Spatial Variability in Growth and Prey Availability of Lobsters in the Northwestern Hawaiian Islands

Vol. 449: 211–220, 2012 MARINE ECOLOGY PROGRESS SERIES Published March 8 doi: 10.3354/meps09533 Mar Ecol Prog Ser Spatial variability in growth and prey availability of lobsters in the northwestern Hawaiian Islands Joseph M. O’Malley1,4,*, Jeffrey C. Drazen2, Brian N. Popp3, Elizabeth Gier3, Robert J. Toonen1 1Hawaii Institute of Marine Biology, University of Hawai‘i at Ma-noa, Ka-ne‘ohe, Hawai‘i 96744, USA 2Department of Oceanography, University of Hawai‘i at Ma-noa, Honolulu, Hawai‘i 96822, USA 3Department of Geology and Geophysics, University of Hawai‘i at Ma-noa, Honolulu, Hawai‘i 96822, USA 4Present address: Joint Institute for Marine and Atmospheric Research, Research Corporation of the University of Hawai‘i, Honolulu, 96822 Hawai‘i, USA ABSTRACT: Proximate composition, bulk tissue and amino acid compound-specific nitrogen isotopic analyses (CSIA) were used to determine whether dietary differences were responsible for the spatial variability in growth of spiny lobster and slipper lobster in the Northwestern Hawaiian Islands (NWHI). Abdominal tissues were collected and analyzed from both species at Necker Island and Maro Reef from 2006 to 2008. Protein and lipid levels did not differ significantly between locations in either species. Bulk tissue 15N of both species was significantly negatively correlated with growth for both species; however, the analysis assumed constant isotopic composition of autotrophs across this region. CSIA, which accounts for 15N variability at the base of the food web, indicated that spiny lobsters at both locations occupied the same trophic position whereas the slower-growing Maro Reef slipper lobsters fed at a lower trophic position relative to Necker Island slipper lobsters. Spatial variability in the abundance or diversity of preferred prey items appears to be responsible for the spatial variability in growth and the specific morphology and behavior of these species dictated how they coped with dietary restraints. These findings increase the understanding of NWHI coral reef ecosystem processes as well as highlight dangers of using consumer bulk tissue isotopic data without considering variation in the nitrogen isotopic composition at the base of the food web. KEY WORDS: Proximate composition · Panulirus marginatus · Scyllarides squammosus · Bulk stable isotope · Compound-specific isotopic analysis · Trophic level Resale or republication not permitted without written consent of the publisher INTRODUCTION vest levels and the potential of stock collapse. Deca- pod crustaceans are particularly vulnerable because Identifying the drivers of somatic growth variability spatial variability in growth has been demonstrated is important when seeking an understanding of eco - in nephrop (Fogarty 1995, Wahle & Fogarty 2006), system dynamics. It becomes essential if the variabil- palinurid (McGarvey et al. 1999, O’Malley 2009) and ity adds spatial structure to a species exploited by a scyllarid lobsters (O’Malley 2011). fishery striving for effective, sustainable manage- A commercial fishery targeted Hawaiian spiny lob- ment (Pollock 1991, Rindorf et al. 2008). Without ster Panulirus marginatus and scaly slipper lobsters understanding the drivers, growth estimates may be Scyllarides squammosus in the Northwestern Hawai- applied erroneously to subsets of a metapopulation, ian Islands (NWHI), a series of islands, reefs, sea - leading to biased yield estimates, inappropriate har- mounts and atolls (hereafter referred to as banks) *Email: [email protected] © Inter-Research 2012 · www.int-res.com 212 Mar Ecol Prog Ser 449: 211–220, 2012 extending approximately 2000 km across the sub- exploitation allozyme frequency analysis found a sin- tropical Pacific (Fig. 1). Recaptures from a 2002−2008 gle panmictic stock throughout the Hawaiian Archi- mark/recapture study revealed spatial variability in pelago (Shaklee & Samollow 1984) and postexploita- the growth of both NWHI lobster species. Specifi- tion of allozyme frequency analysis in Necker Island cally, spiny lobster growth at Necker Island, located and Maro Reef spiny lobster found no differences in at the southeastern end of the NWHI, was approxi- 6 out of 7 loci (Seeb et al. 1990). Likewise, a recent mately one-third that of spiny lobster at Gardner Pin- survey of 27 taxonomically and ecologically diverse nacles and Maro Reef, located in the middle of the species (including reef fishes, marine mammals, gas - NWHI (O’Malley 2009). During the same time, slip- tro pods, echinoderms, cnidarians and crustaceans) per lobsters, particularly males, grew fastest at revealed multiple shared barriers to dispersal along Necker Island with growth declining in a northwest- the length of the Hawaiian Archipelago, but none ern gradient (O’Malley 2011). These results led to between Necker Island and Maro Reef (Toonen et al. a revision of the NHWI lobster population dynamic 2011). Also doubtful is genetic selection for slower- theory from a single archipelago-wide population to growing individuals from intense fishing pressure a series of discrete species-specific meta populations (Con over & Munch 2002), based on the historically separated by the deep water between banks and smaller spiny lobsters at Necker Island (Uchida et al. connected only by larval dispersal. 1980) and the similar levels of exploitation of both spe- Common drivers of crustacean growth were exam- cies at Necker Island,Gardner Pinnacle and Maro Reef. ined to understand the spatial variability in NWHI Diet also has a large influence on crustacean lobster growth. The first, density dependence (Mc - growth (Conklin 1980, Dall & Moriarty 1983, Mente Garvey et al. 1999, Pollock 1991), was not supported 2003). Food availability and quality influenced the because analysis of individual- and bank-specific spatial growth dynamics of South African rock lob- growth rates relative to density indicated no relation- ster Jasus lalandii (Mayfield et al. 2000) and Western ship for either species (O’Malley 2009, 2011). Tem - Australian rock lobster Panulirus cygnus (Edgar pera ture, the primary environmental influence on 1990). The diet of NWHI lobsters is unknown and, crusta cean growth because of its effect on meta bo - despite recent research efforts in the NWHI (Fried- lism (Chittleborough 1975, Wahle & Fogarty 2006, lander et al. 2009), very little is known about the Delestang et al. 2009), did not have an association diversity and abundance of potential lobster prey with annual NWHI spiny lobster growth variability items at any bank. However, opportunistic sampling (O’Malley 2009). Spatially separated stocks, some of abdominal tissue from both lobster species at genetically predisposed to slower growth, were also Necker Island and Maro Reef from 2006 through deemed unlikely because spiny lobster pre- 2008 enables the use of biochemical techniques to infer that differences in diet may be responsible for the spatial variability in growth. Nutritional condition can be as - sessed using proximate composition ana lysis because lipids are important stores of energy (Chang & O’Connor 1983, Torres et al. 1994, Drazen 2002) and protein synthesis is required for growth (Claybrook 1983). Within palinurid lobsters, hepatopancreas lipid content showed a positive correlation with growth of Jasus lalandii (Cock- croft 1997) and abdominal tissue and hepa topancreas protein concentra- tions were significantly lower in starving Panulirus longipes (Dall 1974). Dietary differences can be inferred Fig. 1. The Hawaiian Archipelago, including the Northwestern Hawaiian Is- from the results of bulk tissue stable lands. Study sites are Necker Island, Gardner Pinnacles, Maro Reef and isotope analysis with carbon isotopic Laysan Island composition (13C/12C) identifying the O’Malley et al.: NWHI lobster variability 213 source of primary production (DeNiro & Epstein tissue isotopic analysis) or differences in trophic posi- 1978, Peterson & Fry 1987) and nitrogen isotopic tion that indicate different prey items (bulk tissue iso- composition (15N/14N) revealing trophic dynamics topic analysis and CSIA). CSIA will also indicate (DeNiro & Epstein 1981, Minagawa & Wada 1984). whether spiny lobster and slipper lobster bulk tissue Starvation can also be identified using nitrogen sta- δ15N values are controlled by trophic level or the iso- ble isotope analysis because the tissue of starving topic composition at the base of the food web. individuals can be enriched in 15N relative to healthy individuals due to catabolic processes (Hobson et al. 1993, Adams & Sterner 2000). However, the δ15N MATERIALS AND METHODS value of a consumer reflects not only its trophic level but also the δ15N value of the primary producers at Tissue collection the base of the food web (e.g. Post 2002, Popp et al. 2007). Therefore, spatial comparisons of bulk isotopic Necker Island and Maro Reef spiny lobster and data, parti cularly trophic position, are compromised slipper lobster abdominal tissue samples were col- without establishing an isotopic baseline at each lected during the 2006−2008 NWHI lobster tag/ location (Post 2002, Lorrain et al. 2009). recapture cruises (O’Malley 2009, 2011). Lobsters Two methods are available to quantify isotopic com- were chosen at random during trapping operations at positions at the base of a food web. The first is to de- each bank but individuals within specific carapace termine the bulk isotopic value of primary producers lengths (spiny lobster = 72.0−118.0 mm; slipper lob- or primary consumers supporting the predator’s

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