J. Ocean Univ. Chin.

(Oceanic and Coastal Sea Research)

ISSN 1672-5182, August 30, 2008, Vol.7, No.3, pp.319-326
http://www.ouc.edu.cn/xbywb/
E-mail:xbywb@ouc.edu.cn

Advances in Studies of the Effects of Starvation on

Growth and Development of Fish Larvae
SHAN Xiujuan1), 3), HUANG Wei1), 3), CAO Liang1), 3), and WU Yunfei2), *

1) Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, P. R. China

2) College of Fisheries, Ocean University of China, Qingdao 266003, P. R. China
3) Graduate School, Chinese Academy of Sciences, Beijing 100049, P. R. China

(Received January 29, 2007; accepted February 25, 2008)

Abstract Starvation has important effects on early development of fish. It determines the survival and growth of fish larvae, and
plays an important role in the dynamics of fish population and fisheries recruitment. In this review, we discuss the current studies
about the effects of starvation on growth and development of fish larval stage. The goals of this review are to understand some adap-
tive mechanisms and ecological countermeasures of starved fish larvae and to provide the scientific guideline for exploring early life
history processes, evaluating the nutrition condition and growth of larval fish, protecting fish resource and breeding fish larvae.

Key words starvation; growth; development; fish larvae

DOI 10.1007/s11802-008-0319-3

can resist starvation more successfully than those species

1 Introduction
Larval stage is a critical period of fish development.
The structure and function of fish larvae become more
and more complex with the corresponding morphological,
ecological and physiological changes. In this period,
many biological and physical factors affect interactively
their growth and survival, such as predation, genetic de-
fects, perturbations of the physical environment and star-
vation (Fogarty et al., 1991; Iguchi and Mizuno, 1999).
There is increasing evidence that starvation may induce
poor performance in feeding, cause high mortality and
hinder growth of fish larvae during their early develop-
ment both in nature and in aquaculture (Leggett and De-
blois, 1994; Dou et al., 2002). Especially at the onset of
exogenous feeding period, even short period of food dep-
rivation after yolk exhaustion results in severe behavioral,
developmental and nutritional problems, leading to dras-
tic mortality and deformity (Kjorsvik et al., 1991). Hjort
(1926) also suggested that the food availability to larvae
and their ability to consume it, at the critical time of yolk
exhaustion, could be important factors in determining
larval survival and fish population dynamics in next year.
The susceptibility to starvation of fish larvae appears to
be stage-specific and varies in specific species. In general,
the older fish larvae have better ability to resist starvation;
the species whose larvae are relatively larger at hatching
* Corresponding author. Tel: 0086-532-82031503
E-mail: wuyunfei@ouc.edu.cn
with smaller larvae, because of the latter’s limited energy
reserves, poor hunting abilities and food size limitation
related to mouth gape (Miller et al., 1988). And fish lar-
val ability to resist starvation is also connected with the
quality of egg, the better the quality, the better the ability
to resist starvation (Rana, 1985). In addition, some envi-
ronmental factors, such as temperature and salinity, also
have important effects on larval ability of resisting starva-
tion; fish larvae can endure longer time of starvation un-
der optimal environment (McGurk, 1984).
There are various methods available for evaluating the
nutritional condition of fish larvae, e.g., morphometric
and gravimetric methods (Bisbal and Bengtson, 1995);
histological criteria (Green and McCormick, 1999; Chen
et al., 2007); biochemical methods (Suneetha et al., 1999;
Gwak et al., 1999); some methods based on digestive
enzyme activities (Murray et al., 2003, 2004; Perez-
Casanova et al., 2004; Chen et al., 2007) and changes of
metabolic rate (Mehner and Wieser, 1994; Shen and Lin,
1999) and various method combinations (Bisbal and
Bengtson, 1995; Gwak et al., 1999). Studies on the ef-
fects of starvation on fish larvae will help us to under-
stand the adaptive responses and ecological countermea-
sures against starvation, and offer the scientific guidance
for protection of natural fish resource, fingerling breeding
and fish culturing. Hence, the goals of this review are to
provide an overview of the effects of starvation on fish
larval development, which help better to understand some
adaptive mechanisms and ecological countermeasures of
starved fish larvae.
320 J. Ocean Univ. Chin.
2 The Characteristics of Fish Larvae
During Starvation
2.1 The Characteristics of Survival and Growth
Starvation has significant influences on survival and
growth of fish larvae. Fish larvae differ in their ability to
withstand progressive food deprivation (Yin and Blaxter,
1986), especially in the early developmental stage. Some
species can only withstand starvation for a few days after
hatching, for instance, 2.4 d for anchovy Anchoa mitchilli
at 28℃, 3 d for sea bream Archosargus rhomboidalis at
26℃ and lined sole Achirus lineatus at 28℃ (Houde,
1974). So the first feeding time is very critical for fish
larvae. If there is not sufficient time for the first-feeding
larvae to gain the ability of feeding before the onset of
irreversible starvation, fish larvae will suffer from pro-
gressive starvation, which might be one potential cause of
mortality in this period and influence their subsequent
survival and growth (Dou et al., 2005). Difference in first
feeding time has remarkable effects on growth and sur-
vival of fish larvae, for example, the standard length of
California halibut Paralichthys californicus larvae fed
from 3 dph (days post hatching) was significantly larger
than that of those fed from 4 dph or 5 dph, and the sur-
vival rate of larvae fed from 3 dph was higher than those
fed from 4 dph or 5 dph (Gisbert et al., 2004).
The progressive starvation for delayed first feeding has
important effects on fish larval survival. Survival de-
creases with the increase of delayed first feeding time
(Dou et al., 2005). The PNR (point-of-no-return) is a
good parameter used to understand the relationship be-
tween the first feeding ability of fish larvae and survival
rate. Blaxter and Hempel (1963) introduced the concept
of PNR, which was defined as the time when the cumula-
tive effects of starvation became irreversible and 50% of
starved larvae were still alive but unable to feed even
when food became available, and the survivors could not
successfully complete the ontogenetic development af-
terwards. Fish ecologists also termed it as irreversible
starvation or ecological death (Goshorn and Epifanio,
1991). Early studies indicated that the age to PNR in ma-
rine fish larvae was closely connected with the time of
egg incubation, the time of yolk exhaustion, the volume
of yolk and water temperature (Blaxter and Ehrlich, 1974;
Dou et al., 2005). In general, if fish larvae incubate for a
longer time, having bigger volume of yolk, with lower
metabolic ability in lower temperature environment, their
PNR occur relatively late; adversely, the PNR occur ear-
lier (Dou et al., 2005). So different species or different
developmental stages of the same species differ in their
ability to withstand progressive food deprivation (Yin and
Baxter, 1986). Dou et al. (2005) reported that the PNR of
Japanese flounder Paralichthys olivaceus larvae was
connected with temperature, and survival deteriorated
abruptly on 2, 3 and 4 d delayed feedings at 21℃, 18℃
and 15℃, respectively. The same results were also found
Vol.7, No.3, 2008
in pacific herring Clupea harengus juvenile, the PNR
time being from 6 dph to 7 dph after deprivation of food at
temperatures 9.6℃ and 10.5℃. The PNR time of 32 dph
star plaice Platichthys Stellatus juvenile even reached 23
days at 12.3℃ (Houde, 1974). So the resistance to starva-
tion or the time required to reach the PNR might slowly
decrease as size and age increase, which is a reflection of
metabolism and the quantity of restored energy reserves
(Fuiman and Higgs, 1997).
Fish growth, as also defined by increase in fish flesh, is
mainly accomplished through the synthesis of protein. It
is possible to measure basic components (amino acids)
and products (proteins) of protein synthesis. The most
useful method is to measure the RNA/DNA. The quantity
of DNA in animal cells is believed to be constant, while
RNA quantity varies with physiological status, the re-
quirement for protein synthesis and growth (Buckley et al.,
1999). We can know the state of fish growth by estimat-
ing RNA/DNA ratio levels (Clemmesen, 1988). This ratio
has been proven to be a useful and reliable indicator of
nutritional condition of fish, and widely applied to labo-
ratory-reared as well as wild fishes (Bailey et al., 1995;
Rooker and Holt, 1996). RNA quantities are higher in
rapidly growing organisms (Bergeron and Boulhic, 1994;
Buckley et al., 1999). Any factors preventing or slowing
growth are associated with reduction in the RNA quanti-
ties. Starvation has important influences on RNA/DNA
ratio of fish, which has been proved in Japanese anchovy
Engraulis japonicus larvae (Kono et al., 2003).
2.2 The Characteristics of Morphology
When fish larvae are deprived of food, they live on us-
ing the energy in their tissue. The abnormal characters are
firstly expressed in morphology, such as shrunk larvae
and collapsed soft tissue (Blaxter and Ehrlich, 1974; Yin
and Blaxter, 1987; Bisbal and Bengtson, 1995). Morpho-
logical changes are common phenomena in starved fish
larvae, and morphometric criteria can be obtained easily
without special preparation for specimens, so they are
widely used in natural water areas and laboratory to de-
termine the nutrition condition of fish larvae. For example,
it is very easy to distinguish healthy and starved larvae of
pacific herring, stone flounder Kareius bicoloratus and
star plaice according to the characters of pectoral angle
(Ehrlich et al., 1976). However, pectoral angle is not a
typical character. It occurs in both healthy and starved
individuals of tongue fish Cynoglossus semilaevis and
Japanese anchovy (Wan et al., 2004); but not in larvae of
pacific cod, jack mackerel Trachurus japonicus, red sea
bream Pagrosomus major and Japanese flounder (Xie et al.,
1998; Bao et al., 1998). During starvation, the body of
fish becomes bended and thin, with disproportionately
large head, as is found in jack mackerel (Theilacker,
1978), Chinese grass carp Ctenopharyngodon idellus and
black carp Mylopharyngodon piceus (Bao et al., 1998).
The ratios of tail height to standard length and trunk
length to standard length are sensitive morphometric in-
 SHAN X. J. et al.: Advances in Studies of the Effects of Starvation on Growth and Development of Fish Larvae
dices in California halibut (Gisbert et al., 2004). Mor-
phometric differences in upper and lower jaw lengths
during starvation occur in pejerrey Odontesthes bon-
ariensis (Carlos and Fumio, 1989). When the nutrition of
yolk-sac becomes exhausted, and outer nutrition is not
sufficient just to improve feeding behavioral level and
establish the outer nutrition connection, starved fish lar-
vae will be subjected to negative growth. It is an adaptive
response of fish larvae to starvation that can successfully
make them improve the chances of feeding and survival,
and ensure the supply of living energy when their skele-
ton systems are not completely developed (Yin, 1991). In
addition, the accumulation of pigmentation is obvious in
fish body during starvation. The researchers found that
melanin pigmentation was aggravated in starved Siberian
sturgeon and European grass eel Anguilla anguilla larvae
when compared with those fed normally (Gisbert and
Patrick, 1997; Rodríguez et al., 2005).
2.3 The Characteristics of Behavior
After the first feeding of larvae begins, the digestive
tract, eyes and fins are first developed and swimming
mode established. Some specific behaviors also show the
nutrition condition changes of fish larvae. The average
and biggest round swimming velocity increase sharply in
starved fish larvae, even higher than that in fed larvae,
which shows that the swimming and feeding abilities in-
crease and keep in mutual balance with starvation pro-
longed (Yin and Blaxter, 1987). But when it is near to the
PNR, the larvae have remarkable reduction in swimming
activity, often lie at the bottom of tank, and swim tardily
along the wall of tank. When the wall of tank is knocked
slightly, the larvae disperse; with the time of starvation
prolonged, larvae become dysphoria, then cling to the
wall of tank and negatively react (He et al., 1996; Gwak
et al., 1999; Rodríguez et al., 2005). Robinson and Pitcher
(1989) proved that fish swimming velocity was positively
correlated with diet level. Ivlev (1961) also described the
feeding activity and stamina decreased, and susceptibility
to predation increased with starvation prolonged in some
freshwater fishes. Some fish species have special behav-
ior characters, for instance, miiuy croaker Miichthys
miiuy swallows air during starvation, which might be the
cause that the volume of swim bladder in starved larvae is
bigger than that in fed larvae (Shan and Dou, unpublished
data).① Wight et al. (2004) found that gathering behavior
of three-spined stickleback Gasterosteous acculeatus was
weakened step by step during starvation. Cannibalism is
usually considered as a behavioral response to food
shortage among animals. Dou et al. (2000) suggested that
hunger was the most important factor of facilitating can-
nibalism among juvenile of Japanese flounder. So some
typical fish behaviors during starvation could serve as the
indicators of the nutrition condition.
①
Shan, X. J., and S. Z. Dou, Effects of starvation on ontogeny
and digestive enzymes in miiuy croaker. Unpublished.
321
2.4 The Characteristics of Histology
Digestive system of fish larvae is an elongated tract,
which is composed of cavum oropharyngeum, esophagus,
stomach and intestine. Successful development of diges-
tive system is very crucial for the survival and growth of
fish larvae. Therefore, the histological characteristics of
larval digestive system may serve as sensitive indicators
of nutritional condition of fish larvae (Gisbert and Serge,
2003). Fish larvae have marked degeneration in histo-
logical structure and function of digestive system when
deprived of food (Gisbert and Serge, 2003). Such degen-
eration reduces the surface area for nutrient absorption of
the digestive tract and the digestive capability of
re-feeding larvae (Gisbert et al., 2004). Furthermore, the
changes in digestive tract, liver and pancreas may affect
the synthesis of the digestive enzymes (Cousin et al.,
1987). So the studies about digestive system have mainly
focused on the histological structure of digestive tract and
the associated glands, which included: 1) reduction in size
of the epithelial cells in digestive tract and intestinal mu-
cosa (Bisbal and Bengtson, 1995; Gisbert and Serge,
2003; Gisbert et al., 2004); 2) cellular and nuclear degen-
eration of the exocrine pancreas (Crespo et al., 2001); 3)
atrophy and cellular and nuclear degenerations of liver
and a decrease in glycogen and lipids stored in hepato-
cytes (Green and McCormick, 1999; Crespo et al., 2001);
4) degeneration of trunk muscle fibers, even their lost
parallel structure (Bisbal and Bengtson, 1995; Green and
McCormick, 1999); and 5) increase of gall bladder vol-
ume (Gwak et al., 1999). The height of epithelial cells
and midgut cells has been used as diagnostic index to
evaluate the nutritional condition of larval fish (Gwak et al.,
1999); and starvation usually changes the shape of en-
terocyte cells in the intestine of various fish species
(Domeneghini et al., 2002). The height of epithelial cells
reduces in 5dph California halibut larvae for 2 d food
deprivation (Gisbert et al., 2004). In yellowtail kingfish
Seriola lalandi, summer flounder Paralichthys dentatus
and walleye pollock Theragra chalcogramma, the cell
height of midgut is reduced for starvation, especially in
early life stage (Theilacker and Porter, 1995; Bisbal and
Bengtson, 1995; Chen et al., 2007). The differential fast-
ing resistance of fish is age-dependent and the first feed-
ing larvae are less tolerant to food deprivation than
weaned juveniles. The height of enterocyte cell has more
obvious decrease in 3 d food deprivation on 15 dph yel-
lowtail kingfish than in 3 d food deprivation on 33 dph
(Chen et al., 2007). Similar results were reported by Bis-
bal and Bengtson (1995) in summer flounder, by Mar-
gulies (1993) in Spanish mackerel Scomberomorus sierra
and by Theilacker and Porter (1995) in walleye pollock.
Gao et al. (2004) reported that the volume of liver cell
and nucleolus obviously shrunk in Amur sturgeon
Acipenser schrenckii, and the ultrastructure showed that
the space among liver cells enlarged. In addition, Vacu-
oles, which contain black substance and are not regular in
322 J. Ocean Univ. Chin.
shape and distribution, occur in foregut and middle-gut of
jack mackerel and Japanese flounder during starvation
(Chantanachookin et al., 1990); these vacuoles are the
results of dead cytoarchitecture autolyzed, so the quanti-
ties and sizes of vacuoles are good indicators of starvation
grades. The criteria of the enterocyte height has been
widely used as an indicator of sub-optimal nutrition and
starvation in wild and laboratory fishes, such as common
carp Cyprinus carpio, stone flounder, yellowtail flounder
Limanda ferruginea, cottid fish Pseudoblennius marmo-
ratus and yellowtail kingfish (Theilacker and Porter, 1995;
Theilacker et al., 1996; Green and McCormick, 1999;
Chen et al., 2007). From the above mentioned, we see
that the histological changes during starvation are mainly
embodied by the degeneration of cells in digestive organs,
such as cell shrinkage, separation and loss of intercellular
substance, and other changes which become more severe
with the starvation prolonged.
2.5 The Characteristics of Biochemistry
2.5.1 The changes of biochemical composition
The energy storage in body is the ‘life-strings’ of fish
during starvation. When fish larvae are deprived of food,
many studies showed that the biochemical compositions
of fish larvae, e.g., the percent content of water, protein,
carbohydrate, ash and lipid, had obvious changes. Triglyc-
eride decreases during starvation in all stages of larvae,
and reduces to the smallest percentage of the original
store (Xie et al., 1998; Song et al., 2004). However, triglyc-
eride is not totally depleted during deprivation of food,
suggesting a certain amount triglyceride is needed for
sustaining life or efficiently utilizing other components,
most likely protein (Ehrlich, 1974). Different species first
use different energy substances, even the same species
use different energy substances at different development
stages. White sturgeon Acipenser transmontanus and
European eel Anguilla japonica first use hepatin (Dave,
1975; Domeneghini et al., 2002); it is subcutaneous
grease that is first used in yellowtail kingfish (Chen et al.,
2007). Fish larvae also use different energy resources
under different conditions. Mehner and Wieser (1994)
reported that during starvation sea perch Embiotoca lat-
eralis larvae mainly used protein at l5℃, and used gly-
cogen at 20℃, which could be explained by the key en-
zyme of metabolism, glutamate transaminase (GPT); its
activity decreased at 20℃, starved fish turned to use gly-
cogen in body. Fish larvae use the energy stocked in or-
gan in sequence during starvation. For instance, European
eel mainly consumes triglyceride in liver and muscle be-
tween 0 d starvation and 47 d starvation; but glycogen in
blood and hepatin in muscle are used between 47 d starva-
tion and 96 d starvation; then hepatin in liver and protein
in plasm sharply reduce between 96 d starvation and 164 d
starvation (Dave, 1975). The same results were found in
yellow weever Macquaria ambigua (Collins and Ander-
son, 1995). So fish larvae first use the energy substance
of store tissue, and then use the substance of the essential
Vol.7, No.3, 2008
organs and locomotion system, which is an adaptive
countermeasure of fish to starvation during the process of
evolution (Xie et al., 1998; Zamal and Ollevier, 1995).
When fish larvae step to death, their osmoregulation is
completely breakdown, cell size decreases and extra cel-
lular space increases with the increase of water content
during starvation (Yin et al., 1993; Song et al., 2004), and
then increase the flotage of fish and save more energy to
support fish larval life (Yin and Blaxter 1987; Bao et al.,
1998; Wu et al., 2006). In addition, starved grunion
Leuresthes tenuis larvae have lower Carbon/Nitrogen
ratio than fed larvae (May, 1971), which showed the se-
quence of energy use in fish during starvation.
Mehner and Wieser (1994) suggested that two kinds of
adaptability of metabolism existed during fish larvae
starvation: one was to decrease the metabolism rate and
save the energy consummation; the other was to keep a
relatively constant metabolism rate as far as possible, in
order to produce irritable reaction when the food was
available. Fish larvae can regulate the metabolism rate to
resist the shortage of food, for example, the metabolism
of perch decreases 45% for 15 d starvation (Xie et al.,
1998), and decreases 34% in 5 d starved perch Perca flu-
viatilis (Mehner and Wieser, 1994). In addition, Zhang
et al. (2000) proved the two kinds of adaptability of me-
tabolism in starved southern catfish.
2.5.2 The changes of digestive enzymes
Digestive enzymes change with development, nutrition
and outer environment (Bolasina et al., 2006a, 2006b,
2007). Analyses of digestive enzyme activities are easy
and reliable methods that can be used to obtain some in-
dicators of digestive process and nutritional condition of
fish larvae (Ueberschär, 1988). Chantanachookin et al.
(1990) showed that digestive organs were very sensitive
to food deprivation in Japanese flounder, and activities of
pancreatic digestive enzymes went down when larvae
feeding stopped and became rapidly elevated when feed-
ing restarted (Bloasina et al., 2006b). The same results
were found in sea bass Dicentrarchus labrax and red
drum Sciaenops ocellatus (Zambonino Infante and Cahu,
2001). Due to the lack of a functional stomach in most
fish larvae at first feeding, food is digested in the intestine
and enzymes mainly derive from the pancreas. Trypsin
and amylase are very important in the metabolism of fish
larvae (Chen et al., 2007). No matter what developmental
period of fish is, when it is deprived of food, both trypsin
and amylase have obvious decrease in Japanese flounder
and yellowtail kingfish (Bolasina et al., 2006b; Chen et al.,
2007). These findings agree with the reports on starved
pacific herring (Pedersen et al., 1990), gilthead sea bream
Sparus aurata (Moyano et al., 1996) and Pacific threadfin
Polydactylus sexfilis (Kim et al., 2001). The reduction in
digestive enzymes of starved fish is attributed to the
shrinkage of the epithelium in the digestive tract and
glands such as liver and pancreas (Yúfera et al., 1993;
Zambonino Infante and Cahu, 2001). So the presence of
 SHAN X. J. et al.: Advances in Studies of the Effects of Starvation on Growth and Development of Fish Larvae
digestive proenzymes secreted by the acinus and stored as
granules at its central apex is usually associated with nu-
trition (Bolasina et al., 2006b). The activities of trypsin
and amylase directly reflect the nutrition condition of fish
(Ueberschär et al., 1992; Oozeki and Bailey, 1995; Chen
et al., 2007). In addition, the changes of digestive en-
zymes activities, such as the deteriorated structure of di-
gestive tissue and organs, are direct causes, and also have
something to do with enzymes themselves (Zambonino
Infante and Cahu, 2001). If no food gives mechanical
stimulation to digestive tract, olfaction and vision, the
excretion of digestive enzymes will be reduced (Xie et al.,
1998).
2.5.3 The changes of essential fatty acids
Essential fatty acids are very important for the devel-
opment, survival and growth of marine fish larvae
(Rainuzzo et al., 1997; Sargent et al., 1997). The larval
capacity of digesting dietary lipid is of great importance
for optimal nutrition in early larval stages. The oxidation
of fatty acids plays prominent roles in energy provision
(Halver, 1989). The quantities and kinds of n-3 highly
unsaturated fatty acids (HUFA) can directly affect the
growth rate, survival rate, excitability, and biochemical
compositions of marine fish larvae. The sequence of fatty
acids used in fish larvae varies in specific species. Ki-
essling et al. (1989) reported that there were decrease in
mono-unsaturated fatty acids and relative increase in
polyunsaturated fatty acids after a period of starvation in
rainbow trout Oncorhynchus mykiss and common carp
larvae. Wen et al. (2006) also studied the effects of star-
vation on fatty acids contents in Chinese mittenhanded
crab Eriocheir sinensis, and found that saturation fatty
acids were first used during starvation, and then mono-
unsaturated fatty acids and polyunsaturated fatty acids.
2.6 The Changes of Immunology
Nutrition is the physical base of the development of
immune system; malnutrition has important effects on the
function of immune system. Fish belong to the cold-
blooded vertebrate, and only one antibody lies in blood
serum that is similar to mammiferous IgM. So fish mainly
depend on not-specific immune system to counteract
pathogeny. This system is composed of lymphocyte and
humoral factors. Some lymphocytes have the ability of
licking up pathogeny, and their quantities and abilities of
phagocytosis can directly reflect the immune capabilities
of fish. After these lymphocytes lick up NBT (Nitrotetra-
zolium blue chloride), NBT can accept hydrogen from
glucose-6-phophsate being oxidized in cytoplast, which
makes NBT deoxidized to be one palm-dark substance.
So many scientists regarded the cell number of oxidized
NBT as a guideline of estimating the capability of
not-specific immunity. Spiny finned catfish Pelteobagrus
vachelli has a little increase in NBT during early days of
starvation; however, with the starvation prolonged, the
number of NBT rapidly decreases (Sun et al., 2006). In
323
many humoral factors, total superoxide dismutase, the
activity of bateriolysin, bateriostatic ability and activity of
hemolysin are often regarded as reference and ration in-
dex to assess the ability of immunity. Three-spined stick-
leback has obvious changes in bacteriolysin, hemolysin
and bacteriostatic ability of blood serum during starvation
(Wight et al., 2004).
In addition, in order to decrease the level of metabo-
lism when fish larvae are deprived of food, fish reduce
oxygen utilization by controlling hematopoiesis. Qian et al.
(2002) reported that erythrocyte and hemachrome of
weever Lateolabraz japonicus had remarkable decrease,
only 76.5% and 46.0% of normal, respectively, after four
weeks of starvation. Fish can maintain life by decompos-
ing hemachrome of erythrocyte, and there is a reduction
in the number of erythrocytes during starvation. The same
results in southern catfish juvenile were reported: the
consistence of blood sugar, albumin, glyceryl-3-ester and
Na+, K+, Cl- in starved larvae were lower than those in fed
larvae, but the volume of blood corpuscle and erythtocyte
brittleness increased in starved larvae (Xie et al., 1998).
3 Conclusion
The studies on the starvation of fish larvae have im-
portant significance in wild and reared fish, which will
help us to improve the growth and survival of fish larvae,
and estimate the recruitment of fish in nature by detecting
the quantity and nutrition condition of fish larvae. Previ-
ous studies about the effects of starvation on fish mainly
concentrate on morphological, behavioral, biochemical
and histological characters. The evaluating methods for
adult fish are comprehensive and successful, but not so
for yolk-sac and larval fish, especially in biochemistry. In
the future, we should study fish early development in
combination with practical production, and do some
comprehensive studies, establish good methods to esti-
mate the starved degree of fish larvae, improve and ad-
vance essentially the development of commercial fishery
in China. From the above-mentioned, the research on the
starvation of fish larvae is in its infancy, so we still need
to do more work about the effects of starvation on fish
larvae in the future, for example, the consumption of the
necessary amino acids and fatty acids during starvation;
microorganism population existing in fish digestive tract
and its change with the food; the effects of starvation on
growth, survival and immune system on wild fish larvae;
the population genetics of fish larvae during starvation.
Acknowledgements
This study was supported by the Ministry of Science
and Technology of P. R. China under the grant contracts
Nos. 2007CB407305 and 2006BAD09A02.
References
Bailey, K. M., M. F. Canino, J. M. Napp, S. M. Spring, and A. L.
324 J. Ocean Univ. Chin.
Brown, 1995. Contrasting years of prey levels, feeding condi-
tions and mortality of larval walleye pollock Theragra chal-
cogramma in the western Gulf of Alaska. Mar. Ecol. Prog.
Ser., 119: 11-23.
Bao, B. L., J. X. Su, and M. C. Yin, 1998. Effect of delayed
feeding on feeding ability, survival and growth of red sea
bream and olive flounder larvae during early development. J.
Fish. Chin., 22 (1): 33-38.
Bergeron, J. P., and M. Boulhic, 1994. RNA: DNA ratio and
evaluation of the nutritional state and growth rate of saltwater
fish larvae experimental analysis of the Dover sole (Solea
solea ). ICES J. Mar. Sci., 51: 181-190.
Bisbal, G., and D. A. Bengtson, 1995. Descriptions of the starv-
ing condition in summer flounder, Paralichthys dentatus,
early life-history stages. Fish. Bull., 93: 217-230.
Blaxter, J. H. S., and G. Hempel, 1963. The influence of egg
size on herring larvae (Clupea harengus L.). J. Cons. Int. Ex-
plor. Mer., 28: 211-240.
Blaxter, J. H. S., and K. F. Ehrlich, 1974. Changes in behavior
during starvation of herring and plaice larvae. In: The Early
Life History of Fish. Blaxter, J. H. S., ed., Springer-Verlag,
Berlin, 575-588.
Bolasina, S., M. Tagawa, Y. Yamashita, and M. Tanaka, 2006a.
Effect of stocking density on growth, digestive enzyme activ-
ity and cortisol level in larvae and juveniles of Japanese
flounder, Paralichthys olivaceus. Aquaculture, 259: 432-443.
Bolasina, B., A. Pérez, and Y. Yamashita, 2006b. Digestive
enzymes activity during ontogenetic development and effect
of starvation in Japanese flounder, Paralichthys olivaceus.
Aquaculture, 252: 503-515.
Bolasina, S., T. Masatomo, and Y. Yamashita, 2007. Changes
on cortisol level and digestive enzyme activity in juveniles of
Japanese flounder, Paralichthys olivaceus, exposed to differ-
ent salinity regimes. Aquaculture, 266: 255-261.
Buckley, L. J., E. Caldarone, and T. L. Ong, 1999. RNA-DNA
ratio and other nucleic acid-based indicators for growth and
condition of marine fishes. Hydrobiologia, 401: 265-277.
Carlos, A. S., and T. Fumio, 1989. PNR, Histological and mor-
phometry of starved pejerrey, Odontesthes bonariensis Lar-
vae. Nippon Suisan Gakkaishi, 55 (2): 237-246.
Chantanachookin, C., M. Tanaka, and T. Seikai, 1990. Mor-
phological and histological changes of digestive organs in
starved Japanese flounder larvae Paralichthys olivaceus. The
Second Asian Fisheries, 433-436.
Chen, B. N., J. G. Qin, J. F. Carragher, and S. M. Clarke, 2007.
Deleterious effects of food restrictions in yellowtail kingfish
Seriola lalandi during early development. Aquaculture, 271:
326-335.
Clemmesen, C., 1988. A RNA and DNA fluorescence technique
to evaluate the nutritional condition of individual marine fish
larvae. Meeresforschung, 32: 134-143.
Collins, A. L., and T. A. Anderson, 1995. The regulation of
endogenous energy stores during starvation and refeeding in
the somatic tissues of the golden perch. J. Fish Biol., 47:
1004-1015.
Cousin, J. C. B., F. Baudin-Laurencin, and J. Gabaudan, 1987.
Ontogeny of enzymatic activities in fed and fasting turbot,
Scophthalmus maximus L. J. Fish Biol., 30: 15-33.
Crespo, S., M. MaríndeMateo, and C. A. Santamaría, 2001.
Histopathological observations during larval rearing of com-
mon dentex Dentex dentex L. (Sparidae). Aquaculture, 192:
121-132.
Vol.7, No.3, 2008
Dave, G., 1975. Metabolic and hematological effects of starva-
tion in the European eel, Anguilla anguilla L. Carbohydrate,
lipid, protein and inorganic iron metabolism. Comp. Biochem.
Physiol., 52A: 423-430.
Domeneghini, C., G. Radaelli, G. Bosi, and A. Arrighi, 2002.
Morphological and histochemical differences in the structure
of the alimentary canal in feeding and runt (feed deprived)
white sturgeons (Acipenser transmontanus). J. Appl. Ichthyol.,
18: 341-346.
Dou, S. Z., S. Tadahisa, and T. Katsumi, 2000, Cannibalism in
Japanese flounder juveniles, Paralichthys olivaceus, reared
under controlled conditions. Aquaculture, 182: 149-159.
Dou, S., R. Masuda, M. Tanaka, and K. Tsukamoto, 2002.
Feeding resumption, morphological changes and mortality
during starvation in Japanese flounder larvae. J. Fish Biol., 60:
1363-1380.
Dou, S. Z., R. Masuda, M. Tanaka, and K.Tsukamoto, 2005.
Effects of temperature and delayed firstfeeding on the sur-
vival and growth of Japanese flounder larvae. J. Fish Biol., 66:
362-377.
Ehrlich, K. F., 1974. Chemical changes during growth and star-
vation of herring larvae. In: The Early Life History of Fish.
Blaxter, J. H. S., ed., Springer-Verlag, Berlin, 301-323.
Ehrlich, K. F., J. H. S. Blaxter, and R. Pemberton, 1976. Mor-
phological and histological changes during growth and star-
vation of herring and plaice larvae. Mar. Biol., 35: 105-111.
Fogarty, M. C., M. P. Sissewine, and E. B. Cohen, 1991. Re-
cruitment variability and the dynamics of exploited marine
populations. Trends. Ecol. Evol., 6: 241-246.
Fuiman, L. A., and D. M. Higgs, 1997. Ontogeny, growth and
recruitment process. In: Early Life History and Recruitment
in Fish Populations. Chambers, R. C., and Trippel, E. A., eds.,
Chapoman and Hall, London, 225-249.
Gao, L. J., L. Q. Chen, and X. Q. Zhao, 2004. Starvation and
compensatory growth of Acipenser schrenckii juveniles
−Effects on digestive organs structure and digestive enzymes
activities. J. Fish. Sci. Chin., 11 (5): 413-419.
Gisbert, E., and W. Patrick, 1997. Larvae behavior and effect of
the time of first feeding on growth and survival of Siberian
sturgeon larvae under small hatchery production. Aquaculture,
156: 63-76.
Gisbert, E., and I. D. Serge, 2003. Histology of the developing
digestive system and the effect of food deprivation in larval
green sturgeon (Acipenser medirostris). Aquat. Living Re-
sour., 16: 77-89.
Gisbert, E., H. P. Raul, and E. C. Douglas, 2004. Ontogenetic
development of the digestive system in California halibut
(Paralichthys californicus) with notes on feeding practices.
Aquaculture, 232: 455-470.
Goshorn, D. M., and C. E. Epifanio, 1991. Development, sur-
vival, and growth of larval weakfish at different prey abun-
dances. Trans. Amer. Fish. Soc., 120: 693-700.
Green, B. S., and M. I. McCormick, 1999. Influence of larval
feeding history on the body condition of Amphiprion
melanopus. J. Fish Biol., 55: 1273-1289.
Gwak, W. S., T. Seikai, and M.Tanaka, 1999. Evaluation of
starvation status of laboratory-reared Japanese flounder
Paralichthys olivaceus larvae and juveniles based on mor-
phological and histological characteristics. Fish. Sci., 65:
339-346.
Halver, J. E., 1989. Fish Nutrition. 2nd edition, Academic Press,
New York, 239-345.
 SHAN X. J. et al.: Advances in Studies of the Effects of Starvation on Growth and Development of Fish Larvae
He, X. F., Q. F. Yang, and Z. B. Song, 1996. The preliminary
observation of starving effect on southern sheatfish (Silurus
meridionalis Chen) larvae reared at different temperature. J.
Huaihua Normal Col., 15 (6): 183-186.
Hjort, J., 1926. Fluctuations in the year classes of important
food fishes. J. Cons. Perm. Int. Explor. Mer., 1: 5-38.
Houde, E. D., 1974. Effects of temperature and delayed feeding
on growth and survival of larvae of three species of subtropi-
cal marine fishes. Mar. Biol., 26: 271-285.
Iguchi, K., and N. Mizuno, 1999. Early starvation limits sur-
vival in amphidromous fishes. J. Fish Biol., 54: 705-712.
Ivlev, V. S., 1961. Experimental Ecology of the Feeding Fishes.
Yale University Press, New Heaven, 547pp.
Kiessling, A., L. Johansson, and T. Storebakken, 1989. Effect of
reduced feed ration levels on fat content and fatty acid com-
position in white and red muscle from rainbow trout. Aqua-
culture, 79: 169-175.
Kim, B. G., S. Divakaran, C. L. Brown, and A. C. Ostrowski,
2001. Comparative digestive enzyme ontogeny in two marine
larval fishes: Pacific threadfin (Polydactylus sexfilis) and
bluefin trevally (Caranx melampygus). Fish Physiol. Bio-
chem., 24: 225-241.
Kjorsvik, E., T. van der Meeren, H. Kryvi, J. Arnfinnson, and P.
G. Kvenseth, 1991. Early development of the digestive tract
of cod larvae, Gadus morhua L., during start-feeding and
starvation. J. Fish Biol., 38: 1-15.
Kono, N., Y. Tsukamoto, and H. Zenitani, 2003. RNA: DNA
ratio for diagnosis of the nutritional condition of Japanese
anchovy Engraulis japonicus larvae during the first-feeding
stage. Fish. Sci., 69: 1096-1102.
Leggett, W. C., and E. Deblois, 1994. Recruitment in marine
fishes: Is it regulated by starvation and predation in the egg
and larval stages? Netherland J. Sea Res., 32: 119-134.
Margulies, D., 1993. Assessment of the nutritional condition of
larval and early juvenile tuna and Spanish mackerel (Pisces:
Scombridae) in the Panama Bight. Mar. Biol., 115: 317-330.
May, R. C., 1971. Effect of delayed first feeding on larvae of
grunion, Leuresthes tenuis (AYRES). Fish. Bull., 69 (2):
411-425.
McGurk, M. D., 1984. Effects of delayed feeding and tempera-
ture on the age of irreversible starvation and on the rates of
growth and mortality of Pacific herring larvae. Mar. Biol., 84:
13-26.
Mehner, T., and W. Wieser, 1994. Energetics and metabolic
correlates of starvation in juvenile perch (Perca fluviatilis). J.
Fish Biol., 45: 325-333.
Miller, T. J., L. B. Crowder, and J. A. Rice, 1988. Larvae size
and recruitment mechanisms in fishes: toward a conceptual
framework. Can. J. Fish. Aquat. Sci., 45: 1657-1670.
Moyano, F. J., M. Diaz, F. J. Alarcon, and M. C. Sarasquete,
1996. Characterization of digestive enzyme activity during
larval development of gilthead seabream (Sparus aurata).
Fish Physiol. Biochem., 15: 121-130.
Murray, H. M., J. C. Perez-Casanova, and J. W. Gallant, 2004.
Trypsinogen expression during the development of the exo-
crine pancreas in winter flounder (Pleuronectes americanus).
Comp. Biochem. Physiol., (Part A), 138: 53-59.
Murray, H. M., J. W. Gallant, and J. C. Casanova, 2003. On-
togeny of lipase expression in winter flounder, Pseudopleu-
ronectes americanus. J. Fish Biol., 62: 816-833.
Oozeki, Y., and K. M. Bailey, 1995. Ontogenetic development
of digestive enzyme activities in larval walleye pollock,
325
Theragra chalcogramma. Mar. Biol., 122: 177-186.
Pedersen, B. H., I. Ugelstad, and K. Hjelmeland, 1990. Effects
of a transitory, low food supply in the early life of larval her-
ring (Clupea harengus) on mortality, growth and digestive
capacity. Mar. Biol., 107: 61-66.
Perez-Casanova, J. C., H. M. Murray, and J. W. Gallant, 2004.
Bile salt-activated lipase expression during larval develop-
ment in the haddock (Melanogrammus aeglefinus). Aquacul-
ture, 235: 601- 617.
Qian Y. X., H. Q. Chen, and J. F. Sun, 2002. Effect of starvation
on hematological and blood biochemical indices in cultured
Lateolabrax japonicus. J. Fish. Sci. Chin., 9 (2): 133-137.
Rainuzzo, J. R., K. I. Reitan, and Y. Olsen, 1997. The signifi-
cance of lipids at early stages of marine fish: a review. Aqua-
culture, 155: 103-115.
Rana, K. J., 1985. Influence of egg size on the growth of onset
of feeding, point-of-no-return, survival and starved Oreo-
chromis mossamibcus fry. Aquaculture, 46: 119-131.
Robinson, S. M. C., and T. J. Pitcher, 1989. The effects of hun-
ger and ration level on density, population and swimming
speed of herring Slupea harengus L. J. Fish Biol., 34 (4):
631-633.
Rodríguez, A., E. Gisbert, and G. Rodríguez, 2005. Histopa-
thological observations in European glass eels (Anguilla an-
guilla) reared under different diets and salinities. Aquaculture,
244: 203-214.
Rooker, J. R., and G. J. Holt, 1996. Application of RNA: DNA
ratios to evaluate the condition and growth of larval and ju-
venile red drum (Sciaenops ocellatus). Mar. Freshw. Res., 47:
283-290.
Sargent, J. R., L. A. McEvoy, and J. G. Bell, 1997. Require-
ments, presentation and sources of polyunsaturated fatty acids
in marine fish larval feeds. Aquaculture, 155: 117-127.
Shen, W. Y., and H. R. Lin, 1999, Effects of starvation and
feeding on biochemical composition of grass carp (Cteno-
phrayngodon idellus) fingerling. Acta Zool. Sin., 45 (4): 404-
412.
Song, B., L. J. Chen, and L. J. Gao, 2004. The effects of starva-
tion on feeding, growth and biochemical composition of hy-
brid sturgeon larvae. Acta Hydrobiol. Sin., 28 (3): 333-336.
Sun, H. M., Q. Huang, and B. Cong, 2006. Effects of Starvation
on Factors Associated with Immunity in Yellow Catfish
(Pelteobagrus fulvidraco). Reserv. Fish., 3: 80-81 (in Chi-
nese).
Suneetha, K. B., A. Folkvord, and A. Johannessen, 1999. Re-
sponsiveness of selected condition measures of herring, Clu-
pea harengus, larvae to starvation in relation to ontogeny and
temperature. Environ. Biol. Fish., 54: 191-204.
Theilacker, G. H., 1978. Rearing container size affects mor-
phology and nutritional condition of larval jack mackerel,
Trachurus symmetricus. Fish. Bull., 78: 789-791.
Theilacker, G. H., and S. M. Porter, 1995. Condition of larval
walleye pollock Theragra chalcogramma, in the Western
Gulf of Alaska, assessed with histological and shrinkage in-
dices. Fish. Bull., 93: 333-344.
Theilacker, G. H., K. M. Bailey, and M. F. Canino, 1996. Varia-
tions in larval walleye pollock feeding and condition: a syn-
thesis. Fish Oceanogr., 5: 112-123.
Ueberschär, B., 1988. Determination of the nutritional condition
of individual marine fish larvae by analyzing their proteolytic
enzyme activities with a highly sensitive fluorescence tech-
nique. Meeresforschung, 32: 144-154.
326 J. Ocean Univ. Chin.
Ueberschär, B., B. H. Pedersen, and K. Hjelmeland, 1992.
Quantification of trypsin with a radioinmunoassay in herring
larvae (Clupea harengus) compared with a highly sensitive
fluorescence technique to determine tryptic enzyme activity.
Mar. Biol., 113: 469-473.
Wan, R. J., X. S. Li, and Z. M. Zhuang, 2004. Experimental
starvation On Engraulis japonicus larvae and definition of the
point of no return. J. Fish. Chin., 28 (1): 79-84.
Wen, X. B., L. Q. Chen, and Y. M. Ku, 2006, Effect of feeding
and lack of food on the growth, gross biochemical and fatty
acid composition of juvenile crab, Eriocheir sinensis. Aqua-
culture, 252: 598-607.
Wight, H. A., R. J. Wootton, and I. Barber, 2004. Interpopula-
tion variation in early growth of threespine sticklebacks
(Gasterosteus aculeatus) under laboratory conditions. Can. J.
Fish. Aquat. Sci., 61 (10): 1832-1838.
Wu, Y. Y., X. Z. Liu, and A. J. Ma, 2006. Effect of starvation
on the growth and development of Cynoglossus semilaevis
larvae. Mar. Fish. Res., 27 (2): 87-93.
Xie, X. J., L. Deng, and B. Zhang, 1998. Advances and studies
on ecophysiological effects of starvation on fish. Acta Hydro-
biol. Sin., 22 (2): 181-188.
Yin, M. C., and J. H. S. Blaxter, 1986. Morphological changes
during growth and starvation of larval cod (Gadus morhua L.)
Vol.7, No.3, 2008
and flounder (Platichthys flesus L.). J. Exper. Mar. Biol.
Ecol., 104: 215-228.
Yin, M. C., and J. H. S. Blaxter, 1987. Feeding ability and sur-
vival during starvation of marine fish larvae reared in the
laboratory. J. Exper. Mar. Biol. Ecol., 105: 73-83.
Yin, M. C., 1991. Advances and studies on early life history of
fish. J. Fish. Chin., 15 (4): 348-356.
Yin, M. C., M. S. Harvey, and J. C. A. Craik, 1993. Bio-
chemical changes during development of eggs and yolk-sac
larvae of flounder Platichthys plesus L. Acta Zool. Sin., 39 (3):
272-279.
Yúfera, M., E. Pascual, A. Polo, and M. C. Sarasquete, 1993.
Effect of starvation on the feeding ability of gilthead
seabream (Sparus aurata L.) larvae at first feeding. J. Exper.
Mar. Biol. Ecol., 169: 259-272.
Zamal, H., and F. Ollevier, 1995. Effect of feeding and lack of
food on growth, gross biochemical and fat acid composition
of juvenile catfish. J. Fish. Biol., 46: 404-414.
Zambonino Infante, J. L., and C. L. Cahu, 2001. Ontogeny of
the gastrointestinal tract of marine fish larvae. Comp. Bio-
chem. Physiol., 130C: 477-487.
Zhang, B., Y. Sun, and Q. S. Tang, 2000. Effects of starvation
on growth and biochemical composition of Pagrosomus ma-
jor. J. Fish. Chin., 24 (3): 206-210.