Reviews in Fisheries Science & Aquaculture
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Seahorse Aquaculture, Biology and Conservation: Knowledge Gaps and Research Opportunities
Felipe P. A. Cohen, Wagner C. Valenti, Miquel Planas & Ricardo Calado
To cite this article: Felipe P. A. Cohen, Wagner C. Valenti, Miquel Planas & Ricardo Calado (2017) Seahorse Aquaculture, Biology and Conservation: Knowledge Gaps and Research Opportunities, Reviews in Fisheries Science & Aquaculture, 25:1, 100-111, DOI: 10.1080/23308249.2016.1237469
To link to this article: http://dx.doi.org/10.1080/23308249.2016.1237469
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Published online: 13 Oct 2016.
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Download by: [b-on: Biblioteca do conhecimento online UA] Date: 25 November 2016, At: 10:34 REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 2017, VOL. 25, NO. 1, 100–111 http://dx.doi.org/10.1080/23308249.2016.1237469
Seahorse Aquaculture, Biology and Conservation: Knowledge Gaps and Research Opportunities
Felipe P. A. Cohen a,b, Wagner C. Valenti a,b, Miquel Planas c, and Ricardo Calado d aUNESP–Univ Estadual Paulista, Centro de Aquicultura (CAUNESP), S~ao Paulo, Brazil; bInstituto de Bioci^encias, Campus do Litoral Paulista–Univ Estadual Paulista, S~ao Paulo, Brazil; cInstituto de Investigaciones Marinas (CSIC), Vigo, Spain; dDepartamento de Biologia & CESAM, Universidade de Aveiro, Aveiro, Portugal
ABSTRACT KEYWORDS Seahorses are currently experiencing an unprecedented level of anthropogenic pressure promoted Bibliometry; seahorse trade; by habitat destruction and increasing fishing effort to supply premium markets. This study provides sustainability; sustainable an overview of the scientific literature on seahorses in the 21st century and critically discusses five aquaculture; marine major knowledge gaps and research opportunities to advance the state of the art on this research ornamental species; threatened species field. The average number of publications per year increased from 10 (2001–2002) to »40 (2001– 2015), the majority addressing issues on seahorse ecology, biology, and aquaculture, with the most studied species being Hippocampus kuda, H. guttulatus, H. reidi, H. abdominalis, H. erectus, H. hippocampus, and H. trimaculatus. This study explores the opportunity of using seahorses as flagship species to foster mangrove conservation and decrease trawling fisheries. It also suggests that further scientific studies are needed to better understand and manage the populations of the most heavily traded seahorse species, as well as the need to monitor their vulnerability to emerging pollutants and climate change. Sustainable seahorse aquaculture can play an important role in seahorse conservation, as well as in the development of reliable traceability tools to fight the illegal trade of these highly priced organisms.
Introduction conservation and the protection of its habitat and other Marine habitats are exposed to an unprecedented level of associated species. Several features may qualify a species anthropogenic pressure, including unsustainable fishing, as a suitable flagship, as long as it appeals to the target degradation and loss of habitat, pollution, and global cli- audience, to the conservation issue being addressed and mate change (Pan et al., 2013). For successful conserva- to the local context (Bowen-Jones and Entwistle, 2002; tion actions and plans, the perception of marine Home et al., 2009; Verissimo et al., 2011). Some charis- conservation issues must raise awareness on a broader matic features may favor the selection of a given species community level. Most threats to marine habitats will as flagship (Home et al., 2009). An example is the sea- only be mitigated through a change in human behavior horses (Shokri et al., 2009; Vincent et al., 2011; Yasue through educational and awareness-raising actions, et al., 2012), with their unique morphology similar to which has been the greatest challenge faced by conserva- ponies and their reproduction mode, in which the males tionists (Wright et al., 2015). incubate the eggs in an abdominal chamber. Marketing tools have been successfully used to influ- Currently, 54 extant species of seahorses are taxonom- ence human behavior in favor of conservation (Wright ically recognized as valid, all within a single genus: Hip- et al., 2015). A common marketing approach in biologi- pocampus (according to World Register of Marine cal conservation is the use of flagship species. Flagship Species–available at:
CONTACT Wagner C. Valenti [email protected] UNESP–Univ Estadual Paulista, Centro de Aquicultura (CAUNESP), Via de Acesso Prof. Paulo Donato Castellane s/n, 14884-9000, Jaboticabal, S~ao Paulo, Brazil; Ricardo Calado [email protected] Departamento de Biologia & CESAM, Universidade de Aveiro, Campus Universit ario de Santiago, 3810-193 Aveiro, Portugal. Supplemental data for this article is available on the publisher’s website. © 2017 Taylor & Francis REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 101
Kuiter, 2009). Seahorses are vulnerable species because of Table 1. Criteria employed to assign each reference addressing TM TM their habitat degradation (Vincent et al., 2011; Harasti, seahorses retrieved from Thomson Reuters Web of Science (all databases) from 2001 to 2015 to a given research field. 2016) and also due to the collection of millions of speci- mens every year to supply the traditional Chinese medi- Research fields Criteria cine and, to a lower extent, the marine aquarium and curio trade (Vincent et al., 2011; Foster et al., 2016). Aquaculture Refers to the farming of seahorse in any phase of the life cycle. Indeed, habitat degradation and the pressure arising Biology Refers to behavior, growth, reproductive biology, and from illegal, unreported, and unregulated collection of mating system of seahorses. Conservation Refers to conservation of natural populations. seahorses worldwide prompted the inclusion of all Hip- Ecology Refers to population, habitats, distribution, migration, pocampus species into CITES (the Convention on Inter- abundance, population dynamics, and natural diet. national Trade in Endangered Species of Wild Fauna Morphology Refers to the description and function of body parts, morphological development, muscles, and skeletons. and Flora) Appendix II in 2002—a decision that became Pathology Refers to bacteria, virus, fungus or any other pathogen effective in 2004 (CITES, 2004). isolated from seahorses. Pharmacology Refers to seahorse extract and compounds such as The above rationale is the main driver that encourages peptides, glycoproteins, and antioxidants. scientists worldwide to investigate seahorses. The aim of Physiology Refers to seahorse metabolism, biochemistry, and general physiology, including studies of ecotoxicology. this study was to provide a critical overview on the scien- Taxonomy Refers to species description and identification, including tific literature addressing seahorses in the 21st century works with phylogeny. Trade Refers to the seahorse commerce, including domestic and and discuss research opportunities and gaps of knowl- global markets. edge on these remarkable organisms.
publication did not detail the name of the species being Data survey addressed in the title or abstract, and it was not possible In March 2016, a survey was conducted using all data- to gain access to the original text of the publication, it bases of Thomson ReutersTM Web of ScienceTM (avail- was registered the name as “Absent.” When studies able at: http://apps.webofknowledge.com) to collect all addressed too many species (more than eight) or was a references related to seahorses (Actinopterygii: Syngna- “broad scope” publication addressing seahorses in a gen-
thidae) published from 2001 to 2015. The term “sea- eralist way (e.g., did not detail any species in particular) horse” was used in the “Topic” field to conduct the they were registered as “Hippocampus spp.” search. Except for patents, all types of publications (sci- Overall scientific production on seahorses per year entific journals, book chapters, meetings abstracts, maga- was used to assemble a frequency distribution histo- zines, and short communications) were used for the gram, which also included the cumulative frequency. analyses. A total of 796 references were retrieved, with To provide an overview of the most published topics each one of them being screened individually to deter- on seahorses, all titles were plotted in a word cloud mine whether they were within the scope of this study. (program available at:
increase in scientific publications may be related to the inclusion of seahorses in CITES Appendix II. The need for scientific data to support regulation and management decisions may have promoted research effort towards seahorse-related topics. Therefore, the inclusion of seahorses in this list has contributed to their conservation (Foster et al., 2016), and scientific knowledge. Thirty-five species of Hippocampus were referenced in at least one of the publications selected for this study, which covers 65% of all extant species of seahorses. Figure 1. Number of scientific publications addressing seahorses Nonetheless, most publications retrieved (76%) are retrieved from Thomson ReutersTM Web of ScienceTM (all data- focused on only seven species (»13% of all extant spe- bases) from 2001 to 2015. Bars show the number of publications cies; Figure 2). From these seven species, three are among per year and the line shows the cumulative number of the most heavily traded, either dried for traditional Chi- publications. nese medicine (H. trimaculatus and H. kuda) or live for aquariums (H. kuda and H. reidi; Foster et al., 2016). To end the critical review of scientific literature of sea- This finding shows a trade-driven research effort on horses during the period being covered (2001–2015), five these species. Seahorses were included in traditional Chi- knowledge gaps and research opportunities were identi- nese medicine probably more than 600 years ago (Vin- fied and guidelines for future studies are presented. cent, 1996). The trade of live seahorses for marine aquariums is more recent, dating to the early 1900s, with the beginning of the marine ornamental trade (Vincent, Seahorse scientific literature published in the 1996; Wood, 2001). Trade regulation and management 21st century claims for scientific data, namely in the fields of ecology A total of 423 publications retrieved were relevant for and biology (Figure 2). Thus, it is expected that some of this study and selected for analysis (see Table S1). In the heavily traded species to be among the ones most spite of their recognized iconic character, the knowl- addressed by scientific research. In addition, the increas- edge on biology of seahorses was scarce before the ing demand for knowledge on genus Hippocampus may present century. Over the past 15 years (2001–2015) prompt other countries to conduct research on species there has been an increase in the number of scientific occurring in their national waters, even if not signifi- publications addressing seahorses, with the average cantly traded (e.g., H. erectus in the USA, H. guttulatus number of publications per year raising from 10 in and H. hippocampus in EU countries, and H. abdomina- 2001–2002 to »40 in 2001–2015 (Figure 1). This lis in Australia).
Figure 2. Percentage of scientific publications addressing each seahorse species (orange – left) and the most studied research fields (blue – right) based on data retrieved from 423 scientific publications using Thomson ReutersTM Web of ScienceTM (all databases) from 2001 to 2015. Note: some publications addressed more than one species and/or field. REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 103
Figure 3. Wordcloud detailing the most common words featured in the titles of scientific publications addressing seahorses selected for this study retrieved from Thomson ReutersTM Web of ScienceTM (all databases) from 2001 to 2015.
The word cloud highlighted the most common words Based on the affiliation country of the first author, 43 recorded on the titles of the publications selected for this countries published at least one scientific publication study (Figure 3). As expected, the names of the seven addressing seahorse since 2001; however, nine countries most studied seahorse species ranked among the most accounted for more than 60% of all publications repeated words. Other words highlighted in the word (Figure 4). Canada and the USA produced the most in cloud are mostly related to seahorse aquaculture and this century (Figure 4). From a continental perspective, unique features. Among these, it is possible to see the Europe represented 33% of all publications followed by words “growth,”“juvenile,”“feeding,”“survival,”“devel- Asia (26%), North America (21%), Oceania (10%), South opment,”“fed,”“Artemia,”“cultured,” and “diet,” which America (8%), and Africa (1%). Publications on ecology, clearly refer to some of the bottlenecks in seahorse aqua- trade, and conservation were mostly from Canada culture (e.g., rearing of early life stages; Koldewey and (Figure 4). This country held one of the head offices of Martin-Smith, 2010; Olivotto et al., 2011). The growing the Project Seahorse, which is the largest seahorse con- awareness and concern for the global trade of seahorses servation group in the world. Members of Project Sea- and conservation were drivers fostering research horse have contributed a significant number of scientific reflected by words such as “population,”“conservation,” publications addressing different species of Hippocampus “trade,”“threatened,” and “habitat.” The role of the male (available at:
Figure 4. Number of scientific publications addressing seahorses ranked by country and their main field of study based on data retrieved from Thomson ReutersTM Web of ScienceTM (all databases) from 2001 to 2015. journals, indexed in Thomson ReutersTM Web of Scien- potential of seahorses as flagship species for marine con- ceTM, which published more studies addressing seahorses servation; (2) filling knowledge gaps on the most traded in this century, accounting for 17% of all publications on seahorse species; (3) understanding the potential impact this topic (Figure 5). Aquaculture, Journal of the World of emerging pollutants and climate change on seahorses; Aquaculture Society (Wiley-Blackwell), and Aquaculture (4) developing a sustainable low-cost aquaculture of sea- Research (Wiley-Blackwell) published 60% of all publica- horses; (5) improving the traceability of traded seahorses tions on seahorse aquaculture. to foster marine conservation.
Knowledge gaps and research opportunities Maximizing the potential of seahorses as flagship species for marine conservation The critical analysis of the information retrieved from this survey revealed five major knowledge gaps and Theuniquemorphologyandreproduction makes sea- research opportunities that are essential to advance the horses charismatic animals. These features suggest state of the art on seahorse research: (1) maximizing the that they could be good flagship species for marine
Figure 5. Top 10 scientific journals publishing scientific research on seahorses retrieved from Thomson ReutersTM Web of ScienceTM (all databases) from 2001 to 2015. REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 105 conservation. Nonetheless, more than charismatic, a flag- are recognized as key marine habitats being amongst ship species should fit a specificgoalonconservation,in some of the most threatened tropical ecosystems (Alongi, line with local context (Bowen-Jones and Entwistle, 2002). Regions where mangroves are inhabited by sea- 2002; Home et al., 2009). According to Verissimo et al. horses (e.g., H. reidi in Brazil and H. kuda in Southeast (2011), flagship species are “species used as the focus of Asia) (Foster and Vincent, 2004) should be associated a broader conservation marketing campaign based on its with the species and studies on their potential as flagship possession of one or more traits that appeal to the target to foster habitat conservation should be performed. audience.” Therefore, the question that should be investi- Another goal that could benefit from seahorse image gated is whether the marketing strategies based on sea- would be the conservation of costal seabed through the horse images are efficient enough to raise awareness on reduction of destructive trawling fisheries (namely for people for a specific conservation issue and allow the shrimp). Study the feasibility of raising awareness of wild raising of enough funding to support it. shrimp consumers by a “seahorse safe” label – develop- Seahorses inhabit many tropical and temperate shal- ing and promoting fishing practices that do not harm low water habitats around the globe, including coral seahorse populations. If costumers change their prefer- reefs, mangroves, and seagrass beds (Foster and Vincent, ence for a product originating from a more responsible 2004; Kuiter, 2009). These areas are among the most fishing practices (e.g., “seahorse safe”), it can certainly affected areas in the sea, mainly through fishing, pollu- affect the whole shrimp supply and value chain, and tion, and tourism (Alongi, 2002; Hughes et al., 2003; even benefit other marine species. Waycott et al., 2009). It has been shown that Syngnathids can be efficient flagship species for estuarine seagrass Filling knowledge gaps on the most traded beds conservation, using as rationale that some addi- seahorse species tional species can also benefit from seahorse conserva- tion (Shokri et al., 2009). Indeed, Project Seahorse also Five seahorse species (H. trimaculatus, H. spinosissimus, showed the effective use of seahorses as flagship species H. kelloggi, H. kuda, and H. algiricus) account for more through the creation of some marine protected areas in than 90% of the world trade of seahorses (Figure 6), central Philippines (Vincent et al., 2011). Nonetheless, with most being traded as dried specimens collected further studies are still needed to link seahorses to their from the wild (Foster et al., 2016). Except for H. kuda, habitats and evaluate the true potential of them as flag- scientific studies addressing these species are scarce ship species, as well as on marketing strategies featuring (Figure 6). On the other hand, H. kuda and H. reidi these species. An urgent goal could be the use of sea- species that are more well represented in the marine horses to promote mangrove conservation. Mangroves aquarium trade have greatly been subject to scientific
Figure 6. Number of scientific publications for the most studied and traded species of seahorses according to Thomson ReutersTM Web of ScienceTM (all databases) from 2001 to 2015. The risk of extinction for each species is indicated according to IUCN red list: VU D vul- nerable; and DD D data deficient. Total number of publication for each species – all studied fields included – is indicated in the boxes. Trade percentage was retrieved from Foster et al. (2016), which is an estimated mean of annual trade volume from CITES Trade Data- base (2004–2011). 106 F. P. A. COHEN ET AL. studies, namely in the field of aquaculture (Figure 6). Some highly traded species lack of essential informa- Even though not significantly traded internationally, H. tion for conservation. It is widely accepted that seahorse erectus, H. abdominalis, H. guttulatus, and H. hippo- populations are threatened by overexploitation, bycatch, campus are often referred as potential species for the and generalized habitat degradation (Vincent et al., marine aquarium trade (Koldewey and Martin-Smith, 2011; Harasti, 2016). Nonetheless, 67% of the 40 species 2010) and have been widely studied (Figure 6). There- included in the IUCN red list are classified as “Data Defi- fore, the aquarium trade has driven scientific research cient” (IUCN, 2015-4). Only 11 species are categorized of seahorses, especially their aquaculture (Figure 6). The as “Vulnerable” and one as “Endangered” (H. capensis) higher prices fetched by live specimens, when compared (IUCN, 2015-4). Four of the seven most studied species to dried ones (Koldewey and Martin-Smith, 2010), may are within the “Data Deficient” category (Figure 6). Yet, be the reason of this bias. In some way, it is puzzling most traded species are classified as “Vulnerable” that research efforts are not being target toward the (Figure 6), probably based only on trade and fisheries most heavily traded species. quantification (Perry et al., 2010). The species H. reidi is Current aquaculture practices are not economically highly traded for marine aquariums, but is classified as feasible for seahorses demanded by traditional Chinese “Data Deficient,” although many research efforts have medicine because of the low market price. Nevertheless, been made to study this species. The “IUCN Seahorse, low-cost production of seahorse may be feasible and Pipefish and Stickleback Specialist Group” has developed profitable (Fonseca et al., 2015). Thus, studies addressing significant efforts to provide information to improve the the development of low-cost production systems should conservation of these fish (available at: https://iucn-sea be prioritized. Additionally, studies addressing the popu- horse.org; accessed in May 2016). Nonetheless, there are lation and fishery biology of the traded species should still knowledge gaps on growth, maximum size, longev- also be promoted to allow a better management of the ity, reproduction biology, population structure and dis- fisheries, ensuring the maintenance of natural stocks and tribution, and population size of the most traded species. species conservation. Except for H. algiricus that is from Overall, there are gaps on ecological and biological data West Africa, all other four most traded seahorse species from wild populations that needs to be overcome to pro- are distributed across Southeast Asia (Foster and Vin- mote regulations for a more sustainable fishery and con-
cent, 2004). Therefore, research focusing on the topics servation. Particularly, studies on time series in wild referred above (aquaculture and population biology) populations are imperative to ascertain the right assign- should be encouraged in Asian countries and be priori- ment among IUCN categories and further conservation tized in international funding programs targeting marine plans if required. Currently, there is not enough informa- conservation. tion to assess the endangerment status for most seahorse Transport is one of the highest costs in marine orna- species. mental production, especially in countries where air shipping is necessary. Nevertheless, papers focus on Understanding the potential impact of emerging transport of live seahorses are very scarce. An experi- pollutants and climate change on seahorses ment conducted with H. abdominalis showed that it can tolerate extensive handling and confinement up to 35 hr The low swimming capacity, small home range and pref- of transportation (Wrigth et al., 2007). This shows a erence for coastal habitats, enhance the vulnerability of good opportunity to test the density during transport, seahorses to pollution (Vincent et al., 2011; Delunardo because more animals in the same bag would signifi- et al., 2013) and susceptibility to climate change (Faleiro cantly reduce freight. Cunha et al. (2011) showed that et al., 2015). Nevertheless, seahorses may thrive in pol- essential oil of Lippia alba can be an effective anesthetic luted areas (Tiralongo and Baldacconi, 2014) and even for slight sedation and transport of H. reidi. No informa- increase their populations (Correia et al., 2015). Expo- tion on the effect of the micro environment inside bags sure to crude oil has been studied in seahorses (Delu- is available. Seahorses are very low swimmers, have an nardo et al., 2013). The authors reported that crude oil efficient visual system, and use their camouflage for pro- can damage H. reidi cells, but that at an exposure of 10 tection. Thus, the use of some specific colors background ml/L during a 14-day period was not enough to induce and inert substrates might reduce stress during transport, severe gill damage (Delunardo et al., 2013). Others stud- increasing survival, animal health and welfare. Studies on ies revealed that seahorses can bioaccumulate organo- transportation of traded species are certainly an impor- chlorine pesticide and heavy metals (Nenciu et al., 2014; tant avenue for new research. The optimization in this Zhang et al., 2016), a feature that coupled with their low step may bring significant economic benefits and con- motility suggests that these organisms can be good bioin- tribute to the animal welfare. dicators (Delunardo et al., 2015). Nonetheless, pollution REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 107 type and its extent may vary in marine habitats and gen- specimens from the wild, it can also drive negative envi- eralizations may lead to pitfalls in decision-making. ronmental and social impacts (Tlusty, 2002). As an Thus, it is important to study the effect of pollution on example, H. reidi, a West Atlantic species that has been seahorse individuals and populations to understand in mostly cultured in Sri Lanka (Foster et al., 2016), a prac- which scenarios they might be affected. Additionally, tice that may promote ecological issues through escapees studies should address the bioaccumulation on seahorses (Vincent et al., 2011). The increase of captive bred sea- used for traditional Chinese medicine, as pollution could horses in the trade (Foster et al., 2016) should make hamper any potential medical benefits or even pose a researchers consider the sustainability of these practices risk to human health. There is a knowledge gap in eco- as a whole and not solely focus on the reduction of fish- toxicology assays evaluating the vulnerability of sea- ing effort targeting natural populations. horses to emerging pollutions, such as nanoparticles, Most studies and commercial aquaculture practices of microplastic, and drugs. seahorses rely on the use of intensive monoculture sys- Climate change can affect fish in different levels, from tems, with animals being kept in aquariums or tanks organisms, to populations, communities, and spatial eco- under controlled water parameters and being totally systems (Koenigstein et al., 2016). The main effects of cli- depended on exogenous feeding to thrive. A system that mate change on oceans is the rising of water depends exclusively on exogenous feeding might be inef- temperature, sea level, and acidification. Seahorse low ficient for species that are difficult to feed, as seahorses motility might hamper migration from a changing envi- have no stomach and this feature can reduce their ability ronment, which would require adaptation to survive. to digest nonnatural diets (Palma et al., 2014). Therefore, The dependency of many seahorse species on adequate systems that could somehow allow the provisioning of subtracts, mainly certain species of macroalgae and sea- natural food might be more sustainable than those cur- grass, would certainly be affected by the availability of rently used and even promote better results. An example anchoring elements and the composition, density and is the cage-culture approach within an integrated multi- distribution of natural prey (strongly dependent on the trophic aquaculture (IMTA) system. Some seahorse spe- type of vegetation) in temperature rising environments. cies can support a relatively high range of salinity Therefore, the biogeographical distribution of seahorse (euryhaline) and temperature (eurythermal) (Hilomen-
species could be altered (Planas et al., 2012). It was dem- Garcia et al., 2003; Wong and Benzie, 2003; Curtis and onstrated that the combined effects of ocean warming Vincent, 2005; Lin et al., 2009; Hora et al., 2016), which and acidification negatively affect the behavior and phys- makes them good candidates for cage-culture production iology of adult H. guttulatus (Faleiro et al., 2015). Further in coastal areas, including coastal lagoons and estuaries. studies are therefore necessary to monitor the impact of The natural growth of a periphyton-based community in climate change in seahorses because of their unique the nets of grow-out cages, along with the natural flow- breeding strategy, and the broad distribution of the through of wild plankton, are suitable sources of natural genus from temperate to tropical regions, including habi- food. Pilot trials have reported promising results during tats where fish can be more resistant to climate change the grow-out of H. reidi in floating cages inside ponds (e.g., estuaries; Perry et al., 2015). Early life stages of destined for penaeid shrimp and oyster production (Fon- some fish show abnormal calcification of otoliths (Mun- seca et al., 2015). The authors reported a mean survival day et al., 2011) and skeleton (Pimentel et al., 2014) of »80%, with seahorses attaining commercial size (7–8 when exposed to acidification. The impact on seahorses cm) within approximately three months at a density of should be investigated mainly because their bony plates 40 ind/m3 and without the input of any exogenous food. are essential for protection against predation and their By growing H. reidi in an IMTA system already used to prehensile tail plays a key role in their stability in benthic address the production of penaeid shrimp and oysters, substrates. Moreover, the paternal osmoregulation of seahorse aquaculture could be labeled as low-cost and pouch salinity in seahorses (Stolting€ and Wilson, 2007) economically feasible (Fonseca et al., 2015). Xu et al. is a feature that may also be affected under climate (2010) have also shown that the integration of macroal- change scenarios and may negatively affect the offspring gae (Chaetomorpha sp) grow-out in the production sys- fitness. tem increases survival and growth of juvenile H. erectus. Future studies addressing low-cost production systems should be supported, as this approach can also provide Developing a sustainable low-cost aquaculture an opportunity to low-income coastal communities and of seahorses make conservation efforts more perceptible at a local Although aquaculture of marine ornamental species is and regional scale. By enrolling local communities into often presented as an option to relieve the collection of such aquaculture practices, it can be possible to 108 F. P. A. COHEN ET AL. contribute towards a decrease of illegal, unregulated, and tool for geographical traceability of seafood (Leal et al., undeclared collection of seahorses from the wild and 2015), and might be suitable to trace dried seahorse. enhance environmental and social sustainability. Such Previous biochemical analysis showed significant differ- enrolment would certainly require a simplification of the ence on fatty acids composition among six seahorse rearing system. species from the coast of China (Lin et al., 2008). Recently, Shen et al. (2016) developed and validated a sensitive and specific lipidomic protocol for the detec- Improving the traceability of traded seahorses to tion of phospholipids in dried seahorses. The authors foster marine conservation were able to differentiate five wild species of dried sea- Seahorses are the only group of marine ornamental horse based on phospholipid class. Therefore, future fish traded to supply the aquarium industry that is studies should investigate the reliability of this method currently included in CITES Appendix II (Vincent to differentiate wild seahorses from captive bred ones, et al., 2014;Fosteretal.,2016). This aspect puts sea- and to differentiate specimens from the same species horses in the forefront of trade regulations and man- originating from different origins (regions or farms). agement disputes. Nonetheless, there is still a Concerning the trade of live seahorses to supply marine substantial mismatch in species and volumes reported aquariums worldwide, the production of different col- by CITES export and import records (Foster et al., our morphs and shapes through hybridization might be 2016), with no method being currently available to a good way to differentiate captive bred seahorses. Two confirm the origin of collection, nor to differentiate scientific studies reported interspecific hybridization in wild-caught from captive bred seahorses. Recently, the seahorses so far, one between male H. algiricus and export of H. algiricus, one of the top five most traded female H. hippocampus (Otero-Ferrer et al., 2015), and species (Foster et al., 2016), was banned from Senegal other between male H. erectus and female H. redi (Ho and Guinea (Project Seahorse, 2016) and further et al., 2015). This method however poses environmental restrictions can be anticipated to the trade of others risks due to potential escapees (Cohen et al., 2013). The seahorse species in the future. As captive cultured use of bacterial communities-based signatures present specimens are under less restricting regulations, these in fish mucus for their origin traceability has been
may be an alternative to fulfill demand. Nonetheless, addressed for marine fish in general (Leal et al., 2015) without a reliable traceability toolbox, neither cultured and marine ornamentals in particular (Cohen et al., specimens, nor those originating from sustainable col- 2013). The only study available to date on the phyloge- lection, can be successfully discriminated from speci- netic characterization of bacterial communities associ- mens illegally poached from the wild. Traceability is ated with seahorses showed that the microbiological essential to enforce any conservation effort and avoid composition of the cutaneous mucus and that of both the collapse of their trade and the socioeconomic the surrounding seawater and the live food differ signif- impacts this scenario may pose (Cohen et al., 2013). icantly (Balc azar et al., 2010). The low motility of Before fine tuning traceability methods for seahorses, seahorses may favor the use of this approach to differ- it is essential to identify the end market. Seahorses have entiate wild populations, as well as wild and cultured two key and very distinct markets: the trade of millions specimens, in a noninvasive and nondestructive way. It of dried specimens for human consumption (traditional is reasonable to assume that even in the wild, seahorses Chinese medicine) and the trade of thousands of live would stay in the same geographic area long enough to specimens for marine aquariums (Foster et al., 2016). develop a local-specific bacterial signature in their Clearly, this dichotomy between markets requires differ- mucus that may be used for traceability. With the ent traceability methods and strategies for their imple- advent of a reliable traceability method for seahorses, mentation. The traceability of dried seahorses may be certification and eco-labeling could be implemented by more easily achieved through the use of geochemical, CITES to trace animals throughout the whole supply biochemical, and molecular approaches already chain, supporting a conscious and more sustainable described for the seafood supply chain (Leal et al., trade. 2015). Two studies highlighted the possibility to sample tissues from partial fin-clipping of seahorses for molec- Concluding remarks ular and stable isotopes analysis (Valladares and Planas, 2012; Woodall et al., 2012). Nonetheless, the drying A multitude of factors may motivate researchers to process of specimens may affect the reliability of some study seahorses. Nonetheless, it is important to flag the of these methods and further studies are required to paramount research fields to advance the state of the validate their use. The fatty acid profile is a promising art to subsidize decision makers to address the issues REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 109 affecting production, trade, and upkeep the natural pop- in the Ria Formosa Lagoon, south Portugal. J. Fish Biol., 87: ulations. This study highlights five knowledge gaps and 679–690 (2015). research opportunities that can generate information to Cunha, M. A., B. F. Silva, F. A. Cariello Delunardo, S. C. Beno- vit, L. C. Gomes, B. M. Heinzmann, and B. Baldisserotto. supply dry and live markets and promote seahorse con- Anesthetic induction and recovery of Hippocampus reidi servation. Overall, a well-managed and sustainable trade exposed to the essential oil of Lippia alba. Neotrop. Ich- of these emblematic marine organisms includes sustain- thyol., 9: 683–688 (2011). able fisheries and aquaculture. Research should provide Curtis, J. M. R., and A. C. J. Vincent. Distribution of sympatric science-based information to develop a sustainable seahorse species along a gradient of habitat complexity in a 291 industry. This can contribute to marine conservation seagrass-dominated community. Mar. Ecol.-Prog. Ser., : 81–91 (2005). and foster socioeconomic activities in developing Delunardo, F. A., L. R. Carvalho, B. F. Silva, M. Galao, A. L. regions. Val, and A. R. Chippari-Gomes. Seahorse (Hippocampus reidi) as a bioindicator of crude oil exposure. Ecotox. Envi- ron. Safe., 117:28–33 (2015). Acknowledgments Delunardo, F. A., B. F. Silva, M. G. Paulino, M. N. Fernandes, and A. R. Chippari-Gomes. Genotoxic and morphological This work is dedicated to the memory of Professor Junda Lin, damage in Hippocampus reidi exposed to crude oil. Ecotox. colleague, and friend, for his contributions to seahorse research Environ. Safe., 87:1–9 (2013). and for advocating an ABC approach to advance the state of Faleiro, F., M. Baptista, C. Santos, M. Aur elio, M. S. 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