Reviews in Aquaculture, 1–13 doi: 10.1111/raq.

12461

Moulting in the grow-out of farmed shrimp: a review

Daniel Lemos1 and Delphine Weissman2
1 Aquaculture Laboratory (LAM), Oceanographic Institute, University of S~ao Paulo, S~ao Paulo and Ubatuba, Brazil
2 NEOVIA, Chierry, France

Correspondence Abstract
Daniel Lemos, Aquaculture Laboratory (LAM),
Instituto Oceanogr afico, Universidade de S~ao The importance of moulting for growth in farmed shrimp is reviewed in relation
Paulo, Pracßa do Oceanogr afico 191 - S~
ao Paulo to the physiological cycle, induction triggers, behavioural and compositional
(SP) - Brazil 05508-900. changes, elements for successful moulting and potential strategies for moulting
Email: [email protected] management. Successful ecdysis is also dependent on pond water quality, health
and nutritional status. The stages in the moulting cycle are as follows: premoult,
Received 22 December 2019; accepted 28
the preparation period for moulting that comprises the longest period in the cycle
May 2020.
and includes accumulation of nutrient reserves; post-moult, short and crucial
stage for shrimp recovery after moulting; and intermoult, when feeding is contin-
uous and most of growth occurs. The ecdysis is very rapid and mainly dependent
on suitable physiological status of individuals. Up to 10% of the whole shrimp
moulting cycle may rely on body nutrient reserves, once feeding is decreased or
ceased (premoult and post-moult). Moulting is started by hormonal increments
in haemolymph, 20-hydroxyecdysone and methyl farnesoate, which are found
similar in insects. Beyond health and nutrition, proper environmental conditions
such as good water quality are essential for successful moulting, hardening of
exoskeleton and rapid growth. Moulting prediction and management may result
in significant feed savings in pond farming and potential effects of, for example,
moon phases and stressors have to be further considered. The complex nature of
moulting in shrimp, including different sorts of endocrine regulation and envi-
ronmental stimuli, suggests it is difficult to be precisely controlled in farmed pop-
ulations. Moulting physiology of shrimp is discussed in relation to some farming
practices.
Key words: farming, hormone, moulting, physiology, shrimp.

shrimp physiological features evolved from an overall more

Introduction
stable medium though subjected to predation in the wild
Moulting, the cyclic exchange of exoskeleton, is a growth- (Dall et al., 1990). Behavioural and metabolic adapted
related phenomenon in crustaceans. Moulting, the ecdysis changes over the shrimp moulting cycle have significant
itself, is intercalated by a preparation (premoult), recovery implication in energy balance and thus feed utilization in
(post-moult) following an intermediate (intermoult) per- farming systems. Management of moulting in farmed
iod with the longest time spent in premoult (Dall et al., shrimp population may be considered difficult to be accu-
1990). Successful moulting requires timely and orchestrated rate but ecdysis may be predicted with some degree of suc-
physiological processes accompanied by proper pond water cess (Molina 2009).
quality and adequate nutritional status. Physiological and The present paper reviews some practical aspects of
behavioural changes are typical along shrimp moulting moulting in farmed shrimp in relation to physiological
cycle. Muscle enlargement and nutrient storage are mostly cycle, behavioural and compositional changes, moulting
checked during intermoult. Premoult is characterized by induction, the key elements for successful moulting and
regular swimming and feeding in great part of the stage, potential strategies for moulting management in ponds. It
whereas feeding activity starts reducing when approaching was prepared based on technical, scientific and some farm-
ecdysis. Moulting is an energy demanding ritual that er’s opinion. The topic in review may be of use for shrimp
implies regular challenges over the whole farming cycle – biomass production and management.

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D. Lemos and D. Weissman

time in moulting cycle is dedicated to premoult (up to

Moulting: the cycle, physiology and steps for shell
70%) followed by intermoult if expressed in % of the total
exchange and hardening
moulting cycle (Dall et al., 1990; Lemos & Phan, 2001a)
As all other arthropods, growth in shrimp is achieved by (Table 1).
initially untie the connectives between the living mass and
the extracellular cover, the exoskeleton, followed by leaving
Intermoult
it quickly, water intake to enlarge the new elastic cuticle
and rapidly harden it for body structure, locomotion, feed- Abdominal muscle buildup and accumulation of nutrient
ing and defence (Chang & Mykles, 2011). Shrimp follows a reserves (to be also used in next moulting) occur mainly
diecdysis moulting cycle, with moulting occurring every during intermoult, a rather stable and cell proliferating
few days or weeks (according to individual size), and con- metabolic phase where feeding is elevated and continuous
trasts with the anecdysis cycle of crabs and lobsters, which (Cesar et al., 2006). Replacement of incorporated water by
show longer intervals (Dall et al., 1990). Beyond an obliga- tissue mass occurs during intermoult (C), the interval
tory process for growth over shrimp lifespan, moulting has between stages A (post-moult) and D (premoult).
also reproductive function as to allow fecundation and
accompanying gonad maturation (reproductive versus non-
Premoult and Ecdysis
reproductive growth-related moult). Moulting is essential
for growth but also to remove scar, infection, parasites, The preparation period for moulting represents most of the
damaged parts and limb loss (Panakorn, 2018). life cycle in shrimp. Premoult is a dynamic period when
Intermediated by moulting events, shrimp weight regular activities (feeding, swimming) have to occur con-
increases discontinuously in live mass units (wet weight) – comitantly with physiological processes to enable successful
biggest increment occurs right after moulting by water moulting (Table 2). Premoult period is divided into the
incorporation into body to fill the space of the new and lar- sequence of substages D0, D1, D2, D3 and D4. In early pre-
ger armour (Dall et al., 1990). This contrasts with the con- moult, the proecdysis (D0-D1), shrimp start preparing for
tinuous mass increment if growth is expressed as dry moulting. Premoult begins with the increase in concentra-
matter, since incorporated water is continuously replaced tion of moulting hormones in haemolymph, 20-hydrox-
by tissue in the course of the cycle. yecdysone (20-HE or a precursor of this), secreted by the
Y-organ located at the epithelium of branchial anterior
The different stages in moulting cycle
Table 2 Some behavioural and physiological features during moulting
The moulting cycle of penaeid shrimp is classified accord- stages and substages of penaeid shrimp
ing to the proximity of ecdysis itself (stage E): the prepara-
Moulting stage and Reported features
tion period (premoult, substages D0, D1, D2, D3, D4) and
substage
recovery (post-moult, substages A and B) intercalated by a
‘moult-independent period’ (intermoult, C). The longest Premoult
D0, D1 Rise in levels of moulting hormones (20-
hydroxyecdysone and methyl farnesoate)
Increased volume of hepatopancreas (reserve
Table 1 Time representativeness (%) of moulting stages in penaeid accumulation). Hormonal control triggers
shrimp formation of new exoskeleton
D2 Decreased feeding, increased oxygen
Stage Time in each moulting stage (days)
consumption. Decreased osmoregulatory
Total stage A-B C D0-D1 D2-E capacity
duration (days) D3 Feeding ceased
D4 Water uptake started. Nutrient reserves depleted
Nauplius 2 0.15 0.45 1.2 0.2 Ecdysis (E) Old skeleton released in seconds or few minutes
Zoea or mysis 3 0.22 0.67 1.8 0.3 (in healthy shrimp)
Postlarval 1.5 0.11 0.34 0.9 0.15 Post-moult (A-B) Hardening of new exoskeleton. Replacement of
Juvenile (5 g) 7 0.5 1.57 4.2 0.7 incorporated water by tissue mass starts.
Elevated oxygen consumption. Feeding restarts
Values are hypothetical considering constant/optimal temperature, at B
water and feeding conditions. Drastic variation in such parameters may Intermoult (C) Cell proliferating phase, continuous and high
cease or accelerate moulting stages and substages. Percentage of time feeding rate. Muscle buildup and reserve
per moulting stages: A-B: 7.5%; C: 22.5%; D0-D1: 60%; D2-E: 10% accumulation. Higher expression of actin and
(Dall et al., 1990; Lemos, 2000; Lemos & Phan, 2001a). A, B: post- myosin
moult; C: intermoult; D: premoult; E: ecdysis.

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 Moulting in farmed shrimp

chambers, and methyl farnesoate, secreted by the mandibu- demand to move greater liquid volume along shrimp body
lar organ. Implantation of crab mandibular organ into (Zhu et al., 2004; Wei et al., 2009). In conclusion, the post-
shrimp resulted in shortened moult intervals accompanied moult requires extra energy for synthesis and mineraliza-
by more frequent moulting (Homola & Chang, 1997). Dur- tion of the exoskeleton.
ing premoult, the volume of hepatopancreas (central organ
for digestion and storage in shrimp) increases by nutrient
Factors that affect moulting
accumulation (also checked in muscle) to be used for dif-
ferent functions in the moulting process (Dall et al., 1990; While moulting is largely under intrinsic control, numer-
Bonilla-G omez et al., 2013; Faadila et al., 2013). ous extrinsic factors such as temperature, salinity, nutrition
The exoskeleton is majorly composed by water, chitin and water chemistry may superimpose the hormonal regu-
(glucosamine), protein and minerals. Chitin forms the web- lation (Anger, 2001). Therefore, as a prerequisite for the
like structure for sustaining the exoskeleton and provides increase in body mass, shrimp would achieve the fastest
resistance against tension. Protein fills the chitin strands and growth rate only when moulting coordinates with environ-
confers impermeable material and resistance to compression mental changes and adequate nutrition (Hou et al., 2011).
(Corteel & Nauwynck, 2010). Endogenously secreted chiti- As the main physical variable limiting production in inten-
nase, with expression controlled by 20-HE, provides diges- sive farming systems, dissolved oxygen (DO) is obviously
tion and nutrient resorption of old exoskeleton during critical during moulting and subsequent success of farmed
premoult (total nutrient recovery estimated at up to 38%) shrimp (Wei et al., 2009). Most physiological changes
(Pedrosa-Gerasmio et al., 2019). Prior to premoult, chitinase related to moulting, verified either in premoult or post-
activity increases between moulting stages A/B and D. Dur- moult, result in increased oxygen consumption, reaching
ing premoult, epidermis secretes a new cuticle (exoskeleton) 86% and 50% higher rates in phases A/B and D1-D2,
to replace the old one removed at ecdysis. respectively, compared to oxygen consumption during
Feeding starts declining in substage D2 and ceases by D3 intermoult (C) (Carvalho & Phan, 1998). Thus, farmers are
(D3 to E represents 5% of the whole moulting cycle) that is aware of the importance of keeping elevated DO in ponds,
accompanied by increased metabolic rate (doubles during especially during periods when moulting occurs in a very
E), including bursts of activity (Dall et al., 1990). Decreased significant part of the farmed population. Furthermore, the
feeding prior to moulting may be further related to ecdys- need to incorporate high volumes of water into shrimp
teroids effect in swelling oesophagus (Molina 2009). The body demands proper pond water quality. Elevated levels
renewal of chitinous foregut (stomach) with exuviation of nitrogen or sulphur compounds (poor management of
favours bacteria exclusion, improving stomach and hep- pond water and soil) may thus severely affect shrimp fitness
atopancreas condition (Panakorn, 2018). The ecdysis itself and immune response against pathogen infection at moult-
(E) is a very rapid process, under adequate physiological ing (Mugnier & Justou, 2004). Beyond these physiological
status shrimp gets free of old exoskeleton in seconds or few and energetic contests, the combination of low dissolved
minutes (Dall et al., 1990). oxygen and toxic nitrogen and sulphur levels in the pond
makes moulting even more challenging for survival and
growth of shrimp. Moulting mortality can accentuate water
Post-moult
deterioration by reducing water DO and alkalinity, as well
The early post-moult (stage A) is a critical phase when as elevating certain water components to toxic levels (Pana-
shrimp is very exposed to environment: relatively large korn, 2018).
water uptake and a soft exoskeleton. Water volume uptake Beyond the increased energy demand, exuviation may
determines individual size until next moult, and it starts in represent a net nutrient loss in terms of protein, carbohy-
substage D4 (late premoult) but most of tissue hydration drate and minerals (Sarac et al., 1994). During premoult
occurs in post-moult, stage A (Chang, 1992). Water uptake substages, D2-D3-D4 nutrient reserves reach depletion, that
by influx across epidermis, gills and gut is important is, ca. 10% of moulting cycle relies on reserves, once feeding
because it would not be mechanically appropriate moving is reduced or ceased in late premoult (Corteel & Nauwynck,
with a partially empty exoskeleton (Dall et al., 1990). 2010). It is rather common that shrimp fed diets deficient
Replacement of incorporated water by tissue mass occurs on a not so available individual mineral in water (e.g. phos-
in the interval between stages A and D. Water uptake phorus) to ingest exuvia in order to partially compensate
extends by few hours before and after ecdysis, while shrimp for this nutritional deficiency. Since calcium is the major
has to be able to harden exoskeleton a few hours after mineral in exoskeleton (followed by magnesium), shrimp
moulting (Jasmani et al., 2010). The new soft exoskeleton require high levels of calcium intake, especially after moult-
expands due to increase in haemolymph and muscle vol- ing. This requirement is met mainly by absorbing available
ume with water influx and implies in higher energy calcium directly from pond water, if available in proper

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D. Lemos and D. Weissman

levels (Parado-Estepa et al., 1989). Exoskeleton hardening inhibiting hormone (GIH) (Corteel & Nauwynck 2010; Wu
takes several hours after moulting, depending on total et al., 2016). In contrast, neurosecretory cells – located at
length of cycle, and this varies according to shrimp size eyestalk, protocerebrum, antennular and antennal neurip-
(Dall et al., 1990). Hardening is largely dependent on nutri- iles, suboesophageal ganglion – produce control of Y-or-
ent availability (from water and reserves) but is also energy gans and gonads (Dall et al., 1990). These authors also
consuming (Carvalho & Phan, 1998). Newly moulted report removing inhibition of MIH allows Y-organ to
shrimp require exoskeleton hardening as quick as possible secrete ecdysones, precursors of ecdysteroids that initiate
since chances of cannibalism upon the soft-shelled and and sustain moulting. It is speculated an analogue of
movement-limited shrimp increases (Prangnell & Fotedar, moult-accelerating hormone occurs in Crustacea as verified
2005). On the other hand, the dependence on external fac- in insects (Homola & Chang, 1997; Hosamani et al., 2017).
tors gradually decreases in older moulting stages, suggesting Methyl farnesoate, chemical structure identical to insect
a reduction in integument permeability and greater devel- juvenile hormone III, is reported to stimulate Y-organ to
opment of ion absorption/secretion mechanisms as the synthesize and secrete ecdysteroids (Huberman 2000).
exoskeleton hardens (Ferraris et al., 1987; Lignot et al., Accordingly, moult and reproduction in shrimp brood-
1999). There may be an additional great risk during ecdysis: stock by eyestalk ablation (removal of organs secreting
the moulting fluid found in-between old exoskeleton and MIH and GIH) produce gonad maturation and precocious
epidermis/new exoskeleton containing agents and products ecdysis followed by increased moulting frequency (Kim
from resorbed old exoskeleton (e.g. amino acids, enzymes, et al., 2010). It has common observation in commercial
gelified digested old exoskeleton) is a very strong feeding hatcheries ablated females spawn faster and at high fre-
stimulant and attractant for cannibalism (Chang, 1992; Tan quency but this increased moulting and vitellogenesis rate
et al., 2000; Song et al., 2017). lead to exhaustion of breeders.
The length of the interval period between moults Premoult (D) is initiated by a fall in MIH secretion in
increases with size and may differ among species: larval late intermoult and peak of ecdysteroid level. Crustecdy-
shrimp moult every 12, 24, 36 or 48 h in stages nauplius, sone (synonym of 20-hydroxyecdysone) is considered as
zoea, mysis and early postlarva, respectively, while large the active moulting hormone with ecdysone as its precursor
juvenile shrimp (15–20 g individual weight) may moult (Chang, 1992; Huberman, 2000; Girish et al., 2015). The
every 14–20 days (Dall et al., 1990; Lemos & Phan, 2001a). hormonal control triggers the start formation of new cuti-
In addition, increased moulting frequency may be also a cle (exoskeleton) at substage D1. Proenzymes (chitinases
wound response (Jia et al., 2014). Elevated moulting fre- and proteases) digest the old cuticle, and the reduction in
quency could not only increase the energy expenditure for MIH allows to release more ecdysone in haemolymph. The
exuviae, but also affect the entire energy allocation strategy peak of ecdysteroids is verified at the end of early premoult
of the animal as the process of moulting involves higher (Corteel & Nauwynck 2010).
oxygen and energy consumption (Kibria, 1993; Bonilla- The crustacean hyperglycaemic hormone (CHH) orches-
Gomez et al., 2013). By the body of literature assessed, trates moulting, carbohydrate metabolism, reproduction
weight increase seems not directly related to the length of and osmoregulation (Huberman, 2000). CHH, a neuropep-
moulting cycle. Moulting does not always produce more tide as MIH, inhibits ecdysteroid action (sterol). Selective
growth, for example rapid salinity reduction, and increased degradation of actin myofilaments occurs with increasing
temperature can enhance moulting but with adverse effects ecdysteroids in premoult contrasting with higher expres-
on growth (Allan & Maguire, 1992; Chen et al., 1992). It sion of actin and myosin in intermoult (C) (Cesar et al.,
was reported certain dietary treatments resulting in elevated 2006). The balance of degradation and synthesis can be
growth showed lower moulting frequencies (Guan et al., analysed by RNA:DNA content in tissues: higher ratios at
2016). Shrimp growth depends on the capability of muscle D2-D3 suggests protein synthesis for digestive enzymes and
restoration that includes nutrient resources for this. Com- the production of new cuticle/exoskeleton. Intense muscle
plete inhibition of moulting may be caused by continuous synthesis is also suggested by elevated RNA:DNA in early
lack of food (Anger, 2001). post-moult (stage A) (Wang et al., 2005).
Farming euryhaline crustaceans such as shrimp species
has the advantage of osmoregulation over a rather wide
Endocrine regulation
range of salinities (Ferraris et al., 1987). However, this
Moulting is primarily regulated by a circuit of peptide (the osmoregulatory capacity (OC) is reported to reduce drasti-
moult-inhibiting hormone: MIH), ecdysteroid (20-HE syn- cally before and after ecdysis (higher OC verified at stages
thesized in Y-organ) and terpenoid hormones (methyl far- C to D0) and shrimp may become isoosmotic in these peri-
nesoate synthesized in mandibular organ). Target gland ods, that is, conforming with environment osmolite, espe-
control via inhibition hormones includes MIH and gonad- cially during early post-moult (A) when relatively large

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 Moulting in farmed shrimp

volume of water is incorporated (Charmantier et al., 1994). Table 3 Potential stimulation factors of moulting and effects upon
OC may also decrease with low DO level, and after, DO is feeding management relevant to pond farmed shrimp
increased to saturation OC can be restored. Similar results Potential effects Observations
were found with OC affected by ammonia or combination
of ammonia and hypoxia during premoult (Wajsbrot et al., Moulting Rapid salinity reduction, pond water exchange,
induction factors reduced pond water level, increased
1990). Thus, the combination of low DO, heavy rain (sud-
temperature, mineral supplementation into pond
den salinity decrease), high ammonia and massive moulting water, moon phase
would be a perfect recipe for stress, disease sensible shrimp Feeding Feeding ceases by the end of premoult and
and mortality. management restarts at late post-moult, corresponding to 6 to
The lifespan of farmed shrimp species starts with spawn- 9% of the total moulting cycle. Feeding
ing tenths of thousand eggs that will develop into rapid behaviour becomes regular in the night
transforming larval stages intermediated by moulting subsequent to moulting
Feed delivery should be reduced by 10–30% in
events. The fitness and success of farmed individuals either
the predicted moulting day. Full and continuous
in larval or in juvenile stages depends on the ability in cop- aeration and key minerals provided for proper
ing with the environment (including finding the right food moulting
and in proper amounts), and this may be also related to Feed consumption reported to increase up to
genetic features. Therefore, the asynchrony in the moulting 18% in the period between post-moult and
cycle observed in farmed shrimp populations starts in premoult. Shrimp fed according to moult
hatching and larval development, and there would be no staging: lower FCR and feed savings up to 30%.
Feeding programme adapted to predicted
reason to be synchronized over time (Anger, 2001; Lemos
massive moulting related to moon phase: best
& Phan, 2001b). As explained ahead, there may be syn- yield checked in treatment with feeding
chronicity in a significant percentage of individuals in a suspended at 1st day after new moon
pond population, but it is apparently very difficult to have Feed reduction recommended at 20–30% for
synchronicity in all individuals in species with diecdysis partial population moulting, massive moulting
moulting cycle. may demand up to 50% feed reduction.
Moulting occurs majorly in the absence of light:
78% of the moulting in a shrimp population
What events may induce moulting in farmed occurs between 6 pm and 6 am
shrimp?
Scientific and practical information generally suggest dif-
ferent kinds of stress as induction factors for shrimp Several references suggest moulting cycle significantly
moulting, that is, the acceleration of the moulting cycle affected by moon phases (Molina 2009; Franke & Hoerst-
that may often result in increased mortality and growth gen-Schwark, 2013; Panakorn, 2018). Though there is not a
loss due to the sensitive status of the moulting individual full consensus on this (Dall et al., 1990), there are evidences
(Mugnier & Soyez, 2005; Jia et al., 2014). However, it is to accept that moulting in pond shrimp stocks may be
still not clear the specific reason for stress induction of intense during new moon. This would make sense in evolu-
moulting. Rapid salinity reduction and pond water tionary and adaptive terms once newly moulted (the ecdy-
exchange, reduced pond water level, increasing tempera- sis occurs mostly after sunset) soft-shelled vulnerable
ture (e.g. partial pond drainage), copper and mineral shrimp would better hide and avoid cannibalism under
cocktail addition to pond water have all been reported minimum light conditions. In contrast, and for the lack of
and used by some farmers to stimulate moulting (Abdus- synchronicity previously stated, this seems very difficult to
samad & Thampy, 1994; Rao & Anjaneyulu, 2008; Son affect the whole population. As moulting does not occur in
et al., 2011) (Table 3). However, it is rather clear by the whole shrimp population simultaneously, feed intake
experiments that increased moulting frequency does not will be constantly oscillating over the farming cycle, as well
necessarily improve growth rates (Kanazawa et al., 1984; known under practical conditions (Jory et al., 2001).
Hou et al., 2011). In physiological terms, it becomes clear Observation in pond farmed shrimp (Litopenaeus van-
well-nurtured shrimp will moult as part of the metabolic namei) registered almost 50% population moulting in last
ritual of growth, and so, the main event for moult trigger- quarter moon and up to 80% moulting in new moon
ing would be the physical limitation of exoskeleton to the (Molina 2009). Thus, farmers consider shrimp status in the
continued growth of the whole body. As previously men- last quarter moon the most critical for successful moulting.
tioned, other factors such as scar, infection, parasites, If shrimp is not healthy enough in this phase, significant
damaged parts and limb loss may also be inductive of mortality may occur in the forthcoming intense moulting
moulting (Panakorn, 2018). period of new moon. In addition, there may be also a

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D. Lemos and D. Weissman

significant share of the population affected by moulting in phase. Treatments comprised feeding suspension as follow-
full moon, spring or high tide (Panakorn, 2018). An obvi- ing: treatment I – feed suspended at 1st day after new
ous conclusion regarding the impossibility of moulting syn- moon; treatment II – at the 1st and 2nd day before new
chronization with moon phase would be the length of moon; treatment III – at 1st and 2nd day of new moon;
moulting cycle that varies according to shrimp size and do treatment IV – at new moon day; and control (non-stop
not necessarily match moon phase schedule, for example a feeding). Best yield was checked in treatment with feeding
5 g shrimp would moult at, for example, 5–7 days interval suspended at 1st day after new moon and the following
contrasting with a 20 g individuals moulting every ranking of treatments: treatment IV (feed suspended at
>14 days on average (Dall et al., 1990). new moon day) > control > treatment III (feed suspended
at 1st and 2nd day of new moon) > treatment II (feed sus-
pended 1st, 2nd day before new moon). Summing up feed-
Shrimp behaviour at moulting
ing restriction within different treatments in the whole trial
Behavioural signs of moulting include decreased feeding resulted in 6–12% total feed restriction period over the
that is followed by fluctuation of pond pH water (by grow-out cycle (Molina 2009). Outputs from this trial coin-
increased respiration and CO2 production) (Corteel & cide with commercial pond farm observations where signif-
Nauwynck, 2010). Moulting is thus among the main factors icant decreased feeding was checked (tray observation)
affecting feed intake. Shrimp stops feeding by the end of every 20–30 days over the grow-out cycle that corre-
stage D and restarts at B, relying mostly on reserves during sponded to moulting of an elevated percentage of the pond
this period with the interval D3 – B corresponding approxi- population (Jory et al., 2001). Thus, it could be concluded
mately to 6–9% of the total moulting cycle (Dall et al., the rhythmicity of massive moulting events may be
1990) (Table 2). The behavioural changes related to ecdysis explored for feed savings and better management in pond
start the night before moulting. Burying more than nor- farmed shrimp. Increased survival of farmed shrimp was
mally has been reported at D3-D4 that brings the question also reported with substrates installed in ponds due to pos-
if welfare would be affected in shrimp farmed in lined sible better shelter during moulting (Anand et al., 2013).
ponds. Accordingly, increased burying in poorly managed Feed reduction is recommended at 20–30% for partial
earthen bottom ponds would certainly pose a threat to moulting, and massive ecdysis is suggested to demand up
shrimp moulting and performance. The ecdysis (E) to 50% feed reduction (Mohanty, 2001).
includes short jumps to free from the old exoskeleton that As previously stated, moulting is mostly a night event.
breaks at the junction between carapace and abdomen. The following moulting percentages in a shrimp population
Release from old cuticle includes the withdrawal of foregut were reported according to the time of the day; 18:01–
lining (Dall et al., 1990). The newly moulted shrimp settles 0:00 h: 44% of tested shrimp, 0:01–06:00 h: 34%, 06:01–
on the bottom and remains quiescent stage A individuals 12:00 h: 16% and 12:01–18:00 h: 6% (Parado-Estepa et al.,
are not able to use pereopods as walking legs and spend 1989). It is important to note that at early morning, DO
time swimming; thus, feeding is ceased and shrimp is vul- may reach lowest levels depending of the density of primary
nerable to cannibalism. Walking and swimming restarts at producers in the pond and this may coincide with 1/3 or
stage B. In the night, subsequent to moulting shrimp beha- more of the total population at moulting.
viour becomes as in intermoult. Feeding also restarts at
post-moult stage B. Exuvia ingestion to nutrient recovery
Major physiological and compositional changes
may occur in shrimp fed mineral-deficient diets or farmed
in mineral-deficient pond water. The post-moult is considered as a period conducive to dis-
Practical farm observations recommend feed delivery eases and dysfunction. Accordingly, the potential osmotic
should be reduced between 10 and 30% in the predicted shock caused by the substantial water intake may strongly
massive moulting days (Panakorn, 2018). Once moult is affect shrimp internal medium and result in stress. The
predicted, full and continuous aeration and key minerals hepatopancreas provides energy storage for starvation
should be provided. Feed consumption is reported to (mostly triglycerides) and specific functional compounds as
increase 18% from post-moult to early premoult (stages B enzymes and hormone precursors that are crucial for
to D0). Pond farmed juvenile Litopenaeus vannamei fed moulting (Galindo et al., 2009). In early premoult, the hep-
during 60 days according to moult staging and predicted atopancreas increases in volume by nutrient accumulation.
feeding behaviour showed lower feed conversion ratio and In contrast, reserve depletion advances throughout sub-
higher protein efficiency ratio with feed savings reaching stages D2-D3-D4, and thus, a significant period in the
up to 30% (Molina 2009). A 133 days pond trial in Ecua- moulting cycle shrimp relies mostly upon reserves (Corteel
dor (L. vannamei) checked a possible feeding programme & Nauwynck, 2010) (Table 4). Cholesterol is an essential
adapted to predicted massive moulting related to moon nutrient for shrimp, a precursor for synthesis of

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 Moulting in farmed shrimp

Table 4 Nutrient dynamics and immune response in shrimp according haemolymph reduces in post-moult by dilution effect of
to moulting stages large water uptake. Therefore, it becomes clear the impor-
Nutrient/immune Observations tance of proper dietary supply of protein (muscle and shell
response building, digestive enzymes, hormones), lipids (energy
reserve, hormones), carbohydrates (glucose, circulating
Cholesterol Essential nutrient and precursor of moulting
energy, chitin synthesis) and minerals (calcium, magne-
hormones. Stored in hepatopancreas, levels
increase in haemolymph between stages C and
sium, phosphorus for exoskeleton and copper for haemo-
D1, followed by a decrease in D1 to D4 by cyanin) in the moulting process.
hormone synthesis Haemolymph calcium is reported to increase in pre-
Carbohydrates Stored in hepatopancreas as glycogen in rising moult and decreases subsequently in post-moult (Ferraris
levels between stages B and D3. Released as et al., 1986), while magnesium decreases from D0 to A (Jas-
glucose in haemolymph to attend energy mani et al., 2010). Haemolymph calcium and magnesium
demands. Levels are reduced after feeding is
levels may increase by absorption from water, resorption
ceased during premoult
Amino acids Body content varies with moulting (stages A to D):
from the old exoskeleton and by active feeding (Mugnier &
increasing trend for arginine, histidine, leucine Justou, 2004). The dynamics of mineral levels obviously
and threonine; reduction for phenylalanine. depend on medium salinity; active ion transport is higher
Lysine, methionine: body content higher in in shrimp reared in low salinity as checked with Na/K
stages A and D compared to C while valine levels ATPase activity reaching greatest values between D3 and B
higher in stage C than A and D. Amino acids (Jasmani et al., 2010).
released in exuvia: glutamic acid, aspartic acid,
In contrast, essential amino acid body content shows dif-
glycine, alanine, proline, phenylalanine, arginine,
valine, leucine and threonine
ferent patterns of change over the moulting cycle (Faadila
Phenoloxidase Increasing between stages A and C – higher et al., 2013). Different trends in body content between
activity values in elevated salinity compared to low water stages A and D were observed: arginine, histidine, leucine
salinity medium and threonine showed increasing trend, while phenylala-
Glutathione Expression increased in premoult (D1 and D2) nine decreased in the period. Lysine and methionine
peroxidase showed higher levels in stage A (post-moult) compared to
C (intermoult) that were also lower than stage D. On the
other hand, valine showed higher in stage C compared to A
ecdysteroids and sesquiterpenoids (MF), and must be sup- and D. These trends suggest the importance of essential
plied in diets (Kumar et al., 2018). When stored in hep- amino acids in processes such as synthesis of muscle,
atopancreas, cholesterol is transported by phospholipids to exoskeleton or functional proteins such as digestive
haemolymph increasing levels in C – D1 interval following enzymes. Protein content in exuvia is reported as 12% dry
decrease in D1 to D4, possibly due to ecdysteroid synthesis, weight. Main amino acids composing exuvia (and possibly
cellular membrane construction and growth (Roy et al., lost with it) are reported in the following order of impor-
2006). Carbohydrates are stored as glycogen in hepatopan- tance according to content: glutamic acid, aspartic acid,
creas, increasing at the B – D3 interval (Bonilla-G omez glycine, alanine, proline, phenylalanine, arginine, valine,
et al., 2013). Carbohydrates are released as glucose in hae- leucine and threonine (Sarac et al., 1994).
molymph as source of circulating energy, which is very
important to attend higher demands in premoult and
Immune response and disease resistance
increases between stages C and D1. Reduction in glucose
haemolymph levels in the subsequent moulting stages refers The dynamics of immune indicators also show variation
to feeding reduction at D2. Hepatopancreas also stores cal- among shrimp moulting stages. Phenoloxidase activity (re-
cium and copper that shows increased levels between C and lated to wound healing, immune defence, cuticle forma-
D4, following reduction in post-moult (Faadila et al., tion) increases from stages A to C and reduces thereafter
2013). with increased values in high salinity compared to low
Water uptake during premoult and post-moult increases salinity medium, and low humoral immune function was
shrimp body water content (up to 70% between D0 and E) reported in freshwater compared to marine (Jia et al.,
following reduction between stages A and C that is accom- 2014) (Table 4). Phenoloxidase activity was also verified to
panied by increasing body protein content (Cheng et al., increase with DO (4 – 18 mg L 1 interval) but hypoxic
2002). Haemolymph haemocyanin also rises at premoult stress was shown to affect shrimp resistance to Vibrio sp. as
(D0-D4), related to the higher oxygen demand for respira- well as the phagocytic activity was found reduced in pre
tion (Cheng et al., 2002; Galindo et al., 2009; Bonilla- and post-moult (Liu et al., 2004). On the other hand, activ-
Gomez et al., 2013). As expected, ion concentration in ity of glutathione peroxidase (immune reaction, oxidative

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D. Lemos and D. Weissman

stress – upregulated when subjected to pathogen) mRNA exuviations, that is less nutrient recovered from old
expression was shown to increase in premoult D1-D2 (Liu exoskeleton, lower survival rate, soft carapaces of dead
et al., 2010). In addition, high vulnerability to the White shrimp and cannibalism (Wei et al., 2009). In addition,
Spot Syndrome Virus (WSSV) has been demonstrated dur- hypoxia is reported to delay shrimp recovery from moult-
ing stages A and B of post-moult (Corteel et al., 2009). ing and increase mortality and cannibalism (Mugnier &
Reduced disease resistance at stage A was attributed to a Soyez 2005). Moulting management in farmed shrimp con-
decrease in hemocyte count, phenoloxidase activity, respi- siders regular checking (estimation) of moulting stage in
ratory burst, phagocytic activity and clearance efficiency pond population, keeping a register as to anticipate massive
against Vibrio sp. (Le Moullac et al., 1997). Susceptibility to moultings, especially those possibly affected by moon
WSSV was also found higher in premoult if salinity drops phase, and adjust feed delivery according to moulting
to <10 ppt, and this may be accentuated during ecdysis and events (Molina 2009). Dissolved oxygen management to
early post-moult (Thuong et al., 2016). In contrast, pre- keep proper levels in critical moments (e.g. early morning
moult individuals showed higher resistance to WSSV in in ponds with natural productivity) is necessary by the evi-
higher salinity (20–50 ppt). The large volumes of water dences presented. Mineral management of pond water
incorporated into body during moulting may represent includes elevating ionic content especially in low and oligo-
greater chance to virus acquirement and coincides with a haline waters but also dietary mineral supply (Prangnell &
more immunodeficient shrimp (Corteel et al., 2009). Fotedar, 2005).
Acutely infected shrimp by Taura syndrome virus resulted Proper calcium (mainly from pond water, if available)
in elevated mortality at moulting or early post-moult (Has- and phosphorus (from diet) intake has to be ensured in
son et al., 1999), while Vibrio sp. infection produced 4 order to help the new shell form itself. The addition of the
times more mortality in premoult compared to intermoult so-called osmoregulators (mineral supply) may help reduce
– in this study, the resistance to vibriosis was correlated the extent of osmotic shock during moulting, especially in
with phenoloxidase activity (Le Moullac et al., 1997). The farms in which salinity is reduced or when water renewal is
changes in state of exoskeleton at moulting could also make limited. Significant reduction in water mineral content may
infection easier. occur after massive moulting. If alkalinity decreases during
moulting by intense mineral uptake to form new exoskele-
ton, this should be further corrected to minimum 100–
Some key elements for successful moulting
120 mg L 1 CaCO3 (Panakorn, 2018). In shrimp, magne-
The key elements for farmed shrimp cited in the literature sium is a key element and found to be involved primarily
(scientific or practical) include mineral management of in nerve conduction, muscle contraction and haemolymph
pond water (individual minerals, alkalinity, salinity), pH coagulation during the moult cycle (Tian et al., 2012). Min-
and dietary nutrient supply (minerals, cholesterol, phos- eral shortage causes soft shell individuals regularly accom-
pholipids and fatty acids) (Table 5). However, basic water panied by increased cannibalism. In low salinity farms, the
quality features such as high DO, reduced levels of nitroge- difficulty in maintaining adequate mineral balance in hae-
nous products as ammonia, nitrite and absence of toxic molymph may result in moult-related mortality. Literature
gases (H2S) are prerequisites for moulting management. As reported dietary requirement values for Ca, P, Mg and K to
a basic rule, pond water quality for proper moulting must reach high growth accompanied by moulting frequency
be plenty of DO, as much as possible under species limits. (Kanazawa et al., 1984) may vary according to mineral
Practical pond observation indicates DO levels under availability of dietary sources and total dietary calcium con-
4 mg L 1 for 30 days resulted in more energy lost in tent, among other factors (Tacon et al., 2009). Pond water
pH lower than 8.3 is suggested for mineral extraction from
Table 5 Some key elements for successful moulting in farmed shrimp
the old exoskeleton (Panakorn, 2018). This author also sta-
Parameter Observations ted if pH is higher, moulting is delayed until pH is reduced,
which often occur at evening time after ceasing photosyn-
Pond water quality Sufficient dissolved oxygen level, reduced
thesis. Some farmers report application of probiotic via
concentration of ammonia, nitrite and
absence of toxic gases
feed in the first meal after moulting to minimize risk of
Mineral management Supply and regular checking of essential pathogenic bacteria.
of pond water individual minerals. Control of alkalinity and Moult-specific nutrient requirements in shrimp are a
pH rather scarce topic though the added physiological demand
Moult staging of pond Anticipate massive moultings (e.g. moon for minerals, protein and energy in moulting (Koshio &
population effects), adjust feed delivery Davis, 2011). The fundamental role of protein and amino
Dietary contribution Sufficient supply of cholesterol, phospholipid
acids in discontinuous growth dynamics, either by catabolic
and essential PUFA
or by anabolic processes, and losses, has to be attended via

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 Moulting in farmed shrimp

feed and natural food (Sarac et al., 1994). In mud crab lar- sago pam), Portulaca oleracea (common purslane) and
vae (megalopa, Scylla serrata), high dietary cholesterol level Morus sp., injected at 27.5 µg per shrimp (Penaeus mon-
is recommended due to shortened moulting interval in this odon), resulted in shortened moulting cycle in the following
larval stage (Kumar et al., 2018). Phospholipid deficiency order of efficiency Portulaca >Morus > Cycas (Rosmiati
in Chinese mitten crab (Eriocheir sinensis) may induce et al., 2016).
triglyceride deposition in the hepatopancreas, which cannot Melatonin or serotonin injection (4ng per g body
be transported out in time and lead to an excessive accu- weight) was found to increase ecdysteroid and methyl far-
mulation of neutral lipids in hepatopancreas, causing early nesoate haemolymph level in juvenile mud crab (Girish
moulting as a compensatory measure. Dietary fatty acids, et al., 2015, 2017). Different levels of methyl farnesoate in
especially C18:2, C20:5 and C22:6, and other long-chain water to Artemia sp. larva showed different moulting
polyunsaturated fatty acids are essential for crustaceans and responses according to dosage: 10 6 M moult-related mor-
have a significant impact on growth, reproduction and tality, 10 7 M delayed ecdysis and 10 8 M accelerated ecd-
moulting. It is suggested C20:5n-3 would be mainly ysis (Ahl & Browns 1990). Methyl farnesoate has been
involved in moulting and membrane construction (Li et al., identified as a stimulator of protein synthesis, promoter of
2011). moult cycle and reproduction in crustaceans. Eyestalk abla-
tion was shown to increase 20-HE and methyl farnesoate
haemolymph levels but both hormones can also delay ecdy-
Strategies with potential impact on moulting
sis depending on dose and timing (Homola & Chang,
management
1997). The precise regulation of endogenous 20-HE is con-
Literature reports the use of compounds for moulting sidered fundamental to successful moulting. Evidence from
induction or inhibition in different crustacean species both insects and crustaceans suggests that a pulse (rise and
either with diecdysis or with anecdysis moulting type. Some decline) of the 20-HE is necessary for a complete moulting
phytoecdysteroids, as found in plants from family Amaran- cycle (Song et al., 2017). On the other hand, dietary supple-
thaceae and Moraceae, were shown to have structure analo- mentation of 20-HE (2, 8 and 31 ppm) reported to nega-
gous to growth hormone of insects and crustaceans – these tively affect immune system against pathogen infection in
phytoecdysteroids are produced by plant species as an evo- juvenile L. vannamei (Wu et al., 2016). Injection of 20-HE
lutionary adaptation acting as a defence against insect (0.1–1 µg g 1 live shrimp) shortened intermoult and pre-
attack (Fujaya et al., 2014). Furthermore, the injection of moult (stages C and D) but also caused mortality and
ecdysteroid precursor inokosterone (analogous to crab abnormal development in juvenile of this species (Chan
ecdysteroid) resulted in shortened moulting cycle in shrimp et al., 1990). It was also reported artificially elevated ecdys-
(Dall et al., 1990). Ecdysteroid administration is considered teroid level during late premoult could delay ecdysis in
effective for moulting induction if provided in small and crustaceans (Chang & Mykles, 2011). Note: by the similar-
frequent doses rather than a massive single injection ity of moulting hormones reported between groups, the use
(Chang, 1992). In larval blue swimming crab, dietary sup- of insect meals in shrimp diets should consider potential
plementation of phytoecdysteroid (Vitomolt 230 mg kg 1 moulting effects.
– recovered from blackberry Morus alba) showed to be Nutritional conditions that accelerate lipid accumulation
moulting stimulant (Ahmad et al., 2015). Accordingly, in hepatopancreas may support moulting development in
Morus alba extract in diets for larval crab (1–4 mg/100 g) crustaceans. Accordingly, reduced dietary lipid content has
decreased mortality by moult death syndrome, that is the been associated with lower moulting frequency in Chinese
incapacity to escape from old cuticle during ecdysis (Fujaya mitten crab (Li et al., 2011).
et al., 2014). It could be thus speculated that moult death Water parameters are also reported to affect moulting
syndrome could be related to decreased chitinase activity/ frequency in crustaceans. At 30 ppt salinity, low water pH
efficiency to digest the old exoskeleton. In prawn, Macro- (4.9) significantly decreased dry matter content and ele-
brachium rosembergii juvenile immersion in KK-42 (imida- vated moulting frequency accompanied by reduced growth
zole derivative) at 1.95 9 10 4 mol L 1 resulted in higher rate in juvenile shrimp (P. monodon) in comparison with a
growth and shortened moulting cycle (Guan et al., 2016). It control (pH = 7.8) (Allan & Maguire, 1992). This study
was noted chitinase activity doubled with KK-42, and a also showed moulting frequency was higher at 15 compared
higher 20-HE was found in shrimp haemolymph level (Xia to 30 ppt but weight gain was similar in both salinities.
et al., 2012). Spinach extract was also reported to contain Salinity levels tested at 5–40 ppt resulted in reduced moult-
phytoecdysteroids: either injected (700 ng per g body) or ing frequency at 15–25 ppt but growth was higher at 5–20
added to diet of mud crab (Scylla sp.), it produced moult- ppt, another example of moulting frequency not directly
ing stimulation (anecdysis cycle) (Aslamyah & Fujaya, related to growth in juvenile Fenneropenaeus chinensis
2010). Phytoecdysteroids from Cycas revoluta (Japanese (Chen et al., 1992).

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D. Lemos and D. Weissman

Herbal medicines Withania somnifera, Mucuna prurita, span of shrimp. It represents a periodic fitness test that will
Ferula asafoetida and Piper longum enriching Artemia sp. ultimately determine survival and growth. The complex
fed to spawner shrimp increased fecundity and gonadal nature of moulting in shrimp, integrating endogenous
weight and reduced intermoult period (higher moulting interconnected hormonal control and nutrient dynamics
frequency) (Citarasu, 2010). Additional moulting stimu- with different sorts of environmental stimuli, intuitively
lants include ponasterone, RH 5849, copper sulphate suggests it is difficult to control. Moulting management in
(0.05–0.1 mg L 1 in pond water), malachite green, nys- farmed shrimp populations is still not a precise procedure
tatin, prostaglandin E2 and tea-seed cake, which was shown due to the characteristics of the species, the absence of syn-
the most effective among these compounds (Hu & Cao, chronization between all the individuals within a popula-
1997). A shortened moulting cycle was also reported with tion and the farming systems (e.g. individuals and
dietary supplementation of astaxanthin in Marsupenaeus behaviour not observable in turbid pond water, patchy dis-
japonicus postlarva (Petit et al., 1997). Accordingly, poly-B- tribution in shrimp population), but putting shrimp in the
hydroxybutyrate (PHB), a precursor of B-hydrohybutyric most favourable environment to allow them to moult prop-
acid, increased moulting in Chinese mitten crab at 1% diet erly may be feasible and result in significant gain in farming
inclusion (Deng et al., 2016). Dietary administration of 5- efficiency.
aminolevulinic acid (5-ALA) at 15, 30 and 60 mg kg 1 Though some compounds have been identified as
increased expression of ecdysis-related and chitin metabo- moulting effectors, the complexity and challenging nature
lism (chitinase) genes, enhanced immune response and of moulting still pose significant risks for massive appli-
induced ecdysis. After Vibrio parahaemolyticus infection, 5- cation since, for example, not all the shrimp population
ALA supplementation increased survival by enhanced would be at the same moulting stage or health status
immune response in juvenile L. vannamei (Pedrosa-Geras- when moulting effector is applied. The potential occur-
mio et al., 2019). On the other hand, the use of competitive rence of pathogens may provide additional risk – it is
inhibitors for the moult-inhibiting hormone receptor may worth reminding that in the wild, where shrimp evolved
have a growth promoting effect by interference with the for hundreds of thousands years, pathogen risk is gener-
receptor in the Y-organ and cause a surge in production of ally much lower than in dense farmed population. This
ecdysteroids (Shrivastava & Princy, 2013). Physical stress as same argument would be valid in regard to the risk of
continuous bottom water velocity in ponds (>5 cm s 1) by cannibalism under farming conditions.
use of jet aerators was reported to induce moulting result- The adaptive nature to the wild environment, where
ing in shortened moulting interval. In laboratory and pond most conditions are stable (except food availability) or can
experiments, frequent moulting by this physical stress was rather be manageable according to shrimp physiology and
showed to weaken shrimp (M. japonicus) performance and behaviour, is perhaps the greatest challenge in predicting
make them more accessible to cannibalism (Wijsekara and controlling moulting in pond farming systems, in
et al., 2005). which water quality is subjected to significant fluctuation.
Factors that halt moulting include oxytetracycline that is It could be speculated the best strategy for shrimp biomass
reported to disturb the mineralization process via complex production could consider reduced moulting frequency
formation with calcium and magnesium, and decrease and longer intermoult period with large mass increment
exoskeleton mineral content in juvenile L. vannamei (Far- rather than more frequent, energy demanding and chal-
oongsarng et al., 2013). Further examples of anti-moulting lenging ecdysis.
compounds (anti-ecdysteroid activity) include 4-nonylphe-
nol, propiconazole and bisphenol A. Chitin synthesis dis-
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