Pacific Science (1999), vol. 53, no. 4: 361-366 © 1999 by University of Hawai'i Press. All rights reserved

Some Preliminary Findings on the Nutritional Status of the Hawaiian ( marginatus)l

FRANK A. PARRISH2 AND THERESA L. MARTINELLI-LIEDTKE3

ABSTRACT: Data on the nutritional status of spiny lobster (Panulirus margin­ atus) were collected on the commercial trapping grounds of Necker Bank, Northwestern Hawaiian Islands, in the summers of 1991, 1994, and 1995. Gly­ cogen levels measured in abdominal tissue of intermolt males were used as an index of nutritional health of the field population. The range of glycogen sampled from wild lobster was less than half the level measured in captive lob­ ster fed to satiation in a previous study. An analysis ofcovariance identified sig­ nificant interannual and spatial effects explaining 46% of the variance in the sample ofwild lobsters. Most significant was a decline in lobster glycogen levels between samples collected in 1991 and 1994-1995. Seasonal influences on lob­ ster nutrition are unknown and were identified as an obvious direction for future ecological research.

NUTRITIONAL CONDITION OF lobster, as as­ found to be the best index of nutritional sta­ sessed in the field, could be a valuable tool to tus tested for this (Figure 1). Tests of provide insight to physiological response of within-lobster variability indicated that a lobster to environmental constraints. The single sample per lobster was adequate for nutritional status ofpa1inurids in the wild has analysis (Martinelli 1993). The positive linear been little studied (Kanciruk 1980). Studies relationship between recency of feeding and of lobster nutrition have centered on needs lobster glycogen concentration provided a associated with rearing and aquaculture relational indicator that could be used to (Kanazawa 1994). Only recently have labo­ document spatial or temporal variation in the ratory trials of nutritional indices been ap­ nutritional status of field populations. plied to address ecological issues (Moss 1994, Blood glucose concentration is controlled Robertson et al. 1996). The work reported by homeostatic mechanisms in many deca­ here used an index of lobster nutritional sta­ pod species (Heath and Barnes 1970, Dall tus on a managed field population to provide 1974). Glucose is held in reserve deposits as some preliminary data on field nutrition and glycogen that can be depleted during periods to discuss it in relation to a period of popu­ of reduced food consumption to maintain lation growth. blood glucose concentrations near normal A number of nutritional indices were levels. Although the digestive gland is con­ evaluated by Martinelli (1993) using Pan­ sidered the main organ for storage of nutri­ ulirus marginatus in controlled, replicated, tional reserves in decapods, its importance as month-long laboratory trials. The concentra­ a storage organ relative to muscle tissue is tion of glycogen in abdominal muscle was variable among species (Armitage et al. 1972, Dall 1981, Barclay et al. 1983, Whyte et al. 1986). When P. marginatus is nutritionally 1 Manuscript accepted 29 January 1999. stressed, it catabo1izes abdominal muscle 2 Honolulu Laboratory, Southwest Fisheries Science glycogen reserves (Martinelli 1993). Storage Center, National Marine Fisheries Service, NOAA, 2570 of glycogen in abdominal muscle, like most Dole Street, Honolulu, Hawai'i 96822-2396. physiological processes in lobster, is influ­ 3 U.S. Geological Survey, Biological Resources Divi­ sion, Columbia River Research Laboratory, 5501A enced by molt stage (Heath and Barnes Cook-Underwood Road, Cook, Washington 98605. 1970). 361 362 PACIFIC SCIENCE, Volume 53, October 1999

20 ,------, ment cruises. The annual cruise revisits es­ 18 tablished stations in the NWHI and conducts standardized trap fishing. The annual assess­ 16 ment was conducted just before the commer­ 0;14 cial season, which was open July-December. C> This ensured that lobster sampled had not .s 12 been previously disturbed by the baiting and :ii 10 0) trapping activities of other fishing vessels. In o 8 o this paper we make temporal and spatial >. comparisons of lobsters from the assessment a 6 • Fed lobsters y=13.6-0.005x, 2 stations of Necker Bank (Figure 2). Stations 4 P=0.95, r =0.001, n=42 were selected to represent the range in types 2 0 Starved lobsters y=11.7-0.214x, of bottom habitat that had been documented 2 r O+---'--,...::..:.c:...:....:.;..:-----=-~e..:..:.-.:,.:....-~-~-__lP=0.001, =0.91, n=39 in previous surveys (parrish and Polovina o 5 10 15 20 25 30 1994). Days of Treatment Lobster glycogen concentrations were sampled at stations A and B in July 1991, FIGURE 1. Laboratory trials of lobster glycogen con­ May 1994, and June 1995. For the 1994 and centration plotted relative to days of treatment. Each 1995 collections, two additional stations (C data point represents multiple lobster (mean = 7, and D) were included. At each station, the maximum = 9). Filled circles are lobster fed daily and open circles are lobster starved. Confidence intervals glycogen levels of at least 25 male lobster (95%) are included for both treatments. A consistent representing the size range of the catch were and significant decline is measurable using the glycogen tested. To avoid potential influence of molt assay to assess starved lobsters. (Source: Martinelli 1993) stage on glycogen level (Lipcius and Herrn­ kind 1982), the molt stage of the males was determined using Lyle and MacDonald's The commercial stock of P. marginatus (1983) technique to ensure that only lobsters occurs in the remote Northwestern Hawaiian in intermolt were included in the analysis. A Islands (NWHI) and has been fished ex­ sample of abdominal muscle tissue was ex­ clusively by commercial vessels beginning in tracted from each lobster and analyzed for the early 1970s. Consequently, all fishery glycogen content (Martinelli 1993). Females effort is documented. In 1991, catch per unit were excluded from all analyses to remove of effort (CPUE) dropped to rougWy half the any possible effects on nutrition associated level used to designate optimum sustainable with egg production (Hermkind 1980). yield (i.e., one lobster per trap), prompting Standard analysis of covariance (AN­ temporary closure of the fishery. Since then, COYA) was used with the glycogen data to fishing has been restricted by quota and sea­ assess interannual and spatial effects and son to permit the stock to recover (Haight effects of lobster size. Because of the unbal­ and DiNardo 1995). All glycogen sampling anced design associated with absence of occurred during the period of stock recovery. samples for stations C and D in 1991, the Sampling during a period of increasing pop­ ANCOVA was rerun excluding the 1991 ulation density provided an opportunity to data. look for an expected density-dependent de­ cline in lobster condition using the glycogen index. RESULTS Eleven of the collected lobster were ex­ cluded from analysis because they were in MATERIALS AND METHODS premolt condition. Lobster carapace length Lobster were collected as part of the Na­ ranged between 39 and 110 mm. Plotting the tional Marine Fisheries Service (NMFS) size frequency of lobster measurements in­ Honolulu Laboratory's (HL) lobster assess- dicated that distributions were similar for all Nutritional Status of the Hawaiian Spiny Lobster-PARRISH AND MARTINELLI-LIEDTKE 363

164°50 164°25 23°50 ---- "10 --- 0 /)-;,, \ I \ I I I I I {~:' Necker Is, \ \ \ \ \ \ \ B \ Midway c '- -"" -----­ Ii> Atoll •• Q •• ~, ""'" NECKER BANK 23°30

NORTHWESTERN HAWAIIAN ISLANDS

MAIN PACIFIC OCEAN HAWAIIAN iSLANDS III I lBO' 175' 170' 165' 180' 155'

FIGURE 2, Hawaiian Archipelago with an inset of Necker Bank indicating the locations of the four trapping sta­ tions.

samples except one (mean CL 8 em) (Figure 12 . 3). The exception was the 1991 sample at . 10 . station A, which provided smaller lobsters Ci . ' . (mean CL 4.5 em). The ANCOVA identified -Cl 8 . .' significant temporal and spatial effects ex­ S ~ .. c . . . . plaining 46% of the sample variance (Table Q) 6 '" .' Cl ",., .. 1). No size-specific differences were identi­ 0 ... • ..-•...... (,) i·..... fied. Lobsters collected in July 1991 had sig­ >. 4 .. .. l':'.' .. .. '" .I",t-"~•• nificantly better nutritional condition (higher (; ... , .. 2 .- ;;I~""... , .. ~ ...... glycogen) than the samples of May 1994 and •..'l'., ~.. .. June 1995 (Duncan multiple range test, 0 P < 0.01, df = 279). An a posteriori test of 4 6 8 10 12 spatial effects grouped two stations (A and Lobster carapace length (em) D) as having lobster in significantly better FIGURE 3. Plot of glycogen levels versus carapace condition than at the other two stations length of each lobster sampled. Samples collected in (Duncan multiple range test, P < 0.01, df = 1991 are indicated with triangles. Circles indicate sam­ 279). The 1991 data were then removed to ples collected during 1994 and 1995. 364 PACIFIC SCIENCE, Volume 53, October 1999

TABLE 1

ANCOVA TABLE OF LoBSTER GLYCOGEN LEVELS RELATIVE TO LOBSTER SIZE, YEAR OF COLLECTION, AND STATION

VARIABLE SS df MS FSTATISTIC PVALUE

Size 0.00018 1 0.0001 0.00 0.99 Year 349.4 2 174.7 59 0.0001 Station 125.8 3 41.9 14.1 0.0001 balance the sampling design and fully focus The reason for the significant drop in gly­ the analysis on the spatial effects. Without cogen levels between 1991 and 1994-1995 is the 1991 data, significance for station A dis­ unknown. The change coincides with the appeared, and data from station A were closure of the fishery and regrowth of the lumped with those from stations Band C in stock (Haight and DiNardo 1995). The stock overlapping classifications (Duncan multiple recovery leveled in 1994 and 1995 and the range test, P < 0.01, df = 235). Station D fishery continues to be exploited near opti­ alone was identified as having lobsters in sig­ mum sustainable yield (e.g., CPUE of 1.0) nificantly better condition. Even with the maintaining a constant population density 1991 data excluded, weak interannual effects (DiNardo et al. 1998). The drop in glycogen persisted (P = 0.052, F = 3.82, R2 = 0.16, values from 1991 to 1994-1995 is consistent df = 1). with a reduction in available resources (e.g., food and shelter) associated with increasing lobster density resulting from the stock re­ DISCUSSION covery. This interpretation parallels findings The nutritional condition of a lobster is in of other researchers who identified density­ part dependent on its foraging success. Lob­ dependent responses during declines in the sters foraging in the wild feed as they en­ Hawaiian lobster stock (Polovina 1989, De­ counter and capture food. The amount of Martini et al. 1992). food, as well as the time between feeding Spatial effects were minor but did persist events, varies with local resources and lobster between years, suggesting that station­ activity. Assessing glycogen concentration specific influences on lobster condition could permits comparison of relative nutritional be present. Different habitats are likely to states between groups of lobster. The mean afford different levels of forage and/or shelter glycogen concentrations reported from field resources. Previous research at Necker Bank at Necker ranged from 1.3 to linked lobster catch rates with variable scales 5.3 mg/g. As expected, this range is consid­ of habitat relief (parrish and Polovina 1994). erably lower than the glycogen values of Perhaps greater availability of shelter im­ captive lobster, which were fed daily. Lobster proves access to forage and results in higher fed to satiation had an overall mean glycogen glycogen levels. Enhanced growth in re­ concentration of 12.7 mg/g (Figure 1), and sponse to improved shelter has been identi­ even the lobsters that were starved for 21 fied by researchers working on other lobster days (after being fed to satiation) had higher species (Newman and Pollock 1974, Eggle­ glycogen values (mean = 6.2 mg/g) than ston and Lipcius 1992). those of field lobsters. Influences of life history and ecology on Effect of lobster size was nonsignificant lobster glycogen levels should be fully inves­ and excluded from the analysis. However, tigated. Because of the logistical constraints the sampling design was not structured to on sampling in this study, the observed tem­ evaluate size, so the potential influence ofsize poral variability could actually relate more to in future nutritional studies should not be cyclic seasonal effects than to interannual dismissed. Size was included in this analysis changes (Dow 1969). Data for our study as a precautionary measure only. were collected spanning six summer weeks Nutritional Status of the Hawaiian Spiny Lobster-PARRISH AND MARTINELLI-LIEDTKE 365

(late May to mid-July), which may represent the tiger prawn, Penaeus esculentus Has­ different physiological stages of the lobster. well. J. Exp. Mar. BioI. Ecol. 68: 229-244. For example, the samples with the highest DALL, W. 1974. Indices of nutritional state glycogen levels (1991) were collected latest in in the western rock lobster, Panulirus the season (mid-July), which may have con­ longipes (Milne Edwards). 1. Blood and tributed to their high glycogen values. It is tissue constituents and water content. J. possible that lobster glycogen levels are re­ Exp. Mar. BioI. Ecol. 16: 167-180. lated to the length of time the lobster have ---. 1981. Lipid absorption and utiliza­ fed on high summer benthic productivity tion in the Norwegian lobster, Nephrops (Doty 1971, Glenn et al. 1990, Martin-Smith norvegicus (L.). J. Exp. Mar. BioI. Ecol. 1992). In summer months catch rates im­ 50: 33-45. prove (Polovina et al. 1995), but it is un­ DEMARTINI, E. E., D. M. ELLIS, and V. A. known whether this results from an increase HONDA. 1992. Comparison of spiny lob­ in lobster activity or is caused by calmer ster Panulirus marginatus fecundity, egg weather improving trap catchability (Morgan size, and spawning frequency before and 1974). For captive P. japonicus, a species after exploitation. Fish. Bull. 91 : 1-7. closely related to P. marginatus, Nakamura DINARDO, G. T., W. R. HAIGHT, and J. A. and Kuramoto (1992) found that the heart WETHERALL. 1998. Status oflobster stocks rate doubled in summer months and varied in in the Northwestern Hawaiian Islands, relation to temperature. Peak spawning sea­ 1995-97, and outlook for 1998. Honolulu son for lobster in the Hawaiian Archipelago Laboratory, Southwest Fisheries Science varies with the latitude of the population, Center, National Marine Fisheries Ser­ suggesting that lobster may be influenced by vice, NOAA, Honolulu, Hawai'i. South­ environmental cues such as temperature or west Fisheries Science Center Administra­ photic period (McGinnis 1972, MacDonald tive Report. 35 pp. and Thompson 1987, Polovina and Moffitt DoTY, M. S. 1971. Antecedent event influ­ 1995). Further work is needed to determine ence on benthic marine algal standing and calibrate the source of glycogen vari­ crops in Hawaii. J. Exp. Mar. BioI. Ecol. ability in wild lobster. Future ecological re­ 6: 161-166. search should first focus on detecting any Dow, R. L. 1969. Cyclic and geographic changes in lobster nutrition in relation to trends in seawater temperature and abun­ season. dance of American lobster. Science (Washington, D.C.) 164: 1060-1063. EGGLESTON, D. B., and R. N. LIPCIUS. 1992. ACKNOWLEDGMENTS Shelter selection by spiny lobster under variable predation risk, social conditions, Helpful advice and reviews were provided and shelter size. Ecology 73 : 992-1011. by W. R. Haight, E. E. DeMartini, G. T. GLENN, E. P., C. M. SMITH, and M. S. DOTY. DiNardo, J. D. Parrish, and C. D. Mac­ 1990. Influence of antecedent water tem­ Donald. peratures on standing crop of a Sargassum spp.-dominated reef flat in Hawaii. Mar. BioI. (Bed.) 105: 323-328. HAIGHT, W. R., and G. T. DINARDO. 1995. LITERATURE CITED Status of lobster stocks in the Northwest­ ARMITAGE, K. B., A. L. BUKEMAN, and N. J. ern Hawaiian Islands, 1994. Honolulu WILLEMS. 1972. Organic constituents in Laboratory, Southwest Fisheries Science the annual cycle of the crayfish Orconectes Center, National Marine Fisheries Ser­ nais. Compo Biochem. Physiol. A Compo vice, NOAA, Honolulu, Hawai'i. South­ Physiol. 41 : 825-842. west Fisheries Science Center Administra­ BARCLAY, M. c., W. DALL, and D. M. tive Report H-95-03. 17 pp. SMITH. 1983. Changes in lipid and protein HEATH, J. R., and H. BARNES. 1970. Some during starvation and the molting cycle in changes in biochemical composition with 366 PACIFIC SCIENCE, Volume 53, October 1999

season and during the molting cycle of the ster, Panulirus cygnus George. II. Seasonal common shore crab, Carcinus meanus changes in the catchability coefficient. (L.). J. Exp. Mar. BioI. Ecol. 5: 199-233. Aust. J. Mar. Freshwater Res. 25: 249­ HERRNKIND, W. F. 1980. Spiny lobsters: Pat­ 259. terns of movements. Pages 349-407 in J. Moss, S. M. 1994. Use of nucleic acids as S. Cobb and B. F. Phillips, eds. The biol­ indicators of growth in juvenile white ogy and management of lobster. Vol. 1, shrimp, Penaeus vannamei. Mar. BioI. Physiology and behavior. Academic Press, (Berl.) 120: 359-367. New York. NAKAMURA, M., and T. KURAMOTO. 1992. KANAZAWA, A. 1994. Nutrition and food. Effects of cooling on the heart beat of the Pages 483-494 in B. F. Phillips, J. S. Japanese spiny lobster in vivo. Zool. Sci. Cobb, and J. Kittaka, eds. Spiny lobster (Tokyo) 9 (6): 12-16. management. Blackwell Scientific Pub­ NEWMAN, G. G., and D. E. POLLOCK. 1974. lications, Oxford. Growth of the rock lobster Jasus lalandii KANCIRUK, P. 1980. Ecology ofjuvenile and and its relationship to benthos. Mar. BioI. adult Palinuridae (spiny lobsters). Pages (Berl.) 24: 339-346. 59-96 in J. S. Cobb and B. F. Phillips, eds. PARRISH, F. A., and J. J. POLOVINA. 1994. The biology and management of lobster. Habitat thresholds and bottlenecks in Vol. 2, Ecology and management. Aca­ production of the spiny lobster (Panulirus demic Press, New York. marginatus) in the Northwestern Hawai­ LIPCIUS, R. N., and W. F. HERRNKIND. 1982. ian Islands. Bull. Mar. Sci. 54: 151-163. Molt cycle alterations in behavior, feeding POLOVINA, J. J. 1989. Density dependence in and diel rhythms of a decapod , spiny lobster, Panulirus marginatus, in the the spiny lobster, Panulirus argus. Mar. Northwestern Hawaiian Islands. Can. J. BioI. (Berl.) 68: 241-252. Fish. Aquat. Sci. 46: 660-665. LYLE, W. G., and C. D. MACDONALD. 1983. POLOVINA, J. J., and R. B. MOFFITT. 1995. Molt stage determination in the Hawaiian Spatial and temporal distribution of the spiny lobster, Panulirus marginatus. J. phyllosoma of the spiny lobster, Panulirus Crustacean BioI. 3: 208-216. marginatus, in the Northwestern Hawaiian MACDONALD, C. D., and B. E. THOMPSON. Islands. Bull. Mar. Sci. 56: 406-417. 1987. Characteristics of a recreational POLOVINA, J. J., W. R. HAIGHT, R. B. MOF­ fishery for Hawaiian spiny lobsters at the FITT, and F. A. PARRISH. 1995. The role of Midway Islands. N. Am. J. Fish. Manage. benthic habitat, oceanography, and fishing 7: 194-201. on the population dynamics of the spiny MARTINELLI, T. L. 1993. Nutritional indices lobster, Panulirus marginatus (, for the Hawaiian spiny lobster, Panulirus Palinuridae) in the Hawaiian Archipelago. marginatus. M.S. thesis, University of Crustaceana (Leiden) 68: 203-212. Hawai'i at Manoa, Honolulu. ROBERTSON, D., M. J. BUTLER, and F. C. MARTIN-SMITH, K. M. 1992. Seasonal varia­ DOBBS. 1996. Evaluation of potential in­ tion in tropical benthic Sargassum and as­ dices of nutritional condition of the Ca­ sociated motile epifauna. Proceedings of ribbean spiny lobster. Page 71 in Proceed­ the 7th International Coral Reef Sympo­ ings of the 24th Annual Benthic Ecology sium, Guam 2: 881-886. Meeting, Columbia, South Carolina, 7-10 McGINNIS, F. 1972. Management investiga­ March. tion of two species of spiny lobsters, WHYTE, J. N. c., R. R. ENGLAR, B. L. CAR­ Panulirus japonicus and P. penicillatus. SERLL, and K. E. MEDIC. 1986. Influence Division of Fish and Game, Department of starvation and subsequent feeding on of Land and Natural Resources, State of body composition and energy reserves in Hawai'i. 47 pp. the prawn, Pandalus platyceros. Can. J. MORGAN, G. R. 1974. Aspects of the popu­ Fish. Aquat. Sci. 43: 1142-1148. lation dynamics of the western rock lob-