Marine Ornamental Species Aquaculture

By Ricardo Calado and G. Joan Holt

The global trade of aquatic organisms for home and public aquariums, along with associated equipment and accessories, has become a multi-billion dollar industry. Aquaculture of marine ornamental species, still in its infancy, is recognized as a viable alternative to wild collection as it can supplement or replace the supply of wild caught specimens and potentially help recover natural populations through restocking.

This book collects into a single work the most up-to-date information currently available on the aquaculture of marine ornamental species. It includes the contributions of more than 50 leading scientists and experts on different topics relevant for the aquaculture of the most emblematic groups of organisms traded for reef aquariums. From clownfish, to angelfish, tangs and seahorses, as well as corals, anemones, shrimps, giant clams and several other reef organisms, all issues related with the husbandry, breeding, and trade are addressed, with explanatory schemes and illustrations being used to help in understanding the most complex topics addressed.

Marine Ornamental Species Aquaculture is a key reference for scientists and academics in research institutes and universities, public and private aquaria, as well as for hobbyists. Entrepreneurs will also find this book an important resource, as the culture of marine ornamental species is analyzed from a business oriented perspective, highlighting the risks and opportunities of commercial scale aquaculture of marine ornamentals.

• Language: English
• Publisher: Wiley
• Release date: Feb 15, 2017
• ISBN: 9781119307068

Book preview

Part I

Overview of Marine Ornamental Species Aquaculture

The marine aquarium trade has a worldwide dimension and represents a multi‐million dollars segment of the pet industry. This economic activity has continued to expand in recent years, revealing a voracious appetite for a remarkable range of species (Rhyne et al., 2012a; Rhyne et al., 2012b) that are commonly termed marine ornamentals. While at first we may think of marine ornamental species as colorful reef dwelling organisms, color is not the only feature that makes a marine organism a target of this trade. As an example, drab colored organisms that provide a service for reef aquariums, such as algae grazers and species that can control the growth of nuisance organisms, are also in high demand and heavily collected (Rhyne et al., 2009) (Chapter 1).

In the twenty‐first century, the marine ornamental trade can be described in general terms as relying on the harvest of wild specimens from coral reefs (mostly in the Indo‐Pacific region) and their exporting worldwide, mainly to the USA, EU countries, and Japan (Thornhill, 2012). The poor survival of collected specimens through the first links of a highly diffuse chain of custody, along with the dependence on the collection of specimens from the wild to supply a growing demand, continue to drive researchers to find solutions that can contribute to a more sustainable marine ornamental species trade.

Aquaculture is commonly considered as a potential way of alleviating fishing pressure on the wild populations of marine ornamentals, as the captive production of some of the most heavily collected species would certainly contribute to relieving the current fishing pressure on coral reefs (Tlusty, 2002). The aquaculture of marine ornamentals also provides researchers an excellent opportunity to gain knowledge on their life history (e.g., larval development, reproductive behaviour, age at maturity, fecundity, etc.) in order to improve the management of natural stocks. Additionally, cultured marine ornamentals could provide novelty to an industry that is always willing to pay higher prices for rare or unique specimens. This novelty is commonly associated with the collection and trade of rare and/or endemic species, which invariably drives a surge of fishing pressure targeting those specimens, promoting negative impacts on their natural populations. When culturing marine ornamentals, this novelty can be supplied through the breeding of unique hybrid organisms and/or new color morphotypes without impacting coral reefs. These unique specimens can be reliably traced in the chain of custody (Cohen et al., 2013) and contribute to a more responsible industry (Chapter 2).

With remarkable advances being achieved in the last decades on the aquaculture of marine ornamental species (Olivotto et al., 2011; Moorhead and Zeng, 2010), some constraints continue as relevant today as they were in the early 1980s. The culture of pelagic spawners is still hampered by the lack of suitable live prey for early larval life and cues triggering maturation and metamorphosis are still poorly understood for some marine ornamental species (Chapter 3). While early culture trials were not always successful, recent breakthroughs on the husbandry and production of several species and an unprecedented number of highly motivated researchers, professional marine ornamental fish breeders and hobbyists working in this field opens a window of opportunity for advancing the state of the art of marine ornamental species aquaculture to a whole new level. The role that the leading importing countries of marine ornamental species (with emphasis on the US) can play to foster the aquaculture of these organisms is also addressed, along with potential economic and environmental risks (Chapter 4).

References

Cohen, F.P.A., Valenti, W.C. & Calado, R. (2013) Traceability issues in the trade of marine ornamental species. Reviews in Fisheries Science, 21, 98–111.

Moorhead, J.A. & Zeng, C.S. (2010) Development of captive breeding techniques for marine ornamental fish: A review. Reviews in Fisheries Science, 18, 315–343.

Olivotto, I., Planas, M., Simões, N., Holt, G.J. & Calado, R. (2011) Advances in breeding and rearing marine ornamentals. Journal of the World Aquaculture Society, 42, 135–166.

Rhyne, A.L., Rotjan, R., Bruckner, A. & Tlusty, M. (2009) Crawling to collapse: ecologically unsound ornamental invertebrate fisheries. PLoS ONE, 4, e8413.

Rhyne, A.L., Tlusty, M.F. & Kaufman, L. (2012a) Long‐term trends of coral imports into the United States indicate future opportunities for ecosystem and societal benefits. Conservation Letters, 5, 478–485.

Rhyne, A.L., Tlusty, M.F., Schofield, P.J., Kaufman, L., Morris, J.A., Jr. & Bruckner, A.W. (2012b) Revealing the appetite of the marine aquarium fish trade: The volume and biodiversity of fish imported into the United States. PLoS ONE, 7, e35808.

Thornhill, D.J. (2012) Ecological impacts and practices of the coral reef wildlife trade. Defenders of Wildlife, Washington, DC.

Tlusty, M. (2002) The benefits and risks of aquacultural production for the aquarium trade. Aquaculture, 205, 203–219.

1

The Marine Ornamental Species Trade

Matthew R. Palmtag

Florida Gulf Coast University, Fort Myers, FL, USA

Abstract

Marine aquarium keeping is one of the world’s most popular pastimes. Aquatic life is supplied through the marine ornamental species trade which consists of businesses that collect or culture livestock, transport, maintain, and trade until it reaches the consumer. Over 46,000,000 organisms representing 2500 species are traded annually with a value exceeding US$ 300,000,000. The Philippines and Indonesia supply the majority of livestock, with most specimens being consumed by the USA, Europe, and Japan. Unfortunately, irresponsible parties have caused coral reef destruction through negligent collection practices. Trade professionals and environmental advocates have employed a variety of measures to counteract the malpractice. Production of ornamentals through aquaculture is a leading solution that could reduce destruction by decreasing the need for wild livestock and providing an alternative profession for collectors. To achieve this economic–environmental balance, aquaculture capabilities require improvement through scientific research; additionally the technology must be accessible to countries that depend on collection.

Keywords: Aquaculture; collection of marine ornamentals; environmental impact; sustainability

1.1 Introduction

The marine ornamental species trade is a global industry that provides wild‐caught and aquacultured marine life for consumers. Marine ornamental livestock is supplied to consumers through an international network of artisans, aquaculturists, entrepreneurs, and businesses. Consumer groups primarily consist of home aquarists and public aquaria who maintain marine ornamental livestock for the purposes of aesthetic display, hobby, educational purposes, and pet companionship. This chapter is an overview of the history, economics, organisms, organization, and environmental implications of the marine ornamental species trade.

Home aquarists are the largest consumer of marine ornamental species. They are a diverse group in respect to the species and assemblages of organisms that they desire and care for. Some keep a few small fish, such as clownfish or damselfish (family Pomacentridae), in a small aquarium (e.g., 40 L). Others keep large predatory fish, such as sharks or moray eels, in enormous home aquarium (e.g., 4000 L). Many aquarists maintain a fish only tank, which is typically adorned with a community of fish and decorative rocks. There is also the specialty tank, aquarist who cares for an individual or group of organisms that require special conditions, such as seahorses or jellyfish. Today, the most popular version of the marine home aquarium is the reef tank. The reef tank simulates a natural reef environment, typically a tropical coral reef, and features a diverse assemblage of invertebrates as well as fish.

1.2 History

Fascination with marine life and the practice of keeping aquatic life in captivity can be traced to ancient civilizations. Evidence suggests that before 2000 BC the Assyrians, Egyptians, and Chinese cared for captive fish for the purpose of maintaining a readily available food source, as well as for religious reasons. In ancient China and Egypt, captive fish began to take on an additional decorative role and likely became status symbols (Nash, 2011). Wealthy Romans continued this trend during the first century BC. They constructed elaborate sea‐side pools, vivarie piscinae, to maintain live seafood. The pools eventually acquired the added purposes of entertainment, social status symbols, homes for aquatic pets, and served as social gathering sites (Higginbotham, 1997). The Chinese forged the path for the aquatic ornamental species trade. Historic Chinese literature suggests that they identified ornamental phenotypes of carps (Carassius auratus), now known as goldfish, between 265 and 316 AD (Matsui, 1971). Goldfish were domesticated between 618 and 906 AD; culturing them became popular in Chinese society and they were also used as a tradable commodity (Fossa, 2004). In the 1500s, goldfish were exported to Japan and later to Europe in the 1700s, where they were kept in fish bowls and quickly became a ubiquitous pet (Klee, 1987).

In the 1840s British naturalists collected local marine life, such as sponges (poriferans), and maintained them in glass containers for observation (Johnston, 1842). Soon afterward, the first public marine aquarium exhibit was introduced at the Zoological Gardens of Regent’s Park in London. The aquaria in this exhibit may have been the first to resemble a contemporary reef tank, as they housed an infrastructure of rock and sand with a diverse assemblage of temperate reef dwelling organisms including fish, mollusks, crustaceans, gastropods, echinoderms, anemones, and algae among others (The Aquatic Vivarium). Goldfish made their way into the homes of Americans during the 1850s and articles written for home aquarists in 1857 indicated that the hobby thrived (Klee, 1987). Global expansion of the freshwater aquarium hobby stimulated demand for more and different types of exotic organisms, especially fish. During the late 1800s and early 1900s, an increasing diversity of ornamental species were collected and exported from South America and South Asia, including the chanchito (Australoheros facetus) and paradise fish (Macropodus operculus) (Smith, 1902). Fish were imported to North America and Europe by steam ship and rail and maintained in metal cans during transit (Klee, 1987). Steam ships and trains provided less than ideal accommodations to sustain sensitive species. Air travel and improved airport infrastructure of the 1930s facilitated transport, as well as the volume and number of species available in the trade. By 1935, aquarium publications reported the prevalence of over two hundred species in the freshwater aquarium trade (Innes, 1935).

The expanding interests of home aquarists eventually encompassed the marine environment, and the marine ornamental species trade was born. Sri Lanka, already serving as a hub for freshwater ornamental exportation, became the world’s first commercial site for marine ornamental species export from the 1930s through the 1950s. Collection and export locations expanded to the Philippines and Hawaii in the 1950s and 1960s. The trade was improved by the use of polyethylene bags to package live organisms for shipment, which significantly reduced the weight and cost of freight (Lim et al., 2003). A handful of species, such as clownfish and damselfish, made their way into the homes of aquarists (Innes, 1966).

By the mid‐1950s public aquaria were maintaining and propagating coral. Soon home aquarists were doing the same, and coral too became a staple of the trade (Delbeek, 2001). Live rock (limestone encrusted in a benthic assemblage of invertebrates) also became a popular commodity; it had the dual purpose of decoration, as well as assisting with filtration of the aquarium (Carlson, 1999). Invertebrates other than coral, such as crabs, clams, mussels, oysters, snails, and anemones, also became popular (Axelrod & Shultz, 1978). The growth of the trade in the late 1960s and 1970s was catalyzed by the commercial development of synthetic sea salt, which allowed legions of enthusiasts who did not live near the sea the opportunity to maintain a marine aquarium (Moe, 1992). Steady technological advances in filtration, lighting, temperature control, water chemistry analysis, and husbandry techniques continued to increase the accessibility and popularity of the hobby throughout the 1970s and 1980s (Carlson, 1999).

1.3 Economics of Trade

Recent studies conducted from 1997–2012 estimated that more than 2500 species comprise the marine ornamental species trade. These consist of more than 1800 fish and over 700 invertebrate species, including but not limited to cnidarians, mollusks, arthropods, echinoderms, annelids, and poriferans (Wabnitz et al., 2003; Rhyne et al., 2012). The most recent global estimate indicates that 46,000,000 individual organisms are collected and sold annually to approximately 2,000,000 hobbyists worldwide, with a corresponding value exceeding US$ 300,000,000 (Wabnitz et al., 2003). The Philippines, Indonesia, Solomon Islands, Sri Lanka, Australia, Fiji, the Maldives, and Palau, export the overwhelming majority of livestock. The USA is the most prolific importer and consumer; other major importers include the United Kingdom, the Netherlands, France, Germany, Taiwan, Japan, China, and Italy (Wabnitz et al., 2003).

1.4 Species of Trade

The marine ornamental species trade is composed of an incredible diversity of organisms, but popular taxonomic groups represent the majority of species traded. More than twenty million fish are traded annually, with pomacentrids (damselfish and clownfish) representing nearly half by volume (Rhyne et al., 2012). Coral and live rock have shown the most rapid growth in popularity in recent history, with over ten million corals and millions of kilograms of live rock being exported annually (Wabnitz et al., 2003). A total of 140 species of stony corals (order Scleractinia) dominate the coral trade while approximately 400,000 individual soft corals, representing 61 species, are also traded each year (Wabnitz et al., 2003) (Table 1.1). Sea fans also represent a small proportion of the trade.

Table 1.1 Most popular marine ornamental fish and corals (after Wabnitz et al., 2003; Rhyne et al., 2012).

About 500 species of invertebrates other than coral are popular; roughly ten million individuals are traded each year. These include mollusks (gastropods, bivalves, and cephalopods), echinoderms (starfish, urchins, and sea cucumbers), actinarians (sea anemones), crustaceans (shrimp, crabs, and lobsters), polychaetes (feather dusters and Christmas tree worms) and poriferans (sponges). Of this group, cleaner shrimp of genus Lysmata, boxing shrimp of genus Stenopus, and sea anemones of genus Heteractis compose about 15% of all non‐coral invertebrates traded (Wabnitz et al., 2003). Certain invertebrates are included in aquaria for aesthetics, however, many are chosen for the service that they provide for the aquarium. Often referred to as the cleanup crew, these invertebrates may graze on nuisance algae, sift the substrate, filter, scavenge, prey upon nuisance species, clean parasites from cohorts, or provide habitat (Calado et al., 2003; Rhyne et al., 2009).

1.5 Organization of Trade

The journey of a marine ornamental from its native habitat to the home aquarium requires the services of a variety of players aligned in a complex chain. Approximately 90% of all marine ornamentals in the trade are captured from the wild, a practice that requires the skills and experience of artisan collectors. Live rock and sessile or slow moving invertebrates are typically collected by finding and removing them from their location. The collection of fish and fast moving invertebrates requires snorkeling gear or underwater breathing devices, as well as tools such as nets, slurp guns, traps, hook and line or sedatives. Collectors either work for, or sell their catch to, a wholesaler, who stockpiles and prepares livestock for export. The wholesaler acts as an exporter or sells the livestock to one. Export normally requires government‐mandated permits specific to the locale and import destination, veterinary inspection, treatment of livestock to prepare it for an international flight, and packaging (Olivier, 2003).

Exporters ship livestock by air to importers in destination countries; in some cases the exporter and importer are housed within one company. When a shipment arrives at its destination, importers unpack the livestock, inspect its health, and acclimatize it within a temporary holding facility (Wabnitz et al., 2003). At this point, various importers may repackage the livestock for shipment to another destination, sell it to a wholesaler, or sell directly to a retail outlet (Olivier, 2003). Parties acting as wholesalers also acclimate the livestock and either sell it to a retail outlet or directly to home aquarists via the internet (Larkin & Degner, 2001). Public aquaria and retailers can purchase livestock directly from wholesalers and sometimes from importers. Home aquarists typically can purchase livestock only from a retailer with a physical store or an importer, wholesaler, or retailer that peddles livestock through the internet (Zajicek et al., 2009).

Transshipping, which transpired in the 1970s, is an alternative pathway to trade reducing the number of middlemen involved. A transshipper amasses livestock orders from a consortium of retailers (and sometimes wholesalers) at the import destination, places the order with an exporter, and distributes the order to the consortium upon its arrival (Olivier, 2003). The purchasers of transshipped livestock are often required to pick the shipment up from the airport with no guarantee that the shipment will arrive alive. Destination site retailers and wholesalers save money by avoiding the markup that importers charge (and wholesalers), but lose the timely acclimation and husbandry benefits that they provide. While handling costs are reduced, the amount of time livestock spends packaged in transit increases, which has led to increased acclimation time, disease, and mortality (Olivier, 2003). In recent years, governments and transshipping companies have made progressive efforts to reduce the mortality rates associated with transshipping. Governments have employed quality control laws and licensing to discourage irresponsible practices. Likewise, transshipping companies have sought greater responsibility by guaranteeing the live arrival and quality of their livestock (Olivier, 2003).

1.6 Environmental Impact

The collection of wild marine ornamentals has taken a damaging toll on the environment. Destructive collection practices and nonexistent or ineffective fisheries management have led to a significant amount of coral reef habitat destruction and overfishing (McManus et al., 1997). This outcome has also affected the reputations of collectors as a whole, even though the majority are conservation‐minded collectors who harvest ornamentals sustainably (Dawes, 2003). A significant minority of collectors have resorted to highly damaging collection techniques that improve their catch per unit effort while imperiling the reefs that reward them with their bounty. One of the most notorious techniques involves in situ sedation of fish by means of a variety of chemicals, including plant extracts, bleach, and most notably, cyanide (Bruckner, 2001). Cyanide, banned globally for this purpose, the most popular sedative is linked by abundant evidence to coral bleaching and mass mortality of non‐targeted species. The effects of cyanide extend far beyond the reef; fish captured using cyanide suffer greatly increased mortality rates (Rubec, 1986). The use of cyanide fuels a sinister cycle of habitat destruction and accelerated demand to replace livestock lost due to high post‐collection mortality.

Physical destruction of reefs and ill‐managed removal of livestock is another hazardous result of irresponsible collection. Some collectors have dismembered corals to capture fish that have taken refuge in them (Pet‐Soede & Erdmann, 1998). Fishing nets, which are typically used in an environmentally friendly manner, can become entangled in coral and lead to mortality. Another practice is to beat a coral with a blunt object to drive sheltered fish from its protection (Wood, 2001). The harvest of live rock and coral often requires the force of a hammer, chisel, crow bar, or screw driver and results in a direct loss of habitat (Bruckner, 2001). Coral and live rock harvest can be sustainable but if not managed properly, these sites may become cloaked in turf algae, eliminating much of the productivity of the once thriving ecosystem (McClanahan, 1995). Sustained removal of select species, particular sex, or life stage can compromise the reproductive capability of the species or stress non‐target species causing imbalance to the local ecosystem (Sadovy & Vincent, 2006).

The majority of coral reefs are classified as threatened. The greatest threats result from coastal development, climate change, destructive food fishing methods, pollution, terrestrial runoff, and ocean acidification. The effects of the marine ornamental trade are miniscule by comparison, yet significant nonetheless (McManus et al., 1997). The gravity of the situation may lead one to believe that elimination of the trade would improve the well‐being of coral reefs. Trade professionals and scientists that study coral reefs and the trade, present counter arguments. They point out that public aquariums and conscientious aquarists play a pivotal role in gaining the attention of the general public and educating them about anthropogenic impacts on coral reefs (Tlusty et al., 2013). Ending the trade could popularize a black market that promotes destructive collection techniques and leaves no potential for managed sustainable harvest (Shuman et al., 2004). Marine ornamentals are the most valuable consumer goods that exist in a coral reef; well‐managed, sustainable collection provides communities with an incentive for protecting the resource and sustainably using it (Wabnitz et al., 2003). In the absence of a viable trade, many communities could turn to catastrophically destructive practices such as excavating coral reefs to produce building materials (Teitelbaum et al., 2010).

The marine ornamental industry together with environmental protection advocates, have supported a variety of measures to counteract the negative impacts that negligent parties have caused. Environmental protection organizations have conducted grassroots efforts to educate collectors about the consequences of irresponsible practices and have provided instruction on how to capture and care for livestock using environmentally‐friendly methods (Rubec, 1986). Several countries have employed collection management plans with varying success. These efforts have included specified collection zones, marine protected areas, no‐catch zones, collection area rotations, bans, quotas, size limits, sex restrictions, access limitations, collection equipment restrictions, and exportation limits. These actions have been successful in some areas while ineffective in others. Failure has often been due to noncompliance, coupled with the inability of governing bodies to enforce restrictions (Sadovy & Vincent, 2006). Another strategy has been the education of consumers regarding destructive fishing techniques and the corresponding environmental impacts. Organizations, such as The Marine Aquarium Council (MAC) have facilitated this effort by providing the consumer with the opportunity to promote and support sustainable practices (Shuman et al., 2004). MAC certifies livestock at the retail level under the following stipulations: livestock was collected at a locale that designed and adhered to a certified management plan, and livestock was captured, maintained, and transported throughout the chain of custody using practices that minimize mortality and are deemed environmentally sustainable and humane (MAC, 2001a, b, c).

1.7 Marine Ornamentals Aquaculture

Expansion of the marine ornamental aquaculture industry can impart sustainability to the trade. Aquaculture has the potential to reduce the trade’s dependence on wild collection through the sustainable production of livestock (Figures 1.1 and 1.2) (Palmtag & Holt, 2007). Reduced need of wild livestock could decrease the prevalence of destructive collection practices by incentivizing the use of sustainable collection which provide a competitive environmentally friendly product. The aquaculture industry has its detractors as some methodologies are not sustainable. Additionally, aquaculture production in import locations could reduce or eliminate the need for collectors, resulting in unemployment and reduced motivation for some local communities to protect the livestock’s habitat, potentially resorting to more destructive uses of the reef (Teitelbaum et al., 2010). Many scientists and trade professionals argue that the industry has far more benefits than disadvantages. Sustainable aquaculture practices are well‐developed and prevail in many countries throughout the world (Frankic & Hershner, 2003). It is improbable that aquaculture could fully replace the wild collection trade: under the appropriate conditions, sustainable production of marine ornamentals could be carried out simultaneously in popular collection areas (Teitelbaum et al., 2010). This dynamic could provide new employment opportunities, improve awareness of sustainable practices, and enhance the economic infrastructure originally developed exclusively for wild collection (Pomeroy et al., 2006). Aquacultured livestock suffer significantly less mortality than wild harvested, which reduces the need to resupply ornamentals that have succumb to stress due to wild collection. Aquaculture production could also preserve genetic attributes of endangered populations, preserve species, and serve stock enhancement capabilities (Tlusty et al., 2013).

Figure 1.1 Candy basslet (Liopropoma carmabi). (a) Adult pair of candy basslet; and (b) 58‐day‐old larvae raised by Todd Gardner at Atlantis Marine World in Long Island, New York in 2010.

Figure 1.2 Fire shrimp (Lysmata debelius) raised by Matthew R. Palmtag and Dr. Joan Holt in the late 1990s at the University of Texas Marine Science Institute in Port Aransas, Texas, USA. (a) 68‐day‐old post‐larvae; (b) 83‐day‐old newly metamorphose juvenile; and (c) adult shrimp.

The first cultured marine ornamentals were reared in the 1950s and 1960s, soon followed by the first documented marine ornamental aquaculture company Tropicornium, a coral aquaculture enterprise in Romulus, Michigan, USA (Innes, 1966; Delbeek, 2001). One of the defining achievements that catalyzed the development of the marine ornamental aquaculture industry was Martin Moe’s success in rearing clownfish (Amphiprion ocellaris) in captivity in the early 1970s. Moe then spearheaded the first commercial production of marine ornamental fish with the inception of Aqualife Research Corporation in Walkers Cay, Bahamas in 1972 (Tellock, 1996). Several marine ornamental aquaculture ventures have come and gone since the 1970s, and many thrive today. One of the greatest disparities between the contemporary freshwater and marine ornamental fish trades has been the corresponding success of the aquaculture industry component. Approximately 90% of freshwater ornamental species traded are produced through aquaculture while less than 10% of marine species are cultured. The limited success of the marine ornamental aquaculture industry can be attributed to a variety of causes; two of the foremost are the complex nutrition of early life stages and the husbandry requirements of many popular species (Olivotto et al., 2011). The progress that has been achieved and the obstacles that lie ahead are the focus of this book.

The collective efforts of research scientists, aquaculture professionals, professional and home aquarists over the last six decades have resulted in the successful culture of hundreds of marine ornamental species (Townsend, 2011). Many of these species have been raised with limited success; therefore the majority of them are not commercially viable. Lagging far behind the relative success of the freshwater ornamental aquaculture industry, it is fair to say that the marine component remains in its early stages (Holt, 2003). Yet, the industry thrives through a variety of means. Many proprietors culture marine ornamentals in intensive closed systems in more economically developed countries (MEDC). Several extensive operations also exist worldwide; these ventures utilize ponds in tropical locations to support the feeding and husbandry requirements of the livestock. Another means is to farm ornamentals extensively in their natural habitat; this is a popular and effective method often used for clams, coral, and live rock. A cottage industry exists where an individual or a family produces marine ornamentals intensively or extensively at their homes. A hybrid method also exists, where premarket size larval and juvenile livestock are collected and then raised in captivity until they reach marketable size (Lecchini et al., 2006).

Some exciting new developments involving aquaculture have been introduced to the trade recently. Several aquaculture businesses produce novel phenotypes through artificial selection. This is not a new concept; the freshwater aquaculture industry has practiced this for more than a thousand years (Fosså, 2004). Production of artificially selected marine ornamentals has arisen with the relatively recent capability to culture marine ornamentals in captivity. On another front, improved accessibility and technological advances of submersibles and deep‐diving, self‐contained breathing devices have enabled collectors and deep water enthusiasts to introduce deep‐dwelling species to the trade. The availability of these species to the aquarist are often limited and they typically command an expensive price; some consumers are willing to offer as much as US$ 30,000 for one specimen (Kaneshiro, 2012). To date, a handful of marine ornamental aquaculturists have successfully cultured several of these species (T. Gardner, pers. comm.).

1.8 Conclusions

Aquarium keeping is one of the world’s most popular pastimes and it continues to grow in popularity, especially in the marine component (Livengood & Chapman, 2007). The continued viability of the marine ornamental species trade will undoubtedly depend on the ability to operate in a sustainable manner. Marine ornamental aquaculture has an opportunity to play an instrumental role in achieving a balance between economic feasibility and environmentally sound practice. Research has and will continue to play a key role in developing the capability of the industry to produce a greater number of species and improve efficiency and sustainability. This balance cannot be reached by the enterprises operating in MEDCs alone. To strike a global economic–environmental balance, effective methodologies established through sound scientific research must be published and then employed by the communities that depend on collecting wild livestock (Palmtag & Holt, 2001; Pomeroy et al., 2006).

Acknowledgements

I am grateful to my wife Dr. Rebecca Waggett for her diverse array of assistance. I thank Dr. Joan Holt for her consummate mentorship and support with this project. I express gratitude to colleagues Dr. William Sanders and Todd Gardner for their assistance with editing, and I thank Florida Gulf Coast University for their continued support.

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2

The Need for Cultured Specimens

Ricardo Calado

Departmento de Biologia & CESAM, Universidade de Aveiro, Campus Universitário de Santiago, Aveiro, Portugal

Abstract

The aquaculture of marine ornamental species is commonly advocated as the most suitable alternative to the harvest of wild specimens from coral reefs to fulfil the demand of the marine aquarium trade. In this way, while cultured specimens are certainly needed in this industry, not all species traded should be (or are even suitable) for culture in captivity. If a fishery targeting one or more marine ornamental species is performed in a regulated way, using sustainable practices and contributing to the economic and social sustainability of local populations, the aquaculture of those species should not be promoted. Decision trees and SWOT analysis can play a key role when deciding what species to culture, where and how. The aquaculture of rare and/or endangered species should also be carefully analysed, as an unsuitable supply of cultured specimens may contribute to an increase of the fishing effort already targeting those species. The breeding of designer fish and use of new technological solutions for growing photosynthetic organisms (such as corals) open a new window of opportunity for those culturing marine ornamental species.

Keywords: Decision tree; designer fish; SWOT analysis; sustainability

2.1 Introduction

The sustainability and environmental impact of the marine aquarium trade is commonly questioned due to its heavy dependence on the collection of specimens from the wild to supply an ever growing demand worldwide. Indeed, several studies have already highlighted how the unregulated collection of some marine ornamental fish and invertebrates may be negatively impacting their natural populations (Lunn & Moreau, 2004; Shuman et al., 2005). The over harvesting of certain species, as well as the use of destructive fishing practices (e.g., cyanide fishing), may negatively affect not only the species being targeted for marine aquariums, but other species as well. Nonetheless, it is important to highlight that labeling the collection of marine ornamentals from the wild to supply the aquarium trade as a predatory and destructive activity is not only erroneous but a dishonest claim as well. There are several scientific works reporting that well managed fisheries targeting marine ornamentals may not significantly impact natural populations and even contribute to a growing awareness of the need to preserve marine ecosystems (Williams et al., 2009; Dee et al., 2014). The positive social impacts associated with the collection of marine ornamentals must also be considered, as this activity may generate jobs and help to alleviate poverty in local communities with little or no alternative sources of income. Additionally, the collection of marine ornamentals from the wild is likely to be the economic activity able to aggregate the highest added value to most reef species, with emphasis on those that are solely used to supply this industry. Indeed, several nations already rank the collection and culture of marine ornamentals as key sectors in their economic activity, playing a growing role in the exports of these countries.

2.2 Should All Marine Ornamental Species be Cultured?

The above being said, it is legitimate to ask: is there a need for cultured specimens in the marine aquarium trade? Certainly yes! Does this mean that the collection of specimens from the wild should be banned? No; only when this collection is negatively influencing (or may negatively impact) the target species (or any other non‐target species) should this practice be prohibited. Should all traded species be cultured in captivity? Not necessarily. If the collection of specimens from the wild is performed in a regulated way and that fishery can be reliably labeled as sustainable, contributing to the economic and social sustainability of local populations, than the culture of those species should not be promoted.

The social dimension of the marine aquarium trade, a feature commonly overlooked by fundamental environmentalists advocating the ban of any fishery to support this industry, also acts as a driver for local populations to oppose the culture of marine ornamentals. Those for whom the collection of marine ornamentals is the sole source of income have legitimate concerns that once the species they collect are produced elsewhere (e.g., in importing countries) their activity will cease. To prevent such scenarios it is important that those collectors are given the chance to shift their activity from harvesting to the production of the target marine ornamental species.

The work by Tlusty (2002) entitled The benefits and risks of aquacultural production for the aquarium trade provides an excellent starting point for those willing to determine if the culture of a given marine ornamental species is a suitable option. Responsible producers of marine ornamental species, both in exporting and importing countries, should perform a detailed risk analysis listing the strengths (S), weaknesses (W), opportunities (O) and threats (T) of their endeavor. While S refers to the characteristics of the culture of the species that may result into a competitive advantage, W refers to potential disadvantages associated with the culture of that species. Both S and W have an internal origin and refer to the culture initiative to be developed. On the other hand, O refers to external elements that the culture initiative may explore to its advantage and T to external elements that may negatively affect it. Both O and T have an external origin and refer to the economic, ecological and social environment of the project. Only after performing such exercise, commonly termed as a SWOT analysis (see Figure 2.1), should one decide to give a green or a red light to an initiative targeting the aquaculture of a marine ornamental species.

SWOT (Strengths, Weaknesses, Opportunities and Threats) analysis template.

Figure 2.1 SWOT (Strengths, Weaknesses, Opportunities and Threats) analysis on the construction of a recirculated clownfish hatchery in the EU.

When supplying the marine aquarium trade with cultured specimens, it is commonly overlooked how this activity will impact the fishing pressure on wild population of the species being cultured. As already discussed by Tlusty (2002), three different scenarios may occur: (1) market demand is fulfilled by the culture of the target species, with supply being greater than demand at a given point in time; then aquaculture efforts will eventually promote a decrease in the capture of wild specimens; (2) if the supply of the cultured species largely surpasses demand, then the impact on wild populations will rapidly decrease; and (3) if demand for a given species is considerably higher than the supply of cultured specimens, then an intensification of the fishing effort targeting wild populations will occur. The last scenario described is particularly important when introducing new species to the trade, namely if they are particularly vulnerable to over harvesting (e.g., rare endemic species, species that produce a low number of offspring).

A nice example of how good intentions can go wrong is that of the aquaculture of the Monaco shrimp (Lysmata seticaudata). One of the goals of the aquaculture of this Mediterranean species, which previously had no commercial value, was to minimize the fishing effort targeting Caribbean populations of peppermint shrimp (Lysmata spp.) employed to control pest glass anemones Aiptasia spp. While cultured specimens of Lysmata seticaudata were highly effective in the control of these pests (Calado & Narciso, 2005) and produced by the thousands, it was only a matter of months until specimens collected from the wild entered the aquarium trade in Europe (Calado, 2008). In certain occasions, wild specimens were even mislabeled and sold as being cultured. At present, wild populations of this species continue to be fished solely to supply the marine aquarium trade, with any negative impacts associated with this practice still being ignored.

Tlusty et al. (2013) provided a decision tree (Figure 2.2) that may be useful when evaluating the suitability of a given species to enter the marine aquarium trade (with emphasis on key issues such as its conservation status and potential to become invasive) and whether that species should be supplied to the industry through aquaculture or fisheries targeting wild populations. By following this decision tree, breeders of marine ornamental species will be able to make more conscientious choices at the time of selecting suitable candidate species for aquaculture and contribute to the sustainability of the industry.

Image described by caption.

Figure 2.2 Decision tree to help with the evaluation of the suitability of a given marine species to enter the marine aquarium trade (left side) and whether traded specimens should be collected from the wild or cultured (right side). Sp on the decision arrows indicates that specialists in the hobby have the ability to care for these animals.

Reproduced from Tlusty et al. (2013) with permission from John Wiley and Sons.

2.3 Highly Demanded Marine Ornamental Species Cultured in Captivity

With the advances in the aquaculture of marine ornamentals (Moorhead & Zeng, 2010; Olivotto et al., 2011) a number of species cultured in captivity are now in high demand by this industry. An obvious example is that of clownfish within the genus Amphiprion, namely A. ocellaris, with a remarkable range of unique color morphotypes being supplied to the trade solely through cultured specimens. It is possible to say that we have entered the era of designer clownfish, with commercial breeders advocating WYSIWYG (What You See Is What You Get) policies on their websites to ensure client satisfaction. New color varieties can fetch several hundreds of dollars per specimen, with breeding pairs of those varieties reaching premium values up to several thousands of dollars. Another interesting example is that of lightning maroon clownfish (Premnas biaculeatus). The rare phenotype exhibited by a very limited number of specimens collected from the wild, with solid white bands commonly displayed in the form of a lightning bolt, sparked the interest of breeders all over the world. Only through aquaculture could specimens with this remarkable pattern be available in the marine aquarium trade. There is no need to stress that the value these specimens continue to reach in the industry make their breeding a very appealing endeavor. It is now evident that a process of clownfish guppification is currently on‐going in marine ornamental fish culture. This term has become popular among marine ornamental fish breeders and makes an analogy to what happened to the freshwater guppy (Poecilia reticulata), in the pursuit of even more extreme color and shape diversity through selective breeding. Ultimately, as in the guppy, the varieties arising in cultured specimens will attain such a level that they will vaguely resemble (if at all) the wild morphotype of the species.

The production of hybrids is also an interesting niche market for ornamental fish breeders. While hybrids of some popular marine ornamental fish species are known to occur in the wild (Pyle & Randall, 1994), hybridizing geographically isolated species produces unique specimens that may only be available to the marine aquarium trade through aquaculture. A nice example on this topic is the hybridization in captivity of two geographically isolated pygmy angelfish, Centropyge fisheri vs. C. resplendens (Baensch & Tamaru, 2009). These remarkable specimens can fetch high market prices and the traceability problems so commonly affecting marine ornamentals (Cohen et al., 2013) are certainly not an issue for hybrid fish production.

Cultured seahorses (F2 generation or greater) are also highly demanded marine ornamentals. The shift in demand from wild to cultured seahorses was largely driven by the listing of all species within the genus Hippocampus on the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) Appendix II (listing species perceived as vulnerable, but less likely to be threatened with extinction; these species can be traded with an export permit as long as reliable evidence show that their harvesting is not detrimental to wild population) (Evanson et al., 2011). Cultured seahorses display remarkable colors and suitable sizes for stocking in small sized private aquariums, plus they do not depend on live prey to thrive in captivity as they readily accept frozen diets (some breeders even sell their special frozen diet to be supplied to their cultured specimens) (Koldewey & Martin‐Smith, 2010).

Cultured corals are also increasingly popular in the industry, not only due to the growing awareness of the negative impacts that over‐harvesting of these organisms may have on coral reefs, but also due to the remarkable colorations one may achieve when culturing these organisms ex situ. Recent studies have shown that contrasting light spectra from artificial light sources, such as those from T5 fluorescent lamps, light emitting diodes (LED) and light emitting plasma (LEP), may significantly affect the growth and color of hard corals (Rocha et al., 2013), as well as their macro and microstructure (Rocha et al., 2014). In the future, by fine tuning the spectra of light, coral breeders may be able to favor growth and simultaneously enhance the color of cultured specimens.

Marine ornamental species displaying short life cycles are commonly cultured to ensure that public or private aquariums can continue to display them. A nice example is that of jellyfish, which commonly have lifespans of several months to a few years (Lucas, 2001). Once solely displayed in public aquariums, the mesmerizing beauty of jellyfishes can now also be admired in private aquariums illuminated with state of the art LED technology. Given their lifespan, a permanent supply of specimens is commonly required to assure that displays are kept stocked as desired. This constraint is in fact an excellent business opportunity for some jellyfish breeders.

2.4 Conclusions

Overall, it is unquestionable that a sustainable marine aquarium trade may only be possible if the aquaculture of marine ornamental species continues to expand and a larger proportion of the wild organisms currently being traded are replaced by cultured specimens. Whether captive bred or captive raised (born from larvae spawned in captivity or in the wild, respectively), cultured marine ornamentals must be valued by hobbyists, who ultimately must be willing to pay a higher price for these specimens. If it is true that not all marine ornamentals should be cultured, hobbyists must also be conscious that preferring less expensive organisms collected from the wild using unsustainable practices may cause this industry, as we presently know it, to collapse. Restricting or even banning the harvest of some marine ornamental species from the wild to supply the marine aquarium trade is becoming a growing option when advocating reef conservation (Dee et al., 2014). If all those in the marine aquarium trade look the other way and continue to rely on the harvesting of inexpensive specimens from the wild, it is possible that in the near future the collection of several banner species in the trade will be severely restricted, or even prohibited. This scenario is even more likely to occur for species known to display poor survival in captivity and/or along the supply chain. Wild populations of these species are probably already overfished, as more specimens than those truly needed to fulfil demand must be collected to compensate for all losses along the supply chain. These species will likely be the main targets for future aquaculture efforts, as a drop in the availability of large numbers of inexpensive wild specimens will prompt a surge on demand that can solely be fulfilled through cultured specimens.

References

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Calado, R. (2008) Marine Ornamental Shrimp: Biology, Aquaculture and Conservation, Wiley‐Blackwell, Oxford.

Calado, R. & Narciso, L. (2005) Ability of Monaco shrimp Lysmata seticaudata (Decapoda: Hippolytidae) to control the pest glass anemone Aiptasia pallida (Actiniaria : Aiptasidae). Helgoland Marine Research, 59, 163–165.

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Dee, L.E., Horii, S.S. & Thornhill, D.J. (2014) Conservation and management of ornamental coral reef wildlife: Successes, shortcomings, and future directions. Biological Conservation, 169, 225–237.

Evanson, M., Foster, S.J. & Vincent, A.C.J. (2011) Tracking the international trade of seahorses (Hippocampus species) – the importance of CITES. Fisheries Centre Research Reports, 19, 1–94.

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Lucas, C.H. (2001) Reproduction and life history strategies of the common jellyfish, Aurelia aurita, in relation to its ambient environment. Hydrobiologia, 451, 229–246.

Lunn, K.E. & Moreau, M.A. (2004) Unmonitored trade in marine ornamental fishes: the case of Indonesia's Banggai cardinalfish (Pterapogon kauderni). Coral Reefs, 23, 344–351.

Moorhead, J.A. & Zeng, C.S. (2010) Development of captive breeding techniques for marine ornamental fish: A review. Reviews in Fisheries Science, 18, 315–343.

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Pyle, R.L. & Randall, J.E. (1994) A review of hybridization in marine angelfishes (Perciformes, Pomacanthidae). Environmental Biology of Fishes, 41, 127–145.

Rocha, R.J.M., Pimentel, T., Serodio, J., Rosa, R. & Calado, R. (2013) Comparative performance of light emitting plasma (LEP) and light emitting diode (LED) in ex situ aquaculture of scleractinian corals. Aquaculture, 402, 38–45.

Rocha, R.J.M., Silva, A.M.B., Fernandes, M.H.V., Cruz, I.C.S., Rosa, R. & Calado, R. (2014) Contrasting light spectra constrain the macro and microstructures of scleractinian corals. PLoS ONE, 9, e105863.

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3

Life Cycles in Marine Ornamental Species – Fishes as a Case Study

Ike Olivotto¹, Ming‐Yih Leu² and Mercedes Blázquez³

¹ Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche, Ancona, Italy

² National Museum of Marine Biology and Aquarium/Graduate Institute of Marine Biology, National Dong Hwa University, Taiwan

³ Institut de Ciencies del Mar (ICM‐CSIC, Barcelona, Spain

Abstract

Marine ornamental fish show a great variety of sexual patterns that are the result of specific evolutionary selections and environmental adaptation. Most of the species can be divided into pelagic and demersal spawners. Pelagic spawners usually release gametes in the water column at dusk while demersal spawners have adhesive embryos and parental care. These two modes of reproduction show several differences and specificities, and are fully analyzed in the present chapter. This information is fundamental to the selection of the appropriate species to culture.

Keywords: Fish sexuality; hermaphroditism; demersal spawning; pelagic spawning; embryonic development

3.1 Introduction

Fishes constitute the largest group among vertebrates (Nelson, 2006), with more than 32,000 species known to inhabit our planet; numbers that are still increasing as stated in FishBase, a database of all extant fish species (Froese & Pauly, 2014). Fish have a wide variety of reproductive strategies and thus different expressions of their sexuality (Sadovy de Mitcheson & Liu, 2008; Erisman et al., 2013). This is mainly due to the great plasticity they have regarding sexual determination and sexual differentiation mechanisms (Blázquez et al., 1998a; Munday et al., 2006; Ah‐King & Nylin, 2010; Kobayashi et al., 2013). Different sexual patterns can be found among fish including gonochorism, hermaphroditism and unisexuality. In this chapter we often refer to a comprehensive review (Devlin & Nagahama, 2002), that constitutes an up‐to‐date study for any researcher working on sex differentiation and fish sexuality. Since then, several advances have been made, specifically in the understanding of the molecular basis of sex determination and sex differentiation. This review also shows how molecular biology, and an increase in genomic resources of several species, have boosted our knowledge of these fundamental processes.

3.2 Patterns of Sexuality in Fish

3.2.1 Gonochoristic Fish

Gonochorism is the most abundant pattern and is characterized by the presence of separated sexes, i.e., individuals mature, and thus reproduce, only as males or females along their entire lifespan, regardless of their gonadal morphology. Although this pattern seems simple, it can reach some complexity giving rise to different subclasses.

3.2.1.1 Differentiated Gonochoristics

Also termed primary gonochoristics. The undifferentiated gonad develops directly into an ovary or a testis and during life they produce mature gametes of only one sex. This is the case of European sea bass, Dicentrarchus labrax (Blázquez et al., 1998b; Piferrer et al., 2005), tilapia, Oreochromis niloticus (Nakamura & Nagahama, 1985; Nakamura & Nagahama, 1989), or medaka, Oryzias latipes (Yamamoto, 1969; Satoh & Egami, 1972), all of them widely recognized models for the study of several aspects of fish reproductive biology, including sex determination and sex differentiation.

3.2.1.2 Undifferentiated Gonochoristics

The undifferentiated gonad develops into a rudimentary ovary to reach a point when in half of the individuals the ovarian tissue regresses and is replaced by testicular tissue, whereas in the other half the ovarian tissue continues development into a mature ovary. This is the case of zebrafish, Danio rerio, one of the most widely used fish model species in basic biology, for which sex differentiation in males is characterized by a juvenile ovary‐to‐testis transformation (Maack & Segner, 2003; Wang et al., 2007; Liew & Orban, 2014).

3.2.1.3 Secondary Gonochoristics

Known as non‐functional hermaphrodites. Fish exhibit a period of intersexual stage with developed ovarian and testicular tissue. The difference with a true hermaphrodite depends on the fact that these fish only mature as a male or a female and thus, from a functional point of view they can only be males or females. Examples include European eel, Anguilla anguilla (Colombo et al., 1984; Beullens et al., 1997), and several tropical species such as Nassau grouper Epinephelus striatus (Sadovy & Colin, 1995) or fairy basslet Gramma loreto (Asoh & Shapiro, 1997).

3.2.2 Hermaphrodite Fish

Hermaphroditism has been documented in about 6% of teleost families (Sadovy de Mitcheson & Liu, 2008; Erisman et al., 2013), that is 27 families out of 448. Hermaphrodite fish produce mature gametes of both sexes during their lifespan and they have the ability to change sex. This sexual pattern is quite common among reef‐associated and coastal marine species. Although the definition appears to be quite straightforward, there is an intrinsic difficulty to classify the hermaphrodites into categories (Sadovy & Shapiro, 1987; Sadovy & Domeier, 2005; Sadovy de Mitcheson & Liu, 2008). Different types of hermaphroditism can be found among fish including synchronous, sequential and bidirectional; however, the exact biological mechanism that stimulates sex change is not fully understood (Munday et al., 2006). The size‐advantage model is a widely accepted theory to explain the adaptive significance of sex change in sequential hermaphrodites (Ghiselin, 1969), although it caused some controversy in the late 1980s (Shapiro, 1988, 1989; Warner, 1989). The model considers that sex change occurs when the reproductive success of a given species increases with size or age more rapidly for one sex than for the other. In other words, when an individual reproduces most efficiently as one sex at a given age or size, but as the opposite sex when it gets older or larger.

3.2.2.1 Synchronous Hermaphrodites

Also known as simultaneous hermaphrodites, they are characterized by the presence of testicular and ovarian tissue coexisting in the same gonad. Fish produce mature gametes of both sexes, either alternating sperm and egg delivery or simultaneously, resulting in some instances in auto‐fertilization. This is the case of killifish Rivulus marmoratus, the so far only known obligate self‐fertilizing hermaphrodite among vertebrates (Harrington, 1961, 1971; Soto et al., 1992). Cole & Noakes (1997) demonstrated that the sequence of sex allocation in this species is similar to that of diandric protogynous species (see below) and that only in sex‐changing females to males, where testicular and ovarian mature tissue coexist, can it result in self‐fertilization. However, the triggering mechanisms of ovulation, auto‐fertilization and spawning remain elusive (Sakakura et al., 2006).

3.2.2.2 Sequential Hermaphrodites

Fish start life differentiating and producing mature gametes of one sex for a given period and afterwards they change to the other sex.

Protogynous: Female‐to‐Male Sex Change

This is the most common form of hermaphroditism among fish (Warner, 1984; Avise & Mank, 2009; Kobayashi et al., 2013) and characteristic of many labrids (wrasses), scarids (parrotfishes) and other coral reef‐fishes such