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Notice: ©1998 World Aquaculture Society. This manuscript is an author version with the final publication available at http://www.wiley.com/WileyCDA/ and may be cited as: Zhang, D., Lin, J., & Creswell, R. L. (1998). Effects of food and temperature on survival and development in the peppermint wurdemanni. Journal of the World Aquaculture Society, 29(4), 471‐476. doi:10.1111/j.1749‐7345.1998.tb00671.x JOURNALOFTHE Vol. 29, No. 4 WORLD AQUACULTURE SOCIETY December, 1998

Effects of Food and Temperature on Survival and Development in the Peppermint Shrimp

DONGZHANG AND JUNDALIN' Department of Biological Sciences, Florida Institute of Technology, 150 West Universiw Boulevard, Melbourne, Florida 32901 -6988 USA R. LEROYCRESWELL Aquaculture Division, Harbor Branch Oceanographic Institution, Inc., 5600 US I North, Fort Pierce, Florida 34946 USA

Abstract.-The effects of four kinds of foods (Ar- in captivity. Currently, all cleaner remia nauplii, rotifer, and microalgae Chaetoceros for aquarium industry are collected from gracilis and Isochrysis galbana) and four temperature the natural environment. The effects of re- regimes on survival and development of larval Lys- mata wurdemanni, a marine ornamental shrimp, were moval of them from the ecosys- determined. The larvae fed with Chaetoceros or Iso- tem cause concern. The gap between supply chrysis only survived for a maximum of 17 d, before and demand is expected to be reduced by developing to zoea IV. The survivorship of the larvae aquaculture. fed with Artemia nauplii or rotifer from zoea I1 to post- larvae was 66.7% and 68.9%. respectively, without Efforts to culture Lysmafa under artificial significant difference (P > 0.05). But larvae fed with conditions have been made. Reproductive Artemia nauplii grew significantly (P < 0.05) faster biology, broodstock nutrition, and devel- than those fed with rotifer. Larvae fed with Artemia opment of different life stages in L. debel- nauplii reached postlarvae in 29-32 d, compared with ius and L. ambionensis have been studied 32-36 d in the rotifer treatment. Artemia nauplii are et also suitable food for the postlarvae and juveniles of (Fletcher al. 1995; Simoes et al. 1998a, L. wurdemanni. The 30 postlarvae fed on Artemia nau- 1998b). Debelius (1984) reared the larvae plii all survived to reach sexual maturity in 50 to 70 of L. seticaudata to postlarvae. Blanchard d, growing from about 7 to 28 mm in total length. The (1992) reared L. grabhami larvae, but failed effects of four temperature regimes on larval devel- to culture them to postlarval stage. The lar- opment of L. wurdemanni was also investigated. The vae of L. debelius and L. amboinensis are duration (mean ? SD d) to the postlarvae at temper- atures of 26 C (37.4 ? 5.4) and of 26-30 C daily (40.2 able to feed on rotifers or small strain Ar- ? 5.8) was significantly (P < 0.05) longer than that at temia salina (Fletcher et al. 1995). L. wur- 28.5 C (29.3 2 4.8) and at 27-29 C daily (28.7 t 3.5). demunni larvae fed with rotifer (before day 14) and Artemia nauplii have also been cul- The peppermint shrimp Lysmafa wurde- tured successfully under artificial condi- manni occurs naturally along the Atlantic tions (Crompton 1992). The optimization of and Caribbean coasts of North and South feeding regimes used during the shrimp lar- America from New Jersey to Brazil (Wil- val rearing process is a major objective of liams 1984). It is commonly associated with the larviculture operation. Effect of differ- hard coastal substrates such as jetties, rock ent foods on the larval survival and devel- outcropping, piers and buoys, and in asso- opment has not been tested for L. wurde- ciation with tubular , especially of manni. To develop rearing techniques for the genus Aplysina (Sefton and Webster the , we conducted a study using 1986). The genus Lysmafu is among the four different diets, Arfemia nauplii, rotifer many cleaner shrimps that are popular with Brachionus plicafilis, microalgae Chaefo- aquarists, because of their coloration and ceros gracilis and Isochrysis galbana. Ar- the ease with which they can be maintained remia nauplii were also tested as a potential food for the postlarvae and juveniles.

I Corresponding author. It is well known that temperature affects

Q Copyright by the World Aquaculture Society 1998

47 1 472 ZHANG ET AL. growth rate and development in decapod Artemia nauplii, and rotifer were renewed larvae, but study on the effect of fluctuating everyday. The experiment included the fol- temperature on the larval development is lowing four treatments (each with three rep- limited. In the present study, we also tested licates): newly hatched Artemia nauplii, ro- the effect of constant and fluctuating tem- tifer Brachionus plicatilis, microalgae peratures on larval development of the pep- Chaetoceros gracilis and Isochrysis gal- permint shrimp. bana. The nauplii were obtained daily by hatching (26 C for 20 h) the cysts of small Materials and Methods strain Artemia franciscana (grade 0 (plati- This study was conducted at Harbor num), Argent Chemical Laboratories). The Branch Oceanographic Institution, Inc., rotifer (fed with Chlorella) and algae Chae- Fort Pierce, Florida, USA, between Octo- toceros gracilis and Isochrysis galbana ber, 1995 and October, 1996. used in the experiment were from the cul- ture maintained by the Harbor Branch Larval Hatching Oceanographic Institution. In all the treat- Reproductive biology of L. wurdemanni ments, food was provided in excess. The is similar to that of L. ambionensis and L. density for Artemia nauplii was 5-10/mL, debelius (Fletcher et al. 1995; Simoes et al. rotifer 10-15/mL, Chaetoceros and Iso- 1998a). It is also a simultaneous hermaph- chrysis 50.000-100,000 cells/mL. All ex- rodite species. Fertilization occurs after perimental bottles were arranged randomly. molting and the eggs are retained under the Total length (TL) of 3 haphazardly selected adult’s abdomen where they hatch as zoea larvae were measured (to the nearest 0.1 larvae 10 to 12 d later. mm) using a micrometer under a dissecting The ovigerous shrimp were maintained in microscope every 2 or 3 d starting at day an indoor recirculating seawater system un- two. Number of surviving larvae were der 14 h light and 10 h dark. Temperature counted once every 3 to 5 d. fluctuated about 1-1.5 C daily (between 26 and 29.5 C during the study period). The Temperature Experiment shrimp were fed in excess with frozen Ar- temia or squid once a day. Any shrimp that The temperature study was carried out in was going to hatch was moved to a 270-L 200-mL beakers each containing 150 mL conical fiberglass tank equipped with an in- sterilized seawater of 30 ppt salinity and ternal standpipe with 53-pm mesh. After one larva. The larvae were fed with newly the shrimp had hatched and molted, it was hatched Artemia nauplii. Complete water returned to the broodstock tank. The newly and food changes were conducted daily. hatched zoea I larvae were kept in the fi- The beakers were placed in a water bath. berglass tank (without feeding) for about 26 Two constant temperatures: 26 and 28.5 C h, when they molted to zoea 11, before be- (maintained by a water bath with sub- ing transferred to the experimental beakers merged heaters in an indoor laboratory), for the food or temperature experiments. and two fluctuating temperatures (between 27 and 29 C, and between 26 and 30 C day Food Experiment and night) (maintained by a large and small For the food experiment, sibling larvae water bath with submerged heaters, respec- were placed in 4-L bottles with 2.5 L of sea tively, in an outdoor laboratory) were test- water (33-35 ppt salinity and 29 C temper- ed. Seven replicate beakers were used for ature), with gentle agitation by bubbling. each temperature treatment. The TL of the Each bottle contained 15 zoea I1 larvae. The shrimps was measured to the nearest 0.1 light intensity was 5.3-6.9 pmoVs per m. mm after each molting. Development time Water exchange rate was 50% daily. Algae, to postlarvae was recorded. EFFECTS OF FOOD AND TEMPERATURE ON PEPPERMINT SHRIMP 473

0-

E

0 b-

04 2 7 12 14 17 22 27 Time (d)

FIGURE 1. Total length of Lysrnata wurdernanni larvae fed with different foods.

Culture of Postlarvae and Juveniles Results Thirty postlarvae (mean 2 SD TL: 7 2 Food Experiment 1 mm, measured using a ruler to the nearest Survivorship of larvae fed with Artemia 1 mm), fed with newly hatched Artemia nauplii or rotifer (86.7% and 88.9%, re- nauplii since hatching, were put in a 25-L spectively) is significantly higher than that circular recirculate tank and were also fed fed with Chaetoceros (15.6%) or Zsochrysis with newly hatched Artemia nauplii (10- (13.3%) on day 15. Similar percentages 15/mL daily). The water (26.5-29 C, 30 (66.7% and 68.9%, respectively) of the lar- ppt) was changed (25%) every other day. vae fed with Artemia nauplii or rotifer The shrimp were observed daily until they reached the postlarval stage (t-test, P > reached sexual maturity (indicated by the 0.05). One way ANOVA results show that greenish developed gonad). Fifteen ran- significant (P C 0.001) difference in sur- domly selected shrimp were measured us- vivorship occurred after day 10 among the ing a ruler (TL to the nearest 1 mm) at day treatments. There was no significant (P > 30 and day 60. 0.05) difference between the Chaetoceros and Zsochrysis treatments, or between Ar- Data Analysis temia and rotifer treatments. However, sur- One-way analysis of variance (ANOVA) vivorship in Artemia or rotifer treatment was used to analyze the survivorship of the was significantly (P < 0.01) higher than larvae fed with different diets, and the ef- that in Chaetoceros or Zsochrysis treatment. fects of temperature on development time. A sharp decline in survival of larvae fed The T-method multiple comparison test was with the algae was observed after the 14th used to compare the means when ANOVA day. The larvae in the algal treatments shows significant effect (Sokal and Rohlf stayed at zoea I11 stage until all died on day 1995). Homogeneity of variance was as- 17; at that time the larvae fed with Artemia sessed using Bartlett’s test before ANOVA. nauplii or rotifer had reached mysis 111 stage. Student’s t-test was used to compare the The growth of larvae fed with different percentages of L. wurdemanni larvae fed diets are shown in Fig. 1. The larvae fed with Artemia and rotifer reaching postlarval with the algae did not grow after they be- stage. came zoea 111. Larvae fed with Artemia 474 ZHANG ET AL.

TABLE1. Mean (?SO. N = 7) total lengrh (mm) of different larval stages (2 = zoea, e.g., 21 = Zoea I; M = mysis. e.g., MI = Mysis I) of Lysmata wurdemanni reared at diFerent temperature regimes.

Temperature ZI ZII ZIII ZIV ZV ZVI 26.0 C 2.4 5 0.7 2.7 2 1.1 3.0 t 0.8 3.2 * 1.0 3.7 2 1.1 4.2 ? 0.8 28.5 C' 2.4 2 0.8 2.7 2 0.8 3.0 2 0.7 3.3 2 1.1 3.7 2 0.8 4.2 2 0.7 27-29 C 2.4 2 0.7 2.7 2 0.9 3.0 2 0.5 3.3 2 1.0 3.7 2 1.1 4.2 2 0.8 26-30 C 2.4 2 0.6 2.7 2 0.7 3.0 2 0.7 3.3 2 0.8 3.7 2 1.1 4.2 2 0.9 aN= 6 after zoea VII. nauplii developed faster, reaching postlar- Culture of Postlarvae and Juveniles vae 3 to 4 d earlier than those fed with ro- All the 30 postlarvae (7 2 1 mm TL) tifer. At 29 c, larvae fed with Artemia nau- survived to reach sexual maturity in 50 to plii and rotifer took 29-32 d and 32-36 d 70 d when they reached about 28 mm in to reach postlarval stage, respectively. The TL. The mean TL (fSD)of the shrimp at larvae readily metamorphosed to postlarvae day 30 and day 60 was 20 (52) and 28 in the experimental bottles. (22) mm, respectively. Temperature Experiment Discussion All larvae developed to postlarvae at 27- Food Experiment 29 C and 26 C. At 28.5 C, one larva died at zoea VII. At 2630 C one larva did not Algae are used to feed zoeal larvae of metamorphose to postlarva until day 65, penaeid shrimps (Gopalakrishnan 1976; To- and one larva stayed at zoea until it died on bias-Quinitio and Villegas 1982; Wilken- day 41. Multiple comparisons test (T-meth- feld et al. 1984; Cao et al. 1990). Addition od) revealed that the duration to postlarvae of algae also enable L. grabhami larvae to (mean 2 1 SD d) was not significantly (P survive longer (Blanchard 1992). However, > 0.05) different between 28.5 C (29.3 2 algae may not be appropriate food for L. 4.8) and 27-29 C (28.7 2 33, or between wurdemanni larvae (Crompton 1992). Ar- 26 C (37.4 2 5.4) and 26-30 C (40.2 f femiu nauplii and rotifers are suitable food 5.8). but significantly (P < 0.05) different for a variety of decapod larvae (Mc- between the two groups (28.5 C and 27-29 Conaugha 1985), including newly hatched C vs. 26 C and 26-30 C). The shortest de- larvae of Lysmata species (Crompton 1992; velopment time to metamorphosis, 25 d, Fletcher et al. 1995; present study). This is was recorded at 27-29 C: 13 d for zoeal different from penaeid shrimp larvae which stages (one d for zoea I to zoea 11, then two can only consume Artemia nauplii when d for each of the subsequent stages), and 12 they reach zoea 111, even mysis I stage. The d for the mysis stages (two d for each of zoea I larvae of L. wurdemanni (2.4 mm the stages). Larvae with prolonged devel- TL) is equivalent in size to mysis I stage of opment underwent 7 to 11 molts during the penaeid shrimps. Rotifer can be used as mysis stages with an intermolt of 3 to 4 d. food for L. wurdemanni larvae as well, al- One larva did not reach postlarva at 2630 though the larvae fed with rotifer or mi- C even after molting 17 times. croalgae grew slower than those fed with Although the rates of growth and devel- Artemia nauplii. This may be due to smaller opment were affected by temperature, TL size and/or less suitable nutrition content of of the larvae was similar among the tem- rotifers and microalgae. Food size is an im- perature treatments for each of the 13 larval portant consideration in the larval rearing stages (seven zoea and six mysis) (Table 1). (Frost 1972), as shown in seven decapod In general, larvae metamorphosed to post- species where small algae only occasionally larvae before reaching 8 mm in TL. support larval development compared to EFFECTS OF FOOD AND TEMPERATURE ON PEPPERMINT SHRIMP 475

TABLEI. Exrended.

ZVII MI MI1 MI11 MIV MV MVI 4.720.9 5.321.1 5.821.1 6.421.0 6.621.4 6.921.1 7.1 2 1.0 4.7 5 0.8 5.4 2 1.0 5.9 2 1.0 6.4 2 0.8 6.6 2 1.1 6.9 t 0.9 7.2 2 1.1 4.7 t 0.9 5.3 2 1.0 5.8 2 1.5 6.4 2 0.9 6.6 C 1.2 7.0 2 1.3 7.2 2 1.1 4.7 t 0.7 5.4 2 1.0 5.8 ? 1.4 6.4 2 0.8 6.6 2 1.7 6.9 2 1.2 7.1 2 1.5 larger algae (Harms and Seeger 1989). In Anger (1986) found a trend of decreasing decapod larvae, ingestion rate is normally carapace length with increasing temperature low for small sized food (Grahame 1983). in the shrimp Crangon crangon. However, Larvae may be able to select food based on zoeal larvae of a deep sea shrimp Pandalus size. Larger and later development borealis reach the same length at the same stages may take larger sized food (Grahame stage regardless of temperature (Wienberg 1983). Penaeus kerathurus postlarvae did 1982). Similar results were obtained in our not ingest rotifiers when Artemia were pres- study of L. wurdemanni. ent (Yufera et al. 1984). L. wurdemanni passes through at least 13 larval stages (seven zoea and six mysis) be- Temperature Experiment fore metamorphosing to the postlarval stage Temperature has been recognized as one in about 25 to 40 d after hatching (present of the main environmental factors affecting study), but can be as long as 67 d (Cromp- the development and growth of ton 1992). Variations in time to metamor- (Abele 1982). Within optimal temperature phosis has also been reported in L. ensiros- range, larval development time decreases tris and L. vittata (Abele 1982), and in L. with increasing (constant) temperature debelius (Fletcher et al. 1995). Temperature (Sastry 1977). Customarily, optimal tem- regime may play an important role in the perature for larvae is identified by subject- larval development rate and may be used to ing larvae to different constant tempera- shorten the larviculture duration. The larvae tures. However, larvae live in develop faster in L. wurdemanni than in the fluctuating temperature conditions in the other two Lysmata species that have aqua- natural environment. Larvae of the few culture potential: L. debelius (1 1-15 wk) and crustaceans cultured at fluctuating temper- L. ambionensis (20 wk) (Fletcher et al. 1995). ature survived and developed better than Culture of Postlarvae and Juveniles those at constant temperatures (Costlow and Artemia nauplii are also appropriate food Bookhout 1971; Sastry 1976, 1977). Our for the postlarvae and juveniles of Lysmata study also suggests that small fluctuating wurdemanni, as the 30 peppermint shrimp temperature ( 1.5-2.0 C daily) may be ben- all survived and reached sexual maturity in eficial for the development of L. wurde- 50 to 70 d. These shrimp had been fed with manni larvae. Poikilotherms are capable of Artemia nauplii since hatching. The high temperature compensation. They frequently survivorship of different life cycle stages of exhibit similar metabolic rates at widely L. wurdemanni fed on Artemia nauplii only different habitat temperatures. This process, and relatively short duration to sexual ma- however, consumes energy (Hazel and turity are very encouraging for the mass Prosser 1974). Therefore development and culture prospect of the species. growth, even survival, are affected when temperature fluctuation is too high. Acknowledgments In crustacean larvae, growth is closely This study was funded by Sea Grant, correlated with development. Criales and NOAA, Department of Commerce, USA 476 ZHANG ET AL.

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