The Atlantic croaker (Micropogonias undulatus): An emerging candidate for multiple purpose aquaculture

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1 The Atlantic croaker (Micropogonias undulatus): An emerging candidate for multiple purpose aquaculture To d d D. Si n k 1 a n d Re b e c c a T. Lo c h m a n n 1 The Atlantic croaker (Micropogonias undulatus) is a candidate for multiple purpose aquaculture production, as a baitfish and foodfish. As a live baitfish, Atlantic croaker is a sought after bait for sportfish species such as spotted seatrout (Cynoscion nebulosus) and red drum (Sciaenops ocellatus). Atlantic croaker possesses vast potential for development as high-value live bait, with greater potential market value than many marine foodfish (Oesterling et al. 2004). As a foodfish, Atlantic croaker is a popular wild-caught foodfish that supports important commercial and recreational fisheries. Wildcaught Atlantic croaker was intermittently exported to other countries from the southern United States, but declining commercial landings decreased this practice. Croakers are commonly sought as sport and foodfish for their mild to sweetflavored, firm fillets (Figure 1). Atlantic croakers are subject to seasonal availability, which can increase demand significantly and drive prices higher during off-peak availability. Croakers are typically available inshore from May to September along the Gulf of Mexico coast. Potential threats to wild Atlantic croaker stocks include increased fishing pressure, habitat destruction and environmental pollution. Sustainable utilization of Atlantic croaker to meet bait and foodfish demands cannot rely solely upon capture of wild juveniles. Reliance on capture of wild juvenile croakers is problematic due to inconsistent availability and the possibility of reduced recruitment to wild stocks. Atlantic croaker are hardy fish that tolerate a wide range of environmental conditions and adapt readily to captivity. Aquaculture production of Atlantic croaker could alleviate seasonal availability, establish a steady supply, provide sizespecific baits, diversify aquaculture businesses and contribute to global foodfish sales. These possible benefits contribute to the potential of Atlantic croaker as a cultured species. Natural History The Atlantic croaker is a marine member of the drum family, Sciaenidae. Atlantic croaker received their common name from the drumming or croaking sound that is produced by the swim bladder. Atlantic croaker can range from dull silver to golden yellow with a dark bronze back and black spots forming irregular lines on the sides. Croaker are small to medium-sized fish with three to five chin bar- Fig. 1. Fresh caught Atlantic croaker on ice captured by recreational anglers in the northern Gulf of Mexico. Atlantic croaker are prized as sportfish and as foodfish for their flavor and fillet quality. Photo by Todd Sink. bels located under a downward pointing mouth (Figure 2). Atlantic croaker occur in the eastern Atlantic and Gulf of Mexico from Cape Cod, Massachusetts south to Brazil and Argentina (Mercer 1987). They extend their range during climatically warmer periods. Atlantic croaker undergo dietary shifts throughout life and cannot be assigned to a distinct trophic level (Darnell 1961). Larvae utilize marine algae, rotifers and copepods while small juveniles will ingest detritus and plant material. Common food items for both juveniles and adults include small fish and invertebrates such as shrimp and crabs. Atlantic croaker are capable of rapid growth and have a relatively short life-span. Growth of wild juveniles in Gulf of Mexico estuarine nurseries is 3.5 cm total length (Knudsen and Herke 1978) and 12.3 g or more per month. Growth rate and maturation of adult Atlantic croaker is directly dependent upon latitude and associated mean annual water temperature. Harvest size for wild Atlantic croaker is generally around 454 g, but current angling records of 73.7 cm and 3.94 kg indicate larger sizes are attainable. 38 September 2011

2 Atlantic croaker have a protracted spawning season from October to March, with peak spawning activity occurring in November in the northern Gulf of Mexico. During the autumn, adult Atlantic croaker move from inshore habitats to the mouths of offshore passes where they spawn floating and semi-buoyant eggs. The eggs and developing larvae are carried by currents to estuarine nursery areas. High salinity is not required for sexual maturation, but does aid egg buoyancy and subsequent hatching success. Small changes in latitude and mean annual water temperatures influence maturation rates. Atlantic croaker in subtropical and tropical regions mature earlier in life at smaller sizes than those in temperate regions. The estimated total length of fish at first maturity is 18.2 cm for males and 17.3 cm for females with greater than 85 percent of both genders sexually mature by the end of their first year in Chesapeake Bay (Barbieri et al. 1994). Two hundred forty linear kilometers to the south at Cape Hatteras, North Carolina, all Atlantic croaker mature within one year of age at 14.0 to 18.0 cm (Diaz and Onuf 1985). Atlantic croaker exhibit indeterminate fecundity, with eggs matured and spawned throughout the spawning season. Estimated fecundity for wild Atlantic croaker is 41,000 (Hansen 1970) to 180,000 eggs/female (Hildebrand and Cable 1930). Culture Tolerances Atlantic croaker is an excellent candidate for inshore, low-salinity aquaculture due to its wide range of temperature and salinity tolerances. Juveniles are more tolerant of extremes in temperature than adults. Lower and upper lethal temperatures were 0.6º and 38ºC for juveniles and 3.3º and 36ºC for adults under laboratory conditions (Schwartz 1964). Prolonged exposure to low temperatures or large sudden temperature decreases can cause mortalities. Great variations in daily water temperatures can also cause mortality of broodstock, but daily temperature variations less than 6 C are typically safe (Sink et al. 2010). Broodstock must be overwintered indoors in temperate climates. The life history of Atlantic croaker requires that larvae and juveniles be adaptive to a broad range of salinities and rapid salinity changes (Parker 1971). Wild Atlantic croaker have been collected from 0.2 to 75 ppt salinity (Simmons 1957, Parker 1971) and juveniles are capable of surviving in freshwater for short periods. Juveniles have been acclimated from salinities above 20 ppt to as little as 2 ppt in less than two hours, but rapid salinity changes are better tolerated when salinity is increased. Juvenile Atlantic croaker in culture trials demonstrated greater growth at 5 ppt salinity than at varying (5 to 20 ppt) or 20 ppt (Peterson et al. 1999). Broodfish may be held at salinities as low as 5 ppt, while juveniles may be cultured in as little as 1 to 5 ppt. The ph tolerance of Atlantic croaker is unknown, but they appear to tolerate a wide ph range with no effects on growth at ph levels ranging from 6.0 to 9.3. Culture Methods Atlantic croaker broodstock, generally individuals greater than 20 cm, can easily be obtained using various methods Fig. 2. Atlantic croaker are small to medium sized fish with three to five chin barbells, and range in color from dull silver to golden yellow with a dark bronze back and black spots forming irregular lines on the sides. Photo by Todd Sink. Fig. 3. Atlantic croaker broodstock can easily be obtained using various methods including hook and line, trawl, gill net or purchase from commercial trawlers. Hook and line collection, shown in this photo, is preferable as this method results in the least physical damage to the fish. Photo by Todd Sink. (Figure 3). Regulations and laws should be consulted and applicable permits obtained prior to collection. Collection methods include hook and line, trawl, gill net or purchase from commercial trawlers. Hook and line collection is preferable as the method results in the least physical damage to the fish. Wild-caught broodstock may be fed chopped fish and shrimp as early as two days after capture. Several freshly chopped natural foods should be offered in combination at 0.5 percent of body weight daily until pellet training. A floating, 45 to 50 percent protein, 8 to 12 percent lipid marine fish diet containing high concentrations of fishmeal or oil should be used to pellet train wild broodstock. Diets Wo r l d Aq u a c u lt u r e 39

3 Fig. 4. Synthetic salmon hormones (salmon Gonadotropin- Releasing Hormone analogue; sgnrha) injected under the skin are used to induce and synchronize spawning of captive Atlantic croaker broodstock. Photo by Todd Sink. Fig. 5. Eggs from spawning events for Atlantic croaker broodstock are typically in several different stages of development, depending upon time of spawning and fertilization. This photo depicts several stages of egg and fry development from a single spawning event collected 18 h prior to the time of the photo. Photo by Todd Sink. meeting these criteria have also resulted in good egg production from captive broodstock. Atlantic croaker can be pellet trained by withholding feed for seven days, and then offering floating pellets at 1 percent of body weight on the eighth day. If the pellets are not consumed, feed should be withheld for two additional days prior to offering pellets again. Broodfish typically begin to consume pellets within 8 to 10 days of this regimen (Sink et al. 2010). Mating behavior of captive Atlantic croaker has been observed prior to spawning. Approximately one hour prior to dusk, all fish in a tank including previously lethargic females, swim in a tight group just beneath the water surface. The dorsal and caudal fins often protrude from the water and males frequently dart away from and then back into the group, forcefully bumping females. Actual spawning events have not been observed, inasmuch as they occur in the dark. Measurement of embryo development rates indicate that spawning occurs throughout the night with a peak 1 to 2 hours prior to sunrise (Sink et al. 2010). Atlantic croaker broodstock must be conditioned using photoperiod and temperature changes prior to spawning. Ambient autumn through winter water temperatures and photoperiods have been used successfully to stimulate spawning. Atlantic croaker in captive trials spawn best when exposed to 10 hours of day length and a water temperature of 19ºC during decreasing photoperiod and water temperature. Wild-captured Atlantic croaker will occasionally spawn passively when subjected to natural autumn/winter water temperatures and photoperiods. Passive spawning events yield high fertilization rates (> 70 percent), good hatching success (up to 60 percent) and larval survival (up to 78 percent), but the volume of eggs tends to be small, the quantity of females that successfully spawn is low, and the spawning frequency of each female is low. Spawning is asynchronous and protracted among passive spawning females, which reduces hatchery efficiency (Sink et al. 2010). Synthetic salmon hormone (salmon Gonadotropin-Releasing Hormone analogue; sgnrha) has recently been used to induce captive Atlantic croaker broodstock to spawn. A single 75µg sgnrha implant injected under the skin (Figure 4) when water temperatures fall to 21 C at approximately 10 hours of day length induces and synchronizes spawning. Using this method, female broodfish with a mean weight of 341 g produced an average of five spawns each, with 265,000 eggs per female. In addition to elevated fecundity, the sgn- RHa implant produces controlled, highly-synchronized spawning events (Sink et al. 2010). Atlantic croaker produce 0.6 to 0.9 mm eggs that float or are semi-buoyant in water of 30 ppt salinity. Most viable Atlantic croaker eggs float, although fertilized semi-buoyant eggs can achieve similar hatching rates when properly incubated (Sink et al. 2010). Increasing salinity above 32 ppt results in a greater percentage of floating eggs and will not affect hatch rates up to 40 ppt (Cooke and Mooney 1973). Egg collection can be accomplished through the use of skimming egg collectors or egg collection baskets. The mesh size used for collection baskets should be smaller than 500 µm to ensure retention of eggs. Egg collection baskets should be sufficiently large to allow eggs to collect away from incoming turbulent water, as over-agitation results in suspension of embryo development. Egg collectors should be checked for eggs each morning (Sink et al. 2010). Several methods of egg incubation have been attempted, including static and flowing water systems. Static water systems, all containing fine pore air stones and light aeration, include cylindrical bottom tanks, aquaria, vertical column tubes, rounded jars and brine shrimp hatchers. Flowing water systems include hatching jars with screen sleeves to retain the floating eggs and various marine larval filtration incubators. Eggs are incubated at C and hatch hours post-fertilization depending upon incubation temperature (Figure 5). Newly hatched larvae are typically 1.5 mm (Continued on page 42) 40 September 2011

4 Fig. 6. A developing Atlantic croaker larva 76 hours after placing eggs into an incubation tank. The larvae are horizontally and to a lesser extent vertically mobile at this stage of development. Photo by Todd Sink. Fig. 7. Wild-caught Atlantic croaker of the size shown in this photo, 454 to 680 g, can be found in fresh fish markets along the U.S. Gulf and southern Atlantic coasts. Photo by Todd Sink. (Continued from page 40) long and lack fin buds, mouthparts, digestive tracts and eye pigmentation. Eye pigmentation begins to develop and the pectoral fins are defined within 24 hours of hatching, but the mouth remains closed. After 48 hours, the eyes are partially pigmented, the yolk sac has been absorbed, the mouth is partially gaping open (60µm) and larvae occasionally dart horizontally through the water column (Cooke and Mooney 1973, Middaugh and Yoakum 1974, Sink et al. 2010; Figure 6). Live food organisms from 90 to 150 µm should be provided between 48 and 72 hours post-hatch. Intensive indoor larval rearing of Atlantic croaker using methods developed for red drum larvae production have been successful in laboratory settings (Davis and Arnold 1997). The methods include feeding live rotifers enriched with fatty acid supplements prior to weaning to microparticulate diets. Larval production methods have not been attempted on a large-scale for commercial production. Extensive production of larvae using the fertilized pond system is more promising for large-scale production. High protein (40-45 percent), low to moderate lipid (5-8 percent) diets produce the best juvenile growth. Juveniles fed a 45 percent protein, five percent lipid diet once daily will consume five percent of body weight within one hour. That diet and ration size has produced 400 percent or greater weight increase in three months with survival from percent (Jones and Strawn 1983). Feed efficiency was greater when Atlantic croaker were fed 45 percent crude protein diets containing eight percent lipid than when fed diets containing higher lipid levels. Growth and feed efficiency increase as protein concentrations are increased from 30 to 45 percent (Davis and Arnold 1997). Health and Disease Few health concerns are known for Atlantic croaker during culture, but this is likely to change as culture becomes more prominent. One third of wild-captured broodstock have mild to moderate infestations of intestinal trematodes. Quarantining wild-captured broodfish in recirculation systems with adequate filtration and free of intermediary trematode hosts for six months eliminates most trematode problems. Small percentages of wild-caught broodfish develop dropsy or bloat during pellet training. Crowding and poor water quality has resulted in severe infestations of fish louse (Argulus spp.). Prolonged exposure to water temperatures approaching upper lethal limits (>35ºC) has resulted in outbreaks of parasites (Crytobia spp.) and bacterial infections (Edwardsiella tarda). Erosion of fins in broodstock is frequently observed, although this condition is typically attributed to hormone treatments and has not been documented in passively spawned fish. Markets and Economics Wild-caught Atlantic croaker are found in coastal U.S. bait shops from Maryland to Texas. Markets for Atlantic croaker are defined by local demand, and the preferred baitfish sizes are directly linked with the recreational angling species targeted in a region (Adams et al. 1997). Supply shortages occur during spring and early summer due to inconsistency of supply of wild-caught fish caused by weather conditions, migratory patterns, abundance of fish stocks and time constraints of harvesters. There is a need for size-graded Atlantic croaker that allows bait size adjustment as recreational fishing opportunities change within a region. The most popular bait size range for Atlantic croaker is from cm (Oesterling et al. 2004). Atlantic croaker up to 17.8 cm are occasionally sold when inadequate supplies of smaller sizes are available, but most anglers dislike the larger fish. Bait sized Atlantic croaker can obtain retail values of more than US$1.25/fish, although US$8.90/dozen (US$0.74/fish) was the 1995 mean retail price in Florida (Adams et al. 1997). Larger Atlantic croaker are priced similar to small fish, despite their larger size. No market currently exists for cultured food size Atlantic croaker. 42 September 2011

5 Food size wild-caught Atlantic croaker, 454 g and greater (Figure 7), can be found in coastal fish markets and seafood restaurants along the Gulf of Mexico and southeast Atlantic coasts of the US. Food size fish typically retail in fish markets for US$3.30/kg whole fish. Conclusions The Atlantic croaker is an excellent candidate for multiple purpose aquaculture due to its popularity as a bait and foodfish, environmental tolerances, adaptability to captivity and high market value. Development of Atlantic croaker production practices is still ongoing and fundamental information on larval culture, nutrition, growout, economics and marketing must be elucidated. Significant progress has been made in large-scale reproduction of Atlantic croaker, but less progress has occurred on the culture and feeding of juveniles. Considerable bottlenecks exist for high-density egg incubation, larval culture and feeding to produce enough fingerlings for culture to larger sizes. Growout practices are not yet well defined, but will likely be similar to those of red drum. Notes 1 University of Arkansas at Pine Bluff, Department of Aquaculture and Fisheries, Pine Bluff, AR References Adams, C.M., A.M. Lazur and P. Zajicek An assessment of the market for live, marine baitfish in Florida. Project final report: project DEP MR195. Florida Sea Grant College Program, Gainesville, Florida USA. Barbieri, L.R., M.E. Ctittenden, Jr. and S.L.K. Lowerre-Barbieri Maturity, spawning, and ovarian cycle of Atlantic croaker, Micropogonias undulatus, in the Chesapeake Bay and adjacent coastal waters. Fisheries Bulletin 92: Cooke, C.R., Jr. and R.G. Mooney Marine fish propagation with Atlantic croaker. Journal of the World Mariculture Society 4: Darnell, R Trophic spectrum of an estuarine community, based on studies of Lake Pontchartrain, Louisiana. Ecology 42: Davis, D.A. and C.R. Arnold, Jr Response of Atlantic croaker fingerlings to practical diet formulations with varying protein and energy content. Journal of the World Aquaculture Society 28: Diaz, R.J. and C.P. Onuf Habitat suitability index models: juvenile Atlantic croaker (revised). United States Fish and Wildlife Service. Biology of Reproduction 82 (10.98). Hansen, D.J Food, growth, migration, reproduction, and abundance of pinfish, Lagodon rhomboids, and Atlantic croaker, Micropogon undulatus, near Pensacola, Florida, Fishery Bulletin 68: Hildebrand, H.H. and L.E. Cable Development and life history of fourteen teleostan fishes at Beaufort, North Carolina. Bulletin United States Bureau of Fisheries 46: Jones, F.V. and K. Strawn Growth and food utilization of caged Atlantic croaker and striped mullet reared on various lipid diets in a heated water system. Journal of the World Mariculture Society 14: Knudson, E.E. and W.H. Herke Growth rate of marked juvenile Atlantic croakers, Micropogon undulatus, and length of stay in a coastal marsh nursery in southwest Louisiana. Transactions of the American Fisheries Society 107: Mercer, L.P Fishery management plan for Atlantic croaker (Micropogonias undulatus). Fisheries Management Report No. 10 of the Atlantic States Marine Fisheries Commission, USA. Middaugh, D.P. and R.L. Yoakum The use of chorionic gonadotropin to induce laboratory spawning of the Atlantic croaker, Micropogonias undulatus, with notes on subsequent embryonic development. Chesapeake Science 15: Oesterling, M.J., C.M. Adams and A.M. Lazur Marine baitfish culture: Workshop report on candidate species & considerations for commercial culture in the southeast U.S. Marine Resource Advisory No. 77. Virginia Sea Grant Program, Gloucester Point, Virginia USA. Parker, J.C The biology of spot, Leiostomus xanthurus Lacepede, and Atlantic croaker, Micropogon undulatus (Linnaeus), in two Gulf of Mexico nursery areas. Texas Sea Grant publication no. TAMU-SG Texas A&M University, College Station, Texas USA. Peterson, M.S., B.H. Comyns, C.F. Rakocinski and G.L. Fulling Does salinity affect somatic growth in early juvenile Atlantic croaker, Micropogonias undulatus (L.)? Journal of Experimental Marine Biology and Ecology 238: Schwartz, F.J Effects of winter water conditions on fifteen species of captive marine fishes. The American Midland Naturalist 71: Simmons, E.G An ecological survey of the Upper Laguna Madre of Texas. The Public Institute of Marine Science, University of Texas 41: Sink, T.D., R.J. Strange and R.T. Lochmann Hatchery methods and natural, hormone-implant-induced, and synchronized spawning of captive Atlantic croaker (Micropogonias undulatus). Aquaculture 307: Wo r l d Aq u a c u lt u r e 43