Advances in Breeding and Rearing Marine Ornamentals

JOURNAL OF THE Vol. 42, No. 2 WORLD AQUACULTURE SOCIETY April, 2011

Ike Olivotto1 Department of Marine Sciences, Universit`a Politecnica delle Marche, Via Brecce Bianche, 60131 Ancona, Italy

Miquel Planas ◦ Instituto de Investigaciones Marinas (CSIC), Eduardo Cabello n 6, 36208 Vigo, Galicia, Spain

Nuno Simoes˜ Unidad Multidisciplinaria de Docencia e Investigación – Sisal, Facultad de Ciencias, Universidad Nacional Autonoma de México (UMDI-Sisal, FC, UNAM), México

G. Joan Holt Department of Marine Science, The University of Texas at Austin, Marine Science Institute, Port Aransas, Texas 78373, USA

Matteo Alessandro Avella Department of Marine Sciences, Universit`a Politecnica delle Marche, Via Brecce Bianche, 60131 Ancona, Italy

Ricardo Calado Centro de Estudos do Ambiente e do Mar (CESAM)/Departamento de Biologia da Universidade de Aveiro, Campus Universit´ario de Santiago, 3810-193 Aveiro, Portugal

Abstract This work addresses the most relevant advances in the breeding and rearing of marine ornamental species. The main breakthroughs in marine ornamental ﬁsh culture are discussed, with seahorses deserving a section of their own as a result of their conservation status and unique biology. Details on spawning, embryo development, larval rearing, plankton culturing, and tank design are presented. In addition, with the increase in popularity of ornamental invertebrates in reef aquariums, details on the culturing techniques of some of the most traded invertebrate groups (e.g., live rocks, corals, anemones, polychaetes, mollusks, decapod crustaceans and echinoderms) are also discussed. Finally, the last part of this work highlights the concerns toward the establishment of sustainable collection, production, and trading practices for marine ornamentals as well as the urgent need to develop reliable traceability protocols to distinguish sustainably caught and/or cultured specimens from wild ones. This work represents not only an exhaustive and updated bibliographical source but also a starting point for all those who want to contribute to the development of this fascinating research ﬁeld.

Although coral reefs cover less than 1% Earth. They support over 4000 ﬁsh species, of the marine environment, they are unani- about 800 species of reef-building corals and mously considered among the most biologi- several thousands of other reef invertebrates cally rich and productive ecosystems on the (cnidarians, sponges, mollusks, crustaceans, and echinoderms; Paulay 1997). The past few 1 Corresponding author. decades have been characterized by negative

135 136 OLIVOTTO ET AL. anthropogenic effects on coral reef ecosystems, reefs (Tlusty 2002; Pomeroy et al. 2006). This such as sedimentation, nutrient enrichment due approach may not only generate an alternate to human waste and agriculture run-off, over- supply of marine ornamental specimens but will fishing, and global climate change (Baskett also allow researchers to collect valuable infor- et al. 2010; Selig and Bruno 2010). The inten- mation about their life history (age at maturity, sive fishing effort required to supply the marine fecundity, etc.) to improve the management of aquarium trade may also have played an natural stocks and our understanding of how important role in the decline of coral reefs. these organisms respond to human impacts. Unlike freshwater ornamental species, where This work addresses the most relevant over 90% of fish species are currently pro- advances in the breeding and rearing of marine duced in captivity, the vast majority of marine ornamental species. The main breakthroughs in aquaria are stocked from wild-caught speci- marine ornamental fish culture are discussed, mens (Wabnitz et al. 2003). In addition, less with seahorses deserving a section of their conscientious traders continue to support the own as a result of their conservation sta- use of destructive fishing techniques, namely tus and unique biology. Advances concerning the use of cyanide, to anesthetize highly priced the culture of marine ornamental invertebrates fish species. The use of this poison is known (i.e., live rock production, coral propaga- to harm targeted, as well as non-targeted, tion, anemones, polychaetes, mollusks, decapod reef fishes and its deleterious effects on sev- crustaceans, and echinoderms) are also pre- eral marine invertebrates are also documented sented and discussed. The last part of this work (Barber and Pratt 1998; Hanawa et al. 1998; highlights the need to establish sustainable col- Mak et al. 2005). The promotion of bleaching lection, production, and trading practices for in reef-building corals after exposure to cyanide marine ornamental species as well as to develop is certainly one of the most dramatic effects reliable traceability protocols to distinguish sus- of the use of this poison to collect live reef tainably caught and/or culture specimens. fishes (Jones et al. 1999; Cervino et al. 2003). Nonetheless, it is relevant to highlight that Marine Ornamental Fishes (Except cyanide poisoning is also used to supply the live Seahorses) food fish trade in Southeast Asia (Barber et al. 1997; Pomeroy et al. 2008) and that dynamite In recent years, there has been an increased fishing is only used to collect reef fishes for focus on supplying aquarium fishes through human consumption (Pet-Soede et al. 1999). closed system culturing. The development of It is estimated that from oceans to aquaria, reliable and sustainable hatchery procedures up to 80% of the traded animals die during for the captive breeding of reef fishes is now capture, shipment, handling due to the use of becoming essential to reduce pressure on wild poisons during collection, poor handling prac- populations and also because rearing fish in tices, and diseases (Sadovy and Vincent 2002; closed systems is likely to lead to the produc- Wabnitz et al. 2003). The poor survival of col- tion of hardier specimens that are far better in lected specimens through the chain of custody, captivity and survive longer (Wittenrich 2007). along with the current dependence of the marine It is hoped that much of the market demand aquarium industry on the collection of wild for the more popular ornamentals may even- specimens to supply an ever growing demand, tually be satisfied by cultured fish; however, urges researchers to find solutions to make in reality, most marine ornamental aquaculture the trade of marine ornamental species a more remains problematic. In fact, there are numer- sustainable practice. Aquaculture is commonly ous critical processes in early life history where considered a potential alternative, as the cap- deficiencies could represent a limiting factor tive production of some of the most heavily in captive rearing. Some of the main criti- collected species would certainly contribute to cal steps are spawning (which includes sexing relieving the current fishing pressure on coral the fish and the development of a reproductive ADVANCES IN BREEDING AND REARING MARINE ORNAMENTALS 137 competence), embryo development (which is are much more aggressive, whereas females strictly related to broodstock nutrition, mainte- present a rounder vent. nance, and genetics), hatching (which depends Some fish are able to perform sex rever- on the reproductive strategy), and the transition sal (hermaphrodites). There are simultaneous from endogenous to an exogenous feeding by hermaphrodites, where one individual possesses the larvae. both female and male reproductive tissue and It is well established that the life cycle of can act as either sex during a single spawning most coral reef fishes can be subdivided into event. Physical adaptation usually prevents self- three distinct biological/ecological phases: lar- fertilization. They represent a minority among vae, juvenile, and adult. To cultivate marine ani- aquarium fishes (e.g., Serranidae). Sequential mals, we must work on all life stages from eggs hermaphrodites are dominant and involve an to larvae, juveniles, and adults (Holt 2003). In individual acting as one sex during the early general, the hypothesis of many scientists is part of its life and eventually, if conditions that marine ornamental fish can be spawned and are appropriate, changing sex. They can be raised in captivity and second, the culture tech- subdivided in protogynous (sex change in the niques developed in the research laboratories female–male direction) and protrandrous (sex can be transferred to commercial production change in the male–female direction). Typical (Holt 2003; Olivotto et al. 2008a). examples of protrandrous species are clown- To start, breeding and cultivating marine fishes where the social status determines the sex ornamental broodstock has to be carefully cho- of the fish. The female is the largest, the male sen because high-quality breeders are essential is the second largest, and the nonbreeders are for successful larval rearing. When possible, progressively smaller as the hierarchy descends. captive-bred specimens should be preferred Typical protogynous species are dottybacks and over wild ones because they are hardier, far angelfishes. After determining the sex of the better in captivity, and survive longer, as they fish, the hypothalamus, pituitary gonadal axis are young fish (6–12 mo), and do not undergo should be activated. Environmental conditions, shipment stress. including photoperiod, temperature, and food As reproductive strategies used by fish are availability may be very important for this acti- extremely diverse, knowledge of the life his- vation. Photoperiod and temperature may be tory of the species under study is crucial to manipulated using light timers and heat pumps. the success of captive propagation. Develop- Controlled environments mimic natural spawn- ment of reproductive competence relies on ing conditions with seasonal changes in day the integration of a wide variety of internal length and temperature to promote spawning. and external cues. These signals provide crit- Usually, for demersal spawners, high tempera- ical information on when an animal should ture (28 C) and long photoperiod (14 L/10 D) reproduce: whether it is of sufficient size or are sufficient to get fishes to spawn (Oliv- energy status to reproduce (metabolic cues), otto et al. 2003; Olivotto and Carnevali 2004; whether conditions are optimal for reproduc- Avella et al. 2007), although other combina- tive success (environmental cues), and whether tions (13 L/11 D and 12 L/12 D at 26 C for an appropriate mate is present (social cues). Elacatinus figaro) may work as well (Meirelles When attempting to breed a particular species et al. 2009; Shei et al. 2010). However, for of fish in captivity, it is important to be able pelagic spawners, seasonal changes are needed to sex the organisms: some fish are of a pre- (Holt and Riley 2001) to induce spawning, determined sex (gonochoric fish) and are not with fish being subjected to winter (22 C 10 L/ capable of sex reversal. Couples are usually 14 D), spring (24 C 12 L/12 D), and summer formed through trial and error or by looking (27–28 C 14 L/10 D) temperatures/photoperi- for sexual dimorphism. For example, in both ods (Holt and Riley 2001). Nonetheless, spawn- yellow tail damsel, Chrysiptera parasema,and ing always occurs during the summer period striped blenny, Meiacanthus grammistes, males (Holt and Riley 2001; Olivotto et al. 2006a). 138 OLIVOTTO ET AL.

These temperature and photoperiod conditions, hatching enzymes, and, in demersal spawners together with good water quality (ensured by and egg-ball layers, parental care (Inhoaya et al. suitable filtration equipment) and with heavy 1997; Olivotto et al. 2004). In several species, feeding, generally result in the spawning of successful hatching may depend on ambient marine ornamental fish in captivity. light conditions, with most of demersal spawn- The two dominant modes of egg release ers hatching at night. The development of this among marine fish are demersal and pelagic photo-regulated hatching is most probably an spawning. Demersal spawners usually produce ecologically meaningful life strategy to reduce eggs that are attached to a solid surface or the predatory pressure on these larvae. spawned in small caves as gelatinous egg At hatching, the delicate larvae and prolar- masses in the case of egg ball layers. Demersal vae are extremely sensitive to any turbulence spawning requires parental care. Typically, the and chemical–physical environmental variation male takes care of the fry until they hatch. In (Brons 1995; Holt 2003; Olivotto et al. 2003). the meantime, the female is involved in feed- Demersal-spawned larvae develop in the egg ing to sustain oogenesis. The effort put into until pigmented eyes and a finfold have devel- parental care depends on the water circula- oped. Larvae are competent at this stage with tion in the tank; the more the current, the less functional jaws and pigment in the eyes, the frequently the male has to fan the embryos. yolk sac is almost exhausted and mouth and Males have often been observed mouthing the digestive tract are open and functional. How- embryos. This is a common practice that may be ever, pelagic-spawned larvae are very tiny, important in displacing improperly developing hatch as prolarvae, and lack pigmented eyes, a embryos. digestive system, or mouth. At this stage, they Pelagic spawners display complex courtship still have large yolk reserves which are used to with eggs and sperm being released into the undergo a second developmental phase of about water column. Eggs are usually smaller and pro- 48 h in the water column. After this period, duced in greater number when compared with the prolarvae have developed into active larvae those of demersal spawners. Spawning usually with pigmented eyes and functional digestive occurs at dusk, as during this transition period, system. Prolarvae are extremely vulnerable to the predatory pressure is reduced at the reef predation during this early period. (diurnal predators are seeking refuge and noc- As larvae and prolarvae are very delicate turnal ones are still not fully active). Depending during this early part of their life history, dif- on the reproductive strategy, embryo devel- ferent larval rearing systems have been development lasts from hours in pelagic spawners oped to mimic the open ocean’s conditions (Brothers and Thresher 1985; Wellington and where food organisms are abundant and preda- Victor 1989; Bonhomme and Planes 2000) to tors are few. Microcosms made of 20-L glass days in demersal ones (Russell 1971; Alcala tanks have been successfully used for sev- and Cabanban 1986; Moe 1992, 1997; Brons eral demersal spawners including clownfishes 1996; Allen 2000). Although the embryo is (Amphiprion spp.), gobies (Gobiosoma spp.), developing protected by the chorionic mem- dottybacks (Pseudochromis spp.), and some brane, several different biological processes are blennies (Meiacanthus spp.; Olivotto et al. initiated to prepare it for its independent life 2005, 2009). The sides of the tank are cov- in the environment. After a species-specific ered with black panels to reduce light reflec- process of development, the embryo changes tion, whereas the bottom is usually white into a form that obtains nutrients from external to facilitate bottom cleaning. The water in sources, a stage that is achieved through the these tanks is changed up to 10 times a day breakdown of the chorionic membrane (hatch- through a dripping system (Olivotto et al. 2003; ing) in demersal species. Hatching has an enzy- Olivotto and Carnevali 2004). For prolarvae, matic and a mechanical aspect caused by the small 50-L mesh baskets placed in large tanks synchronized action of embryonic movements, (400–1000 L) have been used with success. ADVANCES IN BREEDING AND REARING MARINE ORNAMENTALS 139

The use of these rearing chambers concentrates and Artemia. Moreover, larvae fed enriched live larvae and food, increases food encounter rates, prey showed a faster growth and completed provides shelter, and decreases potential physi- metamorphosis earlier than those fed on nonen- cal damage. Moreover, heating and aeration are riched Artemia nauplii. These results clearly carried out in the large tank and the water in indicated that live prey enrichment is essential the rearing chamber is very clean, warm, and for rearing this species. In addition, it is well the salinity matches that of the open ocean – all established that anomalous pigmentation, con- conditions that larvae might naturally encounter sisting of partial or total lack of white bands (Holt 2003). (“miss-band”) is a common problem in the pro- The main obstacle in ornamental fish larvi- duction process of the false percula clownfish, culture is the transition from endogenous to Amphiprion ocellaris (Avella et al. 2007). As exogenous feeding by the larvae and because “miss-band” clownfishes are sold at a lower the larval cycle is spent in the open ocean, this price by the companies, there is a great inter- particular environment should be mimicked. est in understanding and solving this problem. The open ocean in the tropics is characterized It has been demonstrated that highly unsatu- by warm, calm waters and appropriate concen- rated fatty acids (HUFAs) administration in the tration of live prey on which larvae are able live prey not only positively affected growth but to feed. From several field studies, it is evi- also reduced the percentage of miss-band organ- dent that in the wild, marine fish larvae mainly isms (Avella et al. 2007). Poor color perfor- feed on wild plankton composed of copepods, mance of juveniles and adults can also reduce protozoan, and larvae of benthic organisms. their price, although this can be easily manip- Recent studies have shown that after feed- ulated through either diet supplements rich ing marine fish larvae with wild plankton and in carotenoids (Ho et al. 2008) or light inten- checking their gut contents, the most abundant sity and background (Yasir and Kim 2009a, ingested live prey were copepod eggs and nau- 2009b). plii (Olivotto et al. 2006a; Baensch and Tamaru Thus, there is a strong need for identifica- 2009a, 2009b). Unfortunately, copepods are dif- tion of alternative food sources that do not have ficult to culture on a continuous basis and most the inadequacies of rotifers and Artemia and of the marine fish species are reared using that can increase the variety, growth, and sur- rotifers, Brachionus spp., and Artemia spp. vival of the species that can be cultivated. Adult nauplii. Despite apparent practical advantages copepods, as well as copepodites and nauplii, in production, rotifers and Artemia are not the are the food items preferred by fish larvae in best live prey for marine fish larvae, as they are the wild and when used as live prey (solely or not their natural food. For some tiny larvae (but- in combination with rotifers and Artemia nau- terfly fish, angelfishes, and groupers), these prey plii), they usually dominate the gut content of are too large, their locomotory patterns (slow larvae (Holt 2003). Delbare et al. (1996) sum- circular movement) do not promote predatory marized the advantages of using copepods in activity, and they do not display a fatty acid pro- larviculture, such as the wide range of body file that matches the nutritional requirements of size between nauplii and adults, their typical marine fish larvae. Our recent studies (Olivotto movement, and their high content of HUFAs. et al. 2006b) demonstrated the importance of These fatty acids, in particular eicosapentaenoic food enrichment of rotifers and Artemia for acid (EPA, 20:5n-3) and docosahexaenoic acid sunrise dottyback, Pseudochromis flavivertex, (DHA, 22:6n-3), are extremely important for larvae. Larvae were divided into experimental larval fish survival and growth and several stud- groups fed on different enriched and unenriched ies have demonstrated that they are essential live prey. Larvae fed on nonenriched rotifers in larval diets (Sargent et al. 1989). Deficien- did not survive past day 7, whereas highest cies in these fatty acids can cause a general survival rates (39% juveniles) were observed decrease in larval health, poor growth, low feed in larvae fed exclusively on enriched rotifers efficiency, anemia, and high mortality (Sargent 140 OLIVOTTO ET AL. et al. 1999; Bell et al. 2003; Olivotto et al. cells/L of each algae. Nauplii and copepodites 2003, 2006b; Faulk and Holt 2005). were collected at different developmental stages With the increasing worldwide interest in from naupliar stage I (NI; 110-μm length) to aquaculture, copepods may be considered a copepodids III (CIII; 560-μm length) and used valid and alternative food source for the culture for feeding studies. Nauplii and copepodites of many larval fish. The use of cultured were attracted into a 155- to 300-μm mesh net copepods in intensive fish larviculture (Van size filter cage using a light, automatically col- der Meeren and Naas 1997; Papandroulakis lected in a 200-L tank, and finally concentrated et al. 2005) has involved calanoids such as in 15 L of seawater. This system was able to Acartia spp. (Schipp et al. 1999), Eurytemora produce enough nauplii for feeding trials and spp. (Shields et al. 1999), Parvocalanus spp. may represent a starting point for the develop- (Olivotto et al. 2006a), Centropages typicus ment of a mass cultivation system for calanoid (Olivotto et al. 2008a, 2008b, 2008c, 2009), and copepods. harpacticoid copepods such as Euterpina acu- Copepods are in fact the ideal diet for tifrons (Kraul et al. 1992), Tisbe spp. (Stottrup marine fish with very tiny larvae. Good can- and Norsker 1997; Olivotto et al. 2008a, 2008b, didates for feeding copepods are angelfishes, 2008c), and Trigriopus japonicus (Fukusho Pomacanthidae, which are among the most 1980). Harpacticoids are easier to culture at requested marine species by the ornamen- higher densities but are predominantly found on tal fish market (Baensch and Tamaru 2009a, the tank walls rather than in the water column. 2009b). The main problem in culturing these For this reason, these live preys are less avail- species occurs at first feeding. The tiny lar- able to fish larvae and are commonly used as vae are too small to eat rotifers and alterna- a supplement to the traditional rotifers/Artemia tive live preys have to be selected to feed diet (Olivotto et al. 2008a, 2008b). the larvae (Holt 2000, 2003). In a study on The best results in larviculture have been lemonpeel angelfish, Centropyge flavissimus, obtained using calanoid copepods which have larvae fed the circumtropical copepod Par- a high content of HUFAs, are entirely pelagic, vocalanus sp. or wild plankton (25–75 μm and thus more available as prey for marine in size) at 28 C had a 10% survival rate to fish larvae. Usually these copepods have very day 14 (Olivotto et al. 2006a). In addition, a small naupliar stages, which are more read- similar experiment was performed on semi- ily captured by fish larvae with small mouth circle angelfish, Pomacanthus semicirculatus. gapes at first feeding (Payne and Rippingale Different diets were tested on larval survival 2001; Olivotto et al. 2006a, 2006b). Unfortu- rate and a diet composed of 30% Gonyaulax nately, there are several difficulties in cultur- sp. (dynoflagellate) + 35% Nannochloropsis ing calanoid copepods on a continuous basis, sp. + 35% Brachionus rotundiformis was the because they are usually cultured at very best choice for larval P. semicirculatus.Further low densities, in large tanks, and need to be studies are necessary to close the reproductive fed different algal combinations (Holt 2003). cycle of this species (Leu et al. 2009). A small- Recently, at the Stazione Zoologica Anton scale culture-technology for Parvocalanus spp. DohrninNaples,C. typicus (Kroyer,¨ 1849) copepods was used to successfully rear some copepods were cultured through different gen- “difficult species” such as the flame angel erations in a 500-L recirculating system (INNO- fish, Centropyge loriculus, and the yellow tang, VAQUA srl, Reggio Emilia, Italy) equipped Zebrasoma flavescens (Laidley et al. 2009). At with biological/mechanical filtration. Copepods present, scientists still need to increase lar- were fed with a mixture of phytoplanktonic val survival through late larval period when cells of Heterocapsa niei, Tetraselmis sue- it becomes increasingly difficult to maintain cica,andIsochrysis galbana at concentrations sufficient numbers of larger copepodites prior of 5.5 × 103,1.25× 104, and 3.4 × 104 cells/ to weaning the larvae onto newly hatched mL, respectively, corresponding to about 1 mg Artemia nauplii. It has been demonstrated that ADVANCES IN BREEDING AND REARING MARINE ORNAMENTALS 141 two genera of copepods, Parvocalanus sp. and (Kuiter 2000), being very popular in Chinese Pseudodiaptomus sp., offer substantial advan- traditional medicine and the marine ornamen- tages in culture techniques (in terms of produc- tal trades (Lourie et al. 1999). Unfortunately, tion numbers, size, and survival) compared with wild populations are declining due to overex- the most widely cultured species Acartia tonsa ploitation (Lourie et al. 1999) and all seahorse (Rhyne et al. 2009a, 2009b). species have been listed in the Appendix II of In conclusion, many fish can be spawned Convention on International Trade in Endan- in captivity; the main critical bottleneck is gered Species of Wild Flora and Fauna (CITES the first feeding. Using rotifers and Artemia 2002a). during the early life history of fish does not Seahorses are interesting for economical, always promote optimal larval growth because cultural, scientific, and educational reasons. these live prey may contain an inadequate fatty Because of the increasing demand for seahorses acid profile and, in some cases, display an for the aquarium trade and the pressure on wild inappropriate size (Kahan 1981; Holt 2003; populations, interest in the biology and rear- Olivotto et al. 2003; Faulk and Holt 2005). ing of seahorses has increased in recent years. Because of this, there is a need for identifi- At least 13 species are commercially produced cation of alternative food sources that do not (Koldewey and Martin-Smith 2010), but most have these inadequacies and can promote ade- seahorse species are potential candidates for quate growth (Sun and Fleeger 1995). Adult the ornamental fish trade. Compared with other copepods, along with copepodites and nau- reef fishes, rearing of seahorses is a relatively plii, are considered good candidates for feed- new industry with high economic potential due ing marine ornamental fish larvae (Holt 2003). to increasing demand and high market prices The advantages of using copepods in larvicul- for commercialized species. Breeding of large ture are mainly related to their wide range of numbers of quality seahorses for fish trade or body sizes between nauplii and adults, their the traditional Chinese market (medicine and typical movement, and their high content of gastronomy) can also contribute to reduce the HUFAs. Bottlenecks still remain; the develop- pressures on wild seahorse populations. ment of a copepod-based commercial produc- Ecological, biological, and physiological tion of marine fish still requires the use of aspects of seahorses have been almost unknown large mesocosms. Research should be focused until recently. There are several characteristics on finding copepod species with short gener- that are unique among reef fishes: low density, ation times and tolerance to high densities, in limited home ranges, reduced mobility, short addition to gaining a better understanding of life span, parental care, sexual dimorphism, low the possible involvement of amino acids, pro- fecundity, pair bonding, mating with courtship tein, pigment, and vitamin contents of copepods displays, batch spawners with repeated mates in larval fish growth and survival. within a breeding season, and genetic monoga- mous pattern within a single breeding season (Foster and Vincent 2004). Although rear- Seahorses ing technology exists for a few species at A very special group of marine ornamen- a commercial scale, improvements are neces- tal fishes are the Syngnathidae, a family that sary to enhance profitability. Some years ago, includes seahorses, pipefishes, and sea dragons. research efforts were directed toward the devel- Seahorses, Hippocampus spp., are bony fishes opment of rearing technology for some tropical whose evolutionary history is so recent that or subtropical species (Koldewey and Martin- the major stages of morphological evolution Smith 2010). More recently, attention has also are still represented in extant species (Teske been focused on temperate species such as the and Behegaray 2009). These iconic fishes are European long-snouted seahorse, Hippocam- distributed in coastal tropical, subtropical, and pus guttulatus or the European short-snouted temperate marine regions throughout the world seahorse, H. hippocampus (Molina et al. 2007; 142 OLIVOTTO ET AL.

Otero et al. 2007, 2009, 2010; Faleiro et al. clutch size, and brood size were not affected 2008; Palma et al. 2008; Planas et al. 2008a, by mysids and improved in cultured H. gut- 2008b, 2009a, 2009b, 2009c; Planas and tulatus fed on enriched Artemia (Planas et al. Quintas 2009). Knowledge on essential aspects 2009a, 2010), when compared with wild sea- is almost lacking, especially on those related horses (Curtis 2007). These findings suggest with reproductive success and mortality of juve- that receptivity for mating could be partially niles. The rearing of seahorses in captivity has inhibited by other unknown factors, not neces- contributed to increased understanding of sea- sarily related to feeding/nutritional conditions. horse biology and physiology, but there is still Egg size has been used as a criterion of insufficient information on growth, breeding, egg/juveniles quality. Although interspecific and feeding/nutritional requirements. differences in egg size within seahorse species Reproduction in captivity has been success- depend on latitude rather than female size fully achieved in a number of seahorse species (Foster and Vincent 2004), intraspecific egg size but still remains a bottleneck for many oth- comparisons would be useful in egg quality ers. Knowledge of reproductive physiology, studies. In seahorses, eggs are typically asym- female maturation, or egg characteristics is metrical, nonbuoyant, and larger (0.9–3.8 mm extremely limited in seahorses (Selman et al. in diameter) than in most tropical marine fishes 1991; Poortenaar et al. 2004). In general, mat- (Ahlstrom and Moser 1980). However, because ing in captive conditions is not a constraint eggs are asymmetrical, measuring them accu- but seems to be especially difficult in the rately has been problematic (Foster and Vincent European long-snouted seahorse, H. guttulatus 2004) due to the lack of a standardized proto- (Faleiro et al. 2008; Planas et al. 2008a). In col. A mathematical model has been proposed this species, courtship displays are accompa- for H. guttulatus egg and yolk size estima- nied by a low breeding success (Planas et al. tion based on length and width measurements 2009a). A possible explanation, which needs to (Planas and Quintas 2009). The model could be confirmed, could rely on unfulfilled nutri- be easily applied to other seahorse species. Egg tional requirements. Adult seahorses are rarely size has been positively correlated with female fed on Artemia alone (Ortega-Salas and Reyes- size in some pipefish species (Berglund et al. Bustamante 2006; Planas et al. 2008a). Other 1986) but not in seahorses (Foster and Vincent prey (mysidaceans, amphipods, and shrimps) 2004; Planas et al. 2010). However, a correla- are usually offered, alone (alive or frozen) tion between clutch size and female size/weight or as Artemia supplementation (Woods and has been found for H. whitei, H. erectus,andH. Valentino 2003; Koldewey 2005; Lin et al. guttulatus (Teixeira and Musick 2001; Vincent 2006, 2007, 2008b; Ortega-Salas and Reyes- and Giles 2003; Planas et al. 2010). In addition, Bustamante 2006; Olivotto et al. 2008a, 2008b, Curtis (2004) pointed out that male size is a rea- 2008c; Murugan et al. 2009). In captivity, adult sonable predictor of brood size in H. guttulatus. seahorses show preference for mysids and Accordingly, reproductive efficiency would be amphipods (Vite et al. 2009). In fact, these enhanced in larger fishes. are their preferred prey in the wild as well Very little is known on feeding and nutri- (Teixeira and Musick 2001; Kitsos et al. 2008). tional requirements for broodstock in seahorses. Adult Artemia promotes high growth rates in The only information available on lipid content seahorses (Planas et al. 2009c), but its nutri- and fatty acids profile was reported by Planas tional adequacy, in terms of reproductive effi- et al. (2008a, 2009a, 2010) and Alvarez´ et al. ciency, has been often questioned. Otero et al. (2009) in eggs released by adults maintained (2009) carried out a comparative study in in captivity and fed on adult Artemia. Lipid H. hippocampus fed on enriched adult Artemia and fatty acid composition has been used as an or on wild-collected mysids, concluding that the indicator of egg quality in fish eggs because n- latter enhanced spawning and quality of newly 3 HUFAs are essential in marine fish (Sargent hatched young. Conversely, female maturation, et al. 1989, 1999) and are largely affected by ADVANCES IN BREEDING AND REARING MARINE ORNAMENTALS 143 the diet (Wiegand 1996). Generally, nutritional Planas et al. 2008b, 2010). Female maturation requirements are inferred from data obtained in in H. guttulatus is dependent on the photope- the wild, especially on the biochemical compo- riod regime, rather than temperature, which can sition of eggs and juveniles, but unfortunately boost up the effect of light regimes (Planas this type of information is lacking (Lin et al. et al. 2009a). Temperature, and not photope- 2008c). In captivity, the highest content of fatty riod, was suggested as the main environmental acids in eggs of H. guttulatus were 18:1n-9, factor governing reproduction in H. capensis 16:0, 18:2n-6, 20:5n-3, 18:0, and 22:6n-3, in (Lockyear et al. 1997). Photothermal manipu- decreasing order. However, it is difficult to pre- lation has been successfully applied to shift the dict to what extent this information could be period of reproduction in H. guttulatus (Lock- extrapolated to other species as the biochemical year et al. 1997; Planas et al. unpublished data). composition of adult seahorses varies largely Rearing procedures with acceptable survival depending on species and origin (Lin et al. rates have been reported for H. abdominalis, 2008a, 2008c), and the fatty acid profile in eggs H. erectus, H. ingens, H. kuda, H. subelonga- can be easily modified by artificial manipulation tus, H. trimaculatus, H. reidi,andH. whitei of parental diet (Planas et al. 2009a, 2009b). (Payne and Rippingale 2000; Job et al. 2002; Skeletal malformations in early stages of Gonzalez´ et al. 2003, 2004, 2006; Woods marine fish might be due to nutritional fac- 2003a, 2003b; Wong and Benzie 2003; Ortega- tors (phosphatidylinositol, DHA, peptides, or Salas and Reyes-Bustamante 2006; Lin et al. retinoic acid) (Cahu et al. 2003). Severe 2006, 2008b; Wilson et al. 2006; Hora and episodes of mouth malformations (jaw defor- Joyeux 2009; Murugan et al. 2009). Improve- mities that impede normal feeding) accompa- ment in rearing methodologies during the nied by the release of premature juveniles have past few years has contributed to significant been reported in newborn juveniles of sea- increases in survival rates (20–90%) in H. erec- horses (Planas et al. 2009b). The problem was tus (50–90%) and H. reidi (20–85%) at com- solved by increasing n-3 HUFA content in the mercial scale (Gomezjurado 2009a, 2009b). diet (three- and fourfold increase in EPA and Newborn seahorses are bigger than larvae DHA content, respectively) and consequently of most marine fish species and sufficiently in eggs (Planas et al. 2009a, 2009b). Newborn developed for active swimming and foraging juveniles are usually released from the male activity. Newborns start feeding immediately pouch in one single batch. When released in after birth due to the lack of yolk reserves, more batches, during several successive days, ascending instinctively to the water surface to the proportion of embryos and underdeveloped capture air for swim bladder inflation. In spite juveniles with yolk sac increased. This problem of these common characteristics, performance, has been solved by isolating breeding males prey preferences, and nutritional requirements some days before the release of juveniles, as vary largely among seahorse species, and ade- it was hypothesized that males may accelerate quate zootechniques must be established for the release of young to be prepared again for each species. The rearing of juveniles is con- mating. ducted differently for each species, with cul- Females are batch spawners with long inter- tures being carried out in green or clear water, clutch intervals, which are dependent and syn- under natural or continuous light regimes, and chronized with gestation duration (9–45 d) in with different types of prey enrichments. Juve- males (Foster and Vincent 2004; Vincent and niles of tropical and subtropical species are Sadler 1995). Optimal temperature for repro- usually raised at 23–28 C, whereas species of duction is unknown for the majority of seahorse temperate waters are raised at 13–24 C. species and needs to be determined due to its Feeding is one of the most decisive factors influence on gonad development and hatching. in the survival of juvenile seahorses (Alexandre Interclutch interval in females seems to be con- and Simoes˜ 2009). The application of a uni- trolled by temperature (Lin et al. 2006, 2007; versal feeding scheme suitable to all seahorse 144 OLIVOTTO ET AL. species is not operative, as biology, size of assimilating the food offered, including Artemia newborns, and especially digestion capability nauplii and metanauplii (Woods 2003a). Juve- are species dependent. Juveniles are fed on live niles are also able to attach to a hold- prey and attempts to culture juveniles on inert, fast very soon after being released from the frozen, or dried food have been unsuccessful male pouch (Quintas, personal communication), (Alexandre and Simoes˜ 2009). Rotifers are fed reducing the risk of swim bladder hyperin- to juveniles of H. reidi, H. kuda,orH. tri- flation. Newborns of H. guttulatus are also maculatus (Garcia and Hilomen-Garcia 2009; active hunters, but their capacity to attach to Gomezjurado 2009b; Murugan et al. 2009). a holdfast develops 3–4 wk after birth, and However, rotifers are not accepted by other their digestive capacity is extremely limited species (low ingestion rates), being probably during the first week, especially when fed on suboptimal for the energetic demand of juve- Artemia nauplii or metanauplii (Alvarez´ et al. niles of H. erectus, H. hippocampus,andH. gut- 2009; Planas et al. 2009a). Under these condi- tulatus (Otero et al. 2007; Gomezjurado 2009a; tions, and accompanied by a progressive deple- Planas et al. 2009a). Copepods are an alterna- tion of energetic reserves, juveniles ascend to tive/complement to Artemia and are known to the water surface, where the swim bladder enhance both survival and growth of cultured hyperinflates due to the capture of air, stop seahorses (Olivotto et al. 2008a, 2008b, 2008c; feeding, and die in only a few days. Differ- Hora and Joyeux 2009). ences in digestive capability among seahorse The effect of different types of water condi- species could be related to the lack of appro- tioning on survival and growth rate was exam- priate chitinolytic enzymes (e.g., N-acetyl-β- ined for newly hatched H. erectus juveniles glucosaminidase; Alvarez´ et al. 2009; Quintas (Alexandre and Simoes,˜ unpublished data). Sur- et al. unpublished data) and/or long diges- vival at 20 d was significantly larger in the tion periods (Murugan et al. 2009). The diges- “green” water treatment, when compared with tive capability in early developmental stages “bio-floc” and the “clear water” control. Sim- can be improved by reducing gut passage ilarly, growth rate expressed in weight and time by dispensing prey in pulses and avoid- length was significantly higher compared with ing the permanent availability of prey (Planas the control. These results are explained as an extra nutritional load of Artemia metanau- et al. unpublished data). In such cases, cope- plii continuously feeding on the live microal- pods would constitute a suitable alternative to gae present, together with a potential probiotic Artemia and/or rotifers (Olivotto et al. 2008a, effect, through the regulation and/or stabiliza- 2008b, 2008c). tion of the system’s microflora, with a conse- Different prey enrichment procedures used quent positive effect on the juvenile digestive in the feeding of seahorses provide satisfac- tract and feeding efficiency. The authors further tory results in terms of growth. In spite of hypothesized that the green color of the water the advances achieved in the rearing of some induces different intensity and distribution of seahorse species, nutritional requirements in light through the aquarium, when compared seahorses are unknown. Diets are commonly with the “clear” water control, which minimized enriched in n-3 HUFA, which are essential the concentration of food Artemia on the sur- to seahorses; however, requirements for n-3 face, reducing air bubbles formation and better HUFA and for protein have not been established consumption efficiency. yet. Nevertheless, the use of mixed diets is rec- Some seahorse species are difficult to cul- ommended to improve the nutritional status of tivate, probably due to two main factors: low the fish and to enhance the adaptation to non- digestive capacity during their early develop- living feeds (Alexandre and Simoes˜ 2009). The mental stages and a high tendency to show adaptation of juveniles to frozen food (mysids, swim bladder hyperinflation. In H. abdominalis, Acetes, amphipods, and adult Artemia) is rou- newborns are perfectly capable of digesting and tine in the commercial production of seahorses ADVANCES IN BREEDING AND REARING MARINE ORNAMENTALS 145 from day 30 to 70 posthatch (Gomezjurado transfer of culture information among seahorse 2009a, 2009b; Lin et al. 2009). species, especially between those from trop- Although grow-out is commonly carried out ical/subtropical waters to those of temperate in indoor tanks, interest for cultivating sea- waters. horses in cages is increasing in areas where ade- Although available rearing technology pro- quate natural conditions are available. A good motes noteworthy survivals for some species, example is the effort for producing H. reidi in more studies are still necessary to optimize cages placed inside aquaculture ponds in Rio culture protocols, especially addressing nutri- Grande (Brazil; Lima et al. 2009). Fish were tional and microbiological aspects. The under- raised with a minimum labor cost and fed on standing of feeding and nutritional requirements natural occurring food (copepods, amphipods, is of paramount importance for rearing suc- and caridean shrimp). The high survival rates cess. In this way, the expansion of knowl- achieved indicate good prospects for the exten- edge on the biochemical composition of natural sive culture of seahorses. prey and seahorse embryos/larvae (in the wild An important source of juvenile mortality and in captivity) will significantly enhance our are diseases caused by protozoan infestations understanding of the nutritional requirements and pathogenic bacteria (Vibrio spp., Flex- for breeding and rearing these highly popular ibacter,andMycobacterium; Blasiola 1979; marine ornamental fishes. Alcaide et al. 2001; Tendencia 2004; Failde et al. 2008; Gomezjurado 2009b; Balcazar´ et al. Marine Ornamental Invertebrates 2009, 2010a, 2010b). Balcazar´ et al. (2010b) pointed out the dominance of Rhodobacter- Over 700 marine invertebrate species are cur- aceae (Phaeobacter, Ruegeria) in the cutaneous rently traded in the marine aquarium indus- mucus of healthy adult seahorses. The bacterial try (Wabnitz et al. 2003). Corals, both soft communities recorded in the feces of adult sea- and stony species, are the most popular and horses were dominated by Vibrionaceae, being most expensive group of marine ornamental strongly influenced by the microflora of the diet invertebrates in the trade. Nonetheless, several (Balcazar´ et al. 2009). Given that the same bac- groups of marine invertebrates are also heav- terial patterns may also occur in juveniles, the ily collected, such as other cnidarians (mostly application of disinfection procedures in live sea anemones), mollusks (namely tridacnid food may contribute to specific treatments for clams and snails), decapod crustaceans (such most generic diseases. However, further studies as shrimp, crabs, and hermit crabs), and live are necessary to determine which phylogenetic rock (although not scientifically a marine groups of bacteria dominate in the associated invertebrate, it is commonly traded under microbiota, as specific groups may play with the designation of Scleractinia, along with variable physiological states (Balcazar´ et al. stony corals; Wabnitz et al. 2003). Some other 2009, 2010b). groups of ornamental invertebrates that are also In conclusion, production of seahorses on a collected for marine aquariums, although in commercial scale is a relatively recent activ- lower amounts, are polychaetes (namely tube- ity and there is good potential for culturing dwelling species commonly known as feather new species. Currently, tropical and subtrop- dusters) and echinoderms (such as brittle stars, ical species constitute the bulk of the com- sea stars, sea cucumbers, and sea urchins) mercial production of seahorses, using knowl- (Sprung 2001; Shimek 2004). edge from research efforts on these species and Most marine invertebrates are traded for other marine fish. However, not all seahorse their dazzling colorations and delicate appear- species perform similarly under culture con- ance (e.g., corals, tridacnid clams, and cleaner ditions due to interspecific differences in bio- shrimp). However, a growing number of logical and physiological characteristics. This hobbyists currently buy several marine constitutes a limiting factor that restricts the invertebrate species not for their coloration or 146 OLIVOTTO ET AL. morphology but rather as members of “clean- exporting marine ornamental species (Wabnitz up crews” employed by hobbyists as “aquarium et al. 2003). However, the prolonged harvest of janitors” to control the growth of nuisance algae live rock is considered by most researchers as a and eat food leftovers (Sprung 2002; Calfo and potentially destructive practice, which may pro- Fenner 2003). In recent years, there has been mote erosion and significantly decrease impor- a growing apprehension by researchers, pol- tant fisheries habitats (Lovell 2001). In certain icy makers, and conscientious marine aquar- regions, the collection of wild live rock has ium traders, collectors, and hobbyists on how already been banned (e.g., Florida, USA) or is dependent the marine aquarium trade still is being heavily monitored and legislated (Falls on the collection of wild specimens from coral et al. 2003; Parks et al. 2003), which opens the reefs (Wabnitz et al. 2003; Rhyne et al. 2009a, window of opportunity for the aquaculture of 2009b). The global concern on the sustainabil- live rock. ity of this industry has promoted the need for Live rock aquaculture may be as “simple” as culturing the most heavily harvested species. providing an adequate substrate for the colo- Making cultured specimens a suitable alterna- nization of adequate microorganisms as well as tive to those collected from the wild has not highly prized benthic fauna and flora (namely been an easy task, mainly because of the lack incrusting coralline algae). Live rock can be of knowledge on the reproductive and larval produced onshore, employing flow-through or biology of most traded species. This scenario recirculating systems, or off-shore in open sys- resulted in several bottlenecks that have lim- tems. Successful live rock onshore aquaculture ited culture procedures from reaching commer- facilities require large surface area and ade- cial scale. Nonetheless, researchers and traders quate light. In this way, most culture tanks are readily share the perception that the captive wide and shallow, with indoor culture facil- culture of marine ornamental invertebrates is ities relaying on fluorescent or metal halide more than a profitable venture, that it is in fact lamps to ensure proper light levels (required a need for the sustainable development of the for the growth of photosynthetic organisms, industry. This synergy between academic and namely coralline algae) and a source of heat commercial goals has already resulted in the (e.g., geothermal or electric energy) to ensure development of feasible culture protocols for optimum water temperature. Concrete race- several species (e.g., Ellis 1998, 2000; Calfo ways, as well as fiberglass tanks are commonly 2007; Calado 2008) and may well promote an employed in outdoor culture, with the shading increase in the number of species and speci- of culture tanks being a common practice to mens bred in captivity that will be made avail- avoid light and thermal stress. An erroneous able for the marine aquarium trade (Calado assumption commonly associated with the pro- 2009). duction of live rock offshore is that once the rock is on the bottom, it will fully develop without any further intervention. In fact, the site Live Rock must be regularly visited and inspected (at least Live rock is the popular name that designates once a month), namely after the occurrence of pieces of coral rock used in reef aquariums storms or hurricanes, to monitor excess algal for functional (e.g., biological filtration) and cover and sedimentation (Falls et al. 2003). aesthetic purposes. Live rock harbors a variety Some aquaculturists choose to employ nat- of invertebrates and algae (namely calcareous ural limestone rocks collected inland, whereas red algae, popularly known as coralline) as well others exclusively use manufactured substrate, as beneficial microorganisms (both nitrifying such as mixtures of limestone sand (aragonite), and denitrifying bacteria) that significantly gravel, shells, and adequate cement (Falls et al. improve water quality (Yuen et al. 2009). 2003). Despite the huge amount of anecdotal Presently, live rock represents an impor- information available online on how to “cook tant part of the revenue obtained by countries your own live rock,” there is still a lack of ADVANCES IN BREEDING AND REARING MARINE ORNAMENTALS 147 scientific studies comparing biological filtra- Corals have been cultured inland using tion efficiency of rocks prepared using differ- recirculated systems, onshore employing flow- ent materials and/or methods. Robles-Gil et al. through or recirculating systems, and off-shore (2009) performed some preliminary trials using in bottom or suspended nurseries (Calfo 2007; ecofriendly materials (white cement and sea Shafir 2006b, 2009; Shaish et al. 2008). The sand on a 2:1 mixture, plus styrofoam balls use of off-shore coral propagation structures is [0.5-mm diameter] in different percentages [0, now also widely used by commercial enter- 15, 30, and 45%]) to prepare artificial live rock. prises, although these techniques were previ- The authors evaluated the degree of coloniza- ously developed to help in the restoration of tion of artificial rock matured under controlled coral reefs (Rinkevich 1995, 2000). The use conditions in an onshore flow-through system of mid-water coral nurseries is now a popular and compared the void volume, weight, and option, as it provides improved environmental oxygen consumption among the different type conditions to growing coral fragments, namely optimized water flow, optimal light, no sedi- of manufactured rocks using natural live rock ment accumulation, and a significant decrease as a control. in the risk of predation by corallivorous With the expected increase in airfreight price organisms (Rinkevich 2005). Another approach in the years to come, imported live rock will employed to promote the growth of coral frag- become even more expensive for marine aquar- ments for coral reef restoration is the induc- ium keepers – shipping rocks by airplane will tion of mineral accretion (Hilbertz and Goreau never be an inexpensive practice. Under this 1996). This technology involves passing a low- scenario, it is likely that traders may try to voltage electrical current through a cathode and push the production of live rock closer to their an anode, which induces electrolysis of seawa- target markets (e.g., by employing inland recir- ter. This procedure triggers the accumulation culating culture systems) and decrease shipping of mineral ions dissolved in seawater within costs (taking it so close to the customer that the vicinity of submerged electrodes and their may allow its shipment by land). This economic deposition through electrochemical processes in aspect, together with the growing restrictions the structure employed as the positive electrode that most countries are implementing toward (e.g., steel bars framework, and steel mesh; the harvest of live rock, may well be the nec- Hilbertz 1992; Sabater and Yap 2004; Borell essary boost that live rock aquaculture needs et al. 2010). The electrochemical deposition of to become a more generalized practice among CaCO3 or Mg(OH)2 in the cathode strengthens those culturing marine ornamentals. coral attachment (Sabater and Yap 2004), which is a feature known to enhance the chances in survival of transplanted corals (Ammar et al. Corals 2000). This technique is yet to be applied in large scale for the production of stony corals for Corals have been propagated asexually for the marine aquarium trade, probably because of several years, either by public institutions, the existence of species-specific responses to private enterprises, or enthusiastic hobbyists. this technique and the lack of consensual opin- There are already a significant number of ion on the suitability of this methodology to manuals on asexual coral propagation (e.g., significantly improve coral growth and survival Ellis 1999; Ellis and Sharron 1999; Shafir (Borell et al. 2010). et al. 2006a; Calfo 2007). The improvements The fragmentation and growth of corals in achieved in the fragmentation of certain reef- recirculated systems located inland has been building corals allowed the production of large widely practiced both by private aquarium number of nubbins and boosted different fields reef keepers, public aquariums, and commer- of coral research, including aquaculture (Shafir cial enterprises. The information available on et al. 2001, 2003, 2006a). the suitability of the propagation techniques 148 OLIVOTTO ET AL. commonly used in this type of system is anec- eliminate the need for public aquariums to har- dotal and mostly relies on empirical, rather vest wild specimens to exhibit in their reef dis- than scientific, knowledge. Some of the most plays (Bruckner and Bruckner 2001; Delbeek relevant aspects that have been scientifically 2001; Precht 2006; Raigoza Figueras et al. addressed concerning the propagation of corals 2009). However, the use of asexually produced in recirculating systems are the types of adhe- coral fragments to recover threaten species sives and substrates employed to attach coral and/or promote reef conservation must take into transplants (Schlacher et al. 2007; Dizon et al. account restoration genetics to be truly effec- 2008), the influence of different light regimes tive (Baums 2008). SExual COral REproduc- (Reynaud et al. 2004; Schlacher et al. 2007; tion was a pioneer project which applied sexual Schutter et al. 2008), and water flow (Khalesi coral recruits on a large scale to stock public et al. 2007). aquariums in a sustainable way (Petersen et al. For 12 species of corals studied, Dizon 2006). Coral recruits were produced either from et al. (2008) showed that corals attached using larvae released from colonies stocked in pub- cyanoacrylate glue detached significantly more lic aquariums or from larvae produced from from their substrates than those attached with gametes collected in situ. This approach can epoxy putty or marine epoxy. Attachment be an economical and sustainable alternative experiments performed by Schlacher et al. for supplying corals for marine aquariums as (2007) with Acropora solitaryensis revealed well as for coral restoration (Petersen et al. that coral fragments grew equally well either in 2006, 2008a). marble or cement bases, but metal halide lamps The need to transport coral larvae over with a color temperature higher than 14,000 K large distances prompted research on this topic. promoted higher survival. The experiments by Petersen et al. (2005a) described that over 90% Schutter et al. (2008) on Galaxea fascicularis of coral larvae shipped at densities less than demonstrated that the enhancement of calcifi- 4 larvae/mL were able to survive for as much cation only seems to be mediated by photosyn- as 10 d of shipping, with best survival results thesis at lower irradiances, whereas at higher being achieved when transportation time was irradiances, skeletal growth is not limited by less than 4 d. Larvae were shipped 4–6 d after photosynthetic potential. Reynaud et al. (2004) fertilization in 10-μm-filtered seawater, with- demonstrated that Acropora verweyi fragments out the addition of oxygen or any disinfec- grew better under high light intensities and tem- tant (Petersen et al. 2005a). The development peratures (400 μmol/m2 s and 29 C) and that of ceramic tiles that maximized the settlement there was a strong correlation between growth of coral larvae was another significant break- rates and strontium uptake. The study address- through in the propagation of sexual recruits ing the effect of water flow on the growth (Petersen et al. 2005b). performance and shape of Sinularia flexibilis Although the presence of biofilms (namely showed that this coral displayed morphological patches of incrusting coralline algae and algal responses to shifts in water velocity and that the turfs) is relevant for the settlement of coral lar- highest growth rate was achieved using a water vae in a specific substrate (such as custom made velocity of 11 cm/s (Khalesi et al. 2007). It is ceramic tiles) (Petersen et al. 2005b), the physi- important to highlight that all previous results cal properties of that substrate is also important. should not be generalized for coral species other The presence of crushed coral rubble on cement than those addressed in the described studies, tiles (at a concentration of only 10%) signifi- as species-specific variations may occur for all cantly enhances the settlement of coral larvae studied parameters. (Lee et al. 2009). These findings confirm the Threatened coral species (such as the elkhorn diversity of natural reef cues that can trigger coral, Acropora palmata) are commonly cul- settlement in larval corals (Heyward and Negri tured in captivity through fragmentation to 1999). Petersen et al. (2008b) described how restore natural populations as well as to the simple addition of Artemia nauplii could ADVANCES IN BREEDING AND REARING MARINE ORNAMENTALS 149 significantly enhance the growth performance from the wild is more urgent than ever, as of young sexual recruits and help them to be it is becoming clear that there is an inter- less prone to mortality during early postsettle- action between coral reef decay and anthro- ment periods. The ongoing standardization on pogenic disturbance (e.g., collection for the the production of coral sexual recruits will cer- marine aquarium trade; Jones et al. 2008). The tainly reinforce the role that this approach is growing awareness of the vulnerability of nat- already playing toward the sustainable produc- ural populations of anemones to overharvest- tion of corals for the marine aquarium trade. ing has urged conscientious researchers, traders, and hobbyists to advocate the captive culture Anemones of the most heavily traded anemone species. Currently, there are already records of success- Anemones have always been one the most ful asexual propagation of anemones in captiv- popular marine invertebrates traded for marine ity by cutting healthy specimens longitudinally aquariums. The main reason for this popu- in half and attaching them to a suitable sub- larity is certainly the symbiotic relationship strate (Calfo 2007; Centurion´ Fernandez´ et al. displayed by anemones and clownfish (e.g., 2009). However, no study has ever addressed Amphiprion spp. and Premnas biaculeatus), in sufficient detail the optimization of asex- as well as several other invertebrates (namely ual anemone propagation (e.g., determining the shrimp; Miyagawa 1989; Fautin 1991; Giese minimum size at which an anemone can be suc- et al. 1996; Silbiger and Childress 2008; Mebs cessfully propagated, the best attachment tech- 2009). However, the most popular anemone nique, and the suitability of different materials species in the trade (e.g., Heteractis and Sti- used in the attachment base). chodactyla spp.) may be highly susceptible It is also relevant to highlight that recent to overharvesting due to their long life span, studies have provided a valuable amount of bio- slow growth rates, and low reproductive rates logical data on the reproductive biology (Scott (Shuman et al. 2005). An additional aspect of and Harrison 2007a, 2009), embryonic and lar- concern is that the intensive harvest of clown- val development (Scott and Harrison 2007b), as fish, as well as symbiotic shrimp, for the marine well as settlement and juvenile grow-out (Scott aquarium trade may also negatively affect the and Harrison 2008) of some of the most heav- survival of host anemones (Spotte 1996; Porat ily traded anemones for marine aquariums (e.g., and Chadwick-Furman 2004, 2005). It is known Entacmaea quadricolor and Heteractis cripa). that anemone cover plays a major role in the Anemones used as broodstock were collected spatial distribution of clownfish (Richardson from the wild and kept in separate flow-through 1999); thus, it was not surprising for Shuman outdoor tanks. Broodstock tank outflow pipes et al. (2005) to verify that the collection of wild were fitted with 250-μm mesh panels employed specimens for the marine aquarium trade sig- to collect spawned gametes (Scott and Harrison nificantly affected the populations of anemones 2007a). Spawned gametes were placed into and their symbiotic fish. A clear example of 60-L plastic tubs filled with seawater and excess the imbalances that an unregulated collection sperm was flushed from the tub according to the of anemones may produce is the absence of procedures described by Harrison (2006). The suitable habitat for new clownfish recruits to tubs were located indoors with a 12-h light:dark settle. As pointed by Shuman et al. (2005), photoperiod, at a temperature ranging from 23.5 the strict regulation of anemone collection to 24.5 C and were continuously aerated with would not only decrease the direct impacts on a slow stream of bubbles from Pasteur pipettes anemone populations but also decrease the cur- placed at each corner of the tub. This gentle rent pressure on the populations of symbiotic aeration ensured not only water oxygenation anemonefish. but also suitable water circulation and overall The need to manage the harvest of anemones water quality (as described by Harrison 2006). and their symbiotic fishes and invertebrates Larvae were cultured until settlement in 33-L 150 OLIVOTTO ET AL. aquaria supplied with flow-through filtered sea- male during its life cycle and later as female; water (approximately 0.6 L/min) and equipped Bybee et al. 2006a). This species displays with a settlement cage made of four, 250-μm a long gametogenic period and an extended mesh panels in the sides and a biologically con- potential spawning season, which seems to be ditioned terracotta tile in the bottom for larval correlated with water temperature (maturation settlement (Scott and Harrison 2008). Cultured appears to coincide with water temperatures of larvae were probably able to ingest nutrients 24–25 C; Bybee et al. 2007). As no significant dissolved in seawater, as well as particulate correlation was found between day length and matter, and certainly received photosynthates maturation stage of the tube worms, the same from their endosymbiotic dinoflagellates (zoox- authors suggested that water temperature may anthellae). Aquasonic™ liquid invertebrate food be the most important factor influencing matu- (Aquasonic, Wauchope, NSW, Australia) was ration and spawning. also provided to the aquariums employed in Spawning induction trials already performed anemone larviculture and peak settlement and in captivity employed several aquaria assem- metamorphosis of planulae into primary polyps bled in a flow-through system at a tem- occurred 10 d after spawning (Scott and Harri- perature of 27 C. Some of the tube worms son 2008). These promising results indicate that employed as broodstock were ablated (nearly the sexual production of anemones to supply the 1 cm of the posterior end of their body was marine aquarium trade may soon be a reality. cut). This procedure may have triggered spawning, as it promoted the release of a chemical substance from the coelom that signaled other Polychaetes mature worms to spawn (Bybee et al. 2006b), Sabellid polychaetes, popularly known as as has been recorded for nereidid polychaetes feather dusters by marine aquarium keepers, (Hardege et al. 1998). are among the 10 top-most imported ornamen- Fertilization is known to occur externally in tal invertebrates (Wabnitz et al. 2003). These S. spectabilis, with trochophore larvae emerg- organisms deserve their popularity in the hobby ing from egg cases and developing over 3 d due to their delicate appearance, stunning col- before reaching the metatrochophore stage. By oration of their tentacle crown, and their rel- day 6–7, larvae are no longer competent to atively large size. These tube worms, such swim and settle on the bottom, where they start as Sabellastarte spectabilis, commonly inhabit the construction of mucous tubes and adopt a cracks and crevices in coral reefs, which makes sedentary life style by day 7–8. No larval food their collection a challenging task. To harvest is required during this period, as S. spectabilis these organisms, collectors commonly employ larvae are lecithotrophic (they rely on inter- destructive techniques (such as the use of crow- nal energy sources, such as yolk reserves, bars) that damage delicate corals and other to fuel their larval development; Bybee et al. organisms surrounding the tube worm. As a 2006b). Grow-out trials conducted in 60-L glass consequence, studies on marine ornamental aquaria stocked with juvenile worms during tube worm reproduction and life cycle is of 100 d revealed that these organisms were able paramount importance for the establishment of to feed on a variety of live and preserved suitable culture protocols (Bybee et al. 2006a). algal forms (live I. galbana [Tahitian strain], By culturing tube worms in captivity, it will live Nannochloropsis oculata, tilapia green- be possible to decrease the fishing pressure water, preserved Isochysis and Nannochlorop- on wild populations as well as contribute to sis; Bybee et al. 2009). Diets were provided the preservation of coral reefs by avoiding the twice per week at a density of approximately use of destructive collecting practices (Bybee 1 million cells/mL. With the exception of pre- et al. 2009). served Nannochloropsis, all other tested diets Presently, it is known that S. spectabilis is promoted satisfactory juvenile growth and sur- a protandric hermaphrodite (first maturing as vival. The best results were achieved with ADVANCES IN BREEDING AND REARING MARINE ORNAMENTALS 151 live and preserved Isochrysis (survival >80%), clam culture protocols are already well estab- opening good perspectives for the commercial- lished for the most heavily traded species in the scale culture of these organisms in the near aquarium trade (e.g., Ellis 2000) and the current future (Bybee et al. 2009). percentage of cultured specimens traded is cer- Another species of tube worm commonly tainly higher than the 20% reported by Wabnitz found in the Mediterranean and the Eastern et al. (2003). At least in Europe, nearly 100% Atlantic that has great potential for marine of traded giant clams are currently captive-bred aquariums is Sabella spallanzanii (Calado and it is unlikely that this scenario may ever 2006). The reproductive biology of these organ- be reversed (imports are strongly surveyed by isms is relatively well known (Giangrande and authorities and hobbyists already prefer cul- Petraroli. 1994; Giangrande et al. 2000), specif- tured specimens, as these display higher sur- ically after their introduction in Australian vival in captivity). waters (Currie et al. 2000). The potential uti- Recent studies addressing the role that lization of S. spallanzanii for the bioremedia- incrusting coralline algae may play in the set- tion of intensive aquaculture effluents revealed tlement of larval Tridacna revealed that it may that these organisms can display remarkable attract larvae but does not promote settlement in growth rates (Giangrande et al. 2005). A signif- Tridacna squamosa (Neo et al. 2009). Another icant biomass increment was also recorded by study by Lebata-Ramos et al. (2010) confirmed Pierri et al. (2006) for juvenile tube worms cul- the potential of using giant clams produced tured extensively in suspended plastic nets com- in captivity for grow-out in ocean nurseries. monly employed for growing mussel. Instead However, this approach is unlikely to ever of using tube worms cultured extensively for be implemented in European waters (or other bioremediation or as a potential feed, it will cer- places outside the natural distribution of giant tainly be more profitable to sell part (or even clams) to supply the marine aquarium trade. all) of these specimens for the marine aquarium Nonetheless, the grow-out of small captive-bred trade! juvenile giant clams using closed recirculated systems is becoming more popular in Europe. This approach allows traders to import a large Mollusks number of small-sized giant clams, grow them Giant clams in the genus Tridacna are in captivity to larger sizes, and sell these large unquestionably the most popular mollusks in specimens for significantly higher prices. the marine aquarium trade. These emblem- Other bivalve mollusks are traded, although atic mollusks were once exposed to intensive most starve to death on the aquariums due fishing pressure (mostly for human consump- to their dependence on abundant phyto- and tion), which pushed wild populations to the zooplankton food. A clear example is the brink of extinction and prompted their list- caribbean fire clam or flame scallop, Lima ing under Appendix II of the CITES (Bell scabra, that has been extensively fished in et al. 2005). Fortunately, giant clams are one Florida, reaching landings higher than 65,000 of the best examples of successful restocking specimens in 1994 (Rhyne et al. 2009a, 2009b). programs addressing marine invertebrates (Bell The dazzling coloration of sea slugs makes et al. 2005, 2006; Gomez and Mingoa-Licuanan them highly appealing for the marine aquar- 2006). The possibility of inducing spawning ium trade. However, the strict feeding habits in captivity, the short larval development of of the most appealing specimens (e.g., Chro- giant clams, and relatively low maintenance modoris spp.) make them a poor choice, even effort required during the grow-out of juve- for the most skilled hobbyists, as they will niles (part of their nutritional needs are satisfied slowly starve to death in captivity (Sprung by their symbiotic zooxanthellae) are some of 2001; Calfo and Fenner 2003). Fortunately, a the features that made these organisms highly growing number of hobbyists are becoming suitable for aquaculture (Beckvar 1981). Giant aware that these organisms are better left in 152 OLIVOTTO ET AL. the reefs and that only a reduced number of and Astraea, with probably all traded speci- sea slug species may be successfully kept in mens from these and related genera being col- marine tanks. One of those sea slug species is lected from the wild (Wabnitz et al. 2003). Aeolidiella stephanieae (still known in the trade It is interesting to point out that at least for by its former scientific name Berghia verruci- some of these species (e.g., Trochus niloticus cornis). This species is commonly employed to and Turbo marmoratus) there are already estab- control the pest glass anemone, Aiptasia spp., lished large-scale culture protocols (Heslinga as it feeds exclusively on this prey. This sea and Hillmann 1981; Murakoshi et al. 1993). slug is very easy to breed, as it is a simul- Culture efforts have mainly addressed restock- taneous hermaphrodite that readily spawns in ing efforts of threatened populations (Amos and captivity. The embryos hatch either as a juve- Purcell, 2003; Bell et al. 2005), although the nile (direct development) or as a lecithotrophic potential use of young juveniles for the marine larva that does not require any food until meta- aquarium trade has long been recognized (Bell morphosis (Carroll and Kempf 1990). Immedi- and Gervis 1999). However, the lower value ately after settlement (or hatching when direct of the organisms commonly traded in “clean- development is displayed), young sea slugs start up crews,” when compared with other marine feeding on small glass anemones. The limiting ornamental species, makes their culture a less factor to ensure a commercial-scale production appealing activity (Calado 2009). Nonetheless, of this sea slug is to ensure that enough glass the increasing awareness of potential negative anemones are available to sustain the vora- impacts associated with the collection of algae cious juveniles! Curiously, there is a shortage grazing species from coral reefs (Rhyne et al. of A. stephanieae in Europe that could be easily 2009a, 2009b) may finally promote the appear- overcome by enthusiastic hobbyists. The culture ance of cultured snails in the marine aquarium of another anemone-eating sea slug, Spurilla trade. neapolitana, seems to be a less interesting alternative, as it has planktotrophic larva that require Decapod Crustaceans adequate feeding for at least 22 d (Schlesinger et al. 2009). The culture of marine ornamental decapods Another group of highly demanded sea slugs has experienced significant advances in the last are the sacoglossans in the genera Tridachia decade, which allowed for the development of and Elysia. These sea slugs are commonly commercial-scale culture protocols for some employed to control the growth of nuisance ornamental shrimp and crab species (Calado algae (generally sold together with other “reef 2008). The development of suitable maturation janitors”; Sprung 2002). These organisms have (Calado et al. 2007a), larviculture (Calado et al. been intensively studied by the scientific com- 2003a, 2008; Palmtag and Holt 2007; Martinez munity, as they retain functional chloroplasts et al. 2009), and grow-out systems (Penha- from the algae they ingest (Rumpho et al. 2000, Lopes et al. 2005; Calado 2008; Pimentel and 2008). Several sacoglossans have already been Calado 2009) was certainly the sign that private raised in captivity for research purposes (e.g., companies were waiting to address the culture Trowbridge 2000; Curtis et al. 2007; Rumpho of these highly prized organisms. et al. 2008), which suggests that published cul- As previously stressed by Calado et al. ture protocols may eventually be adapted to (2003b), current efforts on marine ornamental allow commercial-scale production. decapods continue to be strongly biased toward Gastropod mollusks are commonly traded for the most-valuable species (e.g., ornamental marine aquariums as part of cleaning crews shrimp in genus Lysmata and Stenopus), employed to control unwanted green algae, whereas the culture of some heavily collected diatom biofilms, and food leftovers (Sprung species used in clean-up crews (particularly her- 2002). Some of the most heavily traded species mit crabs) has had little or no attention (Calado are those from genus Trochus, Turbo, Tectus, 2009). The potential for commercial-scale ADVANCES IN BREEDING AND REARING MARINE ORNAMENTALS 153 culture of algae-eating crabs in genus Mithrac- several times a day (six to eight meals) with ulus, namely Mithraculus forceps and M. sulp- small portions of the maturation diet (daily tus, was already demonstrated in several studies adding to 10% of the shrimp wet weight) seems (Penha-Lopes et al. 2005, 2006a, 2006b; Rhyne to be a good starting point to produce large et al. 2005). However, the ongoing “competi- batches of embryos that may hatch as high- tion” from inexpensive conspecifics collected quality larvae (Calado 2008). The suitability of from the wild does not make the culture of these different live foods to newly hatched Lysmata crabs appealing for enterprises. is not consensual, with some researchers advo- For algae-eating hermit crabs (e.g., those in cating the need to provide microalgae, rotifers, genus Calcinus and Clibanarius), the present and/or copepod nauplii to newly hatched lar- scenario is even more disappointing, as no vae, whereas others argue that newly hatched study has ever addressed the suitability of Artemia nauplii may be a suitable food even these highly demanded ornamental decapods for the first larval stage (Simoes˜ et al. 2003; for culture in captivity. Available literature Palmtag and Holt 2007; Calado 2008). from ecological and behavioral studies indi- The need to provide adequate prey in the first cates that suitable shells must be available for hours to newly hatched larvae is also far from developing larvae to metamorphose (Oba and being a consensual issue, as Cunha et al. (2008) Goshima 2004), to maximize juvenile grow-out suggested that newly hatched L. amboinensis and reproduction (see review by Hazlett 1981). would be able to survive 24 h of starvation This need for a permanent supply of suitable and Calado et al. (2007b) suggests that simi- shells appears to be the main bottleneck for lar periods of posthatching starvation signifi- algae-eating hermit crab aquaculture, as produc- cantly decrease larval survival. The study by tion costs would make cultured specimens just Calado et al. (2005) demonstrated that even for too expensive to compete in the marine aquar- Lysmata species, able to develop from the first ium trade with hermits collected from the wild. to the second larval stage in the absence of food, A potential reason for the research bias it is extremely important to provide suitable toward high market value shrimp is the fact feeding immediately after hatching to prevent that reliable large-scale culture protocols are mortality prior to metamorphosis as well as the still missing for the most valuable species: occurrence of asynchronous settlement. Lysmata amboinensis, L. debelius,andSteno- Culture trials of other popular ornamental pus hispidus. Mated pairs of these species decapods (excluding Lysmata and Stenopus) can be easily kept in captivity for long have been limited to a reduced number of periods and produce consecutive batches of shrimp species, namely Thor amboinensis and viable larvae (Calado et al. 2007a; Gregati Saron marmoratus, which have been raised in et al. 2009a, 2009b). Curiously, this aspect commercial numbers by a Portuguese enter- has led researchers to neglect the relevance prise (Brian Schaff, personal communication). of maturation diets for marine ornamental Martinez et al. (2009) have also reported the shrimp broodstock maintenance in captivity. successful culture of Periclimenes pedersoni, This erroneous assumption has promoted the although further studies are required to clarify production of poor-quality larvae, which can the role of settlement cues by conspecifics and be easily ascertained by their poor survival host sea anemones. The breakthroughs achieved during early stages of larviculture trials and by Martínez Pecero et al. (2009) in the culture contrasting biochemical profiles with those dis- of several marine ornamental decapods from played by newly hatched wild larvae (Calado the Gulf of California opens good prospects et al. 2009; Tziouveli et al. 2009). Providing for the entrance of “new species” into the a diversified maturation diet (e.g., a mix of trade (e.g., Palaemonella holmesi and Per- enriched adult Artemia biomass, shrimp, mus- iclimenes lucasi). The recruitment of new sel, Cyclop-Eeze® [Argent, Redmond, WA, marine ornamental decapods for the aquarium USA], or squid) and feeding broodstock pairs trade that do not occur in the Caribbean or 154 OLIVOTTO ET AL. the Indo-Pacific (e.g., Mediterranean species, steadily, increasing in the past few years. such as L. seticaudata) may certainly help to However, cultured specimens currently offered alleviate the fishing pressure on some heavily for sale are far too few to fulfill the grow- collected species. Nonetheless, it is important to ing demand displayed by this industry. With ensure that the specimens available from those the exception of species listed under CITES new ornamental species are cultured in captivity (e.g., hard corals and giant clams), the sup- and not collected from the wild. ply of marine ornamental invertebrate species for marine aquariums still relies heavily on the harvest of wild organisms. This scenario Echinoderms is partly because of the relatively low market With the exception of the dazzling colored value at which some of the most heavily col- sea apples, Pseudocolchirus spp., and sea stars, lected specimens are traded (e.g., species sold echinoderms available in the marine aquarium in clean-up crews). Their low market value industry are commonly traded as members of makes them less appealing for enterprises rais- “clean-up crews.” Sea urchins, serpent stars ing marine ornamental invertebrates, which pre- (also known as brittle stars), and small sea fer to culture highly priced species (e.g., hard cucumbers are collected in significantly larger corals or ornamental shrimp). This trend is numbers than any other echinoderms and are particularly noticeable for invertebrate groups commonly employed by hobbyists to control with well-established culture protocols (e.g., unwanted algae, scavenge on uneaten food, algae grazing snails and echinoderms), where and/or stir up sand beds employed in mod- very little research effort would be required ern reef aquariums (Calfo and Fenner 2003). to successfully breed large numbers of speci- Given the importance that certain species of sea mens. Nonetheless, it is important to stress that cucumbers and sea urchins play for human con- adapting existing culture protocols for marine sumption and the urgent need to promote their invertebrates used for human consumption to conservation (Micael et al. 2009), there has the culture of ornamental species may not be been a growing effort toward the development as straightforward as once assumed. The early of suitable culture protocols for the most com- optimism evidenced by Fletcher et al. (1995), mercially important species (e.g., Yokota et al. toward the culture of marine ornamental deca- 2002; Hu et al. 2010). Despite the existence of pod crustaceans by adapting established pro- relevant technical information on the culture of tocols for penaeid shrimp aquaculture, clearly sea cucumbers and sea urchins, all specimens demonstrated how illusive these assumptions available for the aquarium trade are still col- can be. In fact, suitable protocols for mass rear- lected from the wild. The progress achieved ing marine ornamental shrimp are still missing in the captive culture of the highly priced (Calado 2008). Unless collecting and/or import- diadema sea urchin (Diadema antillarum;Idrisi ing restrictions are imposed on the marine et al. 2003), as well as of the green serpent aquarium trade, the low monetary value of star Ophiarachna incrassata (Fossa˚ and Nilsen many wild marine ornamental invertebrates will 2002), has not been enough to prompt the aqua- discourage and even impair the success of any culture of ornamental echinoderms. As already commercial-scale venture targeting the culture stressed for several other species employed as of those species. “janitors” in marine aquariums, the culture of these organisms is still regarded as not prof- Sustainability and Traceability Issues itable, as long as the large number of specimens The sustainability of the marine aquarium collected from the wild continue to out-price trade is commonly questioned and this indus- cultured ones (Calado 2009). try is often involved in controversy. Although In conclusion, the number of cultured marine traders try to maximize their profits, conser- ornamental invertebrate species available for vationists try to protect endangered habitats the aquarium trade has been slowly, but (namely coral reefs) and policy makers try ADVANCES IN BREEDING AND REARING MARINE ORNAMENTALS 155 to mediate these conflicts by developing suit- differences between cultured and wild corals able legislation that may protect the marine makes their differentiation a challenging task. environment, without impairing legitimate com- Potential marking solutions involving the use mercial activity (Wabnitz et al. 2003). The of barcodes attached to growing coral frag- culture of marine ornamental species is com- ments (which will eventually be embedded in monly regarded as part of the solution of the the coral skeleton as it grows) or the use of marine aquarium trade sustainability issue but artificial dyes may not be sufficient, as there is can accidentally also be the part of the prob- still a lack of knowledge to recommend a reli- lem. An example of this scenario is the harvest able marking system (CITES 2002a, 2002b). of wild postlarvae of fish and marine inver- Even with the implementation of ecocertifica- tebrates for grow-out in captivity (Hair et al. tion programs (such as those implemented by 2004; Lecchini et al. 2006; Bell et al. 2009). the Marine Aquarium Council for net caught The number and size of collected postlarvae, fishes), the traceability of marine ornamentals the by-catch of postlarvae from species with no along the chain of custody is not entirely reli- value for the aquarium trade, and the effects of removing postlarvae from the ecosystem are able (Shuman et al. 2004). some of the concerns expressed about the col- Current solutions for the traceability of lection of marine ornamental species postlarvae live fish used for human consumption (e.g., (Bell et al. 2009). With the exception of small, radio frequency identification tags; Hsu et al. isolated islands with limited postlarval recruit- 2008) are not adequate for marine ornamental ment, the responsible collection of postlarvae fishes, as these “tagged” species (e.g., Cobia appears to be adequate for most locations and and groupers) are significantly larger than the has insignificant negative impacts (Bell et al. majority of marine ornamental fishes traded in 2009). The implementation of fishing strategies the aquarium industry. DNA barcoding solu- similar to those used for the collection of spiny tions already implemented for the identifi- lobster puerulus may be enough to reach “bio- cation of marine ornamental fishes (Steinke logical neutrality” (either by operating through et al. 2009) unfortunately cannot be used a quota lease system and/or returning a number to distinguish cultured specimens from wild of juveniles to area of collection after grow-out conspecifics. The culture of specimens dis- in captivity to compensate for potential negative playing distinct colorations, which can make effects; Gardner et al. 2006). them easily differentiated from wild con- Another pertinent issue is how captive-bred, specifics (e.g., “snowflake” clownfish – captive-raised, and wild marine ornamentals predominantly white with orange blotches) may can be distinguished from each other in a rapid be an interesting way to identify marine orna- and reliable way. To address this issue, the mentals raised in captivity (Calado 2009). The CITES Coral Working Group proposed the fol- aquaculture of species never before traded for lowing source codes for hard (also known as marine aquariums may be a potential short-term stony) corals: “w” for wild, maricultured, or solution to trace cultured organisms, although farmed corals (maintenance or growth of wild coral clippings or fragments in marine-based there is always the risk that, after a certain aquaculture systems); “f” for aquacultured period, wild specimens will start to be traded corals (first-generation cultured corals produced under the label of “cultured specimens.” This in aquaculture systems); “c” for captive-bred scenario was already recorded for the Monaco or cultured corals (second-generation cultured shrimp L. seticaudata, a Mediterranean species corals produced in closed systems); and “r” that was introduced to the aquarium trade only for ranched corals (rearing of whole corals in 2005. All specimens initially traded were or larvae taken from the wild in a controlled raised in captivity, but only 1 yr after the start environment; (CITES 2002a, 2002b). However, of its commercialization, wild conspecifics were the absence of any morphological or biological already being traded as cultured specimens. 156 OLIVOTTO ET AL.

In conclusion, the sustainability of culturing involved in the collection and supply of these marine ornamentals must take into considera- remarkable organisms to the marine aquarium tion potential negative social impacts associated trade. with culture efforts being centered in import- ing and not in the exporting countries, namely Acknowledgments those in Southeast Asia and Central Paciﬁc. As already stressed by Tlusty (2002), it is The authors would like to express their grat- advisable that the know-how for the culture itude to all those who attended the session of marine ornamentals acquired by Western on ornamental species aquaculture that took countries be shared with exporting countries, place during WAS2009 in Veracruz, Mexico, to provide an alternative to impoverished local for their valuable contributions and enthusiastic populations currently depending on the col- support to our effort of sharing acquired know- lection of these marine organisms to survive. how, recruiting new researchers to develop and Tracing the origin of marine organisms is a improve culture techniques for marine orna- huge challenge (Hastein et al. 2001; Moretti mental species and contribute to the sustainabil- et al. 2003), tracing the origin of live marine ity of the marine aquarium trade. We would also ornamentals through noninvading and nondam- like to make a special thanks to Gemma Mar- aging techniques is currently an “impossible tinez and all the students of UMDI-Sisal, Fac- mission.” In conclusion, there is an urgent ultad de Ciencias, UNAM (Yucatan)´ involved need to develop innovative techniques that may in PIECEMO (Programa de Investigaciones en Ecología and Cultivo de Especies Marinas de allow traders, inspecting authorities, and hobby- Ornato) for their valuable support before and ists to reliably determine the origin of marine during the memorable session on ornamental ornamentals. species aquaculture at WAS2009.

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