Growth and Survival of the Tiger Tail Seahorse, <i>Hippocampus comes</i>

Keeping fish in home aquaria is one of the most popular hobbies globally. The United States is the largest single market for aquarium fish (Walton 1994; Wood 2001). An estimated 11% of all U.S. households with pets keep fish (Tlusty 2002), a level similar to that in Australia, the UK, and probably in many other developed countries. Approximately 10% of all aquaria are believed to be marine, and primarily house tropical coral reef fish species (Sugiyama et al. 2004). Marine aquarium hobbyists, in particular, tend to be passionate about their aquaria, well informed, and interested in marine conservation (e.g., http://www.ems.org/marine_aquarium_trade/aquarists_profile.html). It is ironic that well-intentioned hobbyists drive a large industry that may threaten wild populations of some coral reef fish species (Wood 2001). Up to 24 million coral reef fishes of over 1000 species are traded annually, and over 98% of these marine ornamentals are wild caught (Wabnitz et al. 2003). This is in stark contrast to the freshwater aquarium hobby in which less than 2% of fishes traded are wild caught (Sugiyama et al. 2004). While the freshwater aquarium hobby trade has made significant strides over the past few decades in the development of breeding techniques for most fishes in the trade, the marine aquarium hobby trade has lagged behind. Seahorses (family Syngnathidae) are a popular group of marine aquarium fishes. In the wild, they are found worldwide in a diverse range of marine habitats, including sea grass beds, coral reefs, mangroves, and estuaries (Lourie et al. 1999). The conservation status of wild seahorse populations is of concern as populations have declined precipitously in some places (Vincent 1996; http://www.iucn.org). One reason for the observed declines in wild populations is overexploitation: the global trade in seahorses was estimated to consume at least 20 million animals annually in 1996 (Vincent 1996). In addition to the aquarium trade, seahorses are also exploited for the traditional medicines and curios trades. Early evidence suggests that the supply of seahorses to the international marine aquarium trade has been affected by their recent listing on Appendix II of the Convention on the International Trade in Endangered Species (CITES) (Job, personal observation). This decision, which came into effect in 2004, requires 169 countries to withhold export permits unless extraction of the seahorses can be shown to be sustainable. As a result, the global demand for seahorses is currently high, and prices have risen. Average wholesale prices for tropical seahorses in Australia, for example, have more than doubled over the past year (Job, personal observation). Approximately five tropical seahorse species are currently cultured on a commercial scale, primarily in the United States, Australia, New Zealand, Ireland, and Sri Lanka. The scarcity of culturing protocols for tropical seahorse species constrains the more widespread development of seahorse aquaculture, particularly in tropical developing countries. This study presents data on the growth and survival of Hippocampus comes, a popular tropical Indo-Pacific seahorse species. The tiger tail seahorse, H. comes, appears to be endemic to Southeast Asia and has been recorded from Indonesia, Malaysia, the Philippines, Thailand, Singapore, and Vietnam (Lourie et al. 1999, 2004). The major biological and ecological characteristics of H. comes have recently been reviewed by Foster and Vincent (2004). Seahorses are planktivorous in the wild (Wilson and Vincent 1998), and H. comes prefers live moving prey even when maintained in aquaria (Job, personal observation). Hippocampus comes is heavily exploited for both the aquarium and traditional medicines trades, and population declines of as much as 70% have been reported for this species in some areas (Lourie et al. 1999). As a result of these population declines, H.comes is listed as Vulnerable on the International Union for the Conservation of Nature (IUCN) Red List of Threatened Species (www.redlist.org). Moreover, as part of their conservation efforts, the American Zoos and Aquarium Association has identified H. comes as one of the nine syngnathid species for which population management plans may eventually be implemented (Bull 2002). These management plans would include producing husbandry manuals for maintaining H. comes in captivity and establishing captive breeding programs in public aquaria. Hippocampus comes were cultured in Vietnam at the Institute of Oceanography – Nha Trang as part of a joint marine conservation project between Project Seahorse (http://www.projectseahorse.org) and the Institute of Oceanography (Vietnam). Twelve wild-caught broodstock (six males and six females) were obtained from local fishers and held in a 500-L glass aquarium. These broodstock included male seahorses that were already pregnant. Broodstock were fed with a locally available sergestid crustacean (Acetes sp.). Broodstock initially required live prey but were gradually weaned onto frozen Acetes sp. over a 6-wk period. Broodstock were maintained in a controlled-environment room, under a 13.5L:10.5D photoperiod. The broodstock tank was run as a separate recirculating system, with the water continuously filtered through aquarium-grade filter wool pads and a trickle filter. The broodstock tank was given a 10% water change every week, using filtered seawater. Temperature, salinity, pH, ammonia, nitrite, and nitrate levels were measured weekly in the broodstock tank. Temperature, salinity, and pH values were 29 ± 0.45 C, 31.15 ± 0.21 ppt, and 8.25 ± 0.05, respectively. Ammonia, nitrite, and nitrate concentrations were all less than 0.1 mg/L. Four hundred and thirty newly released H.comes were obtained from one of the wild-caught pregnant male seahorses and were reared for a period of 63 d (9 wk). Ten newly released seahorses from the same batch were sacrificed on the first day after hatching, and their standard length (SL) and height (Ht) were measured to provide an indication of size at release. The nursery and grow-out tanks used to culture the seahorses were linked to a 60,000-L recirculating seawater system. Water in this recirculating system was filtered continuously through a trickle filter and a slow-rate sand filter. Weekly water changes of 10% were carried out on the system, using filtered seawater. In addition to the H. comes juveniles, this system also contained tanks that housed other seahorse species, including H. kuda and H. spinosissimus. Temperature, salinity, pH, ammonia, nitrite, and nitrate levels were measured biweekly in the seawater system throughout the culturing period. Temperature, salinity, and pH values were 30 + 0.22 C, 31.74 + 0.31 ppt, and 8.33 + 0.05, respectively. Ammonia, nitrite, and nitrate concentrations were all less than 0.1 mg/L. The flushing rate through each of the H. comes nursery and grow-out tanks was 20 L/min. A strainer over the overflow ensured that no seahorses or food items were flushed out of the tank. The seahorses were maintained under a natural photoperiod of approximately 12L:12D (cf. Job et al. 2002). All the nursery and grow-out tanks were located outdoors under a translucent roof that transmitted approximately 30% of the overhead sunlight, and no additional lighting was provided. From release until the age of 27 d, the young seahorses were reared in a single 3.5-m3, circular unpainted concrete nursery tank. The nursery tank was cleaned daily by carefully siphoning out any debris at the bottom of the tank. The nursery tank was kept bare, except for two suspended airstones, as the young seahorses were pelagic for the first 3–4 wk after release from the pouch. The young seahorses were fed wild-caught zooplankton (approximately 80% copepods; the remaining 20% included cladocerans and amphipods among others) for the first 10 d. The zooplankton were collected from the mouth of a nearby estuary using a 210-μm plankton net and then sieved through a 500-μm net to remove excessively large planktonic organisms (cf. Job et al. 2002). Zooplankton were collected each morning and only used on the same day. Any excess zooplankton was disposed of at the end of each day. From the age of 7 d posthatch, the seahorses were weaned onto 2-d-old brine shrimp (Artemia sp., 550–900 μm in length), which remained their sole diet until the age of 27 d. Brine shrimp were added to the nursery tank twice a day, once at 0900 h and again at 1400 h. Prey density was maintained at 1–2 individuals/mL in the tank during the day. Any uneaten brine shrimp was removed from the nursery tank at the start of each day (0730 h). Ten seahorses were randomly sampled from the nursery tank on the 14th and 21st days after hatching. The sampled seahorses were anesthetized using MS222 and their SL and Ht measured. On the 28th day after hatching, the seahorses were counted, then split into three equally sized groups, and reared for a further 5 wk in three separate 3.5-m3, circular concrete grow-out tanks. As with the nursery tank, the grow-out tanks were cleaned daily by carefully siphoning out any debris at the bottom of the tank. The young seahorses became increasingly demersal from this stage onward, and strands of nylon rope weighted down with small rocks were placed in the grow-out tanks as holdfasts for them. Seahorses in the grow-out tanks were fed with 3- to 4-d-old brine shrimp (0.8–2 mm in length) from the age of 28 d onward to the end of the grow-out period at 63 d of age. Brine shrimp were added to the grow-out tanks twice a day, at the same time as with the nursery tank. Prey density was maintained at 0.1–0.2 individuals/mL in the grow-out tanks. Any uneaten brine shrimp was removed from the grow-out tanks at the start of each day. Five seahorses were sampled from each of the three grow-out tanks at weekly intervals starting from the age of 28 d, and their SL and Ht were measured. All seahorses were counted at the end of the 63 d. In both the nursery tank and the grow-out tanks, sampled seahorses were placed in a separate tank after measurement so as not to recount them in following weeks. Standard length was measured as the sum of the length from the tip of tail to the midpoint of the cleithral ring and the length from the tip of the snout to the midpoint of the cleithral ring (Lourie et al. 1999). Height was measured as the distance from the tip of the coronet to the tip of the tail (Lourie et al. 1999). Brine shrimp used to feed the seahorses were decapsulated prior to hatching using standard techniques (Lavens and Sorgeloos 1996). Decapsulation ensured that cyst-derived bacterial contamination of the brine shrimp would have been negligible (Lavens and Sorgeloos 1996). The brine shrimp were fed with Chaetoceros sp. diatoms from the instar II stage onward. The brine shrimp were enriched with blended Acetes sp. for an hour prior to being fed to the seahorses (cf. Job et al. 2002). Acetes sp. is a planktonic crustacean (family Sergestidae) abundant throughout Southeast Asia. The enrichment product was obtained by blending Acetes sp. paste and sieving it through a 53-μm sieve. Only the filtrate was used to enrich the brine shrimp. For the nursery tank, the mean SL, Ht, and ratio of head length (the length from the tip of the snout to the midpoint of the cleithral ring sensu, Lourie et al. 1999) to body length (trunk length plus tail length sensu, Lourie et al. 1999) of the seahorses were calculated from the 10 individuals sampled at each age. For the grow-out tanks, a mean value was calculated for each of the three tanks for each age and an overall mean then calculated. The mean ratio of Ht to SL was also calculated for both the nursery tank and grow-out tanks (in the same way as for the other measures). Regression analysis (Zar 1998) was used to determine the growth rate of the seahorses. Percentage survival of the seahorses was calculated as the number surviving to a given age divided by the original number at hatching (430 animals), multiplied by 100. Survival in the nursery tank to the age of 28 d was 90% (N = 430), with 387 of the original 430 seahorses surviving. Survival in the grow-out tank from 28 d of age to 63 d of age was 100% in each of the three tanks. Total survival from hatching to 9 wk of age was therefore 90%. The mean SL of the seahorses increased from 10.7 mm ± 0.15 SEM at release from the male’s pouch to 42.9 mm ± 1.45 SEM at 28 d postrelease, and to 59.4 mm ± 1.78 SEM at 63 d postrelease (Fig. 1). The relationship between SL (in mm) and age (in days postrelease) was described by the equation: Growth in standard length and height of Hippocampus comes with age. All values are means ± SEM. with an adjusted r2 of 0.86 (N = 9, SE of estimate = 5.37). The growth rate of the seahorses was therefore 0.66 mm/d. Mean Ht of the seahorses increased from 9.2 mm ± 0.13 SEM at release to 37.1 mm ± 0.76 SEM at 28 d postrelease, and to 50.2 mm ± 1.39 SEM at 63 d postrelease (Fig. 1). The relationship between SL (in mm) and age (in days postrelease) was described by the equation: with an adjusted r2 of 0.84 (N = 9, SE of estimate = 4.83). The ratio of head length to body length decreased rapidly with growth from 0.39 ± 0.01 SEM in the 1-d-old seahorses to 0.22 ± 0.01 SEM in the 14-d-old seahorses. The head length to body length ratio only changed slightly with further growth, and was 0.24 ± 0.01 SEM at 63 d of age. The mean value of the head length to body length ratio over the period from 14 d of age to 63 d of age was 0.23 ± 0.01 SEM. Older juvenile seahorses, therefore, have proportionately shorter heads and snouts relative to the length of their body compared to newly released seahorses. The ratio of Ht to SL remained relatively constant with growth and development. It varied from 0.86 ± 0.01 SEM in the newly released (1-d old) seahorses to 0.85 ± 0.01 SEM in the 63-d-old seahorses, with a mean value of 0.86 ± 0.01 SEM over the period from 1 d of age to 63 d of age. A very high proportion of H. comes from a single batch was successfully reared from release from the male’s pouch through to 63 d of age in this study, and data were obtained on growth and survival in the tank environment. The survival of H. comes observed in this study (90%) was high in comparison to most other seahorse species. Reported survival rates of cultured seahorses vary substantially across studies and species. Survival in H. abdominalis, for example, ranged from approximately 21% (Woods 2000a) to 80% (Woods 2000b) over a 2-mo period. Similarly, stage-specific survival of H.erectus ranged from 30% at 7 mo to 70% for adults (Correa et al. 1989). Mortality in H.comes appears to be confined to the first few weeks after release from the males’ pouch, a pattern similar to that observed in some other seahorse species (Woods 2000a). The growth rate of H. comes observed in this study was relatively similar to that of an Atlantic seahorse species, H. erectus, reared at similar temperatures. Hippocampus erectus reared at approximately 25 C reached a total length (assumed to be Ht, i.e., from the tip of the tail to the tip of the coronet) of 33.29 mm at 35 d of age (Correa et al. 1989). In comparison, H.comes had a Ht of 39.40 mm at 35 d of age. Both H. comes and H. erectus appeared to have substantially faster growth rates than a temperate seahorse species, H. abdominalis, cultured at approximately 16 C. Hippocampus abdominalis achieved a SL of 43.04 mm at 56 d of age (Woods 2000a) and took a year to reach 110.73 mm (Woods 2000b). In comparison, H.comes reached 42.93 mm at 28 d of age and 59.40 mm after 63 d. The average growth rate of H. comes at 0.66 mm/d, however, is substantially less than that of H. kuda, which averaged between 0.90 and 1.53 mm/d in terms of SL, and averaged 85.82 mm SL at 56 d of age (Job et al. 2002). The differences in growth rates were probably at least partially because of differences in the temperatures at which the various species were reared and differences in their final adult sizes (18.7 cm for H. comes, 19 cm for H. erectus, 17 cm for H. kuda and 35 cm for H. abdominalis; Lourie et al. 2004). In general, it appears that tropical seahorse species have substantially faster growth rates than temperate species. The change in the ratio of head length to body length during the first few weeks of growth in H.comes is consistent with available information on other seahorse species (e.g., Job et al. 2002). Newly released seahorses tend to have disproportionately large heads, perhaps as a reflection of the importance of vision-based feeding at this stage relative to other functions. The head length to body length ratio remains relatively constant after the first 2 wk from release, suggesting that the primary morphometric changes associated with development have largely been completed within that period. The relatively constant ratio between SL and Ht may help facilitate intraspecific comparisons, where different size measures have been used. Such comparisons may be useful in the context of the new 10-cm minimum Ht requirement proposed as a management measure under CITES. The marine aquarium trade is at a crossroads in some ways. The rapid rate at which coral reefs are being degraded globally has raised concerns over the overexploitation of coral reef fishes for the marine aquarium hobby (Wood 2001). The commercial captive breeding of a broader range of marine aquarium fishes, particularly in developing countries, could provide a complementary means of reducing overexploitation of reef fishes to industry regulation, while promoting socioeconomic development. Hippocampus comes appears to be a good candidate for aquaculture development. It is a popular species that apparently can be cultured with relatively rapid growth and high survival. Moreover, H. comes is highly exploited in tropical developing countries such as the Philippines (Vincent 1996; Lourie et al. 1999) and Vietnam (Job, personal observation). This study has focused on the development of protocols that are suitable for tropical developing countries, and utilizes low-cost locally available materials such as Acetes sp. Sustainable aquaculture of H.comes in source countries could potentially alleviate some of the pressure on wild populations, if accompanied by other fisheries and habitat management initiatives. This study provides a starting point for understanding the survival and growth of H. comes juveniles in aquaculture. More research, however, is needed in order to optimize culture efficiency. One of the key challenges that the seahorse aquaculture industry faces, for example, is the high cost of producing large adult seahorses. While the aquarium trade accepts cultured seahorses at approximately 60-mm SL (Shaun Kelly, Aquarium Industries Pty Ltd., personal communication), the traditional medicines trade prefers large seahorses (Vincent 1996). The traditional medicines trade offers lower prices than the aquarium trade and requires larger sizes, but the magnitude of the trade still makes it a potentially lucrative market. Further research, however, is needed to develop cost-effective protocols for culturing seahorses through to a size that would be suitable for the traditional medicines trade. We thank S. K. Truong, H. Koldewey, J. Meeuwig, H. H. Do, T. H. Ho, and N. T. P. Duyen for their invaluable assistance in making this study possible. This study was funded by the Community Fund, UK (now the Big Lottery Fund) and the Columbus Zoo and Aquarium (USA). A. V. was supported by the John G. Shedd Aquarium through its partnership for marine conservation with Project Seahorse. Ethics approval was obtained from the Zoological Society of London (UK). This is a contribution from Project Seahorse.

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