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
Ontogeny
Table 9 .1 List of recent reviews of cannibalism in fish and amphibians . Relevant
contributions in book reviews are listed under the book editors
of coeval cannibalism
253
350
Author(s)
Taxa
Emphasis
c
m
Polis (1981)
Hausfater and Hrdy (eds) (1984)
Dominey and Blumer
Several
Several
Pisces
0
Simon
Polis and Myers (1985)
Amphibia
Amphibia
Smith and Reay (1991)
Elgar and Crespi (eds) (1992)
Pisces
Several
Evolution, population dynamics
Infanticide, filial cannibalism
Systematic overview, filial
cannibalism
Systematic overview, evolution
Systematic overview (including
reptiles)
Systematic overview
Systematic overview, ecology,
evolution
Systematic overview, ecology,
evolution
Population dynamics, foraging
Filial cannibalism, modelling
Filial cannibalism, ecology
Systematic overview, ecology
Larviculture
300
250
Elgar and Crespi
Dong and Polis
Sargent
FitzGerald and Whoriskey
Crump
Hecht and Pienaar (1993)
Several
Pisces
Pisces
Pisces
Amphibia
Pisces
Cannibalism in fish is of special concern because it can influence both
aquaculture production and fisheries . Several review papers and books
U)
200
d
150
!0
R 100
N
.g
E
3
Z
N
50
.
o-, - - • I - - - I .
-,
4000
1000
2000
3000
0
Numbers at metamorphosis (thousands)
.
.
,
. 1
5000
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
have recently been published on the topic (Table 9 .1) . This review emphasizes the role of cannibalism in the pelagic environment . Some of the
processes involved in cannibalism among amphibian larvae in ponds
data), and similar reports of cannibalism in the field are well documented
(Bogstad et al., 1993) . Knowledge of the mechanisms underlying canni-
parallel those present in fishes, and some references from this field are
species, and to obtain a better understanding of the dynamics in natural
included as well . In both these groups, cannibalism is mostly a gape-
populations .
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
balism is thus essential to improve juvenile production of cod and other
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
254
Ontogeny of cannibalism in larval and juvenile fishes
255
Ontogeny of coeval cannibalism
Table 9 .2 Ontogeny of coeval cannibalism of cod in enclosures
0.5-
Stage
Mechanism/attribute
Cannibalism
Larval, 4-10 mm
Low initial size variation
Food limitation uncommon
Relatively small mouth ; yolk sac initially large
Low
Metamorphosis,
12-30 mm
Increasing size variation ; zooplankton energy
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
High
Juvenile,
50-150 mm
Reduced growth rate
Lower susceptibility to starvation
Relatively small mouth
Greater feeding flexibility
Completed weaning
Fully functional stomach
Low
Large relative size difference
High
o +
I1
f
I
I
3 .0
4
B
0
2.5 -
2 .03
5
juvenile production enclosures (Blom et al., 1991 ; Folkvord et al ., 1994b) .
Thus it is reasonable to assume that coeval cannibalism among cod larvae
a
6 ' '
in the laboratory and in enclosures is insignificant during the early larval
1 .0
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
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 .
256
Ontogeny of cannibalism
in larval
and juvenile
fishes
Ontogeny
of coeval cannibalism
257
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 1 .0
Metamorphosis
111i
5
10
15
20
1
30
25
Age (days)
35
40
45
50
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
25 8
Ontogeny
of cannibalism in larval
Cannibalism as
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
a selective process
259
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
260
Ontogeny of cannibalism in larval and juvenile fishes
261
Cannibalism as a selective process
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
20
100
50
Population size
200
500
1000
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.
262
Ontogeny of cannibalism in larval and
juvenile fishes
Cannibalism as a
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 :
Average individual growth rate
= Y
[100 * (e5 - 1)] / n
(9 .1)
263
selective process
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
Weight
Weight
Weight
Weight
Weight
Weight
fish
fish
fish
fish
fish
fish
1
2
3
4
5
6
Average weight
Corrected average start weight
Individual growth rate (% day-1 1j
Population growth rate (% day )
Corrected growth rate (% day -')
Start
Final A
Final B
Final C
20
20
5
5
5
5
40
40
10
10
10
10
40
40
-
40
10
10
10
20
10
40
20
20
15
5
5
5
5
10
5
5
5
2
i=1
and
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 :
Population growth rate = 100 * (ea - 1)
(9 .3)
g = [ln(W 2 ) - ln(W1)] / (t2 - t1)
(9 .4)
and
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
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
264
.
Ontogeny of cannibalism in larval and juvenile fishes
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
265
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 .
266
.
Ontogeny of cannibalism
in
larval and juvenile
fishes
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
267
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
268
.
Ontogeny of cannibalism in larval and juvenile fishes
Perspectives
the number and biomass of the youngest cohorts . Without the correction,
the stock appeared older and the calculated age-specific mortalities of the
releases of cod juveniles in a Norwegian fjord did not contribute signifi-
youngest age classes were underestimated . The authors further suggested
that in a stock where cannibalism by older year classes is common, a
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
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
abundance of ii-group cod was not different in release areas compared
reducing cannibalism (Lleonart et al., 1985) . These conclusions were
questioned by Punt and Hilborn (1994), who concluded that little
and other species on young cod is high (Ulltang, .1984), and the possibilities of a successful ranching programme will be higher when the popula-
precision in the management models was lost by omitting cannibalism
interactions in this species . This result was attributed to uncertainties in
tion involved is already at a low level due to overfishing .
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.
have also shown that it can be a major source of mortality and an
269
cantly to recruitment in the area, and attributed this to competition and
with control areas . The effects of cod enhancement programmes will
therefore most likely not be worthwhile if the predation pressure from cod
In summary, studies on intercohort cannibalism in cod and other species
MacCall (1981) incorporated cannibalism on eggs and larvae in a stock-
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
recruitment model and concluded that cannibalism in northern anchovy,
Engraulis mordax, is sufficiently intense to be a regulatory mechanism . The
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
densities of adult clupeoids are not generally proportional to stock size
eggs and larvae they produce, and not necessarily through a direct impact
owing to the expansion and contraction of ranges with varying
abundance . The harvest potential may thus depend on the spatial fishing
of their own abundance (Ricker, 1975) .
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
9 .5
PERSPECTIVES
migration pattern of the adults may, however, be influenced by stock size,
Cannibalism among fishes has in the past often been viewed as an artifact
as happened in the Norwegian spring-spawning herring, Clupea harengus,
following the collapse in the 1960s . The traditional migration pattern into
occurring under artificial circumstances . On the other hand, recent reviews
the Norwegian Sea after spawning was abandoned, and the stock remained
in fishes to be classified as an obscurity (Smith and Reay, 1991) .
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
indicate that cannibalism is far too widespread in the animal kingdom and
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
cannibalism by older conspecifics is responsible for a major part of the
an unequal contest where the smaller victim presents no direct risk to the
cannibal . The structural simplicity of the pelagic habitat, coupled with the
juvenile mortality, the effect of the release will be higher at lower stock
tendency of conspecifics to co-inhabit a common environment, will also
sizes or higher fishing pressure (Ulltang, 1984) . The gain from such a
release may, however, be lost if the fishing pressure exceeds that giving
promote multiple encounters between individuals of the same species . The
the maximum sustainable yield (MSY) of the natural population . Intercohort cannibalism of cod juveniles has been documented by stomach
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
analyses carried out in connection with the major cod enhancement
behavioural repertoire of many fish species (Polls, 1981 ; Edgar and Crespi,
programmes in Norway (Svasand and Kristiansen, 1990 ; Smestad et al .,
1994) . Smestad and co-workers (1994) concluded that the large-scale
1992) . The selective advantage of individuals exhibiting cannibalistic traits
is evident in situations of food shortage . In addition to increasing the fitness
270
271
Ontogeny of cannibalism in larval and juvenile fishes
Perspectives
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) .
of injury or disease, the existence of so-called runts may have evolutionary
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
small individuals serves the same purpose in fish populations, where some
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
tation for the pelagic environment, where the provided offspring in no way
can be 'reserved' for conspecifics, is questionable (Polis, 1988) .
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
polyphenism, i .e . phenotypic differences in behaviour, morphology, growth
rates or life history between cannibal and non-cannibal forms (Polis,
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
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
of the offspring are provided as suitable-sized prey for the largest individuals
later during ontogeny (Polis, 1981) . Whether this is an acceptable interpre-
In some amphibians there are well-documented accounts of cannibalistic
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
(1986), cannibalism of younger planktivorous conspecifics represents such
an intermediate trophic level . In their analysis of the life history of Japanese
to be cannibalistic . There are also polymorphic adaptations to reduce the
effect of predation and possibly cannibalism . Crucian carp, Carassius
fishes, Kawai and Isibasi (1983) observed a between-species discontinuity
in growth patterns during the juvenile period . The authors suggested that
carassius, living in ponds with larger piscivore predators develop enlarged
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
(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
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
body heights compared with those exposed to a lower predation risk
siblings .
Not surprisingly, a genetic component of cannibalistic behaviour has
been demonstrated (Thibault, 1974 ; Hecht and Pienaar, 1993) . Cannibalism 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
of other females rather than their own (Loekle et al ., 1982), but further
studies are needed to determine the mechanisms involved . Lower canni-
individuals (Blom et al ., 1994) . Caution is thus appropriate when selecting
for rapid growth among broodstock in cannibalistic species such as cod,
balism rates were also observed in full-sib groups of pike, Esox lucius,
compared with mixed groups (Bry and Gillet, 1980) . This could possibly
because the fast-growing survivors may also be the individuals with the
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
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
272
Ontogeny of cannibalism in larval and juvenile fishes
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
273
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 .
REFERENCES
Bailey, K .M . (1989) Interaction between the vertical distribution of juvenile walleye
pollock Theragra chalcogramma in the eastern Bering Sea, and cannibalism . Marine
Ecology Progress Series, 53, 205-213 .
Balon, E .K . (1984) Reflections on some decisive events in the early life of fishes .
Transactions of the American Fisheries Society, 113, 178-185 .
Blom, G ., Otters, H., Svssand, T . et al. (1991) The relationship between feeding
condition and production of cod fry (Gadus morhua L .) in a semi-enclosed marine
ecosystem in western Norway, illustrated by use of a consumption model . ICES
Marine Science Symposia, 192, 176-189 .
Blom, G ., Svsstad, K .E ., Otters, H . et al . (1994) Comparative survival and growth
of two strains of Atlantic cod (Gad us morhua) through the early life stages in a
marine pond. Canadian Journal of Fisheries and Aquatic Sciences, 51, 10121023 .
Bogstad, B., Lilly, G ., Mehl, .S . et al . (1993) Cannibalism and year-class strength in
Atlantic cod (Gadus morhua L .) in the Arcto-boreal ecosystems, Barents Sea,
Iceland and Eastern Newfoundland . ICES Marine Science Symposia, 198, 576599 .
Bolz, G .R . and Lough, R .G . (1988) Growth through the first six months of Atlantic
cod, Gadus morhua, and haddock, Melanogrammus aeglefinus, based on daily otolith
increments . Fishery Bulletin, U.S., 86, 223-235 .
van den Bosch, F ., Deroos, A .M . and Gabriel, W. (1988) Cannibalism as a life boat
mechanism . Journal of Mathematical Biology, 26, 619-633 .
Boudreau, P .R. and Dickie, L .M. (1992) Biomass spectra of aquatic ecosystems in
relation in fisheries yield . Canadian Journal of Fisheries and Aquatic Sciences, 49,
1528-1538 .
Brawn, V .M . (1969) Feeding behaviour of cod (Gadus morhua) . Journal of the
Fisheries Research Board of Canada, 26, 583-596 .
274
,
Ontogeny of cannibalism in larval and juvenile fishes
Brett, J .R . (1979) Environmental factors and growth, in Fish Physiology,
Vol . 8
(eds W .S . Hoar, D .J . Randal and J .R . Brett), London, Academic Press, pp . 599675 .
Brodeur, R .D ., Bailey, K .M . and Kim, S . (1991) Cannibalism on eggs by walleye
pollock Theragra chalcogramma in Shelikof Strait, Gulf of Alaska . Marine Ecology
Progress Series, 71, 207-218 .
Bry, C. and Gillet, C . (1980) Reduction of cannibalism in pike (Esox
lucius) fry by
isolation of full-sib families . Reproduction, Nutrition et Developpement, 20, 173182 .
Bry, C., Basset, E ., Rognon, X . and Bonamy, F . (1992) Analysis of sibling cannibalism among pike, Esox lucius, juveniles reared under semi-natural conditions .
Environmental Biology of Fishes, 35, 75-84 .
Campana, S .E . (1990) How reliable are growth back-calculations based on otoliths?
Canadian Journal of Fisheries and Aquatic Sciences, 47, 2219-2227 .
Crump, M .L . (1986) Cannibalism by younger tadpoles : another hazard to metamorphosis . Copeia, 1986, 1007-1009 .
Crump, M.L. (1992) Cannibalism in amphibians, in Cannibalism . Ecology and
Evolution among Diverse Taxa (eds M.A . Elgar and B.J . Crespi), Oxford University
Press, Oxford, pp . 256-276 .
Daan, N . (1973) A quantitative analysis of the food intake of North Sea cod, Gadus
morhua . Netherlands Journal of Sea Research, 6, 479-517 .
van Damme, P ., Appelbaum, S .A . and Hecht, T. (1989) Sibling cannibalism in Koi
carp, Cyprinus carpio L ., larvae and juveniles reared under controlled conditions .
Journal of Fish Biology, 34, 855-863 .
DeAngelis, D .L ., Cox, D.K. and Coutant, C .C . (1980) Cannibalism and size dispersal
in young-of-the-year largemouth bass : experiment and a model . Ecological
Modelling, 8, 133-148 .
van Densen, W .L.T . (1985) Piscivory and the development of bimodality in the size
distribution of 0 + pikeperch (Stizostedion lucioperca L .) . Zeitschrift fur Angewandte
Ichthyologie, 3, 119-131 .
Dong, Q. and Polis, G .A . (1992) The dynamics of cannibalistic populations : a
foraging perspective, in Cannibalism . Ecology and Evolution among Diverse Taxa
(eds M.A . Elgar and B.J . Crespi), Oxford University Press, Oxford, pp . 13-37 .
Dwyer, D .A ., Bailey, K .M . and Livingston, P .A . (1987) Feeding habits and daily
ration of walleye pollock (Theragra chalcogramma) in the eastern Bering Sea, with
special reference to cannibalism . Canadian Journal of Fisheries and Aquatic Sciences,
44,1972-1984.
Economou, A .N. (1991) Is dispersal of fish eggs, embryos and larvae an insurance
against density dependence? Environmental Biology of Fishes, 31, 313-321 .
Elgar, M.A . and Crespi, B .J. (eds) (1992) Cannibalism . Ecology and Evolution among
Diverse Taxa, Oxford University Press, Oxford, 351 pp .
Ellertsen, B ., Fossum, P ., Solemdal, P . and Tilseth, S . (1984) A case study on the
distribution of cod larvae and availability of prey organisms in relation to
physical processes in Lofoten . Fledevigen Rapportserie, 1, 453-477 .
Folkvord, A . (1991) Growth, survival and cannibalism of cod juveniles (Gadus
morhua L .) : effects of feed type, starvation and fish size . Aquaculture, 97, 41-59 .
Folkvord, A . (1993) Prey recognition in stomachs of cannibalistic juvenile cod
(Gad us morhua L.) . Sarsia, 78, 97-100 .
Folkvord, A . and Otters, H . (1993) Effects of initial size distribution, day length and
feeding frequency on growth, survival and cannibalism in juvenile Atlantic cod
(Gad us morhua L .) . Aquaculture, 114, 243-260 .
References
275
Folkvord, A ., Blom, G ., Dragesund, 0 . et al . (1994a) A conceptual framework for
enhancing and stabilizing recruitment of marine fish stocks . Aquaculture and
Fisheries Management, 25, 245-258 .
Folkvord, A., Oiestad, V . and Kvenseth, P .G . (1994b) Growth patterns of three
cohorts of Atlantic cod larvae (Gadus morhua L .) studied in a macrocosm . ICES
Journal of Marine Science, 51, 325-336 .
Foster, S .A ., Garcia, V .B . and Town, M .Y . (1988) Cannibalism as the cause of an
ontogenetic shift in habitat use by fry of the threespine stickleback . Oecologia,
74,577-585 .
Giles, N ., Wright, R .M . and Nord, M.E . (1986) Cannibalism in pike fry, Esox lucius
L. : some experiments with fry densities . Journal of Fish Biology, 29, 107-113 .
Gode, O .R., Valdemarsen, J .W . and Engss, A . (1993) Comparison of efficiency of
standard and experimental juvenile gadoid sampling trawls . ICES Marine Science
Symposia, 196, 196-201 .
Hanson, J.M . and Chouinard, G .A . (1992) Evidence that size-selective mortality
affects growth of Atlantic cod (Gadus morhua L .) in the southern Gulf of St
Lawrence . Journal of Fish Biology, 41, 31-41 .
Hausfater, G . and Hrdy, S .B . (eds) (1984) Infanticide: Comparative and Evolutionary
Perspectives, Aldine Publishing Co ., New York, 598 pp .
Hecht, T . and Appelbaum, S .A . (1988) Observations on intraspecific aggregation
and coeval sibling cannibalism by larval and juvenile Clarias gariepinus
(Clariidae : Pisces) under controlled conditions . Journal of Zoology, 214, 21-44 .
Hecht, T . and Pienaar, A .G . (1993) A review of cannibalism and its implications in
fish larviculture . Journal of the World Aquaculture Society, 241, 246-261 .
Howell, B .R . (1984) The intensive rearing of juvenile cod, Gadus morhua L . Fladevigen Rapportserie, 1, 657-675 .
Hunter, J .R . and Kimbrell, C .A . (1980a) Early life history of Pacific mackerel,
Scomber japonicus . Fishery Bulletin, U.S ., 78, 89-101 .
Hunter, J .R. and Kimbrell, C .A . (1980b) Egg cannibalism in the northern anchovy,
Engraulis mordax . Fishery Bulletin, U.S., 78, 811-816 .
Huston, M.A . and DeAngelis, D .L . (1987) Size bimodality in monospecific populations: a critical review of potential mechanisms . American Naturalist, 129, 678707 .
Katavic, I ., Jug-Dujakovic, J . and Glamuzina, B . (1989) Cannibalism as a factor
affecting the survival of intensively cultured sea bass (Dicentrarchus labrax) fingerlings . Aquaculture, 77, 135-143 .
Kawai, T . and Isibasi, K . (1983) Change in abundance and species composition of
neritic pelagic fish stocks in connection with larval mortality caused by cannibalism and predatory loss by carnivorous plankton . FAO Fisheries Report, 3,
1082-1111 .
Knutsen, G .M. and Tilseth, S. (1985) Growth, development and feeding success of
Atlantic cod larvae Gadus morhua related to egg size . Transactions of the American
Fisheries Society, 114, 507-511 .
Koeller, P .A ., Coates-Markle, L . and Neilson, J .D . (1989) Feeding ecology of juvenile
(age-0) silver hake (Merluccius bilinearis) on the Scotian Shelf . Canadian Journal of
Fisheries and Aquatic Sciences, 46, 1762-1768 .
Kraul, S ., Nelson, A ., Brittain, K . et al . (1992) Evaluation of live feed for larval and
postlarval Mahi mahi Coryphaena hippurus . Journal of the World Aquaculture
Society, 23, 299-306 .
Li, S . and Mathias, J .A . (1982) Causes of high mortality among cultured larval
walleyes. Transactions of the American Fisheries Society, 111, 710-721 .
276
.
277
Ontogeny of cannibalism in larval and juvenile fishes
References
Lleonart, J., Salat, J . and MacPherson, E. (1985) CVPA, an extended VPA with
cannibalism . Application to a hake population . Fisheries Research, 3, 61-79 .
Loekle, D .M ., Christian, J.J . and Madison, D .M . (1982) Time dependency and kin
recognition of cannibalistic behavior among poeciliid fishes . Behavioral and
Neural Biology, 35, 315-318 .
MacCall, A .D . (1981) The consequences of cannibalism in the stock-recruitment
relationship of planktivorous pelagic fishes such as Engraulis, in Workshop on the
effects of environmental variation on the survival of larval pelagic fishes (rapporteur G .
Sharp) . UNESCO Intergovernmental Oceanographic Commission, Workshop
Report, 28, pp . 201-220 .
McIntyre, D .B ., Ward, F .J . and Swanson, G .M. (1987) Factors affecting cannibalism by pond reared juvenile walleyes . The Progressive Fish-Culturist, 49, 264269 .
Macpherson, E, and Gordoa, A . (1994) Effect of prey densities on cannibalism in
Cape hake (Merluccius capensis) off Namibia . Marine Biology, 119, 145-149 .
van der Meeren, T . and Na?ss, T . (1993) How does cod (Gadus morhua) cope with
variability in feeding conditions during early larval stages? Marine Biology, 112,
637-647 .
Mehl, S . (1988) The Northeast Arctic cod stock's consumption of commercially
exploited prey species in 1984-1986 . Rapports et Proces-verbaux des Reunions,
Conseil International Pour ]'Exploration de la Mer, 188, 185-205 .
Nellen, W . (1986) A hypothesis on the fecundity of bony fish . Meeresforschung, 31,
75-89 .
Nesbit, D .H . and Meffe, G .K . (1993) Cannibalism frequencies in wild populations of
the eastern mosquitofish (Gambusia holbrooki, Poeciliidae) in South-Carolina .
Copeia, 1993, 867-870 .
Oiestad, V . (1985) Predation on fish larvae as a regulatory force, illustrated in
mesocosm studies with large groups of larvae . NAFO Science Council Studies, 8,
25-32 .
Olsen, S . and Soldal, A .V . (1989) Observations on inshore distribution and
behaviour of 0-group northeast Arctic cod . Rapports et Proces-verbaux des
Reunions, Conseil International Pour ]'Exploration de la Mer, 191, 296-302 .
Otters, H . (1992) Bias in calculating growth rates in cod (Gadus morhua L.) due to
size selective growth and mortality . Journal of Fish Biology, 40, 465-467 .
Otters, H . and Folkvord, A . (1993) Allometric growth in juvenile cod (Gadus morhua
L .) and possible effects on cannibalism . Journal of Fish Biology, 43, 643-645 .
Otters, H . and Lie, 0 . (1991) Weaning trials with cod (Gadus morhua L.) fry on
formulated diets. Fiskeridirektoratets Skrifter, Serie Ernaring, IV, 85-94 .
Otterlei,-E ., Folkvord, A . and Moller, D . (1994) Effects of temperature and density on
growth, survival, and cannibalism of juvenile cod (Gadus morhua L .) . ICES Marine
Science Symposia, 198, 632 .
Parazo, M.M., Avila, E .M . and Reyes, D .M. Jun . (1991) Size- and weight dependent
cannibalism in hatchery-bred sea bass (Lates calcarifer Bloch) . Journal of Applied
Ichthyology, 7, 1-7 .
Patriquin, D.G . (1967) Biology of Gadus morhua in Ogac Lake, a landlocked fjord on
Baffin Island. Journal of the Fisheries Research Board of Canada, 24, 2573-2594 .
Pedersen, T . and Falk-Petersen, I .B . (1992) Morphological changes during
metamorphosis in cod (Gadus morhua L .), with special reference to the development of the stomach and pyloric caeca . Journal of Fish Biology, 41, 449-461 .
Pepin, P . (1989) Predation and starvation of larval fish : a numerical experiment of
size- and growth-dependent survival . Biological Oceanography, 6, 23-44.
Perry, R.I . and Neilson, J .D. (1988) Vertical distributions and trophic interactions of
age-0 Atlantic cod and haddock in mixed and stratified waters of Georges Bank .
Marine Ecology Progress Series, 49, 199-214 .
Peterman, R .M . (1991) Density-dependent marine processes in North-Pacific
salmonids : lessons for experimental design of large-scale manipulations of fish
stocks . ICES Marine Science Symposia, 192, 69-77 .
Pfennig, D .W. and Collins, J .P . (1993) Kinship affects morphogenesis in cannibalistic salamanders . Nature, 362, 836-838 .
Pfenning, D .W ., Reeve, H .K . and Sherman, P.W. (1993) Kin recognition and cannibalism in spadefoot toad tadpoles . Animal Behaviour, 46, 87-94 .
Pitcher, T .J. and Parrish, J .K . (1993) Functions of shoaling behaviour in teleosts, in
Behaviour of Teleost Fishes, 2nd edn (ed . T .J . Pitcher), London, Chapman and Hall,
pp . 363-439 .
Polls, G .A. (1981) The evolution and dynamics of intraspecific predation . Annual
Review of Ecology and Systematics, 12, 225-251 .
Polis, G .A . (1988) Exploitation competition and the evolution of interference, cannibalism, and intraguild predation in age/size-structured populations, in Size-structured Populations (eds B. Ebenman and L . Persson), Berlin, Springer-Verlag, pp .
185-202 .
Polis, G .A . and Myers, C .A . (1985) A survey of intraspecific predation among
reptiles and amphibians. Journal of Herpetology, 19, 99-107 .
Post, J .R. (1990) Metabolic allometry of larval and juvenile yellow perch (Perca
flavescens) : in situ estimates and bioenergetic models . Canadian Journal of Fisheries
and Aquatic Sciences, 47, 554-560 .
Punt, A.E. and Hilborn, R . (1994) A comparison of fishery models with and without
cannibalism with implications for the management of the Cape hake resource off
southern Africa . ICES Journal of Marine Science, 51, 19-29 .
Rice, J .A ., Miller, T .J ., Rose, K .A . et al . (1993) Growth rate variation and larval
survival : inferences from an individual based size-dependent predation model .
Canadian Journal of Fisheries and Aquatic Sciences, 50, 133-142 .
Ricker, W .E . (1975) Computation and interpretation of biological statistics of
fish populations . Bulletin of the Fisheries Research Board of Canada, 191, 1382 .
Riley, J .D . and Parnell, W .G . (1984) The distribution of young cod . Flodevigen
Rapportserie, 1, 563-580 .
Rosenberg, A .A . and Haugen, A .S . (1982) Individual growth and size-selective
mortality of larval turbot, Scophthalmus maximus reared in enclosures . Marine
Biology, 72, 73-77 .
Rettingen, I . (1990) A review of variability in the distribution and abundance of
Norwegian spring spawning herring and Barents Sea capelin . Polar Research, 8,
33-42 .
Salvanes, A .G .V ., Giske, J. and Nordeide, J .T . (1994) Life-history approach to habitat
shifts for coastal cod, Gadus morhua L . Aquaculture and Fisheries Management, 25,
215-228 .
SalveSandlund, O .T ., Gunnarsson, K ., Jonasson, P .M. et al . (1992) The arctic char
linus alpinus in Thingvallavatn . Oikos, 64, 305-351 .
Shirota, A . (1970) Studies on the mouth size of fish larvae . Bulletin of the Japanese
Society for Scientific Fisheries, 36, 353-368 .
Smestad, O.M., Foss6, J.H., Salvanes, A.G .V . and Nordeide, J.T. (1994) Enhancement of cod, Gadus morhua L ., in Masfjorden, western Norway : an overview .
Aquaculture and Fisheries Management, 25, 117-128 .
278
.
Ontogeny of cannibalism in larval and juvenile fishes
Smith, C . and Reay, P . (1.991) Cannibalism in teleost fish . Reviews in Fish Biology
and Fisheries, 1, 41-64.
Sogard, S . and Olla, B .L . (1994) The potential for intracohort cannibalism in age-0
walleye pollock, Theragra chalcogramma as determined under laboratory conditions . Environmental Biology of Fishes, 39, 183-190 .
Suthers, I .M . and Sundby, S . (1993) Dispersal and growth of pelagic juvenile ArctoNorwegian cod (Gadus morhua), inferred from otolith microstructure and water
temperature. ICES Journal of Marine Science, 50, 261-270 .
Svasand, T . and Kristiansen, T .S . (1990) Enhancement studies of coastal cod in
western Norway . Part IV . Mortality of reared cod after release . Journal du
Conseil, Conseil International Pour l'Exploration de la Mer, 47, 30-39 .
Thibault, R .E . (1974) Genetics of cannibalism in a viviparous fish and its relationship to population density . Nature, 251, 130-140 .
Tonn, W .M ., Holopainen, I .J . and Paszkowski, C .A . (1994) Density-dependent effects
and the regulation of crucian carp populations in single-species ponds . Ecology,
75,824-834 .
Tsukamoto, K ., Kuwada, H ., Hirokawa, J . et al . (1989) Size-dependent mortality of
red sea bream, Pagrus major, juveniles released with fluorescent otolith-tags in
News Bay, Japan . Journal of Fish Biology, 35, 59-69 .
Ulltang, 0 . (1984) The management of cod stocks with special reference to growth
and recruitment overfishing and the question whether artificial propagation can
help to solve management problems . Fledevigen Rapportserie, 1, 795-817 .
Valdes Szeinfeld, E .S . (1991) Cannibalism and intraguild predation in clupeoids .
Marine Ecology Progress Series, 79, 17-26.
Walls, S .C . and Roudebush, R .E . (1991) Reduced aggression toward siblings as
evidence of kin recognition in cannibalistic salamanders . American Naturalist,
138,1027-1038 .
Wiborg, K .F . (1948) Experiments with Clarke-Bumpus plankton sampler and a
plankton pump in the Lofoten area in northern Norway . Fiskeridirektoratets
Skrifter, Serie Havundersekelser, 9 1-23 .
Wiborg, K .F . (1960) Investigations on pelagic fry of cod and haddock in coastal and
offshore areas of northern Norway in July-August 1957 . Fiskeridirektoratets
Skrifter, Serie Havundersekelser, 12, 1-18 .
Young, J.W. and Davies, T .L .O . (1990) Feeding ecology of larvae of southern
bluefin, albacore and skipjack tunas (Pisces : Scombridae) in the eastern Indian
Ocean . Marine Ecology Progress Series, 61, 17-29 .