Endocrine Regulation of Compensatory Growth in Fish: Eugene T. Won and Russell J. Borski

REVIEW ARTICLE
published: 01 July 2013

doi: 10.3389/fendo.2013.00074
Endocrine regulation of compensatory growth in fish

Eugene T. Won and Russell J. Borski *
Department of Biology, North Carolina State University, Raleigh, NC, USA
Edited by: Compensatory growth (CG) is a period of accelerated growth that occurs following the
Yong Zhu, East Carolina University,
alleviation of growth-stunting conditions during which an organism can make up for lost
USA
growth opportunity and potentially catch up in size with non-stunted cohorts. Fish show a
Reviewed by:
Weimin Zhang, Sun Yat-sen particularly robust capacity for the response and have been the focus of numerous studies
University, China that demonstrate their ability to compensate for periods of fasting once food is made avail-
Wanshu Hong, Xiamen University, able again. CG is characterized by an elevated growth rate resulting from enhanced feed
China
intake, mitogen production, and feed conversion efficiency. Because little is known about
Takeshi Miura, South Ehime Fisheries
Research Center, Japan the underlying mechanisms that drive the response, this review describes the sequen-
*Correspondence: tial endocrine adaptations that lead to CG; namely during the precedent catabolic phase
Russell J. Borski , Department of (fasting) that taps endogenous energy reserves, and the following hyperanabolic phase
Biology, North Carolina State (refeeding) when accelerated growth occurs. In order to elicit a CG response, endoge-
University, Box 7617, Raleigh, NC
nous energy reserves must first be moderately depleted, which alters endocrine profiles
27695, USA
e-mail: [email protected] that enhance appetite and growth potential. During this catabolic phase, elevated ghrelin
and growth hormone (GH) production increase appetite and protein-sparing lipolysis, while
insulin-like growth factors (IGFs) are suppressed, primarily due to hepatic GH resistance.
During refeeding, temporal hyperphagia provides an influx of energy and metabolic sub-
strates that are then allocated to somatic growth by resumed IGF signaling. Under the right
conditions, refeeding results in hyperanabolism and a steepened growth trajectory relative
to constantly fed controls. The response wanes as energy reserves are re-accumulated
and homeostasis is restored. We ascribe possible roles for select appetite and growth-
regulatory hormones in the context of the prerequisite of these catabolic and hyperanabolic
phases of the CG response in teleosts, with emphasis on GH, IGFs, cortisol, somatostatin,
neuropeptide Y, ghrelin, and leptin.
Keywords: compensatory growth, fish, aquaculture, growth hormone, ghrelin, NPY, leptin, insulin-like growth factor
INTRODUCTION: COMPENSATORY GROWTH OVERVIEW (Dobson and Holmes, 1984; Jobling et al., 1993; Maclean and Met-
Compensatory growth (CG) is a period of accelerated somatic calfe, 2001; Nikki et al., 2004), cyprinids (Russell and Wootton,
growth following the alleviation of growth-stunting conditions, 1992; Wieser et al., 1992), perciformes (Hayward et al., 1997;
that temporarily induces a steeper growth trajectory than that of Picha et al., 2006, 2008b; Turano et al., 2007, 2008; Ferrando
cohorts not previously exposed to adverse conditions (Figure 1). et al., 2009), flatfish (Cho, 2005; Heide et al., 2006), stickle-
This phenomenon was seminally documented nearly a century backs (Zhu et al., 2003), cichlids (Wang et al., 2000), catfish
ago (Osborne and Mendel, 1916), and the term “CG” coined (Gaylord and Gatlin, 2000), and gadids (Jobling et al., 1994).
40 years later (Bohman, 1955). CG has been documented in all While the degree of growth compensation achieved depends on
vertebrate classes; humans (Prader et al., 1963; Boersma and Wit, species, it is nonetheless typically characterized by hyperpha-
1997; Sapolsky, 1998), other mammals (Bohman, 1955; Wilson gia, improved feed conversion efficiency, and elevated specific
and Osbourn, 1960; Mersmann et al., 1987; Ryan, 1990), birds growth rate (SGR). Although not often assessed, a critical fea-
(Wilson and Osbourn, 1960), reptiles (Bjorndal et al., 2003; Rad- ture of individuals undergoing CG is that their SGR is higher
der et al., 2007), and amphibians (Alford and Harris, 1988; Vonesh relative to similar-sized cohorts (i.e., SGR normalized to body
and Bolker, 2005), but most extensively in fish (Ali et al., 2003 mass) that were never subjected to stunting conditions (Skalski
for review). Despite the diversity of animals and plants that can et al., 2005; Picha et al., 2006). Considering that CG results in
exhibit CG, the underlying mechanisms governing the response enhanced growth rate and feed efficiency, it is not surprising that
are still poorly understood. commercial production appears to be the driving impetus behind
A broad range of teleosts are capable of undergoing investigations into CG in fish, as the majority of studies to date
CG responses following alleviation of various growth-stunting involve cultivated species. Compared to conventional methods
conditions or their combination, including suboptimal temper- of fish farming that deploy a constant regimen, incorporation
ature, crowding, or other stressful environments, and feed restric- of rearing protocols that induce CG shows promise of reducing
tion, the latter reflecting the condition most often studied (Ali the amount of feed needed to grow at least some species of fish
et al., 2003). A CG response has been reported in salmonids commercially.
www.frontiersin.org July 2013 | Volume 4 | Article 74 | 1

Won and Borski Endocrine regulation of compensatory growth
FIGURE 1 | Compensatory growth (CG) paradigm during fasting and

refeeding (dashed line) compared to constant growth rate in fed
controls (solid line). Normal growth (A) is disrupted by feed restriction
(hatched bar), which results in a decline in the growth trajectory (B) and a
size disparity compared to control animals fed a constant regimen. When
feeding resumes, hyperphagia and enhanced growth axis activity drive a
hyperanabolic phase (C) marked by a steeper growth curve than that of
constantly fed animals. The CG response potentially allows stunted animals FIGURE 2 | Endocrine regulation of growth and appetite during normal
to fully compensate for lost growth opportunity and re-converge in size with anabolism, catabolism, and hyperanabolism (CG) resulting from
constantly fed controls before the growth rate returns to normal (D). feeding status. Growth is regulated by the GH/IGF axis; GH secreted into
circulation by the pituitary binds its receptor (GHR) to stimulate hepatic
IGF-I production, which systemically drives somatic growth and exerts
negative feedback on GH secretion. Lipolysis is an alternate function of GH
Because most fish exhibit indeterminate growth and many are
during catabolism. Peripheral signals from a lipostatic mechanism
susceptible to seasonal changes in growth rate associated with nat- (anorexigenic), possibly leptin, and ghrelin (orexigenic) regulate energy
ural variations in temperature and prey availability, they tend to intake by modulating NPY and other neuropeptides in the central feeding
exhibit a robust capacity for CG (Mommsen, 2001). Hence, they center. Ghrelin also functions as a GH secretagogue. Arrows show the
can ostensibly serve as valuable subjects for evaluating the meta- direction of regulatory pathways; widening/narrowing of arrows represents
a dynamic increase/decrease in a component over the duration of a
bolic and endocrine mechanisms that may contribute to anabolic
particular metabolic state. (A) During regular feeding, energy homeostasis
processes generally, and hyperanabolism specifically. Acknowledg- is maintained by matching energy intake and expenditure. Peripheral signals
ing the diversity of fish in which CG has been documented and counter-regulate appetite centrally. Growth is regulated by nominal levels of
the complexity of the response itself, few attempts have been made circulating GH, which stimulates IGF-I production via hepatic GHRs. (B)
to consolidate what is known about the endocrine mechanisms Fasting necessitates catabolic processes to provide energy for basal
metabolism. Rising ghrelin production stimulates both appetite and
that underlie the response; however, the cumulative research on
circulating GH levels. Elevated lipolytic GH levels exploit stored energy
isolated components of CG provides insightful information from reserves, decreasing lipostatic signaling. Reduced hepatic GHR expression
which to extrapolate a fundamental framework. In particular, the desensitizes the liver to GH-induced IGF-I production. (C) Refeeding
CG response can be divided into catabolic (e.g., during fasting, signifies the switch from catabolic to anabolic processes. Temporally
stress, low temperature) and anabolic (during realimentation or a elevated orexigens carried over from fasting drive hyperphagia. The return
to positive energy status is characterized by the resumption of hepatic GH
return to more favorable conditions) phases, which elicit distinct sensitivity and a steep rise in circulating IGF-I levels, which promotes
and sequential endocrine responses (Figure 2; Table 1). The pur- accelerated growth. Eventually, the repletion of energy reserves and
pose of this review is to ascribe possible roles to select appetite negative feedback from IGF-I returns GH and appetite to nominal levels,
and growth-regulatory hormones in the context of the catabolic marking the return to normal growth rates. (PIT, pituitary; HYP,
hypothalamus; NPY, neuropeptide Y; GH, growth hormone; GHR, growth
and (hyper)anabolic phases of the CG response in teleosts, with
hormone receptor; IGF-I, insulin-like growth factor I).
emphasis on growth hormone (GH), insulin-like growth factors
(IGFs), cortisol, somatostatin, neuropeptide Y (NPY), ghrelin, and
leptin.
in stunting, and can be countered with behavioral compensation
CATABOLIC STATE: PRIMING THE COMPENSATORY GROWTH such as decreasing energy expenditure (Ali et al., 2003). Excessively
RESPONSE long periods of fasting, on the other hand, lead to an irrecoverable
In order to induce CG, a preceding catabolic period is necessary, lapse in growth that prevents full catch up to fed cohorts (Bil-
the degree of which affects the overall magnitude of the response ton and Robins, 1973; Gaylord and Gatlin, 2000). Nevertheless,
(Russell and Wootton, 1992; Wieser et al., 1992; Wang et al., 2000). moderate catabolism that taps expendable energy-storing tissues
This negative energy period depletes endogenous energy reserves physiologically primes the CG response by opening pathways that
and alters endocrine profiles that modulate appetite and growth elevate circulating GH and stimulate orexigens such as ghrelin and
potential once feeding is reinstated (Figure 2B). Brief periods of NPY. Studies in striped bass (Morone saxatilis) suggest that a pre-
feed restriction do not sufficiently deplete stored energy or result requisite drop in the hepatosomatic index (HSI) to about 1.5 is
Frontiers in Endocrinology | Experimental Endocrinology July 2013 | Volume 4 | Article 74 | 2

Table 1 | Modulation of select endocrine factors during the transition from catabolism (fasting) to hyperanabolism (refeeding).
Catabolism (fasting) Hyperanabolism (refeeding)
Response Effect Reference Response Effect Reference
GH Elevated levels Lipolysis (protein Sheridan (1986), Deng Residually high, Elevated IGF Collie and Stevens (1985),
sparing) et al. (2004), Albalat then decreasing production, Foster et al. (1991), Sun and
et al. (2005), Small and enhanced protein Farmanfarmaian (1992), Fine
Peterson (2005), uptake et al. (1993), Norbeck et al.
Norbeck et al. (2007), (2007), Picha et al. (2009),
Picha et al. (2009) Pierce et al. (2011), Kling
et al. (2012)
GHR (liver) Downregulated Hepatic GH Gray et al. (1992), Mori Upregulated GH-induced IGF Gray et al. (1992), Small
resistance et al. (1992), Duan production et al. (2006), Picha et al.
(1998), Deng et al. (2008b)
(2004), Saera-Vila et al.
(2005), Norbeck et al.
(2007), Picha et al.
(2008b)
IGFs Suppressed Growth stasis Duan and Plisetskaya Elevated/ Enhanced somatic Uchida et al. (2003),
(1993), Picha et al. Overcompensated growth Beckman et al. (2004), Picha
(2008b) et al. (2008a); Picha et al.
(2008b)
Ghrelin Elevated levels Increased Kaiya et al. (2003a); Ran Residually high, Hyperphagia Riley et al. (2005), Matsuda
appetite, GH et al. (2004), Unniappan then decreasing et al. (2006), Miura et al.
secretion and Peter (2004); Fox (2006)
et al. (2007), Picha et al.
(2009)
NPY Elevated levels Increased Peng et al. (1994), Residually high, Hyperphagia Lopez-Patino et al. (1999),
appetite Silverstein et al. (1998), then decreasing Narnaware et al. (2000),
Leonard et al. (2001) Volkoff and Peter (2001),
Aldegunde and Mancebo
(2006), Kiris et al. (2007)
Leptin Species/tissue Regulation of Kling et al. (2009), Species/tissue Lipostatic signal? Johnson et al. (2000),
dependent energy Rønnestad et al. (2010), dependent Nieminen et al. (2003),
metabolism? Fuentes et al. (2012), Volkoff et al. (2003),
Frøiland et al. (2012), Murashita et al. (2008),
Trombley et al. (2012), Gorissen et al. (2009), Won
Zhang et al. (2012) et al. (2012)
Cortisol Elevated levels GH secretion, Nishioka et al. (1985), Low levels Enhanced somatic Kajimura et al. (2003), Leung
hepatic GH Kajimura et al. (2003), growth et al. (2008)
resistance, IGF-I Small and Peterson
suppression (2005), Leung et al.
(2008), Pierce et al.
(2011)
Somatostatin Elevated levels Hepatic GH Very and Sheridan Low levels Enhanced somatic Very and Sheridan (2002)
resistance, IGF-I (2002), Sheridan and growth
suppression Kittilson (2004)
The response, or relative presence of a component, during a particular metabolic state is paired with what is estimated to be the relevant effect it has in eliciting
compensatory growth (GH, growth hormone; GHR, growth hormone receptor; IGFs, insulin-like growth factors; NPY, neuropeptide Y).

necessary in order to elicit the response (Picha et al., 2006; Turano or anabolic processes are required (de Celis et al., 2003; Saera-Vila
et al., 2007). The rise in appetite and alterations in physiology that et al., 2005; Very et al., 2005; Kittilson et al., 2011). During negative
occur during the catabolic phase preceding CG thereby potentiate energy states, hepatic resistance to elevated plasma GH is evident
hyperphagia and accelerated growth when feeding is reestablished. as decreased IGF-I production (Duan and Plisetskaya, 1993; Picha
Hence, an adequate, but not excessive level of catabolism is essen- et al., 2008b) due to catabolic suppression of ligand binding to
tial to elevating the capacity of an animal to undergo CG and GHRs (Gray et al., 1992; Mori et al., 1992; Duan, 1998). This type of
possibly achieve full catch-up growth when conditions improve. hepatic GH resistance during catabolism is characterized as down-
regulated GHR mRNA levels in striped bass (Picha et al., 2008b)
GROWTH HORMONE: FUNCTION AND REGULATION DURING and gilthead seabream (Saera-Vila et al., 2005), decreased hepatic
CATABOLISM GH binding in gilthead sea bream (Pérez-Sánchez et al., 1994) and
Under differential regulation by a host of neuroendocrine reg- both reduced hepatic GHR transcript and GH-binding in rainbow
ulatory factors, GH serves dual roles depending on metabolic trout (Norbeck et al., 2007) and black seabream (Acanthopagrus
state, mobilizing lipids during catabolism and promoting somatic schlegeli; Deng et al., 2004); alleviated in all cases by refeeding.
growth during anabolism (reviewed in Canosa et al., 2007). Dur- Hepatic GH resistance is likely mediated, in part, by cortisol
ing fasting, rising plasma GH (MacKenzie et al., 1998), along with and somatostatins during fasting. While stimulating GH synthe-
the related somatolactin in fish (Mingarro et al., 2002), protects sis, cortisol simultaneously suppresses hepatic IGF-I production
non-expendable tissue such as muscle and vital organs from being through direct downregulation of transcription and synthesis in
catabolized by preferentially metabolizing fat over protein. This silver sea bream (Sparus sarba; Leung et al., 2008) and Mozam-
lipolytic function has been demonstrated in fish with exogenous bique tilapia (Kajimura et al., 2003; Pierce et al., 2011), or in
GH treatment in vivo in coho salmon (Oncorhynchus kisutch; conjunction with suppression of GHR transcript in channel catfish
Sheridan, 1986) and in vitro in gilthead sea bream (Sparus aurata) (Small et al., 2006). Somatostatins also reduce GH binding in the
adipocytes (Albalat et al., 2005), and is a critical adaptation to liver and suppress IGF-I gene expression (Very and Sheridan, 2002;
surviving negative energy periods. Sheridan and Kittilson, 2004). Hepatic resistance to GH through
Catabolically elevated GH secretion is mediated by reduc- reduced receptor expression and signaling, despite elevated levels
tions in metabolite levels (glucose/amino acids) and is stimulated of circulating ligand, signifies an uncoupling of the lipolytic and
in vitro and in vivo by orexigens, including ghrelin (Picha et al., growth-regulatory functions of GH during negative energy states.
2009) and NPY (Peng et al., 1993), as well as by the lack of The carry over of catabolically elevated GH, in turn, helps drive
negative feedback inhibition from IGF-I. In striped bass pitu- enhanced IGF-I production and may ultimately potentiate hyper-
itaries, IGF-I potently suppresses in vitro GH synthesis and release anabolic growth pending the return to a positive energy state when
(Fruchtman et al., 2000; Picha et al., 2009), which likely con- hepatic GHR signaling resumes.
tributes to elevated GH production during fasting when IGF-I
levels are depressed. Cortisol, the dominant stress corticosteroid GHRELIN: PERIPHERAL MODULATOR OF GH SECRETION AND APPETITE
in fish (Mommsen et al., 1999; Dyer et al., 2004), also stimulates DURING CATABOLISM
in vivo GH transcription in channel catfish (Ictalurus punctatus; The rise in lipolytic GH during fasting is fundamentally impera-
Small and Peterson, 2005) and in vitro release from somatotrophs tive for sparing muscle and organs by deferring catabolism to fat
in Mozambique tilapia (Oreochromis mossambicus; Nishioka et al., stores. Upstream regulation of enhanced GH production during
1985). Plasma GH levels are elevated by as much as twofold in rain- fasting is therefore dependent on an indicator of nutritional state
bow trout (Oncorhynchus mykiss; Sumpter et al., 1991; Farbridge to coordinate catabolic lipolysis with negative energy states. The
and Leatherland, 1992; Norbeck et al., 2007), Nile tilapia (Ore- orexigenic peptide, ghrelin, responds to fasting and is a potent GH
ochromis niloticus; Toguyeni et al., 1996), channel catfish (Small secretogogue, comparable in effect to growth hormone releasing
and Peterson, 2005), and striped bass (Turano, 2007) during fast- hormone (GHRH) (Hataya et al., 2001). The differential regula-
ing when exogenous metabolic substrates are limited and fat tion of appetite and GH secretion by ghrelin in fish relies on spe-
reserves are needed for energy. Elevated GH is therefore able to cific Ser3 modifications (Unniappan et al., 2002; Riley et al., 2005;
mobilize lipids for maintenance of basal metabolism during food Jönsson et al., 2007). Ghrelin’s actions are mediated by the growth
deprivation, but without directing limited energy resources toward hormone secretogogue receptor (GHSR), which is distinct from
growth due to catabolic GH resistance in the liver. the GHRH receptor (Kojima et al., 1999). In fish, ghrelin mRNA is
The actions of GH are mediated by GH receptors (GHRs), for expressed predominantly in the gut and stomach (Unniappan and
which two distinct gene lineages exist in fish and which operate Peter, 2005), and it is interestingly the only known peripheral orex-
via different signaling pathways (Kittilson et al., 2011). The teleost igen originating from the gut considering its proximity to nutrient
GHR-1 is homologous to the single mammalian GHR (Fuka- uptake. To a lesser extent, central ghrelin gene expression has also
machi and Meyer, 2007) and has a shared affinity for both GH been detected in rainbow trout (Kaiya et al., 2003a), eel (Anguilla
and somatolactin (Fukada et al., 2005) whereas the type 2 GHR japonica; Kaiya et al., 2003b), Mozambique tilapia (Kaiya et al.,
is specific to GH activation (Fukada et al., 2004; Jiao et al., 2006; 2003c), and goldfish (Carassius auratus; Unniappan et al., 2002),
Pierce et al., 2007). The degree to which the individual receptor as has GHSR transcript in black sea bream (Chan and Cheng,
types mediate lipolysis or regulate growth is not known, but GH 2004). Ghrelin stimulates GH secretion in vitro in cultured orange
actions in various tissues are likely contingent on the differen- spotted grouper (Epinephelus coioides) pituitaries (Ran et al., 2004)
tial expression of these receptors depending on whether catabolic and in vivo and in vitro in Mozambique tilapia (Fox et al., 2007),

rainbow trout (Kaiya et al., 2003a), goldfish (Unniappan and Peter, 2009). Plasma ghrelin and GH levels in the treatment fish of this
2004), and striped bass (Picha et al., 2009). Besides actively stimu- trial were concordantly elevated during fasting and then even-
lating GH secretion, in mammals ghrelin also independently acts tually returned to control levels after refeeding. Refeeding was
as a functional antagonist to somatostatin (Arvat et al., 2001; Tan- additionally marked by hyperphagia and full catch up growth.
nenbaum and Bowers, 2001; Tannenbaum et al., 2003), itself an Picha et al. (2009) show that in vitro stimulation of GH by ghre-
inhibitor of GH secretion. Ghrelin is therefore capable of peripher- lin occurs in somatotrophs derived from both continually fed and
ally stimulating GH secretion through vagal afferents originating fasted fish, but not from refed fish, suggesting the hypophyseal
near the stomach, as well as by acting directly on the pituitary or GHSR may be downregulated during CG, which would con-
through modulation of central GH release factors. tribute to the eventual decline in GH seen during refeeding of
Ghrelin is also a potent appetite stimulant, serving as a periph- fasted fish. Taken together, the trends in ghrelin regulation and
eral signal to the brain during periods of negative energy balance function observed in fish suggest that catabolically elevated ghre-
(Banks et al., 2002; Cummings et al., 2004). Orexigenic ghrelin lin simultaneously raises lipolytic plasma GH while priming a
signaling operates via vagal afferents as well as central pathways hyperphagic response during refeeding. The coincidence of these
paralleling those of GH regulation, although appetite and GH effects likely contributes significantly to the CG response, and
stimulatory pathways are independent (Tschop et al., 2000; Wren may in part explain why a catabolic phase is needed to precede
et al., 2000; Nakazato et al., 2001; Date et al., 2002). The orexigenic hyperanabolism.
properties of ghrelin have been reviewed in mammals (Ander-
son et al., 2005; Ueno et al., 2005) and fish (Unniappan and Peter, CENTRAL MODULATORS OF APPETITE
2005; Kaiya et al., 2008). Appetite was stimulated by a single IP/ICV Appetite is increased during fasting through the upregulation of
injection of homologous ghrelin in goldfish (Matsuda et al., 2006; central orexigenic neuropeptides (Kalra et al., 1999), with similar
Miura et al., 2006) and by chronic treatment in tilapia (Riley et al., hormones existing in mammals and fish. In the latter, a num-
2005). The effect of ghrelin on appetite is less clear in salmonids, ber of orexigens are expressed in the pre-optic hypothalamic
which undergo seasonal alterations in feeding behavior (Metcalfe region (Volkoff et al., 2005), which appears to be the teleost ana-
et al., 1986; Metcalfe and Thorpe, 1992). In juvenile rainbow trout, log to the mammalian feeding center. Central injection of NPY
IP injection of rat ghrelin was orexigenic (Shepherd et al., 2007) as (Lopez-Patino et al., 1999; Narnaware et al., 2000; Aldegunde and
in other fish, although both IP and ICV delivery of native ghrelin Mancebo, 2006; Kiris et al., 2007), galanin (de Pedro et al., 1995;
suppressed feeding (Jönsson et al., 2010) in similar-sized trout or Volkoff and Peter, 2001), and orexins (Volkoff et al., 1999) stimu-
had no effect (Jönsson et al., 2007) when injected IP in larger fish. late appetite in teleosts. While NPY is considered the most potent
These variable results suggest that ghrelin may have different func- orexigen in fish and has garnered the most research, these other
tions depending on life stage in salmonids, and that homologous central peptides interact with NPY to augment appetite in response
and heterologous peptides could account for the different effects to negative energy status (Volkoff et al., 2005).
observed in these studies. Future research will need to consider Central NPY (Peng et al., 1994; Silverstein et al., 1998; Leonard
these contingencies. et al., 2001) and AgRP (Cerdá-Reverter and Peter, 2003) mRNA
In accord with its orexigenic function, ghrelin levels tend to is regulated by nutritional state and increases during negative
rise during fasting and decline after feeding in mammals (Ueno energy states to promote energy intake. Ghrelin stimulates cen-
et al., 2005) as well as in fish (Unniappan et al., 2004; Canosa tral gene expression of NPY, which has been shown to mediate
et al., 2005; Matsuda et al., 2006; Terova et al., 2008; Picha et al., the orexigenic effects of ghrelin in goldfish (Miura et al., 2006).
2009). Exceptions were observed in tilapia (Riley et al., 2008) and As in mammals (Stephens et al., 1995; Schwartz et al., 2000), the
rainbow trout (Jönsson et al., 2007), however, and may repre- anorexigen, leptin, suppresses the effects of exogenous NPY on
sent species-specific differences in regulation of the ghrelin system appetite in fish (Lin et al., 2000; Volkoff et al., 2003). In rodents,
among teleosts. Ghrelin nonetheless appears to be an important appetite is stimulated by NPY when ghrelin levels are high and lep-
peripheral signal for regulating both GH secretion and appetite tin low (Bagnasco et al., 2002), or during periods of negative energy
based on nutritional status. Studies further suggest that stim- balance; however, leptin’s regulation by metabolic state in fish is
ulation of ghrelin production during fasting and the lag time equivocal (discussed below). The upregulation and interaction of
between refeeding and the return of ghrelin to basal levels may central orexigenic neuropeptides during fasting likely culminates
depend on the degree to which catabolic processes deplete energy in the hyperphagic response during refeeding, thus providing the
reserves. In the short term, gut and hypothalamic preproghre- substrate and energy necessary for a CG response to occur.
lin mRNA along with circulating ghrelin levels increased on the
order of days in fasted goldfish, then went down within several REFEEDING: HYPERPHAGIA AND HYPERANABOLISM
hours after refeeding (Unniappan et al., 2004). European seabass (COMPENSATORY GROWTH)
(Dicentrarchus labrax) stomach ghrelin mRNA levels increased Hyperanabolism, or the accelerated growth phase that charac-
over 35 days of fasting, then dropped back to basal levels after terizes CG, is the result of hyperphagia and heightened growth
10 days of refeeding (Terova et al., 2008). Striped bass exhib- axis activity during refeeding, particularly in the rapid rise in
ited elevated plasma ghrelin levels after 3 weeks of fasting and IGF-I production that occurs when hepatic sensitivity to GH
a 43-fold increase relative to fed controls after continued fast- returns. As discussed in the first half of this review, CG is pre-
ing and cold-banking for 90 days, followed by a return to baseline ceded by a catabolic phase that primes an organism for hyper-
within 21 days of refeeding and temperature warm up (Picha et al., anabolism. If the endurance of the catabolic state is sufficient,

and food is ample when feeding resumes, then a temporal hyper- capacity. Similarly in carp (Cyprinus carpio; Fine et al., 1993) and
phagic response is elicited and a net positive energy state achieved rainbow trout (Foster et al., 1991), protein assimilation, and feed
through the reintroduction of exogenous energy and metabolic conversion were improved by chronic GH treatment. The carry
substrates. When energy stores are regained, orexigenic signaling over of catabolically elevated GH after refeeding, in addition to
declines and hyperphagia subsides. Under these terms, an organ- driving somatic growth through stimulation of IGFs, may also
ism exhibits lipostatic regulation of energy homeostasis (Jobling improve protein assimilation at a time when substrates are in
and Johansen, 1999), a system in which energy reserves are main- abundance due to elevated feeding (Peter and Marchant, 1995;
tained within a certain range by endocrine signals derived from MacKenzie et al., 1998).
energy-storing tissues that regulate feeding and energy expendi-
ture. CG seems to occur during the lag time between refeeding and HYPERANABOLISM: AUGMENTATION OF THE GH/IGF GROWTH AXIS
the lipostatic abatement of hyperphagia and enhanced growth axis Compensatory growth ultimately refers to the rapid growth, or
activity. hyperanabolic, response that occurs during the feeding of previ-
ously fasted animals, and which allows them to recover lost growth
HYPERPHAGIA AND ASSIMILATION EFFICIENCY opportunity. During positive energy states, circulating GH binds
Hyperphagia is an integral component of CG (Ali et al., 2003) and hepatic GHRs to induce production and secretion of IGF-I, the
is a common response to energy deficit in a variety of fish; Euro- prominent mitogen responsible for somatic growth in vertebrates
pean minnow (Phoxinus phoxinus; Russell and Wootton, 1992), (Froesch et al., 1985; Picha et al., 2008a). Like IGF-I, hepatic IGF-
Atlantic salmon (Salmo salar; Bull and Metcalfe, 1997), centrar- II transcription is also stimulated by GH in a broad range of fish
chid sunfish (genus Lepomis; Hayward et al., 1997), Nile tilapia (Shamblott et al., 1995; Duguay et al., 1996; Carnevali et al., 2005;
(Wang et al., 2000), striped bass (Picha et al., 2008b; Turano et al., Gabillard et al., 2006; Moriyama et al., 2008a,b; Pierce et al., 2011)
2008), and stickleback (Gasterosteus aculeatus; Zhu et al., 2003). and remains responsive to GH into adulthood. Hepatic GHR tran-
The magnitude of the hyperphagic response depends on the dura- scription positively correlates with GH binding in gilthead sea
tion of fasting in salmon, and appears to be largely influenced bream (Pérez-Sánchez et al., 1994) and with circulating IGF-I
by the degree to which lipid reserves are depleted by catabolic levels in channel catfish (Small et al., 2006) during fasting and
processes (Bull et al., 1996). Hyperphagia during CG is attributable refeeding, corroborating that metabolic state mediates GH signal-
to catabolically elevated levels of orexigens that are upregulated ing through changes in GHR expression in the liver where the
during negative energy states. majority of endocrine IGFs are produced (Reinecke and Collet,
Hyperanabolism during refeeding is fueled by an influx of 1998; Vong et al., 2003; Terova et al., 2007). Chronic GH treat-
metabolic substrates that are rapidly allocated to somatic growth ment increases growth rate in a diverse range of fish (Markert
through heightened mitogenic activity of the growth axis; how- et al., 1977; Weatherley and Gill, 1987; Agellon et al., 1988; Cavari
ever, hyperphagia alone may not account for the accelerated et al., 1993), suggesting that the catabolically elevated GH levels
growth rate experienced during CG. Gurney et al. (2003) pro- that temporarily persist during refeeding may contribute to an
pose, through energetics modeling, that high substrate assimila- accelerated growth rate by stimulating the growth axis. The return
tion rates during hyperphagia drive CG by partitioning resources of hepatic sensitivity to GH during refeeding, which reinstates
specifically to skeletal growth rather than to energy reserve depo- IGF synthesis, is therefore critical to CG. The duration of high
sition. Skalski et al. (2005) elaborate on the energetics model of plasma GH levels may depend on catabolic history and the extent
hyperanabolism, suggesting that physiological changes, includ- to which energy reserves are depleted during fasting, but appears
ing increased assimilation efficiency during feeding and reduced to decline back to normal levels within 2 weeks of refeeding in
mass-specific maintenance costs during fasting, work in conjunc- rainbow trout and striped bass (Norbeck et al., 2007; Picha et al.,
tion with hyperphagia to drive CG in striped bass. A subsequent 2009).
study that normalizes SGR to body size supports that the growth Consistent with the mitogenic attributes of IGFs, plasma IGF-
rate is significantly higher in fasted/refed hybrid striped bass I (Uchida et al., 2003; Beckman et al., 2004) and hepatic IGF-I
relative to controls (Picha et al., 2008b), and is not merely an and II mRNA (Picha et al., 2008b) levels positively correlate with
allometric artifact of smaller, stunted fish compared to larger, fed SGR in fasted and refed fish. The relative change in circulat-
cohorts. ing IGF-I over a growth increment is an even better corollary
The mechanism that adjusts energy allocation around assim- to SGR in striped bass than absolute IGF-I levels (Picha et al.,
ilation rate is undefined, although the lipolytic and growth pro- 2006), which may indicate enhancement of IGF receptor sensitiv-
moting functions of GH, along with its regulatory profile under ity during the transition from catabolic back into anabolic states as
variable metabolic conditions, suggests an influential role in opti- plasma IGF-I levels are in the process of rising. The steep rebound
mizing substrate conversion to skeletal growth. Long-term GH of depressed plasma IGF-I levels during the refeeding of fasted
treatment in rainbow trout improved feed conversion by 60% striped bass corresponded directly to the hyperanabolic phase of
(Kling et al., 2012). Exogenous GH treatment enhanced amino acid the growth curve (Picha et al., 2008b). Moreover, transcript levels
uptake (Collie and Stevens, 1985) as well as growth rate, appetite, of hepatic GHRs and IGFs in these fish during refeeding actually
and food conversion in coho salmon (Markert et al., 1977). In fed exceeded those of constantly fed control fish, suggesting that over-
striped bass, weekly bovine GH injection increased the number compensation in expression of key growth-regulatory hormones
of intestinal amino acid transporters and intestinal mass (Sun may be contributing significantly to the accelerated growth that
and Farmanfarmaian, 1992), suggesting improved protein uptake occurs with CG (Picha et al., 2008b). This overcompensation is

further exacerbated in striped bass when the alleviation of a pre- though leptin is consistently anorexigenic in fish as in mammals,
vious period of feed restriction is combined with cold-banking, evolutionarily isolated gene duplication events, physiological dif-
similar to what wild fish experience during spring warm up when ferences in energy storage and diverse life histories may underlie
temperature and prey availability are more optimal for growth divergent functions for leptin in fish that only partially resemble
(Perez-Sanchez and Le Bail, 1999; Mingarro et al., 2002; Picha those of higher vertebrates.
et al., 2009). Similarly, overcompensation in circulating IGF-I Leptin centrally regulates feeding by stimulating appetite-
concomitant with enhanced activation of IGF-I signaling in mus- suppressing neuropeptides and inhibiting appetite-stimulating
cle tissue was observed in fine flounder (Paralichthys adspersus; neuropeptides in mammals (Ahima et al., 1999; Elias et al.,
Fuentes et al., 2011). An elevation in muscle IGF-I mRNA levels 1999; Zhang and Felder, 2004) and fish (Volkoff et al., 2003;
has been observed in a number of other fish (Chauvigne, 2003; Murashita et al., 2008). Leptin injection accordingly reduces feed-
Montserrat et al., 2007a,b; Picha et al., 2008b; Kling et al., 2012), ing in goldfish (de Pedro et al., 2006), rainbow trout (Murashita
suggesting a parallel autocrine or paracrine mechanism within the et al., 2008), and striped bass (Won et al., 2012). While its
skeletal tissue itself. Taken together, the coordinated dynamics of anorexigenic property logically integrates into a system in which
the GH/IGF growth axis appears key in eliciting CG, whereby the leptin serves as a lipostat, such as the mammalian paradigm,
expression levels of and sensitivity to growth-regulatory hormones it fits less aptly into a system where leptin expression may
is increased relative to normal animals on a continuous regi- not correlate with energy reserves, as is the case for some
men, subsequently resulting in a hyperanabolic state characteristic teleosts.
of CG. Studies evaluating leptin responsiveness to metabolic state in
teleosts are equivocal. Circulating leptin (Johnson et al., 2000;
THE LIPOSTATIC RETURN TO ENERGY HOMEOSTASIS Nieminen et al., 2003) or mRNA levels in liver (Gorissen et al.,
The CG response to fasting is finite, attenuating once lost energy 2009; Won et al., 2012) are depressed in some fish during fast-
resources re-accumulate and hyperphagia abates. The lipostatic ing, or otherwise reflect energy deposition (Kling et al., 2012).
model of energy homeostasis proposes that adiposity acts as a Conversely, some species exhibit rising plasma (Kling et al., 2009;
regulatory mechanism on appetite in order to maintain a thresh- Fuentes et al., 2012; Trombley et al., 2012) or gene expression levels
old of energy deposition (Kennedy, 1953). Kennedy observed that in lipid storing tissues (Rønnestad et al., 2010; Frøiland et al., 2012;
depletion of adipose stores in fasted rats stimulated feeding, which Gambardella et al., 2012; Trombley et al., 2012; Zhang et al., 2012)
returned to normal levels when reserves returned to a critical during feed restriction, while others show no long-term regulation
mass. Studies support the presence of a teleost lipostat-like mech- by feeding regimen (Huising et al., 2006). Leptin gene expression
anism, as well, although lipid partitioning can vary considerably profiles in different energy-storing tissues during altered meta-
between adipose tissue, liver, and muscle in different fishes (Dias bolic states vary, even among closely related species, and are not
et al., 1999; Frøiland et al., 2012). The hyperphagic response to necessarily concomitant with plasma levels. These studies call into
long-term fasting in salmonids appears to be driven by a decrease question whether leptin functions as a lipostatic endocrine sig-
in whole body lipid content and terminates, along with the CG nal aimed at mobilizing surplus energy stores or might instead
response, when proximate composition is restored (Jobling and drive other catabolic processes in fish. It is important to consider
Miglavs, 1993; Johansen et al., 2001). Fluctuating gross lipid levels that some fish possess multiple leptin genes (Huising et al., 2006;
during fasting and refeeding similarly suggest lipostatic regulation Kurokawa and Murashita, 2009; Rønnestad et al., 2010; Zhang
of hyperphagia in three-spined stickleback (Zhu et al., 2003) and et al., 2012) arising from different genome duplication events
striped bass (Turano et al., 2007) undergoing CG. The liver is a within lineages, and that these paralogs may have different roles.
significant lipid storing and metabolizing tissue in some fish, and If a lipostatic function for leptin, or one form of leptin, is inherent
may also be involved in sensing and maintaining energy reserve in fish, then the replenishment of energy reserves during refeeding
levels. More so than visceral adipose mass, changes in the HSI may eventually attenuate hyperphagia and mark the end of the CG
during cycles of feed deprivation and refeeding in striped bass, response through leptin signaling. If not, then further studies will
in which liver is a major lipid storage organ, are indicative of be needed to reconcile the paradox of rising plasma leptin levels
metabolic state and the likelihood of achieving an elevated SGR, during fasting in some fish in light of its conserved anorexigenic
and hence CG, during refeeding (Picha et al., 2006; Turano et al., property.
2008).
SUMMARY: SEQUENCE OF EVENTS DURING CATABOLIC AND
IS LEPTIN THE TELEOST LIPOSTATIC HORMONE? ANABOLIC STATES LEADING TO CG
The mechanism that represents overall energetic status, endocrine Compensatory growth is a period of accelerated growth follow-
or otherwise, is not well defined in teleosts, in part because differ- ing the alleviation of growth-stunting conditions, such as fasting,
ent fish partition stored energy in various locations. In mammals, that potentially allows an organism to make up for lost growth
the anorexigenic peptide hormone, leptin, reflects fat deposi- opportunity (Figure 1). The response can be divided into a cata-
tion. Leptin modulates food consumption and energy expenditure bolic phase, when growth is impeded and energy reserves are
according to endogenous energy availability, and is considered the tapped, and a hyperanabolic phase, when growth resumes at an
primary lipostatic hormone (Ahima and Flier, 2000; Arora and elevated rate. This review chronologically describes physiological
Arora, 2008). If leptin functions as a lipostat in teleosts as well, it adjustments and endocrine activity in fish during these meta-
would likewise need to be indicative of energy availability. Even bolic phases, and suggests how they may ultimately make CG

possible through enhanced feeding, substrate assimilation, and a growth axis profile representative of a normal growth trajectory
rapid growth. (Figure 2A).
During the precedent catabolic phase (Figure 2B), orexigens Compensatory growth is therefore regulated by sequential
stimulate appetite as endogenous energy reserves are depleted. endocrine responses during distinct metabolic states (Table 1).
Ghrelin and cortisol stimulate GH production and elevate circu- Teleosts have been the subject of numerous CG studies; how-
lating GH levels in order to free energy-storing lipids. However, ever, our understanding of their endocrine mechanisms during
hepatic GH resistance and the growth-inhibitory effects of corti- this phenomenon is commonly limited to observations in a few
sol and somatostatins suppress IGF production under the pretext model species or extrapolations from studies in higher vertebrates.
that conditions are unfavorable for growth. Reduced negative While by no means inclusive, this theoretical composite of docu-
feedback from IGF-I further permits GH levels to rise. A criti- mented hormonal activity during catabolic and anabolic states is
cal period of catabolism is therefore required to induce hormonal intended to provide a basic framework of the endocrine regula-
changes that prime the fish for hyperphagia and super-potentiate tion of CG in fish, and perhaps higher vertebrates. The relevance
the growth axis. of certain hormones, time frames, and even the potential of the
During refeeding (Figure 2C), CG is fueled by the hyperphagic CG response itself are likely contingent on species, size, and life
influx of exogenous energy and substrates. Food is assimilated with stage. Nonetheless, the variables presented in this review are esti-
heightened efficiency as the result of modifications to metabolic mated to be of fundamental importance to CG in fish, although
substrate absorption, in part attributable to residually elevated GH the degree of their relevance in particular species may vary.
levels. Hepatic GHRs are reinstated and GH sensitivity returns,
followed by a steep rise or even overcompensation in IGF-I pro- ACKNOWLEDGMENTS
duction. Production of IGFs during refeeding is also influenced by This research was supported in part by the United States Depart-
a decline in growth-inhibitors. Substrate and energy availability, ment of Agriculture, North Carolina Sea Grant (R/AF-46; 0-
enhanced assimilation efficiency, and augmentation of the growth SSS-B-1), and the AquaFish Collaborative Research Support Pro-
axis culminate in a hyperanabolic, rapid growth phase until a gram of the United States Agency for International Development
lipostat-like mechanism initiates the return to basal appetite and (EPP-A-00-06-00012-00).
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Compensatory larval responses shift 2554 Melanocortin receptors mediate the Copyright © 2013 Won and Borski. This
trade-offs associated with predator- Wilson, P. N., and Osbourn, D. F. excitatory effects of blood-borne is an open-access article distributed under
induced hatching plasticity. Ecology (1960). Compensatory growth murine leptin on hypothala- the terms of the Creative Commons Attri-
86, 1580–1591. doi:10.1890/04-0535 after undernutrition in mam- mic paraventricular neurons in bution License, which permits use, distri-
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mon carp (Cyprinus carpio) IGF-I 185X.1960.tb01466.x doi:10.1152/ajpregu.00504.2003 are credited and subject to any copy-
and IGF-II mRNA by real-time PCR: Won, E. T., Baltzegar, D. A., Picha, M. E., Zhu, X., Wu, L., Cui, Y., Yang, right notices concerning any third-party
differential regulation of expression and Borski, R. J. (2012). Cloning and Y., and Wootton, R. J. (2003). graphics etc.

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published: 01 July 2013

Endocrine regulation of compensatory growth in fish

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FIGURE 1 | Compensatory growth (CG) paradigm during fasting and

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Catabolism (fasting) Hyperanabolism (refeeding)

Response Effect Reference Response Effect Reference

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