- bolic indicators monitored include concentrations

(5.11) of nucleic acids, and enzymatic indicators of aero- bic and glycolytic capacities of muscle, liver and where IW and IL are the weight and length of an in- intestine. Tissue RNA : DNA ratio has often been dividual fish respectively, and m is the exponent in used both to assess fish condition and as an indi- the length–weight relationship. Alternatively, the rect measure of recent growth. It has been argued condition of an individual fish can be calculated as that because the DNA content of a cell is relatively IW /EW, where EW is the ‘expected weight’ of the constant, and RNA content varies with the rate of fish calculated from the length–weight relation- protein synthesis, the ratio of RNA to DNA pro- ship. In practice, because m in the length–weight vides an index of protein synthetic activity and

CF m = [ IW IL ] ¥ 100

Rates of Development and Growth

78 biochemical indices, such as protein synthesis, tis- sue amino acid incorporation and RNA : DNA

76 ratios, used for the assessment of condition and short-term changes in fish growth. Intestinal mi-

74 tochondrial enzyme activity also seems to corre- late with rates of feeding and growth (Couture et al.

1998; Dutil et al. 1998). Nutrient absorption by the

72 enterocytes of the gut involves active transport; this relates to Na + /K + ATPase activity, and

70 the enterocytes are mitochondria-rich cells in Percentage water (moisture)

which ATP is produced aerobically (Ferraris and

68 Diamond 1989; Hirst 1993). Consequently, links between intestinal mitochondrial enzyme activ-

66 ity, nutrient absorptive capacity and growth might

12 14 be expected.

Percentage fat (lipid) Prolonged fasting affects white glycolytic mus- cle more than oxidative muscle, and when food

Fig. 5.5 The percentage of body fat (lipid) and water deprivation lasts a period of weeks there are often (moisture) in samples of turbot, Scophthalmus

maximus , at the start of a growth trial (䊐; weight c.200 marked declines in muscle sarcoplasmic proteins

g), after feeding for 12 weeks (weight c.450 g) on either a and glycolytic enzyme activities (Love 1988; high-fat (䊊, 25% lipid) or low-fat (䉭, 17% lipid) diet, and

Couture et al. 1998; Dutil et al. 1998). Conversely, then after 8 weeks (weight 550 g) of dietary reversal (i.e.

during periods of intense feeding the activity of 䊉 , high-fat to low-fat diet; 䉱, low-fat to high-fat diet).

white muscle glycolytic enzymes, such as phos- The ‘fat–water’ line is described by the following regres-

phofructokinase, pyruvate kinase and lactate de-

hydrogenase, may be positively correlated with (Source: data from Sæther and Jobling 2001.) feeding and growth rates. Activities of mitochon-

sion: %water = 80.11 - 1.08 %fat (n = 44; R 2 = 0.866).

drial enzymes, such as cytochrome c oxidase and hence growth (Bulow 1987). In addition to citrate synthetase, in the oxidative red muscle ap- RNA : DNA ratio, tissue RNA content and concen- pear to be poor predictors of growth. This is not sur- tration and RNA : protein ratio have been used as prising given the fact that during fasting it is the indirect indices of fish condition and growth. In white muscle proteins that are mobilized, whereas studies with fish larvae it is usually the RNA : the aerobic red muscle seems to be preferentially DNA ratio that has been used as the growth corre- conserved (Love 1988). The high activities of gly- late, and results of a study on cod larvae provide ev- colytic enzymes in the muscle and their sensit- idence that the analysis of nucleic acids may ivity to food supply seem to make them useful provide valuable information about the recent indicators of condition and growth, with the moni- growth and condition of individual larvae (McNa- toring of changes in lactate dehydrogenase activity mara et al. 1999).

appearing to be particularly useful (Couture et al. Another biochemical component with the po- 1998; Dutil et al. 1998). tential to correlate with recent growth history is ornithine decarboxylase activity (Benfey 1992; Benfey et al. 1994). Ornithine decarboxylase is the

5.7 ENERGY BUDGET

first, and rate-limiting, enzyme in the biosynthesis

AND BIOENERGETICS:

of polyamines, compounds essential for the

ENERGY PARTITIONING

biosynthesis of nucleic acids and proteins. Thus, it

AND STORAGE

might be expected that changes in ornithine decar- boxylase activity would precede changes in other In simple terms, growth is the change that results

Chapter 5

from the difference between the food that enters The proportion of the food energy lost in the faeces the body and the waste materials that leave it and nitrogenous excretory products may also be (Brett 1979, 1995; Cho et al. 1982; Weatherley and influenced to some degree by the amount con- Gill 1987; Adams and Breck 1990; Elliott 1994; sumed, fish size and temperature (Elliott 1994; Jobling 1994, 1997). This can be represented by:

Jobling 1994).

The metabolic term, M, encompasses fasting pC=M+G

(5.13) metabolism, activity metabolism and feeding me- tabolism. The latter is the metabolism linked to or

the processing of nutrients and the elaboration of tissues. Metabolic rates are usually assessed by an

G=pC-M (5.14) indirect method involving the measurement of oxygen consumption and the application of an where C is the amount of food consumed, p is a co- oxycalorific coefficient (1 ml O 2 =

19.4 J) (Adams efficient indicating the availability of nutrients or and Breck 1990; Cech 1990; Jobling 1994; Brett food energy, M represents catabolic losses (metab- 1995). In an expanded model each metabolic com- olism) and G is the anabolic component, the nutri- ponent will be described using a separate mathe- ents or food energy retained as growth. Implicit in matical function, which will include an allometric this energy budget equation is the dependency of term to account for size effects and will also con- growth on consumption, so the intake of food tain a temperature function: energy is the pacemaker of growth. However, the

increase in growth with increased food intake may M = aW b e cT e dS + eC (5.16) not be monotonic (Brett 1979; Weatherley and Gill 1987; Elliott 1994; Jobling 1994, 1997).

where W is body weight, S is swimming speed and Temperature is the most all-pervasive environ- a–e are constants. The weight exponent, b, for mental factor that influences aquatic organisms fish is about 0.8, and the temperature constant, c, and, via its influences on feeding and metabolism, will generally lie within the range 0.04–0.07, cor-

it affects growth. Increases in temperature initially responding to a Q 10 of 1.5–2.0. Metabolic costs lead to an increase in food consumption; feeding associated with activity show an approximately peaks at some intermediate temperature, and then exponential increase, whereas the metabolic costs declines precipitously as the temperature contin- associated with food processing, tissue synthesis ues to rise (Fig. 5.6). It may be difficult to describe and energy storage are proportional to the quantity the influence of temperature on food intake in of food consumed. mathematical terms, but Hogendoorn et al. (1983)

The difference between the rate–temperature suggested that Hoerls function could be used to de- curves for feeding and metabolism gives an indica- scribe the effects of temperature on food intake of tion of the resources available for growth under fish provided with unrestricted rations:

different temperature conditions, assuming that p represents a constant proportion of C across

C = aT b e cT (5.15) temperatures. The plotting of the growth rate– temperature relationship indicates that growth where T is temperature and a, b and c are

rate reaches a peak at an intermediate temperature constants.

(Fig. 5.6), with the optimum temperature for The proportion of the ingested energy lost as growth being slightly lower than that at which faecal and excretory wastes depends upon the na- food consumption rate reaches its maximum. Re- ture of the diet (Cho et al. 1982; Jobling 1994), so lationships of this type have been obtained in a the value of p differs between fish species that number of growth studies conducted on fish (e.g. differ in trophic habits. For carnivorous species a Brett 1979; Hogendoorn et al. 1983; Woiwode and value of p close to 0.8 may be appropriate, but for Adelman 1991; Xiao-Jun and Ruyung 1992; Elliott

Rates of Development and Growth

high-latitude environments, and there may also be changes in composition that are directly related to body size (Weatherley and Gill 1987; Love 1988; Hislop et al. 1991; Shearer 1994; Jørgensen et al. 1997; Van Pelt et al. 1997; Sogard and Olla 2000; Sutton et al. 2000). In other words, fish tend to ac- cumulate storage lipids during the summer growth season, and the reserves are then mobilized to provide metabolic fuel during the winter, when

food consumption is low, and to support gonadal Ingestion rate ( )

(A)

Metabolic rate ( )

development (Brett 1979, 1995; Weatherley and Gill 1987; Love 1988; Elliott 1994; Jobling 1994; Jørgensen et al. 1997).

Upper

The feeding and growth responses seen in high-

thermal

latitude fish during the summer months resemble

limit for

those observed amongst fish that have been de-

prived of food under laboratory conditions: in- Growth rate

growth

(B)

creased food intake, or hyperphagia, rapid growth and improvement in condition, and the repletion

Temperature of energy reserves (Weatherley and Gill 1987;

Broekhuizen et al. 1994; Jobling 1994; Jobling and Fig. 5.6 Rate–temperature curves illustrating the

Johansen 1999; Sæther and Jobling 1999). It is usu- effects of temperature on rates of ingestion, metabolism

and growth. Note that the temperature at which ally fish that are in poor condition that show

ingestion rate reaches its maximum (A) is a few degrees the greatest response (Fig. 5.7)(Jobling et al. 1994). higher than the optimum temperature for growth (B).

Thus, seasonal cycling may relate to a regulation of (Source: from Jobling 1997.)

the balance between reserves held in the form of lipid depots and mobilizable parts of the muscula- ture and structural components such as the skele- ton and circulatory and nervous tissue. Shifts in

some authors have reported that the temperatures the balance would be reflected in relative changes at which feed intake and growth peak are almost in major chemical components that constitute the coincident (e.g. Larsson and Berglund 1998; tissues, for example in the relative proportions Forseth et al. 2001)

of body lipid and moisture (cf. Fig. 5.5). Large The growth term, G, encompasses somatic shifts would be expected to induce compensatory growth related to tissue elaboration, the storage changes in feeding and energy accumulation. Fol- and mobilization of energy reserves, and reproduc- lowing restoration of the balance between com- tive growth; the latter may be difficult to assess ac- partments, rates of feeding would be predicted to curately for wild fish. Thus, the changes relating to decrease and rates of growth and energy accumula- growth over time include the energy deposited as tion would slow (Broekhuizen et al. 1994; Jobling protein and lipid in the soma, the changes in the and Johansen 1999). This presupposes that specific size of the energy storage depots and the energy di- metabolic signals arising from different tissues are rected towards the production of gametes. Protein integrated within the central nervous system, en- growth may be positive throughout much of the abling continuous assessment of the status of the year but quantities of lipids, and gonad sizes, may energy reserves (reviewed by Kiess et al. 1999; undergo marked fluctuations, including large Magni et al. 2000). net losses at certain times of the year. Seasonal

In studies of fish growth the energy content changes in body composition will usually be most of the tissues is usually determined by bomb In studies of fish growth the energy content changes in body composition will usually be most of the tissues is usually determined by bomb

6 pressure, and heat production is measured. This provides a measure of the heat of combustion,

or gross energy, of the sample. Alternatively, the

4 chemical composition of the sample can be meas- ured using a series of standard laboratory methods

Weight (kg) (Osborne and Voogt 1978; AOAC 1990; Busacker et al. 1990), and conversion factors for the com-

2 plete oxidation of proteins, lipids and carbohy- drates used to estimate gross energy content.

6 weeks

Complete oxidation of proteins, lipids and carbo-

4 hydrates yields approximately 24, 39 and 17 kJ g respectively, although the energy yield from fish

lipids may be slightly lower than that from lipids of

3 terrestrial origin. The chemical analysis of the major components (moisture, protein, carbohy-

2 drates, lipids and ash) of animal tissues is usually Weight (kg)

termed a proximate analysis. 1

A characteristic of the growth of many fish species in nature is the marked seasonal variabil-

0 ity. This seems to be almost universal outside of

Start

the tropics and is by no means rare within them; in the tropics and subtropics the variations in fish growth may be most closely related to seasonal

2 changes in rainfall. It is those species that live at high latitudes that exhibit the greatest seasonal fluctuations in feeding and growth. These seasonal

Weight (kg)

1 growth cycles are often attributed to the temporal changes in food availability that may occur in tem- perate and polar waters, but even in the absence of

0 changes in food availability low water tempera- Group

1 2 3 4 5 6 tures during the winter months would be expected Condition < 0.80.8 –0.9 > 0.9

to restrict growth (Fig. 5.6). However, the seasonal (start)

cycle of growth is not always, and perhaps never, Length (cm)

wholly under temperature control; the growth of (start) several high-latitude fish species seems to track

Fig. 5.7 The effects of initial length (L cm) and the seasonal cycle of photoperiod (Brett 1979; condition (K = [W/L 3 ] ¥ 100) on weight (W) change in

Woiwode and Adelman 1991; Jobling 1994; Boeuf groups of Atlantic cod, Gadus morhua, during 18 weeks

and Le Bail 1999). This comes particularly to the of growth. Note that the cod that were in the poorest

fore when the fish are exposed to constant temper- condition at the start displayed the highest rates of

ature and unrestricted food supply. It is possible weight gain, and that at 18 weeks the body weights

attained by cod within each initial length group were that photoperiod acts to synchronize an endoge-

similar. The boxes indicate 50% of the ‘population’ and nous growth rhythm with prevailing environmen- the bars the 95% confidence limits. (Source: from Jobling

tal conditions. In this case photoperiod acts as a et al. 1994.)

synchronizing timing signal, or zeitgeber. The re- sponse to photoperiod would be expected to be marked amongst high-latitude species, because it

Rates of Development and Growth

is at these latitudes that photoperiodic signals are potential. Thirdly, there may be compensatory strongest and aquatic habitats are most variable on mechanisms that operate to counteract the

a seasonal basis. However, because the natural sea- negative effects of low temperature and a short sonal variations in food availability, temperature growth season on the growth of fish that inhabit and daylength tend to follow similar cycles, it may high-latitude environments. not be easy to distinguish the effects of each vari-

There are two basic models of how compensa- able on growth and energy partitioning.

tory mechanisms might be expressed. One model relates the compensatory mechanisms to local thermal adaptation, such that growth rates are

5.8 maximized at temperatures commonly experi- GROWTH AT

enced by fish within their native environment.

DIFFERENT LATITUDES:

According to this model there would be differences

MODELS OF GROWTH

in optimum temperatures for growth amongst

COMPENSATION

populations inhabiting different thermal environ- ments, and the compensation should be accom-

Many species of fish have wide geographic distri- panied by a change in preferred temperatures (Fig. butions; populations of these species occur at

5.8) (Jobling 1997). The second model focuses on different latitudes and inhabit environments that latitudinal differences in seasonality rather than differ in both mean annual temperature and length temperature per se (Conover 1990, 1992; Conover of the growing season. For many of these species and Schultz 1995). In this model, high-latitude fish the annual growth increment is lower for fish have a higher capacity for growth to compensate from higher latitudes than for those living at low for short growing seasons: latitudinal compensa- latitudes, but the differences appear to be less tion is observed as an elevation in the growth pronounced than expected from the differences in rate–temperature curve (Fig. 5.8). According to temperature and growth conditions experienced this model, genetic and environmental influences by the different populations (Conover 1990, 1992). oppose one another along the gradient of decreas- For example, Conover (1990, 1992) provided ing length of the growing season, i.e. the fastest- evidence that there were minimal differences in growing genotypes are found in environments size at the end of the first growing season for that have the most depressive effect on growth several species of fish that occur on the eastern (Conover and Schultz 1995). seaboard of North America: Atlantic silverside

There are two ways in which these models (Menidia menidia), American shad (Alosa sapidis- could be tested. One method involves common- sima ), striped bass (Morone saxatilis) and mummi- garden experiments in which fish from different chog (Fundulus heteroclitus). There are three ways populations are reared under the same tempera- in which such a situation could arise, which are ture range, and growth rate–temperature curves not mutually exclusive. Firstly, size-selective are plotted for each test population (e.g. Jonassen mortality could be more pronounced in high- et al. 2000). The second method involves recipro- latitude populations leading to survival of only cal transplants, i.e. representatives from the differ- the largest fastest-growing individuals, whereas ent test populations are reared in each of the

a greater proportion of the slower-growing fish original habitats in order to examine the (pheno- might survive at lower latitudes: the net result typic) responses of the different populations would be little or no difference in mean size of the (prospectively different genotypes) to a combina- fish at the end of the growth season. Secondly, tion of environmental influences. growth of fish in the populations at low latitude

The results of transplantation experiments might be subject to greater constraint by food have been equivocal, but when reared under the availability, so that fish in these populations grow same conditions fish from high-latitude environ- at rates substantially below their full physiological ments may grow faster than conspecifics from

Chapter 5

(a) both a higher growth capacity and a lower opti- mum temperature for growth than did halibut from lower-latitude populations. Additional evi- dence that there may be an elevation of the growth rate–temperature curve in fish from high-latitude populations has been obtained in studies conduct-

ed over more limited temperature ranges (Schultz et al. 1996; Conover et al. 1997; Brown et al. 1998; Imsland et al. 2001). Thus, growth compensation

Growth rate (b) across the geographic range of a species may not be based simply on genotype–environmental temper- ature interactions, and it has been hypothesized that latitudinal growth compensations may have evolved to offset the disadvantages of being small at the end of the growing season (Conover 1990, 1992).

Although the ability to grow rapidly within a short growing season would clearly be advanta- geous for fish in high-latitude environments, there

Temperature would also need to be forces operating in a negative Fig. 5.8 Rate–temperature curves illustrating two ways

direction to enable latitudinal variation in growth- in which compensatory adjustments could be made to

rate capacity to be maintained (Conover and counteract the effects of environmental differences on

Schultz 1995). Such forces might, for example, re- growth. (a) The rate–temperature curves are displaced

late to increased incidences of developmental de- in relation to each other; fish from low-temperature

formities or to increased metabolic costs, or could environments have a lower optimum temperature for

growth, and grow faster at low temperatures, than do encompass trade-offs involving negative cor-

fish from warm-water populations (thermal adaptation). relations between growth capacity and disease (b) Compensation is envisaged to occur by means of

resistance, or the ability to withstand prolonged an elevation of the rate–temperature curve; fish with

periods of food shortage. Differences in metabolic the highest growth capacity are found in environments

rate related to latitude of occurrence have often that have the greatest inhibitory effects on growth

been reported, and the metabolic compensations (countergradient variation). Bars indicate the zones

have usually been interpreted as being a response of thermal preferenda predicted for fish from different

environments. (Source: from Jobling 1997.) to temperature (Cossins and Bowler 1987). The po- tential benefits of metabolic compensation in rela- tion to temperature are not immediately clear, but

lower latitudes. This would tend to call into ques- there are links between metabolic rate and the tion the idea that there is a marked downward ability to maintain activity and growth (for dis- shift in the optimum temperature for growth in cussion see Hochachka 1988; Clarke 1991, 1993, high-latitude populations (Fig. 5.8). Results from 1998). Consequently, an elevated metabolic rate some common-garden experiments designed to may be a prerequisite for exploitation of food test growth rate–temperature responses add resources over a short growth season. Thus, the support to this: optimum temperatures for growth possibility arises that differential metabolic costs of different populations have been found to be might represent a trade-off leading to the mainte- similar (McCormick and Wegner 1981; Conover nance of latitudinal variation in growth-rate and Present 1990). However, Jonassen et al. (2000) capacity. Interactions of this sort would have con- reported that juvenile halibut (Hippoglossus hip- sequences for bioenergetic modelling, because it is poglossus ) from a high-latitude population had usually assumed that such models can be con- lower latitudes. This would tend to call into ques- there are links between metabolic rate and the tion the idea that there is a marked downward ability to maintain activity and growth (for dis- shift in the optimum temperature for growth in cussion see Hochachka 1988; Clarke 1991, 1993, high-latitude populations (Fig. 5.8). Results from 1998). Consequently, an elevated metabolic rate some common-garden experiments designed to may be a prerequisite for exploitation of food test growth rate–temperature responses add resources over a short growth season. Thus, the support to this: optimum temperatures for growth possibility arises that differential metabolic costs of different populations have been found to be might represent a trade-off leading to the mainte- similar (McCormick and Wegner 1981; Conover nance of latitudinal variation in growth-rate and Present 1990). However, Jonassen et al. (2000) capacity. Interactions of this sort would have con- reported that juvenile halibut (Hippoglossus hip- sequences for bioenergetic modelling, because it is poglossus ) from a high-latitude population had usually assumed that such models can be con-