Aquaculture 305 (2010) 42–51
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Aquaculture
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / a q u a - o n l i n e
Why is cannibalism so rare among cultured larvae and juveniles of
Pangasius djambal? Morphological, behavioural and energetic answers
E. Baras a,⁎, R. Hafsaridewi b, J. Slembrouck c, A. Priyadi d, Y. Moreau a,c, L. Pouyaud a,c, M. Legendre a
a
IRD, UR 175, BP 5095, Rue J.F. Breton 361, F-34196 Montpellier Cedex 05, France
Loka Riset Pemuliaan dan Teknologi Budidaya Perikanan Air Tawar (LRPTBPAT), Jl. Raya Sukamandi No. 2, Subang 41256, Indonesia
IRD, UR 175, c/o Loka Riset Budidaya Ikan Hias Air Tawar (LRBIHAT), Jl. Perikanan-PO Box 06, Depok 41152, Indonesia
d
Loka Riset Budidaya Ikan Hias Air Tawar (LRBIHAT), Jl. Perikanan-PO Box 06, Depok 41152, Indonesia
b
c
a r t i c l e
i n f o
Article history:
Received 6 July 2009
Received in revised form 3 April 2010
Accepted 6 April 2010
Keywords:
Aquaculture
Ontogeny
Teeth
Prey-size selectivity
Growth
Conversion
a b s t r a c t
The ontogenetic trajectory of Pangasius djambal resembles that of Pangasianodon hypophthalmus. At the start
of exogenous feeding (48 h after hatching), larvae of P. djambal (8.5 mm TL, 4.5 mg WM) exhibit a large gape
(17.5% TL), they possess long oral spines (100 µm) but no pectoral ﬁns. However, the spines do not overhang
from the mouth, and gape height never exceeds body depth, contrary to the situation in P. hypophthalmus.
These differences account for why encounters between larvae of P. djambal never lead to the deadly clashes
observed in P. hypophthalmus. The rarity of cannibalism in older larvae and juveniles of P. djambal originates
from the combination of morphological, behavioural and energetic factors (studied during predation
experiments with cannibals from 20 to 70 mm TL): (1) the negative allometry of mouth parts and positive
allometry of body depth restrict the logistics of cannibalism from 84.9% TL at 10 mm TL to 56.5% TL at
40 mm TL; (2) cannibals of increasing size prefer prey that are increasingly smaller relative to the logistics of
cannibalism (pref:max TL ratios of 99 and 48.5% at 10 and 40 mm TL, respectively); and (3) cannibals need
high maintenance food rations (14.9% DM at 6–10 mg DM), they exhibit a rather low gross conversion
efﬁciency (0.36 DM:DM at 6 mg DM), and gain no growth advantage over siblings fed brine shrimp nauplii
ad libitum. No single factor sufﬁces to account for the rarity of cannibalism in P. djambal, but their
combination almost makes it impossible, even among ﬁsh fed submaximally.
© 2010 Elsevier B.V. All rights reserved.
1. Introduction
Intracohort cannibalism can cause heavy losses during the early
life stages of cultured ﬁsh. The mechanisms that govern the dynamics
of cannibalism are shared by a vast number of ﬁsh species, and closely
related to the factors that govern growth heterogeneity (DeAngelis
et al., 1979; Hecht and Appelbaum, 1988; Smith and Reay, 1991;
Hecht and Pienaar, 1993; Folkvord, 1997; Baras, 1998; Baras and
Jobling, 2002; Kestemont et al., 2003).
Cannibalism is governed by morphological, behavioural and
physiological factors. The heaviest losses among cultured larvae and
juveniles have been reported in species that grow a large gape and
long oral teeth at the start of exogenous feeding (Scomberomorus
niphonius, Shoji et al., 1997; Shoji and Tanaka, 2001; Brycon moorei,
Baras et al., 2000; Sarda orientalis, Kaji et al., 2002). Early cannibalism
is generally incomplete but nevertheless facilitated by size dispersal
⁎ Corresponding author. Tel.: + 33 4 67 04 63 61; fax: +33 4 67 16 64 40.
E-mail address: [email protected] (E. Baras).
0044-8486/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquaculture.2010.04.004
(Folkvord and Otterå, 1993; Baras and d'Almeida, 2001). In turn,
incomplete (type I) cannibalism generally provides cannibals with
some growth advantage, increases size dispersal and facilitates the
transition to complete (type II) cannibalism (Hecht and Appelbaum,
1988; Kestemont et al., 2003; Babiak et al., 2004). The occurrence of
complete cannibalism intimately depends on whether cannibals are
capable of swallowing large prey relative to their size (logistics of
cannibalism e.g. Braband, 1995; Hseu et al., 2003), but also on
whether they are keen or reluctant to do so (prey-size selectivity;
e.g. Baras, 1999). The risk of cannibalism also depends on how fast the
cannibals grow relative to their potential victims. The answer to this
question is not straightforward, as growth depends not only on food
type and availability (Folkvord and Otterå, 1993; Fermin and Seronay,
1997; Kubitza and Lovshin, 1999; Kestemont et al., 2007), but also on
ﬁsh size. Whether the growth advantage provided by cannibalism is
decisive and enables the continuation of cannibalism, thus also
depends on the logistics of cannibalism and on prey-size selectivity,
and on how these factors vary during the ontogeny.
These functional mechanisms and the roles of inﬂuencing factors
are well admitted, but their interactions are generally subtle, and
make it difﬁcult to forecast the actual impact of cannibalism in a
particular rearing environment. Similarly, the risk of cannibalism in
E. Baras et al. / Aquaculture 305 (2010) 42–51
species that have been domesticated recently, or that are candidates
for the diversiﬁcation of aquaculture can hardly be predicted, except
possibly from the analysis of morphological factors, which are
generally good indicators of the risk of cannibalism (e.g. mouth size,
Shirota, 1970). Until now, research on cannibalism among cultured
ﬁsh has largely been ﬁnalistic in that it focused essentially on species
with frequent or intense cannibalistic habits. However, the study of
species that rarely exercise cannibalism under culture conditions can
be equally informative, especially in a comparative context with other
close taxa that exhibit frequent or intense cannibalism.
Such comparison is of particular interest among the family
Pangasiidae (Siluriformes), which comprises 28 species (Gustiano,
2003), but the bulk of the production (over 1 million tons in Southeast
Asia since 2007; Lazard et al., 2009) originates so far from the culture
of three species: Pangasianodon hypophthalmus, Pangasius bocourti
and Pangasius djambal. Several other pangasiids are potential
candidates to the diversiﬁcation of pangasiid culture (Pangasianodon
gigas, Pangasius conchophilus, P. kremﬁ and P. nasutus), but criteria are
needed to select wisely between these. In P. hypophthalmus, by far the
main cultivated pangasiid, episodes of intense mortality and cannibalism are almost systematic during the early life stages (Hardjamulia
et al., 1981; Subagja et al., 1999; Slembrouck et al., 2009), whereas
they are very rare in P. bocourti (Hung et al., 1999, 2002) and P. djambal
(Legendre et al., 2000; Slembrouck et al., 2004). The functional
mechanisms behind the early mortality of P. hypophthalmus have been
elucidated recently (Baras et al., 2010). The present study aimed at
investigating why cannibalism is so rare among larvae and juveniles of
P. djambal. It examined the ontogenetic variations of morphological
traits, but also of prey-size selectivity and bioenergetics, which
intimately govern the dynamics of cannibalism in cultured ﬁsh.
2. Methods
2.1. Fish and rearing conditions
The ﬁsh used in this study were half siblings that were produced
from the artiﬁcial reproduction of captive broodﬁsh at the research
station of LRPTBPAT Sukamandi (Java, Indonesia) (see Slembrouck
et al., 2004 for details on the hormonal induction and egg incubation
techniques). Fish were transported during the egg incubation stage to
the experimental facilities of LRBIHAT Depok (Java, Indonesia), where
all experiments were conducted. Hatching took place 36 h after
fertilization. From 44 h after hatching (hah) onwards, brine shrimp
(Artemia sp.) nauplii were supplied during the hours of light. Fish
larger than 50 mg (wet body mass, hereafter WM) were fed
commercial formulated feed (PS-P, Pt Central Panganpertiwi,
Indonesia, 40% crude protein). Rearing took place in indoor 170-L
aquaria at ambient temperature (mean of 28.3 °C, daily means from
27.3 to 29.4 °C, total range of 25.8–30.2 °C). A group of ﬁsh was fed in
excess at least 5 times per day, and another one only twice per day, in
order to produce rapidly a size differential for the predation
experiments (see below). The third tank was spared for morphological
samples (3 or 4 meals per day). Faeces, excess food and dead ﬁsh were
removed every day with a siphon.
2.2. Morphology
Fish were sampled for morphological examination at least twice
per day during the ﬁrst 5 days after hatching (dah), at daily intervals
until 16 dah, and occasionally thereafter until they attained 50 mm
in total length (TL). At every sampling time, at least ﬁve ﬁsh were
anaesthetised (2-phenoxy-ethanol, 0.40 mL L−1) and placed under
the stereomicroscope (Wild M3, × 6–50) and under the microscope
(Leica Biomed) for examining the jaws and oral teeth at greater
magniﬁcation (x100). The variables under study were limited to
those governing the logistics of complete cannibalism in ﬁsh (mouth
43
width, gape height, body depth and width), and to those identiﬁed
as the keys to the episodes of early mortality among larvae of
P. hypophthalmus (ﬁn development sequence, oral teeth; Baras et al.,
2010). All variables were measured with a graduated eyepiece, and
expressed by reference to the ﬁsh TL. Gape height was calculated
from jaw length and gape opening angle, which was assumed to
attain no more than 120°, by analogy with the study in
P. hypophthalmus (Baras et al., op. cit.). Thereafter ﬁsh were weighed
(nearest 0.1 mg), either individually for ﬁsh N 5 mg or in groups of 5–
10 individuals for smaller ﬁsh, so as to document the relationship
between WM and TL.
2.3. Design of predation experiments
All experiments had the same canvas, inspired by Baras (1999) and
Baras et al. (2000). A single cannibal was placed in a ﬂoating cage
together with smaller siblings (potential prey) of known dimensions.
No food was provided. Every 24 h, ﬁsh were collected and cages were
cleaned to remove faeces. The cannibal was anaesthetised, weighed,
revived and returned to the same cage as on the previous day,
together with a new set of prey ﬁsh. In the meanwhile, surviving prey
ﬁsh were anaesthetised and measured, in order to determine which
prey had been eaten.
Cannibals were studied for several days in a row whereas prey ﬁsh
were changed every day. It mattered that survivors were not pooled
with other prey, because the weight loss on the ﬁrst, second or third
day of food deprivation differ substantially, and because small ﬁsh
might be exhausted by prolonged starvation. Conversely, survivors
might have gained experience in evading the cannibal's attacks, and
this might also bias the analysis of prey-size selectivity. Hence
surviving prey were never re-used in a subsequent experiment. No
more than seven cages were examined each day in order to reduce the
monitoring period to 30 min.
As regards the size of prey ﬁsh, three criteria had to be fulﬁlled:
(1) all (or most) prey had to be small enough to be eaten whole by the
cannibals; (2) the size distribution of prey ﬁsh had to be broad enough
to give the cannibal the opportunity of selecting between prey of
different sizes, and (3) prey ﬁsh should be incapable of eating each
other, otherwise the food intake of the cannibal would be overestimated. The size ratio between the cannibals and their prey, and
the acceptable limits to prey-size heterogeneity were calculated from
the data produced during the morphological part of this study. In
order to ascertain that prey ﬁsh did not consume each other, a control
group, consisting of prey ﬁsh with a similar size distribution but
without any large cannibal, was examined each day.
Prey ﬁsh were distributed in excess of the presumed cannibal's
needs, for three reasons: (1) prey density affects the propensity to
feed (Houde and Schekter, 1980); (2) it was important to avoid
cannibals selecting prey outside of their preferred range, simply
because they had already consumed all those of adequate size, and
(3) numerous prey were needed in case the cannibals aggress and kill
some prey ﬁsh without eating them. Up to 25 prey ﬁsh were offered to
each cannibal during the ﬁrst days of the study, and at least 15
thereafter. This design prevailed throughout the study. However, on
some occasions, no prey was offered for 24 h or the number of prey
ﬁsh was deliberately well below the presumed needs of the cannibal,
so as to document the relationships between ﬁsh growth and food
ration for a broad range of food rations. Situations where the cannibals
were not offered prey in excess were excluded from the database for
studying prey-size selectivity.
All prey ﬁsh were large enough (N9 mm TL) to be weighed
individually without damage. Their TL was back-calculated for the
study of prey-size selectivity, using a model that was constructed with
an independent sample of ﬁsh with empty guts (but having incurred
no period of food deprivation longer than a few hours).
44
E. Baras et al. / Aquaculture 305 (2010) 42–51
2.4. Experimental infrastructure for predation experiments
The predation cages were installed in an indoor 720-L tank
(300 × 60 × 40 (h) cm) tank equipped with a recirculating pump
(Resun SP, 2800 L h−1) that was connected a long plastic pipe set
along the long axis of the tank. Water temperature was maintained
with two 300-W submersible heaters coupled to a Biotherm 2000
thermostat set at 28 °C. The water delivery pipe was sealed and water
was forced through small (b2 mm in diameter) holes drilled at 25-cm
intervals, which contributed to cool water temperature and to buffer
the variations of temperature between different days or periods of the
day (from 27.5 to 28.5 °C here versus 25.8–30.2 °C in non-regulated
systems). Supplemental oxygenation was provided by an air turbine
that was connected to four air stones spread along the long axis of the
tank.
Predation cages were set on the margins of the tank. Each cage was
a 2.0-L cylindrical plastic container (20 cm in diameter, 20 cm in
height), in which three large (15 × 12 cm) windows had been pierced
and covered with ﬁne plastic mesh (mesh size of 0.2 mm) afﬁxed with
silicone. The bottom plate and the lowest part of the cages were left
intact, in order to maintain a minimum water volume when the cages
were removed for examinations. During the predation experiments,
the cages were covered with a translucent plastic top and fully
immersed into the experimental tank to minimise external inﬂuences
on ﬁsh behaviour.
2.5. Identiﬁcation of consumed prey
For each cage and day of experiment, the WM of eaten prey were
estimated with a two-step back-calculation protocol relying on the
primacy of early size differences, which is a valid assumption among
starved ﬁsh (Baras et al., 2000). First, the WM of prey ﬁsh after 24 h of
food deprivation was estimated from the negative growth rate that
was measured in the control group. Thereafter, missing cases in the
ﬁnal distribution were moved by successive iterations in order to test
for all possible combinations and determine the best ﬁt with simple
linear regression tests (i.e. the combination with the highest r2 and a
slope of 1.00).
2.6. Data analysis: bioenergetics
For the analysis of bioenergetics, all data were expressed in terms
of dry body mass (DM), as the water content (WC) of ﬁsh varies
substantially during the ontogeny (Fig. 1). On each day of experiment,
WC was measured in an additional group of prey ﬁsh of similar size as
in the predation cages. The ﬁsh were anaesthetised, weighed (WM),
euthanized (2-phenoxy-ethanol, 2.0 mL L−1), placed at 105 °C overnight, and then weighed again for the measure of DM. The same
protocol was used for measuring WC in the control group after 24 h of
food deprivation, so as to determine the loss of wet body mass over
this period. The exact moments of cannibalism were unknown, so
it was assumed that prey ﬁsh were on average eaten at mid of each
24-h period. The daily food ration of the cannibal (R, mg DM) was thus
calculated as R = ∑0.01(1 − 0.5WCf − 0.5WCi)(0.5WMf + 0.5WMi),
where WC is the water content (%), WM is the wet mass (mg) of eaten
prey ﬁsh, and sufﬁxes f and i stand for ﬁnal and initial, respectively.
WMf was calculated as WMf = WMi(1 − WML), where WML is the
proportion of wet mass lost during 24 h of starvation (data from the
control group).
The food ration was expressed as a proportion of the cannibal's dry
mass at the start of the 24-h period (DMci). Cannibals were weighed
(WM) every day, but their WC could not be determined on a daily
basis, as they were studied several days in a row. It was deduced from
an independent data set, using ﬁsh fed in slight excess with brine
shrimp nauplii, weighed after gut emptying, and processed as above.
The measurements were done on groups of ﬁsh producing at least
Fig. 1. Ontogenetic variation of the dry matter content in P. djambal. Each symbol on the
graph refers to a group of ﬁsh producing at least 30 mg of DM. The curve is restricted to
ﬁsh having fully absorbed their yolk, and comes from a ﬁfth order polynomial model,
i.e. DM (% WM) = 27.489− 52.015(log WM)+ 61.277(log WM)2 − 34.296(log WM)3 +
9.158(log WM)4 − 0.921(log WM)5(R2 = 0.994, F = 633.0, df = 25, P b 0.0001).
30 mg of DM (tens of ﬁsh for larvae, at least three ﬁsh for large
juveniles).
The daily growth rate of cannibals (G, % DMci day−1) was
calculated as G = 100(DMcf − DMci)DMci−1, where DMcf and DMci
are the dry masses of cannibals at 1-day intervals. The gross
conversion efﬁciency (GCE, DM:DM) was calculated as GCE = GR−1,
where G is the daily growth rate and R is the daily food ration (both in
% DMci). The values of GCE, R and G were equated to ﬁsh size. Simple
power regression models were constructed from the highest values in
ﬁsh of different sizes, with the objective of tracking the top
performances of cannibals that determine the maximum risk of
cannibalism. In parallel, G was equated with R (simple regression
analyses) for calculating the (negative) growth during 24-h starvation
(GS) and the maintenance food ration (Rmaint) producing zero growth.
These calculations were made on a discrete basis, using ﬁve classes of
cannibal size. Thereafter, the ﬁve values of Gs and Rmaint were equated
with ﬁsh size, using the mean size of cannibals within each class.
2.7. Calculation of prey-size preference indices
Normalized preference indices (Bovee, 1986) were preferred to
electivity indices, which are still debated (Baras, 1999). For each size
class of cannibals, two indices were calculated. For the ﬁrst index, prey
size was expressed as a proportion of the cannibal TL. For the second
index, it was expressed as a proportion of the largest prey that could
be eaten whole by the cannibal (logistics of complete cannibalism),
with the objective of testing whether cannibals of different sizes
showed similar prey-size selectivity in respect to their predation
capacities. For both ways of calculations, prey sizes were categorized
into classes (2% cannibal TL and 4% logistics, respectively). The
preference index Ip of cannibals for each class of prey size was
calculated as Ip = NcNa−1, where Nc and Na are the numbers of
consumed and available prey in this size class. In order to enable
direct comparisons between cannibals of different sizes, the Ip values
were normalized, with the highest value ﬁxed at 1.00.
2.8. Statistical analyses
Contingency tables analyses were used to test for random prey
selection for each size class of cannibals, and whether cannibals of
different sizes exhibited different preferences with respect to their
logistics of cannibalism. Simple and power regression analyses were
used for the study of bioenergetics (see above) and to model the
E. Baras et al. / Aquaculture 305 (2010) 42–51
relationships between morphological factors. Null hypotheses were
rejected at P b 0.05.
45
20 mm TL but they did not attain their maximum size (8.5% TL) before
the end of the larval period (i.e. when the ﬁnfold had vanished, at
26 mm TL).
3. Results
3.1. General
The yolk of P. djambal averaged 3.5 mm3 at the time of fertilization,
and 2.6 mm3 at hatching, 36 h later. Hatchlings averaged 5.1 ±
0.2 mm TL (mean ± SD). Fish commenced feeding between 48 and
54 hah, at 8.5 ± 0.5 mm TL. The yolk was not fully exhausted before
84 hah (9.9 ± 0.4 mm TL). Fish fed 3–4 meals per day grew at an
average 1.1 mm day−1, and attained 44.2 ± 5.5 mm TL at 35 dah. The
relationship between WM and TL in ﬁsh having completely absorbed
their yolk (8.9–71.2 mm TL, and 5–2853 mg WM) was:
log WM = −2:154½0:020 + 3:020½0:013 log TL
Where values between brackets are the standard errors of coefﬁcients
(r2 = 0.996, F = 52,097, df = 192, P b 0.0001 for intercepts and slopes).
3.2. Morphology
3.2.1. Fin development sequence
At hatching, no ﬁns were developed but the ﬁnfold was already
structured in a series of lobes in the abdominal, anal, caudal and
“adipose” regions. The ﬂexure of the notochord occurred at 12–18 hah
and was accompanied by a rapid development of the upper lobe of the
caudal ﬁn. The caudal ﬁn remained strongly asymmetric throughout
the larval stage, until ﬁsh were 25 mm TL (Fig. 2). The adipose ﬁn had
already attained its longest dimension relative to body length (5% TL)
before the start of exogenous feeding, and exhibited a marked
negative allometric growth after the dorsal ﬁn started elongating (at
about 8 mm TL). The dorsal ﬁn continued growing allometrically up to
15–16% TL until ﬁsh attain 40 mm TL. This pattern strongly contrasted
with that of the anal ﬁn, which had already attained its longest
dimension (10% TL) when ﬁsh were about 13 mm TL.
The pectoral ﬁns did not start growing before ﬁsh were 7.5–
8.0 mm TL. Their growth was parallel to that of the dorsal ﬁn, and they
did not attain their longest dimension (13% TL) before ﬁsh were 40–
45 mm TL. Pelvic ﬁns grew last. Their anlagen were not conspicuous
before larvae were 12 mm TL. Thereafter, they grew rapidly until
Fig. 2. Fin development sequence in P. djambal (observations in 191 ﬁsh). Symbols refer
to measurements in individual ﬁsh.
3.2.2. Mouth width, gape and body depth
Body depth (BD) at hatching was 35% TL, but declined rapidly as
the yolk was absorbed. It attained its minimal dimension (16% TL) at
84 hah, when the yolk was fully absorbed (ﬁsh of 9.9 mm TL; Fig. 3A).
Thereafter, BD increased slowly up to 19–20% TL at 40–50 mm TL.
The mouth opened between 14 and 20 hah, when ﬁsh were about
6.5 mm TL. Both jaws exhibited a rapid positive allometric growth and
attained their largest dimension relative to ﬁsh size soon at the start of
exogenous feeding (ﬁsh of 8.5 mm TL). With a gape opening angle as
large as 120°, gape height (GH) amounted to slightly less than 18% TL
at this moment (Fig. 3A). Thereafter, both jaws exhibited a negative
allometric growth, GH decreased in a curvilinear way and amounted
to no more than 10% TL at 40–50 mm TL. By contrast, mouth width
(MW) did not exhibit such a marked allometry during this interval: it
peaked at 14.5% TL at 10 mm TL, but was still as large as 13.0–12.5% TL
at 40–50 mm TL. The ontogenetic variations of MW paralleled those of
head width (the largest transversal body dimension until 50 mm TL;
16.5 and 14.0–13.5% TL at 8.5 and 40–50 mm TL, respectively).
The models between HW, MW, GH, BD and TL are given in Table 1.
They indicate that mouth dimensions (GH or MW) of P. djambal were
Fig. 3. A. Ontogenetic variation of gape height (GH, grey squares, n = 164) and body
depth (BD, open circles, n = 141) in P. djambal. Symbols refer to measurements in
individual ﬁsh. Curves were produced by interpolation. B. Ontogenetic variation of the
logistics of cannibalism (i.e. the largest prey that can be ingested whole by the
cannibal). The curve is constructed from the ratio between GH and BD, except in ﬁsh
ranging from 7.5 to 11 mm TL (grey area with dashed borders), for which the ratio
between mouth width and head width is lower (see text and Table 1).
46
E. Baras et al. / Aquaculture 305 (2010) 42–51
Table 1
Morphological relationships (simple linear regression analyses) between head width
(HW), mouth width (MW), gape height (GH), body depth (BD) and total body length
(TL) in Pangasius djambal greater than 10 mm TL. All variables are expressed in mm. GH
is calculated from the lengths of the maxillar (Mj) and mandibular jaw (mj) and a gape
opening angle of 120°, i.e. GH = 0.866(Mj + mj). Values between brackets in the
equations are the standard errors of coefﬁcients. P b 0.0001 for intercept and slope in all
four models.
Equation
r2
F
df
HW = 0.417[0.004] + 0.123[0.001]TL
MW = 0.085[0.016] + 0.126[0.001]TL
GH = 0.568[0.017] + 0.093[0.001]TL
BD = −0.495[0.029] + 0.205[0.001]TL
0.999
0.996
0.992
0.995
214,899
27,423
13,390
20,801
115
114
105
105
never larger than the body sectional dimensions (HW or BD) at any
developmental stage. Based on the comparisons between transversal
(MW versus HW) and vertical dimensions (GH versus BD), the size
ratio that rules the exercise of complete cannibalism in P. djambal is
governed by a transversal limitation until 11–12 mm TL and by a
vertical limitation thereafter. The resulting logistics of cannibalism
(Fig. 3B) was used to select prey for the predation experiments.
3.2.3. Oral teeth and spines
As in P. hypophthalmus, the two jaws of P. djambal embryos and
larvae bear massive conical oral teeth and peripheral slender spines.
Both types of structures were conspicuous at 24 hah. Spines were
originally embedded into a gangue of tissues. At 36 hah, their tip had
pierced the gangue. The longest spines, located in the front part of the
mouth and on the sides, just anterior to the eyes, were as long as
100 µm, exceeded the cumulated height of the true teeth and gums
(about 90 µm), and slightly overhung from the mouth. Twelve hours
later, when the ﬁsh started feeding exogenously, the spines had
grown by less than 5 µm, whereas oral teeth and gums had gained 10–
15 µm in height, so spines were not overhanging any longer. Spines
were visible until 7.5 dah (14 mm TL), but their size was almost
identical as at the start of exogenous feeding, whereas teeth and gums
had grown at an average 20 µm day− 1.
As in the study on larvae of P. hypophthalmus (Baras et al., 2010), it
was tested whether young P. djambal were capable of re-opening their
mouth after forced closure. This was evaluated in anaesthetised ﬁsh
Fig. 4. Variation of prey-size selectivity in cannibalistic P. djambal of different sizes (size
classes 1–5, see Table 2). In graph A, prey size is expressed as a proportion of the
cannibal's total length (TL), and in graph B as a proportion of the TL of the largest prey
that can be ingested by the cannibal (calculated from the abacus shown in Fig. 3B).
Table 2
Characteristics of the experiments used for the study of bioenergetics and prey-size selectivity in larvae and juveniles of P. djambal. WM is the ﬁsh wet body mass, DM is the dry body
mass and TL is the total body length. The lower part of the table gives results of the contingency table analyses testing for random prey selection in each of the ﬁve size classes. Two
types of tests are given, the ﬁrst one for prey size relative to cannibal size, and the second one for prey size relative to the logistics of cannibalism (i.e. the largest prey that can be
eaten whole by the cannibal; see Fig. 3B).
1
2
3
4
5
Cannibal WM (mg)
Cannibal size class
Mean
Range
76
56–90
115
91–152
398
318–494
594
525–694
2074
1702–2630
Cannibal DM (mg)
Mean
Range
8.2
6.0–9.5
13.0
10.0–17.5
52.9
40.0–66.1
80.6
70.0–95.9
326.7
262.0–424.8
Cannibal TL (mm)
Mean
Range
21.9
20.0–23.3
25.2
23.4–27.6
37.9
35.1–40.1
43.2
41.4–45.4
65.0
60.9–70.2
24
436
46
15
474
136
11
151
62
13
141
53
29
805
134
n observations (day × ﬁsh)
n prey offered
n prey consumed
Prey TL (mm)
Prey-size selectivity
(2% TL classes)
Range
χ2 (df)
P
9.3–12.5
18.7 (9)
0.0281
9.3–13.2
95.2 (11)
b 0.0001
11.0–18.8
25.3 (11)
0.0083
11.1–21.6
37.0 (13)
0.0004
15.3–24.9
118.8 (7)
b 0.0001
Prey size (% logistics)
Prey-size selectivity
(4% logistics classes)
Range
χ2 (df)
P
62.9–91.6
15.7 (7)
0.0280
53.8–88.8
95.59 (9)
b 0.0001
42.7–84.2
18.3 (9)
0.0323
41.2–84.0
37.6 (11)
b0.0001
34.3–66.3
148.9 (7)
b 0.0001
E. Baras et al. / Aquaculture 305 (2010) 42–51
47
Fig. 5. Relationships between growth (G) and daily food ration (R) in cannibalistic P. djambal of different sizes (1–5, see Table 2). DMci is the dry body mass (mg) of cannibals at the
start of the 24-h cycle over which growth and food intake are measured (calculated from the model in Fig. 1). Data points refer to individual measurements. The vertical dotted lines
show the food ration that produces zero growth (Rmaint). The equations and statistics of the simple regression models are given in Table 3.
48
E. Baras et al. / Aquaculture 305 (2010) 42–51
Table 3
Energetics of cannibalism in P. djambal. The ﬁrst ﬁve equations in the upper part of the table refer to the models between growth (G, % DMci day−1) and daily food ration (R, %
DMCi) illustrated in Fig. 5 (see Table 2 for further information on size classes). DMci is the dry body mass (mg) of the cannibal at the start of a 24-h period over which the food
intake and growth of cannibals are measured (see Methods). The lower part of the table gives the equations that model the ontogenetic variations (against DMci) of maximum daily
food ration (Rmax), maximum growth (Gmax), maximum gross conversion efﬁciency (GCEmax, DM:DM), maintenance food ration (Rmaint,% DMci) and negative growth during 24 h of food
deprivation (GS, % DMci day−1). The models for Rmax, Gmax and GCEmax are deduced from the highest scores observed in cannibals of different sizes (Fig. 6). The models for Rmaint and GS are
obtained from the ﬁve models given in the upper part of the table. Values between brackets in the equations are the standard errors of coefﬁcients.
Equation
Size class
Size class
Size class
Size class
Size class
1: G = −6.710[0.531] + 0.450[0.013]R
2: G = −5.246[0.536] + 0.490[0.012]R
3: G = −4.678[0.377] + 0.530[0.012]R
4: G = −3.785[0.350] + 0.557[0.019]R
5: G = −2.151[0.138] + 0.591[0.014]R
log Rmax = 2.181[0.016] − 0.320[0.010] log DMci
log Gmax = 1.704[0.018] − 0.252[0.012] log DMci
log GCEmax = −0.469[0.012] + 0.064[0.008] log DMci
log Rmaint = 1.481[0.080] − 0.351[0.046] log DMci
log (−Gs) = 1.083[0.080] − 0.280[0.046] log DMci
r2
F
df
P intercept
P slope
0.982
0.992
0.996
0.989
0.985
1230.9
1690.1
1926.0
870.1
1727.0
23
14
10
12
28
b 0.0001
b 0.0001
b 0.0001
b 0.0001
b 0.0001
b 0.0001
b 0.0001
b 0.0001
b 0.0001
b 0.0001
0.987
0.972
0.841
0.951
0.925
985.8
456.0
68.6
57.8
37.0
14
14
14
4
4
b 0.0001
b 0.0001
b 0.0001
0.0003
0.0009
b 0.0001
b 0.0001
b 0.0001
0.0047
0.0089
from the start of exogenous feeding (2 dah) until 7 dah (i.e. closure
was induced by pumping with dry paper the anaesthetic solution
around the ﬁsh, and opening, was induced by pouring the anaesthetic
solution over the ﬁsh). On all occasions, the ﬁsh that were forced to
close their mouth could open it again, thereby supporting the view
that spines were not overhanging from the mouth during the larval
period.
3.3. Predation experiments
Cannibals ranging from 20.0 to 70.2 mm TL (corresponding WM of
56 and 2630 mg, respectively) were studied over 92 days × ﬁsh
(Table 2). All ﬁsh recovered quickly (b1 min) from anaesthesia and
measurement, and cannibalism generally resumed within the ﬁrst
30 min following measurement. This suggests that the monitoring
procedure had little impact on the food intake of cannibals. No cannibal
died during the experiments, and no ﬁsh from the control groups was
consumed in part or totality. Hence, it was assumed that all missing
prey ﬁsh in the predation cages had been eaten by the cannibals. A total
of 2007 prey (9.3–24.9 mm TL, 4–125 mg) were offered, 431 of which
were consumed. This high ratio supports the hypothesis that cannibals
were never underfed during the experiments.
3.3.1. Prey-size selectivity
In all ﬁve size classes, the hypothesis of random prey selection was
rejected at the 0.05 level (Table 2). Cannibals of increasing sizes
preferred prey of relatively decreasing sizes. The preferred TL ratios
for prey passed from 43 to 23% TL in cannibals of 21.9 and 65 mm TL,
respectively (Fig. 4A). This was expected because of the increasing
constraints on cannibalism that result from the allometric growth of
mouth parts and body depth (Fig. 3B). Nevertheless, when prey size
was expressed by reference to the logistics of cannibalism (i.e. the
largest prey size that could be eaten whole by the cannibal), the
preferred prey size still decreased signiﬁcantly in cannibals of
increasing size (contingency table analyses, P b 0.0001 for all comparisons between size classes; Fig. 4B).
The preferred size of prey relative to the logistics of cannibalism
(Sp, % logistics) was equated to the TL of cannibals. The model stood
as: log Sp = 2.512[0.017] − 0.515[0.011] log TL, where values between
brackets are the standard errors of coefﬁcients (R2 = 0.990,
F = 2139.4, df = 4, P b 0.0001 for both the intercept and slope). This
model predicts that at the start of exogenous feeding, cannibals would
prefer prey as large as the logistics of cannibalism, whereas 100-mm
juveniles would prefer prey of about 30% of their logistics.
3.3.2. Bioenergetics
For each of the ﬁve size classes of cannibals (see Table 2), the
relationship between G and R was best described by a simple linear
regression model (Fig. 5). All ﬁve models were highly signiﬁcant
(P b 0.0001, Table 3). They indicated that young P. djambal had a high
daily maintenance food ration (Rmaint) and incurred substantial
negative growth during 24-h starvation (Gs) (respectively 14.9%DM
and 6.7% DM day−1 at 6–10 mg DM). Both variables decreased in ﬁsh of
increasing size and attained no more than 3.6% DM and 2.2% DM day−1
respectively in the largest ﬁsh examined in this study (260–
425 mg DM).
The linear nature of the models between G and R implied that the
gross food conversion efﬁciency (GCE) was proportional to R, so the
highest food ration consumed by the cannibal (Rmax) also corresponded to Ropt in these circumstances. Rmax decreased signiﬁcantly
(P b 0.0001) in ﬁsh of increasing size (log–log relationship, Table 3),
from 88% DM at 6 mg DM to 22% at 400 mg DM (Fig. 6). Cannibals of
increasing size consumed lower food rations, but their GCEmax was
higher (about 0.50 at 400 mg DM versus 0.36 at 6 mg DM; Fig. 6). The
increase of GCE in ﬁsh of increasing size (log–log relationship, Table 3)
was not restricted to ﬁsh feeding maximally, as indicated by the slopes
of the G-to-R relationships in the ﬁve classes of cannibal size (from
0.45 to 0.59 in classes 1 and 5, respectively; Fig. 5, Table 3). This
increase in GCE buffered the decrease of Gmax in ﬁsh of increasing size,
as indicated by the comparison between the slopes of the log–log
models between Gmax and DMci (−0.252), and between Rmax and DMci
(−0.320) (Table 3). Nevertheless, Gmax decreased substantially
between the smallest and largest ﬁsh under study (from 34.5 to
11.5% DM day−1, at 6 and 400 mg DM, respectively; Fig. 6).
4. Discussion
4.1. Why are episodes of early mortality so rare in P. djambal?
The present study revealed that the ontogenetic trajectory of
P. djambal closely resembles that of P. hypophthalmus, with a large
gape (peaking at 18% TL in both species), an early development of long
(100 µm) oral spines and a very late development of pectoral ﬁns.
However, these traits obviously do not sufﬁce to trigger the episodes
of mass mortality that are so frequent among cultured larvae of
P. hypophthalmus. The major difference between the two species
refers to their sizes at the start of exogenous feeding (5.6 versus
8.5 mm TL, in P. hypophthalmus and P. djambal, respectively). At 6.5–
7.0 mm TL, the oral spines of both species overhang from the mouth,
whereas at 8.5 mm TL, they have already stopped growing and do no
longer overhang from the mouth. Similarly, gape height systematically exceeds body depth when larvae of P. hypophthalmus start
feeding exogenously at 5.6 mm TL (Baras et al., 2010), whereas it
never exceeds body depth in any of the two species at 8.5 mm TL. The
combination of these two factors might sufﬁce to account for why no
mass mortality due to cannibalism has ever been reported among
E. Baras et al. / Aquaculture 305 (2010) 42–51
49
No other detailed morphological study has ever been conducted on
any other pangasiid catﬁsh, so these traits cannot be generalised
without proper validation. However, there is striking evidence that
episodes of mass mortality due to cannibalism do not occur either
among larvae of P. bocourti, which also produce large eggs (Hung et al.,
1999, 2002). If this tendency were shared by other taxa, it would
foster the idea that the risk of early mortality and cannibalism among
cultured ﬁsh species with similar ontogenetic trajectories might be
largely dictated by egg size. This comparison between close taxa in a
cannibalistic perspective adds to the general statement that the
viability of ﬁsh larvae is positively affected by egg size (review in
Kamler, 2005), for reasons other than those pertaining to cannibalism,
and it strengthens the idea that egg size could be a valid and easy
criterion for evaluating the adequacy of taxonomically related species
that are candidates to domestication.
4.2. Functional mechanisms behind the rarity of cannibalism in young
P. djambal
Fig. 6. Variation of daily food ration (R), growth (G) and gross conversion efﬁciency
(GCE, DM:DM) in cannibalistic P. djambal of different sizes. DMci is the dry body mass
(mg) of cannibals at the start of the 24-h cycle over which growth and food intake are
measured. Data points refer to individual measurements. The log–log models (plain
lines) are constructed from the highest points only (equations and statistics in Table 3).
young larvae of P. djambal (Legendre et al., 2000; Slembrouck et al.,
2004): because of their abundant yolk, young P. djambal start feeding
exogenously at a developmental stage that is beyond the risk period
depicted for P. hypophthalmus, which originate from much smaller ova
(0.6 versus 3.5 mg in P. djambal).
4.2.1. Morphology
This study provided several reasons for why cannibalism among
older larvae and juveniles of P. djambal is rare and never triggers the
cascading pattern that was expounded in the introduction of this
article. In particular, the rapid positive allometric growth of body
depth, combined with the equally rapid negative allometric growth of
jaw length during the early ontogeny of P. djambal contributes to
complicate the exercise of cannibalism. Based on gape height and ﬁsh
body depth, the size (TL) ratios that enable the exercise of complete
cannibalism at 10, 20 and 40 mm TL are 84.9, 68.5 and 56.5%,
respectively (Fig. 3B).
These morphological constraints force potential cannibals of
P. djambal to select victims that are increasingly smaller relative to
their own body length, and this might impact on the risk of
cannibalism among cultured ﬁsh. However, these traits are not
exceptional at all. In the vast majority of ﬁsh species, except for those
that produce very small larvae, the predation capacities are maximal
at the start of exogenous feeding and decrease thereafter, for the same
reasons as those expounded above (synthesis in Baras and Jobling,
2002). The logistics of cannibalism in juveniles of P. djambal might
look restrictive, especially by reference to piscivorous species. The size
(TL) ratios that enable the exercise of cannibalism by a 40-mm TL
juvenile can be as high as 66% in Gadus morhua (Folkvord and Otterå,
1993), 69% in Esox lucius (Bry et al., 1992) and 76% in Epinephelus
coioides (Hseu et al., 2003), whereas it does not exceed 56.5% in
P. djambal. However, this ratio is not exceptionally low either in
comparison to other species that frequently exhibit cannibalism
under culture conditions. Still for a 40-mm TL cannibal, the TL ratios
are 47% in Clarias gariepinus (Hecht and Appelbaum, 1988), 48% in
Seriola lalandi (Ebisu and Tachihara, 1993), 50% in Seriola quinqueradiata (Sakakura and Tsukamoto, 1996), 51% in Engraulis capensis
(Brownell, 1985) and Perca ﬂuviatilis (Brabrand, 1995), 53% in
Dicentrarchus labrax (Katavic et al., 1989), 58% in Heterobranchus
longiﬁlis (Baras, 1999) and 59% in Lates calcarifer (Parazo et al., 1991).
This comparison clearly emphasizes that morphometric factors can be
used to predict the risk of cannibalism in populations of a particular
species with contrasting levels of size heterogeneity (see also Baras
and d'Almeida, 2001; Babiak et al., 2004; Mandiki et al., 2007), but
their predictive value can hardly be transposed between species.
4.2.2. Behavioural factors: prey-size selectivity
This study provided evidence that cannibals of P. djambal never
consumed prey as large as the logistics of cannibalism, and that the
size of preferred prey relative to the logistics of cannibalism decreased
in cannibals of increasing sizes (Fig. 4). The size (TL) ratio between the
preferred prey and the largest prey that can be ingested by P. djambal
(hereafter pref:max TL ratio) was modelled as 99% at 10 mm TL, and
50
E. Baras et al. / Aquaculture 305 (2010) 42–51
no more than 48.6% at 40 mm TL. This study was not designed to
examine the factors behind this ontogenetic variation as all predation
experiments were run with a black box design, without any insight
into the behaviour of cannibals. By analogy with other ﬁsh species and
food types, it can be postulated that large prey possess greater escape
capacities and are more difﬁcult to handle than smaller prey
(e.g. Anguilla anguilla; Knights, 1983).
Detailed studies on prey-size selectivity are scarcer than those on the
logistics of cannibalism, and these studies rarely investigated whether
size selectivity varied between ﬁsh of different sizes, so the scope for
between-species comparisons is more restricted than for morphological
factors (synthesis in Baras, 1998). Nevertheless, some general trends
can be drawn from existing studies. On the one hand, it is frequent that
highly cannibalistic species exhibit a high pref:max TL ratio: N90% in
juvenile H. longiﬁlis (Baras, 1999), 88% in juvenile E. lucius (Bry et al.,
1992), 78% in larvae of C. gariepinus (Hecht and Appelbaum, 1988), and
75% in juvenile G. morhua (Folkvord and Otterå, 1993). On the other
hand, species that are much less cannibalistic can also exhibit very high
pref:max TL ratios (86% in koi carp Cyprinus carpio, Van Damme et al.,
1989). Conversely, B. moorei, which exhibits intense cannibalism and
can engulf large prey (Vandewalle et al., 2005), prefers consuming the
smallest prey available (Baras et al., 2000).
This brief comparison emphasizes the idea that prey-size selectivity alone cannot be used as a reliable predictor of the risk of
cannibalism among cultured ﬁsh. Yet, the combination of morphological and behaviour factors makes cannibalism less likely in cultured
P. djambal than on the exclusive basis of morphological factors.
However similar combinations were reported in species that exhibit
frequent cannibalism under culture conditions. In young E. capensis,
which frequently exhibits cannibalism, the logistics is 51% TL, and the
pref:max TL ratio is 58%, thereby giving a preferred prey size of 29.6%
TL (Brownell, 1985). This is similar to the situation in P. djambal
(corresponding values of 56.5% TL, 48.6% and 27.5% TL at 40 mm TL),
but cannibalism is rare in this species.
4.2.3. Bioenergetics
Cannibals frequently enjoy some growth advantage over siblings,
for reasons pertaining to food availability, but also to digestibility, as
ﬁsh are generally more digestible than planktonic prey. However, the
fastest growth of cannibalistic P. djambal in this study was slightly
slower than in ﬁsh fed in excess 7 times per day with brine shrimp
nauplii then with formulated feed (Legendre et al., 2000). Using the
model produced in this study for Gmax (Table 3) together with the
models between DM and WM, and between WM and TL, cannibals
feeding maximally would attain 32 and 60 mm TL after two and four
weeks of exogenous feeding, respectively. The corresponding values
for the top growers in the study by Legendre et al. (op. cit.) were 40
and 69 mm TL, respectively (recalculated from WM; Fig. 7).
The reasons for why the growth of cannibalistic P. djambal is rather
slow can be deduced from their bioenergetics, in particular from their
high Rmaint (Fig. 5) and rather low GCE during the larval stage (Fig. 6).
As a matter of fact, the GCE of P. djambal larvae or juveniles is not
particularly low in comparison to other cultured ﬁsh species. The
GCEmax observed in the smallest ﬁsh under study was 0.36 at
6 mg DM. Data for comparisons with larvae of this size are scarce.
Using the model in Table 3, the GCEmax of P. djambal for a standard
body mass of 0.5 mg DM was modelled as 0.33 versus 0.06–0.07 in
Sparus aurata (Parra and Yúfera, 2001), 0.21–0.26 in C. carpio
(recalculated from Bryant and Matty, 1980 and Kamler et al., 1987),
0.26 in Solea senegalensis (Parra and Yúfera, 2001) and 0.33 in
S. niphonius (Shoji et al., 1997). Many other marine species fall within
this range (Houde, 1989). However, the GCE of a 0.5-mg DM larva can
be much higher (over 0.70) in several other species that frequently
exhibit cannibalism (C. gariepinus, Conceição et al., 1998; Appelbaum
and Kamler, 2000; B. moorei, recalculated after Baras et al., 2000 and
Baras and Jobling, 2002). As for morphological factors or prey-size
Fig. 7. Integration of the morphological, behavioural and energetic factors for
determining why cannibalism is rare among young P. djambal. a. Growth of cannibals
feeding maximally (based on the Gmax model in Table 3), b. Size of the largest prey that
can be ingested by cannibals (calculated from the abacus in Fig. 3B). c. Size of prey
preferred by cannibals (calculated from the model on prey-size selectivity, see text and
Fig. 4B). d. Growth of ﬁsh fed submaximally (3–4 times per day) for the morphological
study. e. Supposed maximum growth of ﬁsh fed 7 times per day (recalculated from the
data of Legendre et al., 2000).
selectivity, young P. djambal are just average as regards bioenergetics,
but the combination of three average scores leads to an overall low
performance for cannibalism.
An additional factor that might contribute to make cannibalism in
P. djambal less proﬁtable than in many other ﬁsh species lies in the
rather low proportion of dry matter in larvae of P. djambal (≤11% in
ﬁsh b 5 mg DM; Fig. 1), in comparison to brine shrimp nauplii (16–
17%, Sorgeloos et al., 1986). The degree of stomach fullness, which
intimately conditions the propensity to feed, is conditioned by the
prey's volume, and thus by its wet mass, rather than by its dry mass.
Henceforth, the low DM content of larvae of P. djambal might be a
reason for why cannibalism brings no growth advantage over siblings
feeding on brine shrimp nauplii. Larvae of P. djambal are large at the
start of exogenous feeding (8.5 mm TL and 4.5 mg WM), and have no
problem with swallowing and digesting nauplii.
4.3. Conclusions
The absence of marked growth advantage from the exercise of
cannibalism together with the increasing morphological constraints
upon predation and the increasing preference for small prey during
the ontogeny of P. djambal, tend to make cannibalism extremely rare
among their larvae and juveniles, at least when fed maximally.
However, there is no need feeding maximally larvae and juveniles of
P. djambal to get rid of cannibalism in this species. The ﬁsh raised for
the characterization of morphology during this study were fed no
more than 3 or 4 times per day, but they grew fast enough to put them
beyond the reach of cannibals, even if cannibals had consumed prey as
large as physically possible (Fig. 7). This substantial security margin
makes the culture of P. djambal very permissive with respect to the
feeding strategy, and accounts for why reports over cannibalism in
this species have been so rare (Legendre et al., 2000; Slembrouck
et al., 2004), even when their larvae and juveniles were not fed
maximally or with performing feeds.
From a methodological viewpoint, this study emphasized that
morphological, behavioural and energetic criteria taken separately did
not sufﬁce to account for the rarity or frequent occurrence of
cannibalism in larvae and juveniles of P. djambal, whereas their use
in combination was much more informative. Similar protocols could
be implemented in any species that is considered as a potential
candidate to the diversiﬁcation of aquaculture, as they would provide
E. Baras et al. / Aquaculture 305 (2010) 42–51
a rapid estimate of the risk of cannibalism and ﬂexibility or constraints
when culturing their larvae and juveniles.
Acknowledgements
The authors wish to thank ﬁve anonymous referees for useful
comments on previous versions of this article. We are indebted to
Retna Utami, Sularto and Kamlawi (LRPTBPAT Sukamandi) for
providing the biological material. Special thanks the technical staff
of LRBIHAT Depok (Slamet Sugito, Made Agus Widjana, Mertayasa,
Moch Hasan, Marjono) for their assistance during the rearing and
measurement protocols. Mrs. Dominique Caseau-Baras contributed to
improve the English style of the manuscript. Etienne Baras is an
honorary research associate of the Belgian FNRS.
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