Nursery-phase culture of green sea urchin Strongylocentrotus droebachiensis using "on-bottom" cages.
Article Type: Report
Subject: Sea urchins (Growth)
Fish industry (Management)
Fisheries (Management)
Mariculture (Methods)
Authors: Kirchhoff, Nicole T.
Eddy, Stephen
Harris, Larry
Brown, Nicholas P.
Pub Date: 08/01/2008
Publication: Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2008 National Shellfisheries Association, Inc. ISSN: 0730-8000
Issue: Date: August, 2008 Source Volume: 27 Source Issue: 4
Topic: Event Code: 200 Management dynamics Computer Subject: Company growth; Company business management
Product: Product Code: 0900000 Fishing, Hunting & Trapping NAICS Code: 114 Fishing, Hunting and Trapping SIC Code: 0912 Finfish; 0913 Shellfish; 0921 Fish hatcheries and preserves
Geographic: Geographic Scope: United States Geographic Code: 1USA United States
Accession Number: 184230626
Full Text: ABSTRACT Sea urchin hatchery techniques are well established, but cost effective grow-out strategies are still under development. Juvenile green sea urchins (Strongylocentrotus droebaehiensis) with a test diameter of less than 15 mm are vulnerable to predation when released into the wild and mortality can be high; therefore a protected nursery phase is required. This study investigated the feasibility of a cost effective on-bottom nursery cage system to provide protection at this stage. Wild-caught juvenile urchins (average diameter 7.93 [+ or -] 0.65 mm) were held in specially designed high-density polyethylene (HDPE) mesh tubes, 50 per tube, at two lease sites in Penobscot Bay, ME. Replicate tubes were placed on 3 bottom types (mussel, cobble, and ledge) at the Sloop Island site and on cobble bottom type at the Job Island site. Groups of urchins were counted and measured 5 wk, 3 mo, and 6 mo after placement to gauge handling mortality, growth, and survival. Handling mortality after 5 wk was 5% with no significant difference between treatments. Final survival indicated that cobble bottom type supported the highest survival at Job Island (89%) and Sloop Island (71%), followed by Sloop mussel (59%) and Sloop ledge (56%). After 6 mo the average diameter reached 11.08 [+ or -] 1.49 mm. Final average test diameter was significantly larger at Sloop ledge (12.17 mm) and Sloop mussel (12.58 mm), than at Sloop cobble (9.83 mm) and Job cobble (9.66 mm). These results suggest on-bottom culture through the critical nursery phase is technically feasible and may represent an economical way to rear hatchery produced green sea urchin seed to the "planting out" size.

KEY WORDS: Strongylocentrotus droebachiensis, sea urchin, aquaculture

INTRODUCTION

Worldwide, sea urchin gonads are one of the most valuable seafood products, worth over US$100 per kilogram processed (National Marine Fisheries Service 2008). Sea urchins are also important biological models of early development and are the primary herbivore in marine ecosystems, controlling the population of numerous algal species, especially kelp (Scheibling et al 1999). Commercial demand for many urchin species has steadily increased, leading to the depletion of several sea urchin species worldwide (McBride 2005). Despite a high level of conservation in Maine, the slow rate of population recovery of the green sea urchin (Strongylocentrotus droebachiensis, O. F. Muller 1776) has caused concern within the industry and among researchers that wild stocks will not recover without assistance from aquaculture for all or part of the lifecycle. Studies on basic ecological parameters such as size-specific growth rate and mortality rates of green sea urchins did not begin until 1994 when the industry was already in decline (Russell et al. 1998). Since then, research in the field has dramatically increased, yet our knowledge about the green sea urchin is still poor compared with other species worldwide.

Whereas reliable methods exist for hatchery production of large numbers of juvenile urchins, grow-out methods are not well described (McBride 2005). A nursery system is necessary to grow green sea urchin juveniles to at least 15 mm test diameter before release to bottom sites because of the high rate of predation within the first year (Dumont et al. 2004). Technology for cage grow-out operations is presently being investigated in many countries as an economic alternative to space, power, and labor-intensive land-based nursery facilities (Grosjean et al. 1998, McBride 2005).

Predation is believed to be the most important factor controlling the density of juveniles (McNaught 1999, Balch & Scheibling 2000, Dumont et al. 2004). From settlement until about one year of age, juveniles are found under rocks, in crevices, or under debris (Cameron & Schroeter 1980, Dumont et al. 2004), as an adaptation to escape predation. Here they graze on diatoms, coralline algae, and detritus (Raymond & Scheibling 1987). Movement of juveniles less than 15 mm diameter, whereas difficult to measure because of their cryptic behavior, is believed to be confined to within 1 [m.sup.2] (Dumont et al 2004). An ontogenetic shift in behavior from cryptic to active foraging has been found by Dumont et al. (2004) to occur after 15 mm diameter. At this size, active foraging of macroalgae increases the quantity and quality of food available, increasing their growth rate. In addition, after 15 mm in size there is a significant reduction in vulnerability to predators. This ontological shift suggests a trade-off between risk of predation and increased access to food (Dumont et al. 2004).

Cage grow-out of sea urchins is currently being investigated as a method of sea urchin aquaculture (McBride 2005). The appropriate size for moving juveniles from the hatchery to grow-out cages has been commonly set at 5 mm for several species and in several countries (McBride 2005). Cage systems, if designed properly, may provide adequate protection from predation during the critical nursery phase (i.e., from 5 mm up to 15 mm in test diameter). Initial research for out-planting methods began in 1989 in Japan (Agatsuma et al. 2003). Bennett et al. (1994) attempted to identify the environmental factors influencing reseeding success for the red sea urchin (Strongylocentrotus franciscanus, Linnaeus) and found the best results were obtained when planting out at intermediate depth (about 11 m), at least 4-5 mo prior to winter storms and in close proximity to adults. Harris et al. (2003) found the optimal timing of release of green sea urchins to also correspond to the period prior to winter. He observed the one-month survival of out-planted S. droebachiensis to be 100% for 20-25 mm test diameter juveniles and 93% for 10-15 mm diameter juveniles when out-planting was done between November and December in the Gulf of Maine. Survival was significantly less for other release dates during the year.

The placement of cage grow-out systems is an important factor for evaluating success. Observations on natural green sea urchin densities found substantially more urchins on hard substrata (i.e., ledge or cobble, 73 individuals per [m.sup.2]) compared with soft substrata (i.e., sand or bivalve debris, 18 individuals per [m.sup.2]) (Brady & Scheibling 2005). The environmental effects causing the occurrence of these particular bottom types may also be the same factors (i.e. current, food availability, exposure, and similar), which influence sea urchin survival and growth. In addition, bottom types are an easily distinguishable physical characteristic, which could be used to identify optimal sea urchin aquaculture lease sites in the future. In this study, the survival and growth of juvenile Strongylocentrotus droebachiensis within a cage system were investigated and compared at two different lease sites and on a variety of bottom types within each particular site.

METHODS

In July 2005, two experimental lease site permits were obtained from the Maine Department of Marine Resource (DMR) in Penobscot Bay by Jim Wadsworth of Friendship International. Each lease site was 2 acres (0.81 hectares). Site 1 was located off of Northaven near Sloop Island (44012.2' N, 68[degrees]50.1' W) and Site 2 was off of Camden near Job Island (44[degrees]13.5' N, 68[degrees]50' W). Site selection criteria included proximity to port, depth, bottom types, tidal exchange (moderate to high), and minimal opposition from other commercial fisheries. In May 2006, 12 wire mesh oyster cages (150 cm x 150 cm x 12 cm) were distributed among the two lease sites and anchored to the sea floor. Nine cages were set out at Sloop Island in 2-5 m mean water depth; three for each of the distinct bottom types: cobble (granite rocks 6.35-25.4 cm in diameter), ledge, and >90% live mussel cover. The remaining three were placed at Job on cobble bottom at a comparable depth to Sloop Island. The cages were used as anchors for nine culture tubes each, elevating the tubes 4" above the substrate. In June, 5,400 wild juvenile urchins between 4 and 12 mm (mean 7.93 [+ or -] 0.65 mm) were collected from the lease sites by a diver, measured (test diameter) and distributed among 108 specially designed tubes at 50 per tube. The tubes were 35 cm long x 9 cm diameter cylinders constructed of high-density polyethylene (HDPE) 3/16" (4.76 mm) square mesh. Each tube was identified with an orange, numbered livestock ear tag (Allflex Global Tag Systems). The tubes were preconditioned with a diatom film for two weeks in a greenhouse covered flow through seawater system at the Center for Cooperative Aquaculture Research (CCAR), and a 7.5 cm x 12.5 cm piece of kelp (Laminaria saccharina L.) was enclosed inside to provide additional food. Tubes were filled on the same day that the urchins were collected, and they were attached to the cages with wire ties by the diver, nine tubes per cage.

Assessment of Survival and Growth

After five weeks, three tubes per cage were assessed for handling induced mortality. Urchins were removed, mortalities counted, and live urchins were replaced into the tube and reattached to the cage. At three months, and again at six months, survival and growth were assessed for another, previously untouched, set of three tubes per cage. Growth was assessed by measuring urchin test diameter with rulers to the nearest 1 mm. After six months, all 108 tubes were removed and transported to the CCAR for complete evaluation of test diameter and survival. A large mortality event within several culture tubes was observed at this time and shells of dead urchins were also counted and diameter measured.

Environmental Evaluation: Current Speed

A Nortek Aquadopp Doppler current meter (Nortek USA, Annapolis, MD) was deployed to monitor the currents through a 16-day tidal cycle at the observed extremes at Sloop Island, mussel and ledge bottom types, in late July to early September 2006. In this way, site selection would not confound current velocity as a variable. The meter was anchored vertically, about 30 cm from the bottom, with the top secured to a partially submerged buoy. Current speed was not measured at the Sloop Island cobble bottom location or at the Job Island site.

Statistics

Data was interpreted using the R 2.31 statistical package ([c] 2006, The R Foundation for Statistical Computing). Survival was calculated from each culture tube and percentage data were arcsin transformed for all statistical analysis. An ANOVA analysis was performed on pooled data from all culture tubes for each of the sampling periods to determine if data varied significantly between collection dates. Because there appeared to be a significant mortality event between the three-month collection date and the six-month collection date, survival was evaluated before and after the event. A linear regression analysis was performed on pre and postmortality event survival to examine the effect of the predictors and their interaction on culture tube survival. Because differences between bottom types were detected, a t-test was used to test for differences within pooled replicates.

Because the timing of on-bottom release is determined by the test diameter, we compared the average final test diameter using ANOVA for each bottom type and lease site. Pooled final diameters for all culture tubes were compared using ANOVA for each collection period to determine change over time. Because final diameters were found to be significantly different between the three-month and six-month collection periods, growth was evaluated for each culture period separately. Growth was calculated as specific growth rate (SGR), defined as percent increase in test diameter per day. The SGR is calculated as: [ln(final diameter)-ln(initial diameter)]/number of days x 100. A linear regression analysis was performed as earlier and a t-test used to examine remaining differences within each group.

Each linear regression model was checked for normality using the Shapiro test, constant variance with the residual versus fitted plot, and outliers by Jack residuals and Cooks distance.

RESULTS

Handling Mortality

Assessment after five weeks postdeployment indicated a handling mortality of 5.3 [+ or -] 6.6%. Mortality was distributed equally between cages, bottom type, and lease site. Because of recruitment of new juveniles (urchins [less than or equal to] 4-mm diameter) smaller than the culture tube mesh size (4.76 mm), several tubes were found to have higher than 100% survival. Average recruitment was 0.2 individuals per tube. No correlation was found between tube location and recruitment. Recruited urchins were not included in the assessment of handling mortality.

Survival

Survival gradually declined over the first three months of culture, with no significant difference between cages, bottom type, or lease site (ANOVA, P > 0.25). Mean survival was 94.7 [+ or -] 6.6% on June 30, 2006 after five weeks, and 91.9 [+ or -] 10.6% on August 24, 2006 after three months postdeployment. After six months, 100% of the tubes at Sloop Island and 31% at Job Island contained numerous mortalities, manifested as intact tests stripped of all soft tissue. In previous survival estimates, carcasses of mortalities were not found. We hypothesize that the mortalities occurred simultaneously and relatively recent to the assessment of the tubes because of the fact that we found very few intact tests previously and also in view of the similar state of decay in the newly observed empty tests. Absolute mean survival at the termination of the culture period, on November 21, 2006, was 68.0 [+ or -] 18.3%.

The large standard deviation found within the same bottom type in the six-month survival compared with previous estimates suggests a possible spatial relationship. A linear regression analysis on counts of surviving individuals indicated that specific growth rate (SGR), bottom type, and the interaction between SGR and bottom type had a significant effect on survival (P < 0.001), with bottom type the major predictor. Initial diameter, final diameter, and their interactions with other variables were not significant to the model (P = 0.54, P = 0.45, P = 0.26, respectively) because of the use of SGR, which incorporates both of these variables in its calculation. Survival for the cobble bottom type at both Job (88.8%) and Sloop (71.3%) was significantly higher than at Sloop ledge (59.1%) and Sloop mussel (56.3%) (ANOVA, P < 0.001) (Fig. 1). It was also determined that slower specific growth rates (SGR) had a significant correlation with higher survival rates (ANOVA, P = 0.002).

[FIGURE 1 OMITTED]

The number of synchronous mortalities was plotted as a percent of the remaining population using the equation: number of cleaned tests from dead individuals/total number of individuals alive and dead remaining in the culture tube. The proportion of the population affected by the mortality event was not significantly different among bottom types, but it was significantly different between lease sites (Fig. 2). Groups at the Job Island site had significantly less mortalities (1.4 [+ or -] 2.7%) than Sloop mussel, ledge, and cobble collectively (29.5 [+ or -] 15.8%) (t-test, P < 0.001) caused by the synchronous event.

Survival prior to the mortality event was estimated by including fresh mortalities in the total, and was determined to be 90.0% [+ or -] 9.8% (Fig. 2). Standard deviation of the estimated survival remained stable over the duration of the experiment and no significant difference was found between treatments.

Growth

Initial test diameter at deployment on May 23, 2006 averaged 7.93 mm [+ or -] 0.65. After three months there was a significant difference between the bottom types and lease sites (Fig. 3). Sloop Island (11.41 mm [+ or -] 1.44) had significantly greater test diameter than Job Island (9.48 mm [+ or -] 0.27) (t-test, P < 0.01); with Sloop Island mussel (12.60 mm [+ or -] 1.18) and Sloop ledge (11.78 mm [+ or -] 0.74) out-performing Sloop Island cobble (9.86 mm [+ or -] 0.59) and Job cobble (9.48 mm [+ or -] 0.27) (ANOVA, P < 0.001). Urchins after 3 mo were observed to have longer spines in the tubes at Sloop Island mussel and ledge compared with Sloop Island cobble and Job Island cobble, though this was not measured.

After six months, a similar relationship was found between bottom type or lease site and final diameter (Fig. 3). Sloop Island (11.56 mm [+ or -] 1.69) had significantly larger test diameter than Job Island (9.74 mm [+ or -] 0.75) (t-test, P = 0.01), with Sloop Island ledge (12.33 mm [+ or -] 1.33) and Sloop Island mussel (12.56 mm [+ or -] 1.16) out performing Sloop Island cobble (9.83 mm [+ or -] 0.92) and Job Island cobble (9.74 mm [+ or -] 0.75) (ANOVA, P < 0.001). After six months, the divers observed that the juveniles in all of the tubes had longer spines than those they usually find in the wild. Again, no direct measurement on spine length was taken during this experiment.

Mean growth was difficult to estimate because of the continued occurrence of recruited juveniles into the culture tubes, which could not be definitively identified once the nonstudy juvenile was [greater than or equal to] 4 mm diameter. For this reason, the specific growth rate (SGR) was calculated from the third quartile initial and final values to avoid artificially skewed growth measurements. Pooled specific growth rate for all cage-culture treatments after three months was 0.35%/day [+ or -] 0.14 and from three to six months was 0.04%/day [+ or -] 0.09 (Fig. 4). Growth slowed considerably in all treatments after the three-month sample in August 2006. After both three months and six months, lease site and bottom type were found to significantly affect growth rate (P < 0.05). Over the six-month culture period, Sloop Island had a significantly higher growth rate (0.18%/ day [+ or -] 0.13) than Job Island (0.09 %/day [+ or -] 0.04) (t-test, P < 0.01). Job Island cobble had a significantly slower growth rate (0.09%/ day [+ or -] 0.04) than Sloop Island cobble (0.12%/day [+ or -] 0.06) (t-test, P = 0.03) and Job Island and Sloop Island cobble collectively had a significantly slower growth rate than Sloop Island ledge (0.21%/day [+ or -] 0.06) and Sloop Island mussel (0.23%/ day [+ or -] 0.07) (ANOVA, P < 0.001) (Fig. 5).

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

Environmental Evaluation: Current Speed

Greater current speeds on the flood and ebb tides were measured at the Sloop Island mussel bottom type location (0.054 [+ or -] 0.002 m/s flood; 0.114 [+ or -] 0.003 m/s ebb) compared with the ledge bottom type (0.025 [+ or -] 0.001 m/s flood; 0.089 [+ or -] 0.002 m/s ebb) at the same site. All results were corrected for vertical orientation of the current meter and horizontal directionality of the current. Current was observed to be slower at Job Island, but was not measured in this project.

[FIGURE 4 OMITTED]

[FIGURE 5 OMITTED]

DISCUSSION

This study showed that juvenile urchins held in tubes for six months on cobble habitat had higher survival but lower growth than their cohorts on mussel or ledge habitat. This raises the question of whether the observed differences in growth and survival were because of density dependent factors, the inherent ecology of the individual habitats, or a combination of the two.

The optimal rearing density for caged juvenile green sea urchins is unknown and needs to be further investigated. When stocking densities in cage culture for juvenile Psammenchinus miliaris (9-mm test diameter) were examined, urchins at the higher stocking densities (4 individuals/L) grew significantly slower than at the lower stocking densities (2 individuals/L) after six months (Kelly 2002). That study, as well as other studies of juvenile S. droebachiensis and S. franciscanus (Nishizaki & Ackerman 2004), expressed density in terms of volume, rather than in terms of surface area. Because urchins are attached to surfaces, a more appropriate measure might be to express density in terms of surface area. This has implications for food availability in mesh cages, because it gives a measure of the amount of surface area available for diatom growth and subsequent grazing by the urchins.

In our study, we calculated urchin density in terms of the percent surface area occupied by urchins, which takes into account the size of the urchin test diameter (Table 1). Thus, large urchins would occupy a greater proportion of the available surface area than small urchins. We found that stocking densities just prior to the mortality event were higher at the Sloop Island ledge and mussel habitats than at the cobble habitats at either lease site, reflecting the larger size of the urchins found there. After the mortality event, percent area coverage was about equal in all cohorts, indicating the higher loss of individuals at the Sloop Island sites. The tubes with faster growth rates may have more quickly surpassed their density threshold compared with those with slower growth rates, to a point where food and/or space became limiting, resulting in mortality.

Environmental conditions unique to each bottom type (i.e., food availability, current velocity, wave exposure, and native fauna) were also likely responsible for the differences in growth and survival seen in this study. Juvenile urchins feed on whole algae, diatom films, and water-borne detritus (Nishizaki & Ackerman 2004, Raymond & Scheibling 1987). Xling et al. (2007) found that postsettlement juveniles (Strongylocentrotus intermedius) had different growth rates depending on the diatom composition in their food supply. In our study, even though each of the tubes was anchored at equal depth, differences in current velocity, direction, and photosynthetic available radiation (PAR) may have created a location-specific diatom assemblage at each habitat. Sea urchins feed continuously, but digestibility varies from >80% for organic matter, protein, and carbohydrates to 50% for lipids and insoluble carbohydrates (Klinger et al. 1998, Lares 1999).

At the termination of this study, all of the caged urchins were observed to have longer spines than their "wild" relatives. Biologists at the Maine Department of Marine Resources and commercial urchin divers suspect that longer spines are an indication of low food availability (Hunter 2002). The observation at the three-month evaluation (June to August) of longer spines in the mussel and ledge site cohorts could have been early evidence of lack of food compared with the cobble cohorts. The caged urchins likely consumed all of the introduced kelp and the initial diatom film within the first two months, and underwent most of their growth during this period. Any further food would have had to come from floating detritus and additional diatom growth. This was a deliberate aspect of the experiment, as one of the objectives was to minimize cost during the nursery phase of urchin culture. Very little growth

was observed in any of the treatments during the final three months, and at the six-month evaluation all of the urchins were observed to have longer spines. The abundance of food sources such as diatom growth on the mesh tubes and waterborne detritus is undoubtedly affected by such environmental factors as currents, sunlight intensity, and water temperature. The three- to six-month period of this experiment occurred during the months of late August through November, when light intensity and temperature in the Gulf of Maine decline. Reduced food availability could explain the reduction in the SGR in all culture treatments from three to six months, although it could also be attributed in part to a decline in water temperature (Ebert 1968), which in our study decreased from 16[degrees]C in August to 11[degrees]C in November in Penobscot Bay.

Current velocity and exposure are also important environmental aspects to consider. Tollini et al. (1997) demonstrated that lower flow rates result in higher feed assimilation rates in adult S. droebachiensis. Kawamata (1998) found smaller urchins (Strongylocentrotus nudus) (53 mm) had a lower tolerance for high current velocities than larger urchins (80 mm), with feeding markedly reduced for the larger urchins at velocities of 0.3 m/s and at somewhat lower velocities for the smaller urchins. He ascribed the size related difference in tolerance to current to the reduced "grasping" ability of tube feet in smaller urchins. Increased wave action can also result in greater energy allocation to spine repair, especially in smaller urchins, resulting in slower growth (Ebert 1968). Dumont et al. (2007) showed that small juvenile S. droebachiensis engaged in "covering" behavior in response to relatively weak currents of 0.1 m/s, presumably as protection and as ballast for anchoring.

In the present study, current velocity measurements at Sloop Island ranged from 0.054 m/s to 0.11 m/s at the mussel bottom site, and 0.025 m/s to 0.089 m/s at the ledge bottom site. No significant difference in growth was seen between these two bottom types, but both of these sites showed significantly greater growth than did urchins at the Job Island and Sloop Island cobble bottom sites. Unfortunately, no current measurements were taken at those sites, making it difficult to draw firm conclusions from the current data. However, the divers involved in this project had fished commercially in this area for many years, and it was their belief that currents at Job Island were consistently slower than at Sloop Island. It is therefore interesting to note that the caged urchins at the Sloop mussel site had the highest growth rate of all bottom types in this study (Fig. 3), despite the presence of tidal currents that were within the range of those causing behavioral adaptations (Dumont et al. 2007). It is likely that the culture tubes may have provided some protection from the current. In addition, currents will increase the availability of waterborne detritus, which can be used as feed. Some urchin juvenile species, such as S. fransiscanus, tend to shelter under adults, and it has been suggested that one of the benefits offered by this cohabitation may be protection from excessive current speeds (Nishizaki & Ackerman 2004). However, these authors noted that this behavior is less prevalent in S. droebachiensis, which exhibits size-independent aggregation. In laboratory studies designed to examine the effects of aggregation on juvenile urchins, Nishizaki and Ackerman (2004) found that S. franeiscanus and S. droebachiensis showed lower growth rates when they aggregated with adults than when they did not. They attributed this effect to intercohort competition. The use of cage culture techniques to grow small juvenile urchins to larger sizes would eliminate any intercohort competition, as well as provide some protection from excessive currents.

Other important conclusions related to survival were also noted here. We demonstrated that transport and handling of juvenile S. droebachiensis could be achieved with low mortality. The handling mortality (5.3% [+ or -] 6.6%) was comparable to other restocking projects such as the study by Leland et al. (2002), where only 3% of adult urchins (Strongylocentrotus droebachiensis) were lost. In addition, we observed a high long-term survival, prior to the mortality event and overall, which shows promise for future cage grow-out studies. When the study was ended at six months, survival (68.0 [+ or -] 18.3%) was well within the range of previous cage culture studies. Raymond and Scheibling (1987) reported an average survival of 62% [+ or -] 5 for juvenile S. droebachiensis after one year in cage culture.

The causes of the synchronous mortality event seen in this study remain open to conjecture. There are several possible explanations, including density-dependant effects, cannibalism, an ontological shift in behavior, and storm exposure. Whereas sea urchins normally eat algae, several studies claim they can also be carnivores or scavengers (McBride 2005). Under low food availability, intraspecific predation becomes a risk, one that is possibly greater for juveniles (Himmelman & Steele 1971, Himmelman et al. 1983a, Raymond & Scheibling 1987, Dumont et al. 2004). Storm exposure is also a possible explanation for the mortality event. Two weeks before the final collection of the tubes, a strong storm from the northeast occurred in the Gulf of Maine with wind strengths of over 80 km/h. Although the exact timing of the mortality event is unknown, circumstantial evidence (i.e., intact tests still remaining in culture tubes) indicates that it may have been within that time frame. Tubes exposed to the directionality of the storm would likely have been more strongly affected than the more sheltered ones. Mortalities occurred almost exclusively at the Sloop Island lease site, which has a channel oriented to the northeast and open to the bay on each end. No measurements on current velocity were recorded at the time of the storm; therefore no firm conclusion can be drawn based on wave action exposure. In this study, we observed that the growth rate within culture tubes was comparable to and at times surpassed rates reported in nature (Table 2). The caged juveniles came close to attaining the target size of 15 mm (11.41 mm [+ or -] 1.44 at Sloop and 9.48 mm [+ or -] 0.27 at Job) after the first three months. The cage grow-out model used in this experiment has been shown to produce comparable growth (Schorygin 1928, Swan 1958, Miller & Mann 1973, Propp 1977, Himmelman et al. 1983b, Raymond & Scheibling 1987) and survival (Raymond & Scheibling 1987) to previous culture studies at a significantly reduced cost compared with land-based culture. The optimal release time from a nursery cage system is unknown, but it may be related to an observed behavioral shift at 15 mm, when green urchins change from cryptic to active foraging (Dumont et al. 2004), are less likely to seek cover, and may be more tolerant of wave and current motion (Dumont et al. 2007).

More research is needed to optimize production of sea urchin cage culture. Rearing densities, current velocities, and timing of release should all be further investigated before substantial aquaculture investment is made. Sea urchins, in general, share complicated relationships with several commercial species (Mayfield & Branch 2000) and ecologically important habitats throughout the world (Steneck et al. 2004); therefore their survival is key to the sustainability of our marine environment at large. Aquaculture could aid in the commercial and ecological recovery of the green sea urchin, Strongylocentrotus droebachiensis, in the Gulf of Maine; preserving an ecological keystone species and the livelihoods of harvesters, buyers, and processors statewide.

ACKNOWLEDGMENTS

The authors thank Jim Wadsworth of Friendship International and his divers Brad and Adam Scott for their assistance accessing the field sites and processing samples and also the Center for Cooperative Aquaculture Research staff for their assistance with sample processing in the field. Funding for this research came from the United States Department of Agriculture Small Business Innovative Research grant (SBIR), the Maine Aquaculture Innovation Center, and the Department of Industrial Cooperation at the University of Maine.

LITERATURE CITED

Agatsuma, Y., Y. Sakai & N. L. Andrew. 2003. Enhancement of Japan's sea urchin fisheries. In: J. M. Lawrence & O. Guzman, editors. Sea urchins: fisheries and ecology. Proceedings of the International Conference on sea urchin fisheries and aquaculture. pp. 18-36.

Balch, T. & R. E. Scheibling. 2000. Temporal and spatial variability in settlement and recruitment of echinoderms in Kelp Beds and Barrens in Nova Scotia. Mar. Ecol. Prog. Set. 205:139-154.

Brady, S. M. & R. E. Scheibling. 2005. Repopulation of the shallow subtidal zone by green sea urchins (Strongylocentrotus droebachiensis) following mass mortality in N. Canada. J. Mar. Biol. 85:1511-1517.

Bennett, L. R., H. C Fastenau, T. Hibbard-Robbins, Z. Kain & C. M. Dewees. 1994. Culturing red sea urchins for experimental out-planting in Northern California. DMR final report, contract FG-2230-MR.

Cameron, R. A. & S. C. Schroeter. 1980. Sea urchin recruitment: effect of substrate selection on juvenile distribution. Mar. Ecol. Prog. Ser. 2:243-247.

Dumont, C., J. H. Himmelman & M. P. Russell. 2004. Size-specific movement of green sea urchins Stronglyocentrotus droebachiensis on urchin barrens in eastern Canada. Mar. Ecol. Prog. Ser. 276:93-101.

Dumont, C., D. Drolet, I. Deschenes & J. H. Himmelman. 2007. Multiple factors explain the covering behavior in the green urchin, Strongylocentrotus droebachiensis. Anita. Behav. DOI: 10.1016/j.an behav.2006.11.008.

Ebert, T. A. 1968. Growth rates of the sea urchin Strongylocentrotus purpuratus related to food availability and spine abrasion. Ecology 49:1075-1091.

Grosjean, P., C. Spirilet, P. Gosselin & D. Vaitilingon. 1998. Land-based, closed-cycle echinoculture of Paracentrotus lividus (Lamark) (Echinoidea: Echinodermata): a long-term experiment at a pilot scale. J. Shellfish Res. 17:1523-1531.

Harris, L. G., P. Madigan & K. Waters. 2003. A hatchery system for green sea urchin aquaculture in the Gulf of Maine. World Aquacult. 34:32-36.

Himmelman, J. H. & D. H. Steele. 1971. Foods and predators of the green sea urchin stronglyocentrotus droebachiensis in Newfoundland waters. Mar. Biol. 9:315-322.

Himmelman, J. H., A. Cardinal & E. Bourget. 1983a. Community development following removal of urchins, Stronglyocentrotus droebachiensis, from the rocky subtidal zone of the St. Lawrence Estuary, eastern Canada. Oecologia 59:27-39.

Himmelman, J. H., A. Cardinal & E. Bourget. 1983b. Sea urchins in the St. Lawrence Estuary: their abundance, size-structure, and suitability for commercial exploitation. Can. J. Fish. Aquat. Sci. 40:474-486.

Hunter, M. 2002. Large-mesh sea urchin diver catch bags, results of experimental tests. Maine Department of Marine Resources. Research Ref. Doc. 02/07.

Kawamata, S. 1998. Effect of wave-induced oscillatory flow on grazing by a subtidal sea urchin Stronglyocentrotus nudus (A. Agassiz). J. Exp. Mar. Biol. Ecol. 224:31-48.

Kelly, M. S. 2002. Survivorship and growth rates of hatchery-reared sea urchins. Aquacult. Inter. 10:309-316.

Klinger, T. S., J. M. Lawrence & A. L. Lawrence. 1998. Digestion, absorption, and assimilation of prepared feeds in echinoids. In: R. Mooi & M. Teleford, editors. Echinoderms: San Francisco. Rotterdam, The Netherlands: A. A. Balkema. pp. 713-721.

Lares, M. 1999. Evaluation of direct and indirect techniques for measuring absorption efficiencies of sea urchins (Echinodermata: Echinoidea) using prepared feeds. J. World Aquacult. Soc 30:201-207.

Leland, A., J. Vavrinec & R. S. Steneck. 2002. Reseeding the green sea urchin in depleted habitats. Final report to the Maine Department of Marine Resources.

Mayfield, S. & G. M. Branch. 2000. Interrelations among rock lobsters, sea urchins, and juvenile abalone: implications for community management. Can. J. Fish. Aquat. Sci. 57:2175-2185.

McBride, S. C. 2005. Sea urchin aquaculture. Amer. Fish. Soc. Symp. 46:179-208.

McNaught, D. C. 1999. The indirect effects of macroalgae and micropredation on the post-settlement success of the green sea urchin in Maine. Ph.D. University of Maine, Orono, ME. pp. 161.

Miller, R. J. & K. H. Mann. 1973. Ecological energetic of seaweed zone in a marine bay on the Atlantic coast of Canada. III. Energy transformation by sea urchins. Mar. Biol. 18:99-114.

National Marine Fisheries Service. 2008. Japanese Sea Urchin Market. Southwest Regional Office, NMFS. 34 pp.

Nishizaki, M. T. & J. D. Ackerman. 2004. Juvenile-adult associations in sea urchins Strongylocentrotus franciscanus and S. droebachiensis: is nutrition involved? Mar. Ecol. Prog. Set. 268:93-103.

Propp, M. V. 1977. Ecology of the sea urchin Strongylocentrotus droebachiensis of the Barents Sea: metabolism and regulation of abundance. Biol. Morya (Vladivostok) 1:39-51.

Raymond, B. G. & R. E. Scheibling. 1987. Recruitment and growth of the sea urchin Strongylocentrotus droebachiensis (Muller) following mass mortalities off Nova Scotia, Canada. J. Exp. Mar. Biol. Ecol. 108:31-54.

Russell, M. P., T. A. Ebert & P. S. Petraitis. 1998. Field estimates of growth and mortality for the green sea urchin Strongylocentrotus droebachiensis. Ophelia 48:137-153.

Schiebling, R. E., A. W. Hennigar & T. Balch. 1999. Destructive grazing, epiphytism, and disease: the dynamics of sea urchin-kelp interactions in Nova Scotia. Can. J. Fish. Aquat. Sci. 56:2300-2314.

Schorygin, A. A. 1928. Die Echinodermen des Barentsmeeres. Ber. D. Wiss. Meeresinst. (Moscow) 3:1-128.

Steneck, R. S., J. Vavrinec & A. V. Leland. 2004. Accelerating trophiclevel dysfunction in kelp forest ecosystems of the western North Atlantic. Ecosystems 7:323-332.

Swan, E. F. 1958. Some observations on the Growth rate of sea urchins in the genus Strongylocentrotus. Biol. Bull. 120:420-427.

Tollini, C. D., T. S. Klinger, J. M. Lawrence & A. L. Lawrence. 1997. Effect of water flow and protein content of feed on absorption efficiency and production of Strongylocentrotus droebachiensis (Echinodermata). Am. Zool. 37:57.

Vadas, R. L. & B. F. Beal. 1999. Temporal and spatial variability in the relationships between adult size, maturity, and fecundity in green sea urchins: The potential use of roe-yield standard as a conservation tool. Report to the Maine Department of Marine Resources. 136 pp.

Xling, R. L., C. H. Wang, X. B. Cao & Y. Q. Chang. 2007. The potential value of different species of benthic diatoms as food for newly metamorphosed sea urchin Strongylocentrotus intermedius. Aquaculture 263:142-149.

NICOLE T. KIRCHHOFF, (1) * STEPHEN EDDY, (1) LARRY HARRIS (2) AND NICHOLAS P. BROWN (1)

(1) Center for Cooperative Aquaculture Research, University of Maine, Franklin, ME 04634; (2) Zoology Department, University of New Hampshire, Durham, NH 03824

* Corresponding author. E-mail: Nicole.Kirchhoff@umit.maine.edu
TABLE 1.
Stocking density. Density was measured as percent surface area
covered by the urchin's tests within an average culture tube
(%SA Cover). It was calculated using the average test diameter of
each cohort to determine the 2D area each urchin would cover,
multiplying that number by the average total number of urchin
remaining within each culture tube, and dividing the entire
calculation by total available surface area in the tube.

                              Initial

               #/[cm.sup.2]    #/L     % SA Cover

Job Cobble        0.049        22.4     3.5890%
Sloop Cobble      0.049        22.4     3.5890%
Sloop Ledge       0.049        22.4     3.5890%
Sloop Mussel      0.049        22.4     3.5890%

                     Final-Prior to Mortality

               #/[cm.sup.2]    #/L     % SA Cover

Job Cobble        0.044       20.161    3.2301%
Sloop Cobble      0.042       19.265    3.1988%
Sloop Ledge       0.045       20.385    5.1887%
Sloop Mussel      0.044       19.937    5.4222%

                      Final-After Mortality

               #/[cm.sup.2]    #/L     % SA Cover

Job Cobble        0.044       19.937    3.1942%
Sloop Cobble      0.035       15.905    2.6408%
Sloop Ledge       0.029       13.441    3.4211%
Sloop Mussel      0.028       12.769    3.4727%

TABLE 2.
Recorded measurements of Strongylocentrotus droehachiensis
test diameter versus age from the literature.

 Diameter     Diameter     Location of Study            Reference
(mm) at 1 y  (mm) at 2 y

   12-20        21-31     Barents Sea           Schorygin 1928
   8-10         24-26     York, ME              Swan 1958
   11-17        20-25     St. Margaret's Bay    Miller & Mann 1973
    10           24       Barents Sea           Propp 1977
  2.6-4.3        6-7      St. Lawrence Estuary  Himmelman et al. 1983b
    6-8          19       St. Margaret's Bay    Raymond & Scheibling
                                                  1987
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