Ontogeny of cannibalism in larval and juvenile fishes with special ...

Chapter nine 

Ontogeny of cannibalism 

in larval and juvenile 

fishes with special 

emphasis on Atlantic cod 

Arild Folkvord 

9 .1 INTRODUCTION 

Cannibalism can be defined as : "the act of killing and consuming the whole, 

or major part, of an individual belonging to the same species, irrespective of 

its stage of development" (Smith and Reay, 1991) . It has been documented 

in a wide range of taxa, including Pisces (Smith and Reay, 1991 ; Elgar and 

Crespi, 1992) . Cannibalism is encountered among most of the well-studied 

teleost families, and is classified according to the developmental stage of 

prey, genetic relationship of cannibal to prey, and/or the age relationship of 

cannibal and prey (Smith and Reay, 1991) . In this chapter intracohort 

cannibalism is defined as cannibalism involving members of the same year 

class, and intercohort cannibalism as cannibalism involving members of 

different year classes . Cannibalism among similar-aged individuals within a 

year class (in culture, for example) is termed coeval cannibalism . Aggressive 

behaviour may be a precursor of cannibalism, but inflicted mortality 

without subsequent ingestion of the victim is not considered as cannibalism 

in this context (Hecht and Pienaar, 1993) . 

Early Life History and Recruitment in Fish Populations . 

Edited by R . Christopher Chambers and Edward A . Trippel . 

Published in 1997 by Chapman & Hall, London . ISBN 0 412 64190 9 .

252 . Ontogeny of cannibalism in larval and juvenile fishes 

Table 9 .1 List of recent reviews of cannibalism in fish and amphibians . Relevant 

contributions in book reviews are listed under the book editors 

Author(s) Taxa Emphasis 

Polis (1981) Several Evolution, population dynamics 

Hausfater and Hrdy (eds) (1984) Several Infanticide, filial cannibalism 

Dominey and Blumer Pisces Systematic overview, filial 

cannibalism 

Simon Amphibia Systematic overview, evolution 

Polis and Myers (1985) Amphibia Systematic overview (including 

reptiles) 

Smith and Reay (1991) Pisces Systematic overview 

Elgar and Crespi (eds) (1992) Several Systematic overview, ecology, 

evolution 

Elgar and Crespi Several Systematic overview, ecology, 

evolution 

Dong and Polis Pisces Population dynamics, foraging 

Sargent Pisces Filial cannibalism, modelling 

FitzGerald and Whoriskey Pisces Filial cannibalism, ecology 

Crump Amphibia Systematic overview, ecology 

Hecht and Pienaar (1993) Pisces Larviculture 

Cannibalism in fish is of special concern because it can influence both 

aquaculture production and fisheries . Several review papers and books 

have recently been published on the topic (Table 9 .1) . This review empha- 

sizes the role of cannibalism in the pelagic environment . Some of the 

processes involved in cannibalism among amphibian larvae in ponds 

parallel those present in fishes, and some references from this field are 

included as well . In both these groups, cannibalism is mostly a gape- 

limited process without manipulation of the prey by external limbs . 

Finally, this review is biased towards case studies from extensive juvenile 

production and fisheries . In both these systems, temporary food shortage 

is expected to occur, in contrast to ongrowing under intensive aquaculture 

conditions, where cannibalism can be significantly reduced by satiation 

feeding (Hecht and Pienaar, 1993) . 

Atlantic cod, Gadus morhua, is one of the most important species in world 

fisheries . Large efforts have recently been made to produce juvenile cod 

extensively for aquaculture and sea ranching purposes . Many of the 

examples are therefore taken from this species . Observations of cannibalism 

in cod in outdoor enclosures were recorded in the late 1800s, and recent 

experimental studies have confirmed this cannibalistic propensity (Howell, 

1984) . Due to the lack of other plausible causes of mortality, cannibalism 

was hypothesized to be responsible for the apparent density-dependent 

c 

m 

0 

U) 

350 

300 

250 

d 150 

!0 

200 

R 100 

N 

Ontogeny of coeval cannibalism 

N 

- , 

.g 

E 

3 

50 

Z o - , - - • I - - - I . 

0 1000 2000 3000 4000 5000 

Numbers at metamorphosis (thousands) 

. . . , . 1 

Fig . 9 .1 Numbers of metamorphosing cod (age 35-40 days) and corresponding 

number of juveniles harvested (about age 100-140 days) from various ponds 

(separate symbols for different ponds) . Lines represent 1%, 10% and 100% survival 

between the two periods . 

mortality (1 .5-5% day- ) after metamorphosis in extensive juvenile 

production units (Fig . 9 .1 ; Oiestad, 1985) . Cannibalism has been 

confirmed by stomach analyses in juvenile rearing ponds (own unpublished 

data), and similar reports of cannibalism in the field are well documented 

(Bogstad et al., 1993) . Knowledge of the mechanisms underlying cannibalism 

is thus essential to improve juvenile production of cod and other 

species, and to obtain a better understanding of the dynamics in natural 

populations . 

9.2 ONTOGENY OF COEVAL CANNIBALISM 

Larval stage 

Cannibalism has not been observed among early cod larvae in the laboratory 

(Howell, 1984 ; own observations) . This is not surprising because the 

larval mouth height is significantly smaller than the larval body height at 

this stage (average mouth height is 0 .2-0 .4 mm at first feeding and 

average body height (including yolk sac) is 1-1 .2 mm) (Fig . 9 .2(A) ; 

Wiborg, 1948 ; Knutsen and Tilseth, 1985) . Typical widths of common 

prey organisms ingested during the first days of exogenous feeding are 

0 .1-0 .3 mm (Ellertsen et al ., 1984) . The possibility of coeval cannibalism 

is further decreased by the relatively low initial size variability commonly 

253

2 5 4 Ontogeny of cannibalism in larval and juvenile fishes 

0 

a 

0.5- 

3 .0 

2.5 - 

2.0- 

1 .0 

B 

o + 

I 1 f 

5 

4 

I 

3 

6 ' ' 

5 10 20 40 80 160 

Standard length (mm) 

Fig . 9 .2 (A) Size-specific mouth height (solid curve) and body height (dashed 

curve) of Norwegian coastal cod (Otters and Folkvord, 1993) . Average values of 

mouth' height are denoted by + for Arcto-Norwegian cod (Wiborg, 1948) and by 

squares for Pacific cod, Gadus macrocephalus (Shirota, 1970) . (B) Lowest possible 

predator :prey ratios based on morphological relations (mouth height of cannibal 

= body height of prey) . Data on cod (from Fig . 9 .2(A) ; line 1, Otters and 

Folkvord, 1993), koi carp (line 2, van Damme et al., 1989), walleye pollock (line 

3, Sogard and Olla, 1994), sharptooth catfish (line 4, Hecht and Appelbaum, 

1988), sea bass (line 5, Parazo et al ., 1991) and pike (line 6, Bry et al ., 1992). 

observed among coeval conspecifics after hatching (Knutsen and Tilseth, 

1985 ; Folkvord et al ., 1994b) . Cannibalism is also more common during 

periods of hunger and starvation (Folkvord, 1991), and the cod larvae are 

usually not food limited during the transition to exogenous feeding in the 

I 


Table 9 .2 Ontogeny of coeval cannibalism of cod in enclosures 

Stage Mechanism/attribute Cannibalism 

Larval, 4-10 mm Low initial size variation Low 

Food limitation uncommon 

Relatively small mouth ; yolk sac initially large 

Metamorphosis, Increasing size variation ; zooplankton energy High 

12-30 mm 

unevenly distributed in size fractions 

Food limitation common 

Relatively large mouth 

High growth rate 

Incomplete weaning, starvation 

Stomach not fully developed 

High density, patchy distribution 

Juvenile, Reduced growth rate Low 

50-150 mm Lower susceptibility to starvation 

Relatively small mouth 

Greater feeding flexibility 

Completed weaning 

Fully functional stomach 

Large relative size difference 

High 

juvenile production enclosures (Blom et al., 1991 ; Folkvord et al ., 1994b) . 

Thus it is reasonable to assume that coeval cannibalism among cod larvae 

in the laboratory and in enclosures is insignificant during the early larval 

stage (Table 9 .2) . 

The larvae of freshwater fishes are generally larger and more developed 

at hatching than marine fish larvae (Balon, 1984) . It is not surprising 

therefore that coeval cannibalism in freshwater species has been reported 

to take place shortly after initiation of exogenous feeding . In the koi carp, 

Cyprinus carpio, cannibalism commenced one week after onset of feeding, 

and was highest the following three weeks (van Damme et al ., 1989) . 

This is presumably partly due to the relatively large mouth of this species 

during this period (Fig . 9 .2(B)) . In African sharptooth catfish, Clarias gariepinus, 

the mouth is relatively small compared with the body depth at the 

larval stage, and complete ingestion is only observed at cannibal lengths 

larger than 45 mm (type ii cannibalism, Fig . 9 .2(B) ; Hecht and 

Appelbaum, 1988) . Several accounts of coeval cannibalism are also 

reported among amphibian larvae (Polls and Meyers, 1985), and in some 

species this is due to cannibalistic morphs (Crump, 1992) . The cannibalistic 

larval morphs typically have enlarged dentition and mouth dimensions and 

increased jaw musculature compared with normal morphs . 

255

256 Ontogeny of cannibalism in larval and juvenile fishes 

Metamorphosis 

Metamorphosis is defined as the stage when the larvae develop anatomical 

and morphological characteristics similar to those of adults (Balon, 

1984) . Metamorphosis in cod commences with the replacement of the 

larval fin fold with dorsal and anal fins at larval lengths around 12 mm 

(Pedersen and Falk-Petersen, 1992) and is completed at lengths around 

2 5-30 mm . 

Around metamorphosis, the mouth morphology makes the cod a more 

capable predator (Fig . 9 .2, Ottera and Folkvord, 1993) . At lengths of 

about 20mm the cannibal will theoretically need to be only 25% longer 

than the prey to completely ingest it (Fig . 9 .2(B)) . Pike, Esox lucius, is one 

of the few species that is morphologically capable of ingesting relatively 

larger siblings (Fig . 9 .2(B) ; Bry et al ., 1992) . The relatively large mouth 

size of cod at this stage may also be an adaptation to its most common 

prey during the larval and early juvenile stage, Calanus finmarchicus 

(Folkvord et al., 1994a) . Prey width :mouth gape ratios in Japanese 

mackerel, Scomber japonicus, larvae average around 0 .3-0 .4 (Hunter and 

Kimbrell, 1980a) . With these ratios, the cod will have to be around 

20 mm long to ingest the later copepodite and adult stages of C. finmarchicus 

(Folkvord et al ., 1994a) . 

The relatively large mouth of cod during metamorphosis may create a 

cannibalism problem, especially when food availability and suitability are 

reduced . Such a reduction in zooplankton biomass is commonly observed 

in the juvenile rearing ponds around metamorphosis (Blom et al., 1991, 

1994 ; Folkvord et al ., 1994b) . Modelling studies on other species have 

shown that larvae and early juveniles are particularly vulnerable to 

reduction in prey availability due to their high metabolic activity (Post, 

1990) . 

A semistarvation situation might also occur during weaning due to failure 

to accept formulated feed (Howell, 1984 ; Folkvord, 1991 .) . The problems of 

accepting formulated feed at this stage may to some extent be due to the 

relatively slow development of a functional stomach in cod compared with 

other species (Pedersen and Falk-Petersen, 1992), which make this a 

critical stage in their ontogeny. Recent experiments with improved formulated 

feeds have shown, however, that survival over 90% during weaning 

is possible at a size of 20 mm and above (Ottera and Lie, 1991) . 

The size variability within a cohort is larger after metamorphosis than 

before metamorphosis (Folkvord et al ., 1994b) . Increased size variability 

has been shown to lead to increased cannibalism in cod and other species 

at similar stages (DeAngelis et al., 1980 ; Katavic et al., 1989 ; Folkvord and 

Ottera, 1993) . At this stage a max :min body length ratio of 1 .5 :1 is 

required for cannibalism to occur, and cannibalism can be a major source 

1 .2 - 


Metamorphosis 

1 .0 1 1 1 i 1 

5 10 15 20 25 30 35 40 45 50 

Age (days) 

Fig. 9 .3 Estimated max :min length ratios of cod cohorts in an 

enclosure (solid 

curve, cohort 1 ; dashed curve, cohort 2) (Folkvord et al ., 1994b) . Horizontal 

dotted lines represent ratios required for cannibalism to occur (1 .5) and for cannibalism 

to be the main mortality cause (2 .0) (Folkvord and Ottera, 1993) . 

of mortality at ratios above 2 :1 . Size differences of this magnitude do not 

normally occur within a cohort before metamorphosis (Fig . 9 .3) . 

The large amount of energy available for the cod around metamorphosis 

may itself cause a spread in size within a cohort as they reach this stage 

(Folkvord et al ., 1994b) . The increase in spread can to some extent be a 

result of only the largest size fraction of cod (or the first cohort released) 

having the opportunity to prey on the largest and most energy-rich 

zooplankton organisms, C . finmarchicus copepodite stages ' rv-vi, before the 

collapse in the zooplankton biomass in the ponds . 

The highest growth rates of juvenile cod are encountered in the period 

around metamorphosis (Blom et al., 1991) . If conspecifics account for a 

fixed proportion of the diet, the cannibalism rates would also be highest at 

this stage because high growth rates are accompanied by high feeding rates 

(Folkvord, 1991) . Although cannibalism rates have been observed to be 

higher at elevated rearing temperatures, experimental studies have not 

indicated a temperature effect on cannibalism per se because survival to 

any given size was similar between treatments (Otterlei et al., 1994) . 

Cannibalism rates are therefore expected to be proportional to growth 

rates when other factors are equal . 

Increasing spatial patchiness of fish during the late larval and juvenile 

257

2 5 8 Ontogeny of cannibalism in larval and juvenile fishes 

stages is common, and several experimental studies have shown cannibalism 

to be density dependent in these stages (Li and Mathias, 1982 ; 

Giles et al ., 1986 ; Hecht and Appelbaum, 1988) . Density-dependent cannibalism 

rates have also been observed among juvenile cod in the laboratory 

(Otterlei et al ., 1994), where only one incidence of cannibalism in 8 weeks 

was observed in the low-density group (100 fish M-3), whereas 4 .9% were 

eaten in the high-density group (1000 fish m3 ) . The cod start shoaling 

and schooling after metamorphosis, and local densities in the juvenile 

rearing ponds of 500-1000 fish m -3 have been estimated from dipnet 

catches (own unpubl . data) . These fish densities are comparable to the 

highest densities used in intensive culture experiments (Otterlei et al ., 

1994) and are typically found among schools feeding on zooplankton 

entering through the screens in the dam . Thus the local densities of 

juvenile cod in the rearing ponds are sufficiently high for cannibalism to 

be significant . 

In flatfishes, the morphological changes around metamorphosis 

drastically alter an individual's vulnerability to cannibalism and intraspecific 

aggression . The increased body height post metamorphosis is not 

accompanied by a corresponding increase in mouth gape, thus reducing 

the possibility of being eaten by coeval conspecifics . Substantial aggression 

and cannibalism is observed prior to settling of turbot, Scophthalmus 

maxim us, during periods of food shortage (own observations), but the 

mortality under culture conditions is generally low after metamorphosis . 

In treefrog tadpoles, Osteopilus septentrionalis, the risk of predation and 

cannibalism is especially high during metamorphosis, possibly because 

the metamorphosing tadpole is less adapted to the aquatic habitat 

(Crump, 1986) . Contrary to the common situation, these metamorphosing 

larvae are attacked by smaller and less-developed tadpoles . 

Juvenile stage 

The problems associated with coeval cannibalism of cod in culture are 

reduced later in the juvenile stage (Table 9 .2) . The growth rate is 

reduced to less than a third of its maximum value within 1-2 months 

after metamorphosis . During this period, the stomach becomes fully 

functional and few problems are encountered during weaning onto 

formulated feeds (Ottera and Lie, 1991) . Once weaning is completed, 

proper management will prevent food shortage and starvation . It 

has been shown in several studies that the role of cannibalism is 

reduced in the presence of sufficient quantities of alternative food (Li and 

Mathias, 1982 ; Katavic et al., 1989 ; Folkvord, 1991 ; Hecht and Pienaar, 

1993) . 

Due to their reduced growth rate and metabolism, larger juveniles are 

Cannibalism as a selective process 

also more resistant to starvation (Post, 1990 ; Folkvord, 1991) . In addition, 

the larger fish generally have more food available owing to their wider 

range of acceptable prey sizes (Shirota, 1970 ; Hunter and Kimbrell, 

1980a) . The potential for cannibalism is further reduced by the relatively 

large predator :prey size difference needed for cannibalism to occur, and 

the relatively small mouth size at this stage (Fig . 9 .2(B), Ottera and 

Folkvord, 1993) . The potential for cannibalism in the juvenile stage may 

also increase, however, due to the common increase in relative size 

between the largest and smallest individuals in a cohort (Folkvord et al., 

1994b) . In a culture situation, this can easily be resolved by satiation 

feeding with suitable feeds and size grading of the fish (Hecht and 

Pienaar, 1993) . 

9 .3 CANNIBALISM AS A SELF''TIVE PROCESS 

Effects on size distribution 

Cannibalism is both a cause and an effect of size variation (Hecht and 

Pienaar, 1993) . In fish it is generally a size-selective process, usually 

limited by the mouth size of the cannibal (Fig . 9 .2(B) ; Hecht and 

Appelbaum, 1988 ; van Damme et al ., 1989 ; Parazo et al ., 1991 ; Bry et 

al., 1992 ; Sogard and Olla, 1994) . It follows that intracohort cannibalism 

will selectively remove the smallest individuals . The effect can be very 

dramatic when the size variation in the population is sufficiently large 

(Fig . 9 .4 ; Folkvord and Ottera, 1993) . The proportion of cannibals in the 

population need not be very high to cause high mortalities . Two large cod 

individuals were capable of consuming 56 siblings (56% of the population) 

within 4 weeks (Folkvord, 1991) . 

The importance of the largest individuals in the cannibalism process 

indicates that the relative size difference between the largest and smallest 

individual in a co-occurring group of conspecifics may be a better 

measure of cannibalism risk than the coefficient of variation (CV) of 

length or weight . It is important to note that large relative size differences 

are more likely to be present in a large group of fish than in a small group 

of fish . A simple simulation study illustrates this point . Theoretical populations 

generated randomly from the same original population (same CV) 

show a logarithmic increase in max :min length ratios with increasing 

population size (Fig . 9 .5) . Thus not only does the number of encounters 

increase with increasing density, but also higher relative size differences 

between individuals will be present at higher densities . The increase in 

max:min length ratios with increasing population size is more rapid when 

the population size variability is high (Fig . 9 .5(A,B)) . 

Size variation within a fish population also depends on previous growth 

259


Fig. 9 .4 Size-selective cannibalism mortality in juvenile cod (Folkvord and Otters, 

1993). Estimated relative loss of small cod in tanks with 2 (solid line) and 10 

(broken line) large siblings added (out of 50 fish) relative to control tanks with no 

large siblings added . The percentages missing are calculated at 0 .05 g intervals (see 

points) . The experiment lasted 16 days, and the initial CVs (length) averaged 12%, 

15% and 20% respectively for the groups with 0, 2 and 10 large siblings added . 

and mortality history (Pepin, 1989), and can remain relatively constant or 

even be reduced depending on the extent of cannibalism (Folkvord and 

Otters, 1993) . Individual-based models (IBMs) seem particularly useful in 

evaluating the effect of size variation on cannibalism because these models 

are effective at dealing with rare events or individual characteristics of the 

population members (Dong and Polis, 1992) . The appearance of size 

bimodality in the population is, however, not necessarily the result of interaction 

between individuals . Huston and DeAngelis (1987) listed four 

possible factors influencing the changes in size distribution : (1) initial 

sizes, (2) distribution of growth rates among individuals, (3) size- and 

time-dependent growth rate, and (4) selective mortality . These factors may 

also act in concert . In the case of cod, a size bimodality is in part due to 

increased growth rate of the cannibals (Folkvord and Otters, 1993) . 

Prolonged cannibalism can eventually lead to the removal of the smallest 

size mode, resulting in a unimodal distribution (DeAngelis et al ., 1980) . 

Modelling studies have also predicted that the variation in growth rates 

would decrease with increasing predator abundance (Pepin, 1989), but the 

estimates of mean and variance in size-frequency distributions would have 

to be very precise to detect changes in predator abundance . In a similar 

50 100 200 500 1000 

Population size 

Fig . 9 .5 Simulated max :min length ratios in randomly generated populations . 

These populations were generated from underlying populations with a CV (length) 

of 10% (A) and 15% (B) respectively . Fifty populations were generated for each 

population size in both (A) and (B) . Regression equations are (A) : 

y = 1 .071 + 0 .305*loglO(x) and (B) : y = 1 .066 + 0 .623*log10(x) . Note differing 

vertical scales . 

study (Rice et al ., 1993), high variance in growth rate within a cohort 

gave substantially higher survival when size-selective predation pressure 

was present . This simulation study was based on a piscivore predator 

(intercohort predation), and the results cannot necessarily be transferred 

to cases of intracohort cannibalism. 


20 

261


Bias in growth estimation 

Growth in fish can be related to size in two ways . First, growth rate 

generally declines with increasing size (Brett, 1979), with the exception of 

the early larval period and periods of compensatory growth after temporary 

food shortage (Blom et al ., 1991 ; van der Meeren and Nmss, 1993) . 

Secondly, the individual growth rate in a group may vary according to 

relative size and social hierarchy (Brawn, 1969) . This can be caused by 

various size fractions of the population feeding on different-sized food 

particles (Folkvord and Otters, 1993 ; Folkvord et al., 1994b), genetic differences 

or behavioural differences (Brawn, 1969) . 

When estimating growth in populations with size-selective mortality it is 

necessary to distinguish between growth estimates based on individual 

growth trajectories and estimates based on average sizes of fish at various 

periods . In the following I refer to average individual weight (or length) 

growth rates in cases where the estimates are based on separate individual 

growth rates : 

and 

Average individual growth rate = Y [100 * (e5 - 1)] / n (9 .1) 

i=1 

gi = [ln(W12) - ln(W,1)] / ( t2 - t1) 

where W11 and Wit are the weights of individual i at times t 1 and t 2 respectively, 

and n is number of individuals in the population (or sample) . 

Population growth rates, on the other hand, are obtained by using 

average population weights (or lengths) as input and are defined as : 

and 

Population growth rate = 100 * (ea - 1) (9 .3) 

g = [ln(W2 ) - ln(W1)] / (t2 - t1) (9 .4) 

where W1 and W2 are the average weights in the population at t1 and t2 . 

When cannibalism rates are high, large differences between population 

growth rates and individual growth rates are observed (Patriquin, 1967 ; 

Ricker, 1975) . Similar effects can also be observed when predation or 

fishing rates are strongly size selective (Hanson and Chouinard, 1992) . 

Thus one cannot infer individual growth rates from population growth 

rates without any measures of size-dependent mortality (Otters, 1992) . 

On the other hand, knowledge of size-dependent growth is essential 

because it may influence overall survival and recruitment (Tsukamoto et 

al ., 1989) . 

In juvenile cod it has been shown that population growth rate can be 


Table 9 .3 Calculation of growth rates under three different mortality scenarios : 

(A), no mortality ; (B), selective mortality of the smallest individuals ; (C), nonselective 

mortality . Rates were calculated as 100*(ee-1), where g is the 

instantaneous rate of weight increase during a 14 day growth period . The 

corrected average start weight was obtained by omitting the fraction of the 

smallest fish corresponding to the mortality in the following period (arbitrary 

weight units) 

Variable Start Final A Final B Final C 

Weight fish 1 20 40 40 40 

Weight fish 2 20 40 40 - 

Weight fish 3 5 10 - 10 

Weight fish 4 5 10 10 

Weight fish 5 5 10 

Weight fish 6 5 10 

Average weight 10 20 40 20 

Corrected average start weight 10 20 15 

Individual growth rate (% day-1 1 5 5 5 

j ) 

Population growth rate (% day 5 10 5 

Corrected growth rate (% day -') 5 5 2 

more than twice as high as the estimated average individual growth rate 

(Folkvord and Otters, 1993) . During the early juvenile stage, it is difficult 

to sample cod quantitatively in the enclosures . Thus it is common to only 

estimate average mortalities from metamorphosis to harvest (Blom et al ., 

1991) . Taking into account the possibility of prominent size-selective 

mortality, any population growth estimates during this period most likely 

overestimate the average individual growth rates and should be treated 

with caution . Using population growth rates is equivalent to assuming no 

size-selective mortality at all (see also Miller, Chapter 7, this volume) . 

If the mortality rate is known, approximate individual growth rates can 

be estimated using a subpopulation concept (Rosenberg and Haugen, 

1982 ; Folkvord and Otters, 1993 ; van der Meeren and Nmss, 1993) 

(Table 9 .3) . This estimate will be an underestimate of the average individual 

growth rate if any of the larger and presumed surviving individuals 

died during the growth period (Table 9 .3, scenario C) . In a population 

where cannibalism and removal of the smallest individuals is likely to 

occur, the corrected estimate will be a good approximation to the average 

individual growth rates (Folkvord and Otters, 1993) (Table 9 .3, scenario 

B) . The reliability of the method is, however, dependent on the accuracy 

of the mortality estimate and the obtained size-frequency distribution . 

In the field, individual larval and early juvenile growth rates can be 

263


inferred from otolith microstructure . These rates are dependent on accurate 

age determination for size-at-age studies (Bolz and Lough, 1988) . Growth 

can also be back-calculated based on known otolith size :body size relations 

(Campana, 1990) . Although there are few reliable estimates of individual 

growth rates of cod at present (Suthers and Sundby, 1993), otolith microstructure 

analysis still remains as one of the few promising applicable 

techniques for obtaining individual growth estimates of larval and juvenile 

cod in the field . 

9 .4 IMPORTANCE OF CANNIBALISM IN THE FIELD 

Intracohort cannibalism 

The spawning season of the Arcto-Norwegian cod stock typically lasts 2-3 

months, and this should produce co-occurring larvae of sufficiently large 

size disparity for cannibalism to occur. Still, no accounts of intracohort 

cannibalism on cod larvae in the field are documented in the literature 

(e.g . Ellertsen et al ., 1984) . Until recently, intracohort cannibalism among 

0-group cod juveniles had not been encountered either (Wiborg, 1960 ; 

Perry and Neilson, 1988) . The findings of two 0-group cod (7-14 cm) off 

Iceland in 1990 with conspecific juveniles in their stomachs is the first 

documentation of intracohort cannibalism in cod in the field (Bogstad et 

al., 1993) . 

The low incidences of intracohort cannibalism in the field are to some 

extent due to density effects . First, the average abundance of larval and 

juvenile cod compared with their most common prey organisms is low 

(Wiborg, 1960) . Secondly, the density of cod juveniles itself tends to be 

low, although some exceptions have been observed . Olsen and Soldal 

(1989) observed over 3 million juvenile cod in northern Norway in large 

aggregations with average densities of 5-8 fish M-3, which is higher than 

the average density i "the juvenile production ponds (Blom et al ., 1991) . 

The highest local deities in the field may, therefore, be close to 100 fish 

M-3 , the lowest density used in the experiments by Otterlei et al . (1994) . 

Very low cannibalism rates were observed at this density when the 

juvenile cod were fed ad libitum . 

In the field, intracohort cannibalism and competition may be reduced by 

spatial segregation of the offspring due to advection (Economou, 1991) . 

The 0-group cod will also be vertically segregated as the settling process 

commences among the larger juveniles (God® et al ., 1993) . In addition, 

the shoaling behaviour of fish may reduce cannibalism in the field . It has 

been documented for several species that fish prefer to shoal with conspecifics 

of a similar size (Pitcher and Parrish, 1993), and the relatively low size 

variation in the shoal will reduce the probability of intracohort canni- 

Importance of cannibalism in the field 

balism . In summary it therefore seems unlikely that intracohort cannibalism 

among young cod is of any importance in the field . 

Intracohort cannibalism and predation among other 0-group gadiforms 

have been observed in the field, but these instances have usually been 

coupled with poor feeding conditions (Perry and Neilson, 1988 ; Koeller et 

al ., 1989) . Intracohort cannibalism occurred among silver hake, Merluccius 

bilinearis, as small as 22-25 mm, and accounted for over 25% of the 

stomach content by weight in juveniles larger than 46 mm (Koeller et al ., 

1989) . 0-Group cod occurred in the stomachs of 0-group haddock, Melanogrammus 

aeglefinus (intracohort predation), at a site characterized by low 

zooplankton biomass (Perry and Neilson, 1988) . 

Young and Davies (1990) observed intracohort cannibalism in 1 .5% of 

the southern bluefin tuna, Thunnus maccoyii, larvae with food in their 

stomachs . The consumed larvae were smaller than 4 mm, and occurred 

in 3 out of 16 (19%) of the larvae between 8 and 9 .5 mm length . Larval 

and juvenile tunas generally have relatively high mouth size :body size 

ratios (Shirota, 1970 ; Kawai and Isibasi, 1983), and this most likely 

facilitates cannibalism to take place earlier in ontogeny compared with 

other species . 

The degree of piscivory and intracohort cannibalism in 0-group 

pikeperch, Stizostedion lucioperca, showed marked annual variations during 

the period 1976-1983 (van Densen, 1985) . Cannibalism was highest in 

1982, when the abundance of pikeperch initially was more than 10 times 

higher than in the other years . Density effects were also found to be 

important during a large-scale mark-recapture study . Tsukamoto and coworkers 

(1989) found seven 20mm newly released red sea bream, Pagrus 

major, in the stomachs of simultaneously released fish of 40 mm length . 

Cannibalism was, however, not considered to have a serious effect on 

mortality of red sea bream juveniles in the field, because this phenomenon 

was limited to the stocking area on the first 2 days after release . The high 

cannibalism rate during this period was considered an artifact due to 

unnaturally high concentration of juveniles following the release 

(756 000 individuals on the same site) . 

In summary, there is little information from the field that points to 

intracohort cannibalism as being of importance in regulating overall 

survival or ultimately recruitment (Smith and Reay, 1991) . Intracohort 

cannibalism is only expected to be operating in some species under special 

conditions with limited food availability . The possibility of detecting 

cannibalism among 0-group fish in the field is higher in areas with low 

food availability, but rapid digestion of smaller conspecific prey will still 

require large numbers of potential predators to be investigated (Folkvord, 

1993) . Thus, the local importance of intracohort cannibalism cannot be 

ruled out . 

265


Intercohort cannibalism 

Numerous accounts of intercohort cannibalism in cod and other gadoids in 

the field have been reported (Daan, 1973 ; Dwyer et al., 1987 ; Mehl, 1988 ; 

Bailey, 1989) . Large regional and temporal differences in the frequency of 

cannibalism have been observed . These were usually coupled with the cooccurrence 

of 0-group fish and older conspecifics (Daan, 1973 ; Dwyer et 

al ., 1987) . It is conceivable that cannibalism in gadoids is of special importance 

at the time of settling of the 0-group fish, but horizontal and vertical 

separation of 0-group and older cod may to some extent reduce predation 

at this stage (Riley and Parnell, 1984 ; Godo et al ., 1993) . Intercohort 

cannibalism has, however, been shown to account for over 20% of the 

diet of older cod, and 40% of the annual mortality of 0-group cod in years 

when the abundances of 0-group cod have been relatively high compared 

with other prey items (Daan, 1973 ; Mehl, 1988) . Adult walleye pollock, 

Theragra chalcogramma, have been shown to consume larger-than-average 

0-group juveniles, and this was related to the vertical distribution of 

juveniles (Bailey, 1989) . The smaller juveniles found near the surface 

were not recovered in the stomachs of adults . Large and faster-growing 0group 

fish settling early may thus experience a higher mortality during this 

period than their smaller conspecifics . 

In a study on Cape hake, Merluccius capensis, Macpherson and Gordoa 

(1994) found that large adult hake preferentially selected smaller hake 

irrespective of their density or of the occurrence of alternative prey . This 

lack of density-dependent regulation was possibly compensated for by the 

distributional pattern of the different size groups of hake . The majority of 

the large adult hake were distributed in an area which only partially 

overlapped with the area occupied by the smaller conspecifics . Cannibalism 

presure by adult threespine sticklebacks, Gasterosteus aculeatus, has been 

suggested to be responsible for an ontogenetic shift in habitat use of 

juveniles in this species (Foster et al ., 1988), but similar mechanisms were 

not confirmed for hake . A shift from the pelagic habitat to the benthic 

habitat for coastal cod was modelled based on mortality rate/growth rate 

ratios, and the predictions from the model were consistent with field observations 

(Salvanes et al ., 1994) . Although intercohort cannibalism was 

documented to be important in the benthic habitat, this was possibly 

compensated for by increased prey availability in the same habitat . 

Egg cannibalism is a special case of cannibalism that has been confirmed 

for several clupeoid filter-feeding species, and field estimates have shown 

that it can account for 6-70% of the daily mortality (Hunter and 

Kimbrell, 1980b ; Valdes Szeinfeld, 1991) . The overall consequences of 

cannibalism are, however, strongly dependent upon the degree of overlap 

between adults and their spawning products (MacCall, 1981) . Interspecific 

Importance of cannibalism in the field 

predation by co-occurring species (intraguild predation) has been shown in 

some cases to account for an even larger proportion of the mortality . Up to 

56% of the daily anchovy, Engraulis capensis, egg mortality was due to 

sardine, Sardinops ocellatus, predation, while 6% was due to cannibalism 

(Valdes Szeinfeld, 1991) . Egg cannibalism rates are expected to be lower 

in particulate-feeding fishes such as most gadiforms, and egg cannibalism 

in walleye pollock is estimated to account for less than 3% of the total egg 

mortality (Brodeur et al ., 1991). Several of the largest pelagic fish stocks in 

Norwegian waters have demersal eggs (Clupea, Mallotus and Ammodytes), 

and this reproductive strategy effectively eliminates egg cannibalism in 

these species . 

Management implications 

Extensive cannibalism will have implications for both fish production and 

stock assessment of the given species . The effects of cannibalism should 

therefore be modelled in fisheries models . During the mid 1980s the 

capelin, Mallotus villosus, stock in the Barents Sea was drastically reduced 

(Mehl, 1988) . As a consequence, the young year classes of cod were significantly 

reduced due to cannibalism . Up to 85% of the mortality of the igroup 

to in-group stage was due to cannibalism from older year classes 

(Mehl, 1988) . The failure to take this effect into account resulted initially 

in far too optimistic predictions of cod recruitment and projected total 

allowable catch in the region . The failure to anticipate this dramatic 

reduction of some of the year classes led to the inclusion of cannibalism in 

the multispecies models for the Barents Sea region . Through an extensive 

stomach-sampling programme undertaken by Norwegian and Russian 

researchers, the managers are now able to monitor the annual variations 

in cannibalism intensity (Bogstad et al ., 1993) . 

An increase in the occurrence of cannibalism with size/age is observed 

for several cod stocks (Bogstad et al ., 1993) . The age structure of the 

Arcto-Norwegian cod stock in the late 1940s and early 1950s was 

dominated by older individuals, partly due to reduced fishing pressure 

during the period after the Second World War . It is interesting to note 

that the overall occurrence of cannibalism in this period seemed to be 

higher than during the 1980s, when the age distribution has been shifted 

towards younger individuals (Bogstad et al., 1993) . This example emphasizes 

the importance of understanding the age- and size-related predation 

processes occurring in a stock . 

Cannibalism in hake was included in a virtual population analysis (VPA) 

model developed by Lleonart and co-workers (1985) . Mortality due to 

cannibalism accounted for 48%, of natural mortality . As a consequence, it 

was shown that the standard VPA model systematically underestimated 

267


the number and biomass of the youngest cohorts . Without the correction, 

the stock appeared older and the calculated age-specific mortalities of the 

youngest age classes were underestimated . The authors further suggested 

that in a stock where cannibalism by older year classes is common, a 

management regulation of mesh size will be more effective than a regulation 

of total effort . An increased mesh size will selectively remove large 

potential cannibals, enhancing survival of younger year classes by 

reducing cannibalism (Lleonart et al., 1985) . These conclusions were 

questioned by Punt and Hilborn (1994), who concluded that little 

precision in the management models was lost by omitting cannibalism 

interactions in this species . This result was attributed to uncertainties in 

other important aspects of the population regulation in hake . In addition, 

considerable effort would have to be made to estimate the parameters 

needed in the external model. 

MacCall (1981) incorporated cannibalism on eggs and larvae in a stock- 

recruitment model and concluded that cannibalism in northern anchovy, 

Engraulis mordax, is sufficiently intense to be a regulatory mechanism . The 

densities of adult clupeoids are not generally proportional to stock size 

owing to the expansion and contraction of ranges with varying 

abundance . The harvest potential may thus depend on the spatial fishing 

pattern of juvenile and adult clupeoids relative to the distribution of eggs 

and larvae (MacCall, 1981) . Usually the spawning migrations undertaken 

by most clupeoid species will reduce the potential for filial cannibalism . The 

migration pattern of the adults may, however, be influenced by stock size, 

as happened in the Norwegian spring-spawning herring, Clupea harengus, 

following the collapse in the 1960s . The traditional migration pattern into 

the Norwegian Sea after spawning was abandoned, and the stock remained 

near the Norwegian coast, in the drift route of their own offspring 

(Rottingen, 1990) . The presence of adult herring in the Norwegian 

coastal current may thus have delayed the recovery of the stock due to 

cannibalism on larvae . 

Special attention to the role of cannibalism and other density-dependent 

mechanisms is needed prior to the onset of large-scale enhancement enterprises 

(Peterman, 1991) . Theoretical considerations have shown that when 

cannibalism by older conspecifics is responsible for a major part of the 

juvenile mortality, the effect of the release will be higher at lower stock 

sizes or higher fishing pressure (Ulltang, 1984) . The gain from such a 

release may, however, be lost if the fishing pressure exceeds that giving 

the maximum sustainable yield (MSY) of the natural population . Intercohort 

cannibalism of cod juveniles has been documented by stomach 

analyses carried out in connection with the major cod enhancement 

programmes in Norway (Svasand and Kristiansen, 1990 ; Smestad et al ., 

1994) . Smestad and co-workers (1994) concluded that the large-scale 

Perspectives 269 

releases of cod juveniles in a Norwegian fjord did not contribute signifi- 

cantly to recruitment in the area, and attributed this to competition and 

predation from other gadids . The production of cod in this fjord depends 

to a large extent on advected zooplankton from outside the fjord, and the 

abundance of ii-group cod was not different in release areas compared 

with control areas . The effects of cod enhancement programmes will 

therefore most likely not be worthwhile if the predation pressure from cod 

and other species on young cod is high (Ulltang, .1984), and the possibilities 

of a successful ranching programme will be higher when the popula- 

tion involved is already at a low level due to overfishing . 

In summary, studies on intercohort cannibalism in cod and other species 

have also shown that it can be a major source of mortality and an 

important density-dependent mechanism in natural fish populations 

(Hunter and Kimbrell, 1980b ; Ulltang, 1984 ; Valdes Szeinfeld, 1991) . In 

the dome-shaped Ricker curves of stock against recruitment, this is 

apparent as a drop in recruitment at high stock levels . It is likely, 

however, that the density effect of adults is often exerted via the density of 

eggs and larvae they produce, and not necessarily through a direct impact 

of their own abundance (Ricker, 1975) . 

9 .5 PERSPECTIVES 

Cannibalism among fishes has in the past often been viewed as an artifact 

occurring under artificial circumstances . On the other hand, recent reviews 

indicate that cannibalism is far too widespread in the animal kingdom and 

in fishes to be classified as an obscurity (Smith and Reay, 1991) . 

Genetic and evolutionary aspects 

The evolution of non-predatory interference (e .g . territoriality) is unlikely in 

an open environment such as the pelagic ecosystem where resource 

monopolization is impossible (Polls, 1988) . Cannibalism in fish is usually 

an unequal contest where the smaller victim presents no direct risk to the 

cannibal. The structural simplicity of the pelagic habitat, coupled with the 

tendency of conspecifics to co-inhabit a common environment, will also 

promote multiple encounters between individuals of the same species . The 

schooling behaviour of many fish species will also further increase the 

encounter rate between conspecifics . There are thus several sound ecological 

and evolutionary reasons for cannibalism being a part of the natural 

behavioural repertoire of many fish species (Polls, 1981 ; Edgar and Crespi, 

1992) . The selective advantage of individuals exhibiting cannibalistic traits 

is evident in situations of food shortage . In addition to increasing the fitness


of the cannibal, the resulting reduced competition for food will possibly 

increase the fitness of all other surviving juveniles (Polis, 1981 ; Elgar and 

Crespi, 1992) . 

The cannibal benefits directly from obtaining a meal of high nutritional 

value (Polis, 1981) . The proximal composition of the prey is also similar to 

the proximal composition of the predator . There are also some indications 

that cod and other fishes and amphibians grow better on a diet of conspecifics 

(Crump, 1992 ; Folkvord and Otters, 1993) . Postlarval mahi-mahi, 

Coryphaena hippurus, grew better on a diet of conspecific yolk-sac larvae 

than on live brine shrimp, Artemia, and the growth rates were up to 34% 

day l (Kraul et al ., 1992) . The authors attributed this result to the 

proximal composition of yolk-sac larvae, which had relatively high levels 

of polyunsaturated fatty acids . 

One of the many striking differences between the terrestrial and aquatic 

ecosystems is the common size disparity between members of the lower and 

higher trophic levels . In the marine environment this is also manifested in 

the high biomass density of relatively small planktonic organisms 

(Boudreau and Dickie, 1992) . Intermediate-sized organisms are often 

needed in order to obtain an efficient energy transfer between these 

plankton resources and the higher trophic levels . According to Nellen 

(1986), cannibalism of younger planktivorous conspecifics represents such 

an intermediate trophic level . In their analysis of the life history of Japanese 

fishes, Kawai and Isibasi (1983) observed a between-species discontinuity 

in growth patterns during the juvenile period . The authors suggested that 

this was due to differential adaptation of the various species to food acquisition 

during the early juvenile stage . Species with relatively large mouths, 

and resulting high piscivory and cannibalism potential, were expected to 

outgrow the plankton-eating species during this period . 

Whether fish preferentially cannibalize non-siblings is unclear . There is, 

however, some evidence that certain species of amphibians are able to 

recognize their own kin . The ability to recognize their own kin is 

necessary for kin selection to take place, and such mechanisms are 

documented for salamanders and toads (Walls and Roudebush, 1991 ; 

Pfennig et al ., 1993) . Female poeciliids preferentially consumed individuals 

of other females rather than their own (Loekle et al., 1982), but further 

studies are needed to determine the mechanisms involved . Lower canni- 

balism rates were also observed in full-sib groups of pike, Esox lucius, 

compared with mixed groups (Bry and Gillet, 1980) . This could possibly 

have been due to the lower inherent size variation of the full-sib groups 

and not directly to genetic effects . 

Many aquaculturists have noted the presence of unusually small and 

slow-growing individuals during rearing of various fish species (own observations 

; Polis, 1981) . Although the size of these individuals may be a result 

Perspectives 

of injury or disease, the existence of so-called runts may have evolutionary 

significance . In snails it is common for some of the offspring to feed on 

trophic eggs (Polis, 1981) . It has been suggested that the production of 

small individuals serves the same purpose in fish populations, where some 

of the offspring are provided as suitable-sized prey for the largest individuals 

later during ontogeny (Polis, 1981) . Whether this is an acceptable interpre- 

tation for the pelagic environment, where the provided offspring in no way 

can be 'reserved' for conspecifics, is questionable (Polis, 1988) . 

In some amphibians there are well-documented accounts of cannibalistic 

polyphenism, i .e . phenotypic differences in behaviour, morphology, growth 

rates or life history between cannibal and non-cannibal forms (Polis, 

1981) . In most cases the development of the cannibal morph seems to be 

environmentally induced when larval densities are high or food levels are 

low (Crump, 1992) . The development of cannibalistic morphs is also 

dependent on the presence of close kin and alternate prey (Pfennig and 

Collins, 1993) . 

Few examples of cannibalistic polymorphism are found among fishes, but 

in Arctic charr, Salvelinus alpinus, several coexisting morphs have been 

identified (Sandlund et al ., 1992) . The morph with the largest mouth 

dimensions was mainly piscivorous, and was the only morph documented 

to be cannibalistic . There are also polymorphic adaptations to reduce the 

effect of predation and possibly cannibalism . Crucian carp, Carassius 

carassius, living in ponds with larger piscivore predators develop enlarged 

body heights compared with those exposed to a lower predation risk 

(Tonn et al ., 1994) . Although cannibalism is documented in carp, it is not 

clear if this morphological response is triggered in the presence of large 

siblings . 

Not surprisingly, a genetic component of cannibalistic behaviour has 

been demonstrated (Thibault, 1974 ; Hecht and Pienaar, 1993) . Canni- 

balism may also indirectly be affected by genetic effects because inherent 

size variation within full-sibling groups tends to be lower than that 

between mixed-sibling groups (Knutsen and Tilseth, 1985 ; Folkvord et al ., 

1994b) . During the extensive rearing process of juvenile cod, periods of 

food limitation are common, and are expected to favour cannibalistic 

individuals (Blom et al ., 1994) . Caution is thus appropriate when selecting 

for rapid growth among broodstock in cannibalistic species such as cod, 

because the fast-growing survivors may also be the individuals with the 

highest cannibalistic propensity (Hecht and Pienaar, 1993) . 

There are also mathematical derivations which show that cannibalism 

can function as a 'lifeboat' mechanism, preventing all specimens in a 

population from becoming extinct (van den Bosch et al ., 1988) . Such 

mechanisms should be explained in terms of selection at the individual 

level . It can, however, be concluded, regardless of whatever selective 

271


agent is responsible, that cannibalism has the potential of preventing a 

population from becoming extinct by self-regulation (Polis, 1981) . 

Concluding remarks 

Through evolutionary processes, larval and juvenile fish are adapted to 

variable feeding conditions . In a farming or experimental situation these 

adaptations represent in some cases undesirable features that have to be 

dealt with . In extensive juvenile rearing, it is important to match the 

released numbers of fish larvae with the timing and production of suitable 

prey . The potential zooplankton production (and supply) in the ponds has 

been shown to impose a limit on the juvenile production of cod and other 

species (McIntyre et al ., 1987) . A common error has been to release 

relatively high numbers of larvae to be certain that some will survive . 

Almost without exception, this has led to a zooplankton collapse in the 

ponds before the fish are readily harvested or weaned . Future r studies on 

extensive rearing with lower initial larval densities and/or earlier harvest 

are therefore needed . 

In a culture situation, coeval cannibalism represents an undesirable 

trophic level reducing the potential output given a limited food resource, 

and should thus be avoided . On average, around 60% of the zooplankton 

energy ingested by the cannibal victims will be added heat loss in an 

extra trophic level (Blom et al ., 1991), and continued cannibalism will thus 

quickly reduce the population biomass (Kawai and Isibasi, 1983) . An 

exception is the use of added fish larvae as a direct food source for the 

older conspecifics . Studies on postlarval mahi-mahi have demonstrated 

that this can be a viable strategy if available broodstock can produce sufficient 

quantities of eggs . It was estimated that four females could produce 

enough eggs and yolk-sac larvae to raise a few hundred postlarvae 

through weaning (Kraul et al ., 1992) . 

Cannibalism in the field is highly dependent on the co-occurence of 

older conspecifics . The process of settling in cod and other fishes stands 

out as an important event which is poorly described and documented . 

Spatial and temporal variations in the time of settling are expected to 

have an important impact on intercohort cannibalism rates (Bailey, 1989) . 

Cannibal morphs are well documented in amphibians and future studies 

on fish should look for polymorphic traits in situations where cannibalism 

is important . Kin recognition in fish, if it exists, can have wide-ranging 

implications in our culture strategies . At present there is no evidence of 

kin recognition playing an important role in reducing fish cannibalism, 

but this possibility needs to be addressed . Comparative studies on allometric 

mouth morphology can also yield new insight to ontogenetic changes in 

the intracohort cannibalistic propensity . 

References 

A final comment regarding the role of cannibalism in the field : although 

it undoubtedly does occur in a large range of species under captive conditions, 

special care should be taken to avoid extrapolation of laboratory data 

to the field (Nesbit and Meffe, 1993) . Controlled experiments in the laboratory 

are well suited for isolating factors of importance, but the rates of 

cannibalism cannot be directly transferred to the field . The ultimate 

evidence of the role of cannibalism has to be found in the respective 

habitats of the species under investigation . 

ACKNOWLEDGEMENTS 

The constructive comments of G . Blom, C . Booman and A . Johannessen 

and three anonymous referees are greatly appreciated . The work has been 

funded by research fellowships from the Norwegian Research Council 

(former NFFR) and the University of Bergen . 

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