See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/297676689

Marine ornamental species culture: From the past to “Finding Dory”

Article  in  General and Comparative Endocrinology · March 2016

DOI: 10.1016/j.ygcen.2016.03.004

CITATIONS READS

9 676

6 authors, including:

Ike Olivotto Giulia Chemello

Università Politecnica delle Marche Università Politecnica delle Marche
75 PUBLICATIONS   1,723 CITATIONS    9 PUBLICATIONS   27 CITATIONS   

SEE PROFILE SEE PROFILE

Arturo Vargas Basilio Randazzo

Università Politecnica delle Marche Università Politecnica delle Marche
10 PUBLICATIONS   17 CITATIONS    28 PUBLICATIONS   34 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Reproduction View project

2016- Ministero delle Politiche Agricole Alimentari e Forestali (MIPAAF), (note 6775, Art.36 Paragraph 1 Reg (UE9 n 508/2014), 2016. Blue fin Tuna Reproduction View
project

All content following this page was uploaded by Ike Olivotto on 31 March 2016.

The user has requested enhancement of the downloaded file.

 General and Comparative Endocrinology xxx (2016) xxx–xxx

Contents lists available at ScienceDirect

General and Comparative Endocrinology

journal homepage: www.elsevier.com/locate/ygcen

Marine ornamental species culture: From the past to ‘‘Finding Dory”

Ike Olivotto a,⇑, Giulia Chemello a, Arturo Vargas b, Basilio Randazzo a, Chiara Carla Piccinetti a,
Oliana Carnevali a
a
Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche, via Brecce Bianche, 60131 Ancona, Italy
b
Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Circuito Exterior, Ciudad Universitaria, 04510 Mexico city, Mexico

a r t i c l e i n f o a b s t r a c t

Article history: The present article revises the major topics related to fish and coral reproduction. In particular after a
Received 3 February 2016 short review of the ornamental trade and the destructive fishing methods that are still used in some
Accepted 6 March 2016 areas, the present review revises the principal modes of fish and coral reproduction introducing the main
Available online xxxx
critical bottlenecks in their captive propagation. Regarding fish these include sexing the fish, pair form-
ing, the embryo development, the hatching process and of course the transition from an endogenous to
Keywords: an exogenous feeding by the larvae. As concerns corals, great attention is given to the main modes of
Clownfish
reproduction as well as to nutrition and lightening.
Tropical fish
Coral reef
Ó 2016 Elsevier Inc. All rights reserved.
Coral
Fish reproduction
Reproductive strategies
Finding Dory

1. Marine ornamentals trade
Coral reefs cover a very small portion of the marine environ-
ment but they are considered as the most biodiversified ecosys-
tems on Earth (Olivotto et al., 2006a). They support several
species of fish and of reef building corals as well as a great number
of invertebrates. At date, there are several negative pressures on
coral reefs that include the climate change, the increasing trend
of the temperature that might cause coral bleaching, the unsus-
tainable fishing, that caused a serious decline of fish stocks and
the nutrient enrichment of coastal waters, due to human wastes
and agriculture runoff (Olivotto et al., 2011b). Among these the
aquarium trade can also have a negative impact on the coral reef
ecosystem.
If we consider modern reef tanks and we virtually imagine to
dive in these tanks, we can really observe a small portion of coral
reef within the tank walls. Nowadays, tanks host not only fish
but also a great variety of reef building corals and other inverte-
brates. However, the question that still remains is: from where
do these fish and invertebrates come from?
Unlike freshwater aquaria species, where more than 90% of the
species are currently farmed, most of marine aquaria are still
stocked from wild caught species (Green, 2003; Wabnitz et al.,
2003; Olivotto et al., 2011b). The great majority of the animals
⇑ Corresponding author.
E-mail address: i.olivotto@univpm.it (I. Olivotto).
used in the aquarium trade are collected from the wild using envi-
ronmental friendly collecting methods such as nets and traps, but
others are still collected using methods that harm the delicate
marine ecosystems. Among these the use of cyanide and dynamite
are the more destructive ones (Wabnitz et al., 2003).
Cyanide is used as an anesthetic and is spread by divers on coral
reefs. This method is non selective and kills not only the fish but
also invertebrates and many other organisms including larvae, bac-
teria and plankton (Barber and Pratt, 1998). Dynamite, which is a
common practice for food fishing, is based on the use of small arti-
sanal bombs that are built using empty glass bottles filled with fer-
tilizers and sand. By the blast, this extremely non selective fishing
method, kills fishes and invertebrates and destroys the physical
structure of the reef making it more difficult for new planulae to
settle. As a consequence the reef recovery is delayed in a severe
way.
Also coral collection can harm the reef ecosystem (Ellis, 1999;
Calfo, 2007). Coral collection for the aquarium trade is mainly
based on the collection of coral fragments: divers often use ham-
mers and other equipment to extract coral fragments; however
they do not really take care of saving the reef. As a consequence,
the use of these destructive fishing methods causes the destruction
of most corals and coral reef physical structure with a consequent
decline in fish populations and loss of biodiversity.
After collection the animals are usually transferred to an expor-
ter facility where they should undergo quarantine and acclimation
to captive conditions. Nowadays, the use of jet airplanes allows to

http://dx.doi.org/10.1016/j.ygcen.2016.03.004
0016-6480/Ó 2016 Elsevier Inc. All rights reserved.

Please cite this article in press as: Olivotto, I., et al. Marine ornamental species culture: From the past to ‘‘Finding Dory”. Gen. Comp. Endocrinol. (2016),
http://dx.doi.org/10.1016/j.ygcen.2016.03.004
2 I. Olivotto et al. / General and Comparative Endocrinology xxx (2016) xxx–xxx
ship live animals from coral reefs to almost anywhere in the world.
Typically, they are packed for shipping so that they can withstand
several hours of transit time. Corals and fish are first shipped to a
wholesale facility, where they are either directly sold, distributed
in the proximity of the wholesale facility, or transhipped to their
next destination. During transport, the animals can be subject to
large temperature oscillation and prolonged confinement in the
dark. In addition, during the shipment, unnatural or inadequate
conditions, with respect to water flow, pH, nutrition, and light,
often occur causing severe stress response in the organisms. It is
thus estimated that from oceans to aquaria about 60–70% on the
traded animals die during capture, shipment and handling because
of the use of chemicals during collection, poor handling practice
and disease (Wabnitz et al., 2003).
The aquarium trade is also very often a ‘‘victim of fashion”. In
2003, Disney and Pixar released their hit movie, ‘‘Finding Nemo”.
The primary goal of the movie was to portray the message that fish
are better off left in the wild, however, the final result was that
most of the people did not realize, the responsibility, the cost
and maintenance, and the ethical responsibility to care for a living
creature such as Amphiprion ocellaris.
From here the importance of studying the reproduction of some
of the species most commonly used in the aquarium trade in order
to produce an alternate supply of fish and to have a better knowl-
edge about their biology (Olivotto et al., 2003, 2004, 2006a,b).
These information together are essential for a better management
of natural stocks and for understanding responses of human
impacts (Tlusty, 2002).
2. Fish
At date there are still numerous critical factors in the early life
history of fish where deficiencies may represent a limiting factor in
captive propagation (Holt, 2000, 2003; Wittenrich, 2007;
Moorhead and Zeng, 2010; Olivotto et al., 2011b). For example to
breed and culture a certain fish species we need to be able to sex
the fish, to induce spawning, to have a proper embryo develop-
ment, to hatch the embryos and of course to promote the transition
from an endogenous to an exogenous feeding by the larvae
(Thresher, 1984; Holt and Riley, 2001; Holt, 2011). The life history
of most marine ornamental fish is made of different biological/eco-
logical phases: (a) the adults that are sexually mature and produce
eggs and sperm; (b) the embryos that develop for a species specific
time protected by the chorion membrane and rely on yolk
reserves; (c) the hatching that consists in breaking the chorion
membrane and reaching an independent life by the larvae
(Olivotto and Carnevali, 2004); (d) the larvae that usually spend
a period in the plankton feeding on a great variety of microorgan-
ism; (e) and the juveniles that after metamorphosis settle down on
the reef and will secondly reach sexual maturity closing the cycle.
In order to cultivate marine ornamentals we need to understand
and study on all these stages (Olivotto et al., 2009).
The reproductive strategies developed by fish are extremely
diverse and a deeper knowledge about this topic is a crucial factor
in determining the success of captive propagation.The two domi-
nant modes of egg dispersal among marine fish are the demersal
and pelagic spawners (Setu and Kumar, 2010; Olivotto et al.,
2011a,b).
Demersal spawners produce eggs that are attached to a solid
surface or laid as egg balls. Spawning occurs in the morning/after-
noon and the average number of eggs/clutch is 100–1000. All the
demersal species display parental care until the embryos hatch.
Typical examples are damselfish, clownfishes, dottybacks, gobies
and blennies (Brons, 1996; Moe, 1997; Asoh and Yoshikawa,
2002; Olivotto et al., 2005; Avella et al., 2007; Meirelles et al.,
Please cite this article in press as: Olivotto, I., et al. Marine ornamental species culture: From the past to ‘‘Finding Dory”. Gen. Comp. Endocrinol. (2016),
http://dx.doi.org/10.1016/j.ygcen.2016.03.004
2009; Olivotto et al., 2011a,b; Setu et al., 2010; Madhu and
Madhu, 2014;.
Pelagic spawners usually display complex courtship, eggs and
sperm are released in the water column, eggs are smaller and pro-
duced in greater number (300–1,000,000) if compared to demersal
spawners, and they usually spawn at dusk. This is actually a tran-
sitional period on the reef: diurnal predators are seeking refuge on
the reef, nocturnal ones are not fully active and predatory pres-
sures are thus lower at this time.Spawning starts near the bottom
and ends with an ascent movement close to the water surface
where the gametes are released above the reef structure to reduce
predatory activity of planktivore species and to assist the eggs in
their up-ward migration. Typical examples of pelagic spawners
are angelfishes, wrasses, surgeonfish and snappers (Holt and
Riley, 2001; Olivotto et al., 2006a; Leu et al., 2007; Baensch and
Tamaru, 2009; Leu et al., 2009; Bushnell et al., 2010; Leu et al.,
2010; Laidley et al., 2011; Leu et al., 2012; Callan et al., 2013;
Chen et al., 2013).
Both for demersal or pelagic spawners the fish have to develop
the reproductive competences that include the integration of inter-
nal and external cues (Thresher, 1984; Olivotto et al., 2011b). Of
great interest are the metabolic cues (size and energetic status of
the fish), the environmental cues (proper environmental condi-
tions for offspring survival) and the social cues (presence of both
female and male fish).
Regarding sexuality, fish show a great plasticity (Thresher,
1984; Wittenrich, 2007). There are in fact gonochoristic species
that are born as males or as females and are not able to change
their sex during the life, and the hermaphroditic ones. Some are
simultaneous and have both female and male gonads (i.e. Ser-
ranidae) but usually avoid self-fertilization, while others are
sequential.
Most of the fish species are sequential hermaphrodites (Moe,
1997; Messmer at al., 2005; Munday et al., 2010) and this means
that a same individual can change sex during the life time. Some
species are protandrous changing sex from male to female
(Olivotto et al., 2008a,b). A typical example is the clownfish soci-
ety: the biggest fish is the dominant female, which was originally
a male, while the second biggest is the sexual active male. All the
other fishes that are part of the social structure are immature
males. Some other species are protogynous and this means that
the sex can change from female to male. Typical examples are dot-
tybacks and angelfishes (Brons, 1996; Moe, 1997; Holt and Riley,
2001; Laidley et al., 2004).
Environmental cues also play a key role in the development of
the reproductive competences in fish (Holt and Riley, 2001). In fact,
environmental conditions should be optimal to guarantee repro-
ductive success and offspring survival. At this regard the hypothala
mus–pituitary–gonadal axis plays a key role in translating external
cues such as photoperiod, food availability and temperature in hor-
monal signals that are able to promote ovulation and spermiation
in fish. Several studies have shown the importance of temperature
and light/dark regimes and fish reproduction, and in general for
ornamentals, there is a strong positive correlation between high
temperatures and long days and number of eggs produced
(Olivotto et al., 2011a). As a consequence spawning events are
reduced in November–anuary in the Northern hemisphere and in
June–August in the Southern one.
Technology is thus essential in manipulating these parameters
in captivity, and in the reproduction of marine ornamentals a key
role is played by heaters, chillers, lights and light timers. By con-
trolling these parameters we can naturally induce spawning in
many fish species by mimicking natural environmental conditions
(Holt and Riley, 2001; Olivotto et al., 2003, 2006a, 2008c). For dem-
ersal spawners it is sufficient to provide the fish with high (>27 °C)
temperatures and long days (14 h light) (Olivotto et al., 2009),
 I. Olivotto et al. / General and Comparative Endocrinology xxx (2016) xxx–xxx
while pelagic spawners need a seasonality by varying water tem-
perature and daylength by 8 °C and 3 h respectively, during the
reproductive cycle (Holt and Riley, 2001; Olivotto et al., 2006a).
After spawning the embryo development takes place. The
embryo development in demersal and pelagic spawners is extre-
mely different. Demersal spawners have larger eggs (2–3 mm)
and the embryo development can last 3–10 days depending on
the species and water temperature. Demersal spawners always
show parental care and protect the embryos during the whole
development until hatching (Olivotto et al., 2011a). On the con-
trary pelagic spawned eggs are usually smaller (about 1 mm) and
hatch in a few hours from fertilization (14–24 h). Demersal
spawned larvae are very competitive and present functional jaws
and eyes, the yolk sac is almost exhausted and mouth and digestive
tract are open and functional. Larvae usually start feeding on the
same day they hatch. On the contrary pelagic spawned embryos
hatch as pro-larvae which are very tiny (2 mm), without pig-
mented eyes, the mouth and digestive tract are not functional
and they still have a large yolk sac (Holt, 2003; Wittenrich 2007).
These yolk reserves will sustain the pro-larvae for about 48 h dur-
ing which they undergo a second developmental phase in the
water column reaching the larval stage. Pro-larvae are extremely
sensitive to predation and physical damage during this early period
in life history. As a result, the total number of larvae/juveniles/
adults resulting from a demersal or pelagic spawn is almost the
same (Thresher, 1984).
2.1. Larviculture
The main critical bottleneck in marine ornamental production is
the larval rearing with the major obstacle represented by the
change from an endogenous to an exogenous feeding by the larvae
(Olivotto et al., 2011a).
Many live preys have been used as larval food. These include
several microalgae such as Isochrysis galbana, Nannochloropsis ocu-
lata, Rhodomonas baltica, and the heterotrophic dinoflagellate Oxy-
rrhis marina and marine copepods such as Acartia tonsa,
Parvocalanus crassirostris, Centropages typicus and C. hamatus
(Delbare et al., 1996; Stottrup and Norsker, 1997; Marcus and
Murray, 2001; Olivotto et al., 2003, 2006a; Olivotto et al., 2008a,
b,c; Gopakumar and Santhosi, 2009; Laidley et al., 2009).
However, most marine ornamentals are presently cultured
using rotifers (Brachionus plicatilis and B. rotundiformis) and Arte-
mia salina nauplii as preys (Olivotto and Carnevali, 2004). To
bypass size problems during the use of rotifers and Artemia nauplii
the naked ciliate Euplotes sp has also been tested as food for larvae
because of its small size (Olivotto et al., 2005).
Rotifers and Artemia are widely used especially because of their
planktonic nature, because they are easily cultured at high densi-
ties and because their nutritional profile can be modified by an
enrichment procedures (Sargent et al., 1997; 1999; Olivotto
et al., 2011b). Enrichment with fatty acids is able to significantly
increase survival and growth rate, and reduce time to metamor-
phosis and malpigmentation in several species including clowns
and dottybacks (Olivotto et al., 2003, 2006b, 2010; Avella et al.,
2007). At date several species such as seahorses, damselfish, blen-
nies, gobies, clowns and dottybacks can be cultured in commercial
numbers using these live preys. However, despite these apparent
advantages rotifers and Artemia are not always the best live preys
for marine fish larvae. In fact, for some small larvae (like the pela-
gic ones) that can be too large; their locomotory patterns do not
always promote predatory activity in fish larvae, and they are
not their natural food items since they are not abundant in the
oceans (Delbare et al., 1996; Olivotto et al., 2011a). In fact in the
planktonic waters, where the larval cycle is usually spent, marine
fish larvae usually feed on copepods. Copepods not only have a
Please cite this article in press as: Olivotto, I., et al. Marine ornamental species culture: From the past to ‘‘Finding Dory”. Gen. Comp. Endocrinol. (2016),
http://dx.doi.org/10.1016/j.ygcen.2016.03.004
3
wide range of body size making them ideal to cover the whole lar-
val cycle, but they are also rich in essential fatty acids and have a
typical movement that might stimulate the predatory skills of
the larvae (Delbare et al.1996; Laidley et al., 2009). At date there
are still several difficulties in rearing copepods on a continuous
basis because they are usually cultured at low densities, they suffer
of cannibalism, they need large tanks and need to be fed on differ-
ent algal combinations (Stottrup and Norsker., 1997; Drillet et al.,
2006). In addition, copepods are cultured with greater and more
expensive labor-requirement to that for rotifers and thus the tech-
nology for mass scale production of copepods is still in the research
stage.
Copepods usually produce or subitaneous or resting eggs. Both
subitaneous and diapauses eggs have been investigated for possi-
ble applications in aquaculture (Marcus and Murray, 2001;
Drillet et al., 2006; Olivotto et al., 2012). While diapauses eggs
can be stored for quite long periods of time (up to 17 months,
Marcus and Murray, 2001), there are still a lot of difficulties in
the forced induction of their production.
Considering subitaneous eggs they are usually produced by a
wider number of copepod species and are thus more available for
scientific studies. A cold storage at low temperatures may be an
appropriate storage technique since the eggs switch to a quiescent
state due to the suboptimal environmental conditions (Drillet
et al., 2006; Olivotto et al., 2012). Acartia tonsa is for sure the most
studied species to produce cold stored eggs. A. tonsa eggs are usu-
ally collected from a continuous culture letting them settle and
siphoning the tank bottom. The eggs are then harvested, cleaned
and stored in pasteurized filtered seawater (18 ppm) in closed
test-tubes at 4 °C turning anoxic in 3–4 weeks. After a certain per-
iod of time, the egg batches of stored eggs can be opened, rinsed
with 30 ppm salinity filtered seawater on a 30 lm mesh, checked
under the microscope and then transferred to 1 L beakers and stir-
red. After that, the eggs can be hatched in 50L tanks with moderate
aeration at room temperature in 24 h (Drillet et al., 2006; Olivotto
et al., 2012).
Most of the copepods species have been successfully used for
the first feeding of pelagic spawned larvae. Recent success in first
feeding have been reported for Centropyge flavissimus larvae using
wild plankton and Parvocalanus sp. copepods (Olivotto et al.,
2006a); for Pomacanthus semicirculatus using ciliates (Euplotes
sp.) and copepods (Euterpina acutifrons and Eucalanus sp.) nauplii
(Leu et al., 2009); for Zebrasoma flavescens using copepods and wild
plankton (Laidley et al., 2004; Callan, 2013); for Paracanthurus hep-
atus using copepods (Euterpina acutifrons and Eucalanus sp.) nauplii
(Chen et al., 2013). Recently the great news of the successful rear-
ing of some Zebrasoma flavescens fish was delivered on the web by
the Oceanic Institute in Hawaii. This is one more success to the cul-
tivation of marine ornamentals. The hope is that this technology
will soon be available and possibly transferred to commercial
hatcheries in order to provide the industry with captive reared
yellowtangs.
In 2017 a second major event will happen. The release of the
new Disney-Pixar movie ‘‘Finding Dori”. Be sure to remember that
nowadays Paracanthurus hepatus is 100% wild collected and thus
each Dory fish is unique, delicate and wild caught! Remember this
when you watch the movie and especially in the case you decide to
buy this species. Provide your animal with plenty of space to swim,
good culturing conditions, and plenty of healthy food.
3. Coral culturing
The major part of the global trade of marine ornamental species
is sustained by corals that represent a multi-million dollar industry
mainly based on the collection of wild organisms (Thornhill, 2012;
4 I. Olivotto et al. / General and Comparative Endocrinology xxx (2016) xxx–xxx
Tissot et al., 2010; Tlusty, 2002). The inclusion of corals in the reef
tanks provides a more natural aspect as well as a better environ-
ment for the fish. Since the late 1980 s, the popularity of home
aquariums that host living corals has increased dramatically
(Delbeek, 2001) causing concerns about the sustainability and
environmental impacts of the industry (Wabnitz et al., 2003;
Shuman et al., 2004). Collection often occurs on coral reefs in
developing countries, where it is difficult to implement effective
management and harvesting (Wood, 2001a, 2001b). As a conse-
quence many Indo-Pacific nations have now banned or restricted
the collection of aquarium specimens from their waters (Shuman
et al., 2005; Gasparini et al., 2005); indeed, it is estimated that over
500,000 coral colonies were imported in 2010 by the U.S. only
(Rhyne et al., 2012).
Nowadays, in order to reduce the gap between aquarists’ pas-
sion and biodiversity conservation, several government and non-
government organization funded programs (NGOs) have been
developed to supply the trade with artificially propagated corals
(Pomeroy et al., 2006). The two main modes of coral reproduction
include fragmentation and sexual reproduction. Propagation by
fragmentation is a common asexual reproductive mode of many
reef-building corals (Highsmith, 1982) during which the body of
the parents brakes or is broken into distinct pieces, each of which
can produce a new offspring. This way of reproduction has been
manipulated to artificially produce large quantities of fragments,
or ‘nubbins’, as small as a few polyps, with high survival rates
(Rinkevich, 1995, 2000; Shafir et al., 2001). In captivity, fragments
are usually put on stubs using a special glue. After a short period of
recovery, the fragment will start growing and producing a new col-
ony. Fragmentation can also produce large samples with minimal
genetic variation, which is ideal for scientific experimentation
(Bongiorni et al., 2003).
On the other hand, sexual reproduction has both advantages
and disadvantages when compared to asexual propagation meth-
ods, but for sure is much more interesting from a biologically point
of view. First of all, it involves much greater genotypic diversity
and, in case of collection from the wild, collateral damage to donor
reefs is reduced because there is no need to fragment corals, and
sexual methods potentially provide access to millions of propag-
ules (Baird et al., 2009). On the other hand, sexual methods require
a greater effort in terms of costs respect to asexual techniques
since this technique is more labor intensive, may necessitate land
based hatcheries and specific personnel for larval rearing
(Epstein et al., 2001).
In addition, it has to be taken into account that some corals are
gonochoristic while others are hermaphrodites and can show
internal (brooders) or external (broadcasters) fertilization
(Brazeau and Lasker, 1990).
Brooding species are most often ahermatypic (not reef-
building) and distributed in areas of high current or wave action,
showing the planulae development within the polyps (Veron,
2000). On the contrary, broadcasters release sperm and eggs into
the water column simultaneously and the planulae development
occurs in the water column.
Eighty-five% of the corals are broadcast spawners and are char-
acterized by a mass spawning event which is essential to allow
male and female gametes meeting and maximize the number of
successful fertilizations by reducing the number of eggs that
predators can consume. Synchronous spawning is extremely
dependent on .environmental cues, such as temperature changes,
lunar cycle, day length, and chemical signaling (Hatta et al.,
1999; Veron, 2000). The spawning event can be visually dramatic,
and is very suggestive on the Great Barrier Reef in Australia.
While sexual reproduction is extremely fascinating, there are
still some major obstacles in its development in captivity. As a con-
sequence, at date, the most widespread technique in coral farming
Please cite this article in press as: Olivotto, I., et al. Marine ornamental species culture: From the past to ‘‘Finding Dory”. Gen. Comp. Endocrinol. (2016),
http://dx.doi.org/10.1016/j.ygcen.2016.03.004
is fragmentation which can be conducted in outdoor or indoor
facilities (Pomeroy et al., 2006).
The former kind of facilities are based directly into the sea sig-
nificantly reducing productive costs; corals are put over nets and
supports from which they can take advantage of the natural sun-
light and the ocean itself. Nevertheless, as described by Ellis and
Sharron (1999), there are several aspects to take into account when
starting an outdoor coral farm. A suitable ocean site should be
characterized by clear water, absence of pollution and freshwater
sources, protection from wave action, good lighting and water
exchange. Moreover, depending on the remoteness of the farm site
from land the use of a land-based holding facility or the need of
water transport, such as small /large boats, have to be considered.
On the other hand indoor facilities are essential in areas that are
far away from the ocean or in cold/temperate latitudes. These facil-
ities have a higher maintenance cost, because of the use of specific
equipment for water filtration and heating/chilling, the use of
specific lamps as well as for the use of chemicals for sea water
production.
Light is extremely important for corals which contain symbiotic
algae. In fact, life and reef building capacity of corals is strongly
dependent on the symbiotic relationship between the coral and
the microalgae of the genus Symbiodinium (commonly named
‘‘zooxanthellae”) (Osinga et al., 2011; Schutter et al., 2012;
Wijgerde et al., 2012). Light is in fact necessary to fuel algal photo-
synthesis, which in turn contributes to coral nutrition and growth,
up to 95% of the products of algal photosynthesis are transferred to
the animal; (Muscatine, 1990; Houlbrèque and Ferrier-Pagès 2009;
Rocha et al., 2013). Inadequate light (eg. intensity, spectral compo-
sition) is one of the major causes of death for corals in aquaria
(Schlacher et al., 2007). New technologies are now focusing on
specific illumination with the intent to increase light quality, lamp
efficiency and in the meanwhile, to reduce the associated costs.
Different light sources may thus influence algal productivity and
the quantity and quality of products transferred to the animal.
The use of the right light source could facilitate and speed up coral
recovery, growth and survival; on the contrary, the use of the
wrong light source may increase losses among corals. HQI (Metal
Halide Bulbs) lamps have been successfully used for years in coral
culture. However, new light sources such as LEP (light emitting
plasma) or LED (light emitting diode) are replacing the HQI light-
ening systems because of their energetic efficiency and broad light
spectrum (Pimputkar et al., 2009).
Nowadays, aside the importance of autotrophy for corals, both
scientists and hobbyist agreed on the main role played by
heterotrophy (Anthony and Fabricius 2000; Iluz and Dubinsky
2005). Even though autotrophy should be enough to coral survival
it is also true that photosynthates are often lacking of organic and
inorganic compounds such as nitrogen and phosphorous which are
essential for coral growth (Houlbreque and Ferrier-Pagès, 2009).
Heterotrophy is probably necessary to maintain an appropriate
elemental stoichiometry of the animal, provided that the algae typ-
ically export to the animal mostly organic C skeletons poor in other
nutrients (Bachar et al. 2007; Seemann, 2013). Thus, the contribu-
tion of heterotrophy to coral nutrition, growth and welfare can be
substantial in several species (Anthony and Connolly, 2004). Coral
heterotrophy can be supported by various substrates, including
particulate organic matter (Rosenfeld et al., 1999; Anthony and
Fabricius 2000), bacteria (Sorokin, 1973; Fitt and Cook 2001), zoo-
plankton and phytoplankton (Coles, 1969; Widdig and Schlichter,
2001). Several studies evidenced that corals fed on phyto and zoo-
plankton improved their growth, in terms of calcification and
organic matrix synthesis (Ferrier-Pages et al., 2003; Treignier
et al., 2009) and maximized resilience to stress and recovery
(Grottoli et al., 2006) increasing their tolerance to stressful condi-
tion such as light variations and chemical fluctuations.
 I. Olivotto et al. / General and Comparative Endocrinology xxx (2016) xxx–xxx
While in outdoor facilities corals can feed on wild plankton,
indoor facilities are dependent on the culture of phyto and zoo-
plankton including different microalgae species, rotifers, Artemia
salina nauplii and possibly copepods. However, the production of
live preys is extremely expensive and time consuming.
In each case the sustainability of a ‘‘coral culture project” is not
only dependent on the biology of the selected species but also on
its economic feasibility. As a consequence better knowledge of
coral physiology and biology is necessary to improve coral culture
with the main scope of reducing labor and economic costs, improv-
ing product quality and protecting the marine ecosystems.
4. Conclusions
The next time you will look at a reef tank, think about the origin
of the hosted organisms and the fact that most of them are wild
caught, usually undergo a very stressful and long shipment and
that they come from a fantastic coral reef.
But also keep in mind the efforts that scientists and hobbyist are
putting everyday into this topic and the successes obtained in the
last decades. It is really hoped that one day all the organisms
hosted in reef tanks will be captive bred.
Acknowledgments
The authors acknowledge the support of Giorgia Gioacchini and
Francesca Maradonna researchers for their help with the analyses.
References
Anthony, K.R.N., Connolly, S.R., 2004. Environmental limits to growth: physiological
niche boundaries of corals along turbidity–light gradients. Oecologia 141 (3),
373–384.
Anthony, K.R.N., Fabricius, K.E., 2000. Shifting roles of heterotrophy and autotrophy
in coral energetic under varying turbidity. J. Exp. Biol. Ecol. 252, 221–253.
Asoh, K., Yoshikawa, T., 2002. The role of temperature and embryo development
time in the diel timing of spawning in a coral-reef damselfish with high-
frequency spawning synchrony. Environ. Biol. Fishes 64, 379–392.
Avella, A.M., Olivotto, I., Gioacchini, G., Maradonna, F., Carnevali, O., 2007. The role
of fatty acids enrichments in the larviculture of false percula clownfish
Amphiprion ocellaris. Aquaculture 273, 87–95.
Bachar, A., Achituv, Y., Pasternak, Z., Dubinsky, Z., 2007. Autotrophy versus
heterotrophy: the origin of carbon determines its fate in a symbiotic sea
anemone. J. Exp. Mar. Biol. Ecol. 349, 295–298.
Baensch, F., Tamaru, C.S., 2009. Spawning and development of larvae and juveniles
of the rare blue Mauritius angelfish, Centropyge debelius (1988), in the hatchery.
J. World Aquacult. Soc. 40, 425–439.
Baird, A.H., Bhagooli, R., Ralph, P.J., Takahashi, S., 2009. Coral bleaching: the role of
the host. Trends Ecol. Evol. 24 (1), 16–20.
Barber, C.V., Pratt, V.R., 1998. Poison and profits: cyanide fishing in the Indo-Pacific.
Environment 40, 28–34.
Bongiorni, L., Shafir, S., Angel, D., Rinkevich, B., 2003. Survival, growth and gonad
development of two hermatypic corals subjected to in situ fish-farm nutrient
enrichment. Mar. Ecol.-Prog. Ser. 253, 137–144.
Brazeau, D.A., Lasker, H.R., 1990. Sexual reproduction and external brooding by the
Caribbean gorgonian Briareum asbestinum. Mar. Biol. 104, 465–474.
Brons, R., 1996. Reproduction and captive breeding of two red sea dottybacks:
Pseudochromis fridmani and P. flavivertex. Freshwater Mar. Aquarium 19, 48–62.
Bushnell, M., Claisse, J.T., Laidley, C.W., 2010. Lunar and seasonal patterns in
fecundity of an indeterminate, multiple-spawning surgeonfish the yellow tang
(Zebrasoma flavescens). J. Fish Biol. 76, 1343–1361.
Calfo, A.R., 2007. Book of Coral Propagation,, .. Reef Gardening for Aquarists, second
ed., vol. 1. Reading Trees, USA, pp. 1–27.
Callan, C.K., Laidley, C.W., Rietfors, M.D.C., Kline, M.D., Martinson, E.W., 2013.
Oceanic Institute achieves breakthroughs in culture technology for yellow tang
(Zebrasoma flavescens). Global Aquacult. Adv. 16 (1), 79–81.
Chen, C.-H., P.-J., Meng, K.S,. Tew, M., Leu, Y., 2013. Natural spawning and early life
history of the palette surgeonfish, Paracanthurus hepatus (Linnaeus, 1766) in
captivity. In: The 9th Indo-Pacific Fish Conference, Okinawa, Japan.
Coles, S.L., 1969. Quantitative estimates of feeding and respiration for three
scleractinian corals. Limnol. Oceanogr. 14, 949–953.
Delbare, D, Dhert, P., Lavens, P., 1996. Zooplankton. In: Lavens, P., Sorgeloos, P.
(Eds.), Manual on the Production and Use of Live Food for Aquaculture. FAO, pp.
252–282.
Delbeek, J.C., 2001. Coral farming: past, present and future trends. Aquarium Sci.
Conserv. 3 (1–3), 171–181.
Please cite this article in press as: Olivotto, I., et al. Marine ornamental species culture: From the past to ‘‘Finding Dory”. Gen. Comp. Endocrinol. (2016),
http://dx.doi.org/10.1016/j.ygcen.2016.03.004
5
Drillet, G., Iversen, M.H., Sørensen, T.F., Ramløv, H., Lund, T., Hansen, B.W., 2006.
Effect of cold storage upon eggs of a calanoid copepod, Acartia tonsa (Dana) and
their offspring. Aquaculture 254, 714–729.
Ellis, S., 1999. Farming Soft Corals for the Marine Aquarium Trade, vol. 140. Center
for Tropical and Subtropical Aquaculture Publication, pp. 1–6.
Ellis, S.C., Sharron, L., 1999. The Culture of Soft Corals (Order: Alcyonacea) for the
Marine Aquarium Trade, vol. 137. Center for Tropical and Subtropical
Aquaculture Publication, pp. 1–77.
Epstein, N., Bak, R.P.M., Rinkevich, B., 2001. Strategies for gardening denuded coral
reef areas: the applicability of using different types of coral material for reef
restoration. Restor. Ecol. 9 (4), 432–442.
Ferrier-Pages, C., Witting, J., Tambutté, E., Sebens, K.P., 2003. Effect of natural
zooplankton feeding on the tissue and skeletal growth of the scleractinian coral
Stylophora pistillata. Coral Reefs 22 (3), 229–240.
Fitt, W., Cook, C., 2001. The effects of feeding or addition of dissolved inorganic
nutrients in maintaining the symbiosis between dinoflagellates and a tropical
marine cnidarians. Mar. Biol. 139, 507–517.
Gasparini, J.L., Floeter, S.R., Ferreira, C.E.L., Sazima, I., 2005. Marine ornamental trade
in Brazil. Biodivers. Conserv. 14 (12), 2883–2899.
Gopakumar, G., Santhosi, I., 2009. Use of copepods as live feed for larviculture of
damselfishes. Asian Fish. Sci. 22, 1–6.
Green, E., 2003. International trade in marine aquarium species: using the global
marine aquarium database. In: Cato, J.C., Brown, C.L. (Eds.), Marine Ornamental
Species: Collection, Culture and Conservation. Iowa State Press, pp. 31–47.
Grottoli, A.G., Rodrigues, L.J., Palardy, J.E., 2006. Heterotrophic plasticity and
resilience in bleached corals. Nature 440, 1186–1189.
Hatta, M., Fukami, H., Wang, W., Omori, M., Shimoike, K., Hayashibara, T., Ina, Y.,
Sugiyama, T., 1999. Reproductive and genetic evidence for a reticulate
evolutionary theory of mass spawning corals. Mol. Biol. Evol. 16 (11), 1607–
1613.
Highsmith, R.C., 1982. Reproduction by fragmentation in corals. Mar. Ecol. Prog. Ser.
Oldendorf 7 (2), 207–226.
Holt, G.J., 2000. Ornamental fish culture. In: Stickney, R.R (Ed.), Marine Encyclopedia
of Aquaculture. John Wiley & Sons, Inc, pp. 610–614.
Holt, G.J., 2003. Research on culturing the early life history stages of marine
ornamental species. In: Cato, J.C., Brown, C.L. (Eds.), Marine Ornamental
Species: Collection, Culture and Conservation. Iowa State Press, pp. 251–254.
Holt, G.J., 2011. Larval Fish Nutrition. Wiley-Blackwell Publishing, Oxford,UK, pp 1-
120.
Holt, G.J., Riley, C.M., 2001. Laboratory spawning of coral reef fishes: effects of
temperature and photoperiod. In: 28th U.S.-Japan Natural Resources
Aquaculture Panel: Spawning and Maturation of Aquaculture Species. U.S.–
Japan Cooperative Program in Natural Resources (UJNR), Technical Report No.
28, pp. 33–38.
Houlbreque, F., Ferrier-Pagès, C., 2009. Heterotrophy in tropical scleractinian corals.
Biol. Rev. 84 (1), 1–17.
Iluz, D., Dubinsky, Z., 2005. Coral photobiology: new light on old views. Zoology
118, 71–78.
Laidley, C.W., Burnell, A.F., Shields, R.J., Molnar, A., Kotani, T., 2004. Marine
ornamentals: captive culture progress at the oceanic institute. Global Aquacult.
Adv. 7 (2), 53–54.
Laidley, C.W., Bradley, C., Callan, C.K., Martinson, E., Klin, M., 2009. Development of
‘‘copepod-based hatc hery technology” for marine fishes with extremely small
larvae. In: Book of Abstracts, World Aquaculture 2009. World Aquaculture
Society, Veracruz, México, p. 472.
Laidley, C.W., Callan, C.K., Rietfors, M.D.C., Kline, M.D., Martinson, E.W., 2011.
Development of captive culture technology for the yellow tang (Zebrasoma
flavescens). Center for Tropical and Subtropical Aquaculture Regional Notes 3
(3), 1–3.
Leu, M.Y., Meng, P.J., Huang, C.S., Liou, C.H., Wang, W.H., 2007. Embryonic and larval
development of five-lined snapper, Lutjanus quinquelineatus (Pisces:
Lutjanidae). In: 2007 Symposium of the Fisheries Society of Taiwan,
Kaohsiung, Taiwan.
Leu, M.Y., Liou, C.H., Wang S, W.H., Yang, D., Meng, P.J., 2009. Natural spawning,
early development, and first feeding of the semicircle angelfish Pomacanthus
semicirculatus (Cuvier, 1831) in captivity. Aquacult. Res. 40, 1019–1030.
Leu, M.Y., Meng, P.J., Huang, C.S., Tew, K.S., Kuo, J., Liou, C.H., 2010. Spawning
behaviour, early development, and first feeding of the bluestriped angelfish
Chaetodontoplus septentrionalis (Temminck & Schlegel, 1844) in captivity.
Aquacult. Res. 41, e39–e52.
Leu, M.Y., Meng, P.J., Tew, K.S., Kuo, J., Hung, C.C., 2012. Spawning and development
of larvae and juveniles of the Indian Ocean oriental sweetlips, Plectorhinchus
vittatus (Linnaeus, 1758), in the aquarium. J. World Aquacult. Soc. 43, 595–606.
Madhu, K., Madhu, R., 2014. Captive spawning and embryonic development of
marine ornamental purple firefish Nemateleotris decora (Randall & Allen, 1973).
Aquaculture 1–9, 424–425.
Marcus, N.H., Murray, M., 2001. Copepod diapause eggs: a potential source of
nauplii for aquaculture. Aquaculture 201, 107–115.
Meirelles, M.E., Tsuzuki, M.Y., Ribeiro, F.F., Medeiros, C.R., Silva, I.D., 2009.
Reproduction, early development and larviculture of the barber goby,
Elacatinus figaro (Sazima, Moura & Rosa 1997). Aquacult. Res. 41, 11–18.
Messmer, V., van Herwerden, L., Munday, P.L., Jones, G.P., 2005. Phylogeography of
colour polymorphism in the coral reef fish Pseudochromis fuscus, from Papua
New Guinea and the Great Barrier Reef. Coral Reefs 24, 392–402.
Moe Jr., M.A., 1997. Breeding the Orchid Dottyback, Pseudochromis fridmani: An
Aquarist’s Journal. Green Turtle Publications, Islmorada, FL.
6 I. Olivotto et al. / General and Comparative Endocrinology xxx (2016) xxx–xxx
Moorhead, J.A., Zeng, C., 2010. Development of captive breeding techniques for
marine ornamental fish: a review. Rev. Fish. Sci. 18 (4), 315–343.
Munday, P.L., Kuwamura, T., Kroon, F.J., 2010. Bi-directional sex change in marine
fishes. In: Cole, K.S. (Ed.), Reproduction and Sexuality in Marine Fishes: Patterns
and Processes. University of California Press, Berkeley, pp. 241–271.
Muscatine, L., 1990. The role of symbiotic algae in carbon and energy flux in reef
corals. Ecosyst. World 25, 75–87.
Olivotto, I., Carnevali, O., 2004. In: Brockmann, D. (Ed.), Nachzuchten für das
Korallenriff-Aquarium. BirgitSchmettkamp Verlag, Bornheim, Germany, pp.
222–229.
Olivotto, I., Cardinali, M., Barbaresi, L., Maradonna, F., Carnevali, O., 2003. Coral reef
fish breeding: the secrets of each species. Aquaculture 224, 69–78.
Olivotto, I., Yasumasu, S., Gioacchini, G., Maradonna, F., Cionna, C., Carnevali, O.,
2004. Cloning and expression of High Choriolytic enzyme, a component of the
hatching enzyme system, during embryonic development of the marine
ornamental teleost, Chrysiptera parasema. Mar. Biol. 145, 1235–1241.
Olivotto, I., Zenobi, A., Rollo, A., Migliarini, B., Avella, A.M., Carnevali, O., 2005.
Breeding, rearing and feeding studies in the cleaner goby Gobiosoma evelynae.
Aquaculture 250, 175–182.
Olivotto, I., Holt, S.A., Carnevali, O., Holt, J.G., 2006a. Spawning, early development
and first feeding in the Lemonpeel angelfish Centropyge flavissimus. Aquaculture
253, 270–278.
Olivotto, I., Rollo, A., Sulpizio, R., Avella, A.M., Tosti, L., Carnevali, O., 2006b. Breeding
and rearing the Sunrise Dottyback Pseudochromis flavivertex: the importance of
live prey enrichment during larval development. Aquaculture 255, 480–487.
Olivotto, I., Capriotti, F., Buttino, I., Avella, A.M., Vitiello, V., Maradonna, F., Carnevali,
O., 2008a. The use of harpacticoid copepods as live prey for Amphiprion clarkii
larviculture: effects on larval survival and growth. Aquaculture 274, 347–352.
Olivotto, I., Buttino, I., Borroni, M., Piccinetti, C.C., Malzone, M.G., Carnevali, O.,
2008b. The use of the Mediterranean calanoid copepod Centropages typicus in
Yellowtail clownfish (Amphiprion clarkii) larviculture. Aquaculture 284, 211–
216.
Olivotto, I., Avella, A.M., Sampaolesi, G., Piccinetti, C.C., Navarro Ruis, P., Carnevali,
O., 2008c. Breeding and rearing the longsnout seahorse Hippocampus reidi:
rearing and feeding studies. Aquaculture 283, 92–96.
Olivotto, I., Avella, M.A., Buttino, I., Cutignano, A., Carnevali, O., 2009. Calanoid
copepod administration improves yellow tail clownfish (Amphiprion clarkii)
larviculture: biochemical and molecular implications. AACL Bioflux. 2, 355–367.
Olivotto, I., Piccinetti, C.C., Avella, M., Molina-Rubio, C., Carnevali, O., 2010. Feeding
strategies for striped blenny Meiacanthus grammistes larvae. Aquacult. Res. 41,
307–315.
Olivotto, I., Di Stefano, M., Rosetti, S., Cossignani, L., Pugnaloni, A., Giantomassi, F.,
Carnevali, O., 2011a. Live prey enrichment, with particular emphasis on HUFAs,
as limiting factor in False percula clownfish (Amphiprion ocellaris,
Pomacentridae) larval development and metamorphosis: molecular and
biochemical implications. Comp. Biochem. Physiol. Part A 159, 207–218.
Olivotto, I., Planas, M., Simões, N., Holt, G.J., Calado, R., 2011b. Advances in breeding
and rearing marine ornamentals. J. World Aquacult. Soc. 42, 135–166.
Olivotto, I., Gaiot, G., Holste, L., Tulli, F., Cardinaletti, G., Piccinetti, C.C., Gioacchini,
G., Carnevali, O., 2012. Are Acartia tonsa cold stored eggs a suitable food source
for the marine ornamental species Amphiprion polymnus? A feeding study.
Aquacult. Nutr. 18, 685–696.
Osinga, R., Schutter, M., Griffioen, B., Wijffels, R.H., Verreth, J.A., Shafir, S., Henard, S.,
Taruffi, M., Gili, C., Lavorano, S., 2011. The biology and economics of coral
growth. Mar. Biotechnol. 13 (4), 658–671.
Pimputkar, S., Speck, J.S., DenBaars, S.P., Nakamura, S., 2009. Prospects for LED
lighting. Nat. Photonics 3, 180–182.
Pomeroy, R.S., Parks, J.E., Balboa, C.M., 2006. Farming the reef: is aquaculture a
solution for reducing fishing pressure on coral reefs? Mar. Policy 30 (2), 111–
130.
Rhyne, A.L., Tlusty, M.F., Kaufman, L., 2012. Long-term trends of coral imports into
the United States indicate future opportunities for ecosystem and societal
benefits. Conserv. Lett. 5, 478–485.
Rinkevich, B., 1995. Restoration strategies for coral reefs damaged by recreational
activities: the use of sexual and asexual recruits. Restor. Ecol. 3 (4), 241–251.
Rinkevich, B., 2000. Steps towards the evaluation of coral reef restoration by using
small branch fragments. Mar. Biol. 136 (5), 807–812.
Rocha, R.J., Pimentel, T., Serôdio, J., Rosa, R., Calado, R., 2013. Comparative
performance of light emitting plasma (LEP) and light emitting diode (LED) in
ex situ aquaculture of scleractinian corals. Aquaculture 402, 38–45.
Please cite this article in press as: Olivotto, I., et al. Marine ornamental species culture: From the past to ‘‘Finding Dory”. Gen. Comp. Endocrinol. (2016),
http://dx.doi.org/10.1016/j.ygcen.2016.03.004
View publication stats
Rosenfeld, M., Bresler, V., Abelson, A., 1999. Sediment as a possible source of food
for corals. Ecol. Lett. 2, 345–348.
Sargent, J.R., McEvoy, L.A., Bell, J.G., 1997. Requirements, presentation and sources
of polyunsaturated fatty acids in marine fish larval feeds. Aquaculture 155, 85–
101.
Sargent, J., McEvoy, L.A., Estévez, G., Bell, Bell M., Henderson, J., Tocher, D., 1999.
Lipid nutrition of marine fish during early development: current status and
future directions. Aquaculture 179, 217–229.
Schlacher, T.A., Stark, J., Fisher, A.B.P., 2007. Evaluation of artificial light regimes and
substrate types for aquaria propagation of the staghorn coral Acropora
solitaryensis. Aquaculture 269, 278–289.
Schutter, M., van der Ven, R.M., Janse, M., Verreth, J.A., Wijffels, R.H., Osinga, R.,
2012. Light intensity, photoperiod duration, daily light flux and coral growth of
Galaxea fascicularis in an aquarium setting: a matter of photons? J. Mar. Biol.
Assoc. UK 92 (4), 703.
Seemann, J., 2013. The use of 13C and 15N isotope labeling techniques to assess
heterotrophy of corals. J. Exp. Mar. Biol. Ecol. 442, 88–95.
Setu, S.K., kumar, A.T.T., 2010. Spawning behaviour and embryonic development of
Regal Damsel Fish, Neopomacentrus cyanomus (Bleeker, 1856). World J. Fish
Mar. Sci. 2, 410–415.
Setu, S.K., Kumar, A.T.T., Balasubramanian, T., Dabbagh, A.R., Keshavarz, M., 2010.
Breeding and rearing of Regal Damselfish Neopomacentrus cyanomos (Bleeker,
1856): the role of green water in larval survival. World J. Fish Mar. Sci. 2, 551–
557.
Shafir, S., Van Rijn, J., Rinkevich, B., 2001. Nubbing of coral colonies: a novel
approach for the development of inland broodstocks. Aquarium sci. Conserv. 3
(1–3), 183–190.
Shuman, C.S., Hodgson, G., Ambrose, R.F., 2004. Managing the marine aquarium
trade: is eco-certification the answer? Environ. Conserv. 31 (04), 339–348.
Shuman, C.S., Hodgson, G., Ambrose, R.F., 2005. Population impacts of collecting sea
anemones and anemonefish for the marine aquarium trade in the Philippines.
Coral Reefs 24 (4), 564–573.
Sorokin, Y.I., 1973. On the feeding of some scleractinian corals with bacteria and
dissolved organic matter. Limnol. Oceanogr. 18, 380–386.
Stottrup, J.G., Norsker, N.H., 1997. Production and use of copepods in marine fish
larviculture. Aquaculture 155, 231–248.
Thornhill, D., 2012. Ecological Impacts and Practices of the Coral Reef Wildlife
Trade. Defenders of Wildlife, Washington, DC, p. 179.
Thresher, R.E., 1984. Reproduction in Reef Fishes. T.H.F. Publications, New Jersey,
USA, pp. 1–180.
Tissot, B.N., Best, B.A., Borneman, E.H., Bruckner, A.W., Cooper, C.H., D’Agnes, H.,
Fitzgerald, T.P., Leland, A., Lieberman, S., Mathews Amos, A., Sumaila, R.,
Telecky, T.M., McGilvray, F., Plankis, B.J., Rhyne, A.L., Roberts, G.G., Starkhouse,
B., Stevenson, T.C., 2010. How U.S. ocean policy and market power can reform
the coral reef wildlife trade. Mar. Policy 34, 1385–1388.
Tlusty, M., 2002. The benefits and risks of aquacultural production for the aquarium
trade. Aquaculture 205, 203–219.
Treignier, C., Tolosa, I., Grover, R., Reynaud, S., Ferrier-Pagès, C., 2009. Carbon
isotope composition of fatty acids and sterols in the scleractinian coral
Turbinaria reniformis: effect of light and feeding. Limnol. Oceanogr. 54 (6),
1933.
Veron, J.E.N., 2000, . Corals of the World, third ed., vol. 3. Australian Institute of
Marine Sciences and CRR Qld Pty Ltd, Australia, ISBN 0-642-32236-8.
Wabnitz, C., Taylor, M., Green, E., Razak T., 2003. From Ocean to Aquarium UNEP.
World Conservation Monitoring Centre, Cambridge. pp. 1–64.
Widdig, A., Schlichter, D., 2001. Phytoplankton: a significant trophic source for soft
corals? Helgol. Mar. Res. 55, 198–211.
Wijgerde, T., Henkemans, P., Osinga, R., 2012. Effects of irradiance and light
spectrum on growth of the scleractinian coral Galaxea fascicularis—
applicability of LEP and LED lighting to coral aquaculture. Aquaculture 344,
188–193.
Wittenrich, M.L., 2007. The Complete Illustrated Breeder’s Guide to Marine
Aquarium Fishes. T.F.H Publications Inc, Neptune city, NJ, USA, pp. 234–242.
Wood, E., 2001a. Global advances in conservation and management of marine
ornamental resources. Aquarium Sci. Conserv. 3 (1–3), 65–77.
Wood, E.M., 2001b. Collection of Coral Reef Fish for Aquaria: Global Trade,
Conservation Issues and Management Strategies. Marine Conservation
Society, Ross-on-Wye, UK, p. 80.