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Population Structure of Spiny Lobsters in Hawaii Following a Fishery Closure and the Implications for Contemporary Spatial Management

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Population Structure of Spiny Lobsters in Hawaii Following a Fishery Closure and the Implications for Contemporary Spatial Management Bull Mar Sci. 90(1):331–357. 2014 research paper http://dx.doi.org/10.5343/bms.2013.1042 After the gold rush: population structure of spiny lobsters in Hawaii following a fishery closure and the implications for contemporary spatial management 1 Hawai‘i Institute of Marine Matthew Iacchei 1, 2 * Biology, School of Ocean and Joseph M O’Malley 3 Earth Science and Technology, 1 University of Hawai‘i at Mānoa, Robert J Toonen P.O. Box 1346, Kaneohe, Hawaii 96744. 2 Department of Biology, ABSTRACT.—We compared mitochondrial genetic data University of Hawai‘i at Mānoa, for two spiny lobsters in Hawaii with different geographic 2450 Campus Road, Honolulu, ranges and histories of fishing pressure. Panulirus Hawaii 96822. marginatus (Quoy and Gaimard, 1825) is endemic to Hawaii, 3 NOAA Fisheries, Pacific Island and experienced a short, intense fishery in the Northwestern Fisheries Science Center, 2570 Hawaiian Islands (NWHI) and long-term, less intense Dole St., Honolulu, Hawaii 96822. exploitation in the Main Hawaiian Islands (MHI). Populations * Corresponding author email: show significant overall structure F( ST = 0.0037, P = 0.007; <[email protected]>. Current Dest_Chao = 0.137), with regional differentiation F( CT = 0.002, P = address: School of Ocean and 0.047) between the MHI and the NWHI. Haplotype diversity Earth Science and Technology, did not differ significantly between regions (F2, 8 = 3.740, P = University of Hawai‘i at Mānoa, 0.071); however, nucleotide diversity is significantly higher at 1000 Pope Rd., Honolulu, Hawaii the primary NWHI fishery banks (0.030) than in the MHI 96822. (0.026, Tukey’s P = 0.013). In contrast, Panulirus penicillatus (Olivier, 1791), found across the tropical Indo-West Pacific region, was not targeted by the NWHI fishery, but has experienced long-term exploitation in the MHI. Panulirus penicillatus has no significant overall population structure in Hawaii (FST = 0.0083, P = 0.063; Dest_Chao = 0.278), although regional differentiation F( CT = 0.0076, P = 0.0083) between the MHI and the NHWI is significant. Neither haplotype nor nucleotide diversity differed significantly between regions for P. penicillatus. While neither species has suffered a loss of genetic diversity from fishing, our results highlight that only by incorporating knowledge of fishing history with genetic connectivity data can we understand the most beneficial management strategy for each species. Neither exemplar Date Submitted: 15 May, 2013. Date Accepted: 20 November, 2013. species nor specific suites of traits are reliable predictors of Available Online: 7 January, 2014. the spatial scales of management. Interest has increased in establishing effective marine protected areas for species conservation and management to meet the goals of ecosystem-based management (Browman and Stergiou 2004, 2005, Gerber et al. 2007, Beger et al. 2014). An es- sential data requirement for evaluating whether marine protected areas are properly sized and located for effective species management is detailed information regarding connectivity among disjunct habitats (e.g., Botsford et al. 2001, Botsford et al. 2003, Halpern and Warner 2003, Palumbi 2004, Cowen et al. 2006). The size and number of connected populations and frequency of larval influxes can profoundly influence Bulletin of Marine Science 331 © 2014 Rosenstiel School of Marine & Atmospheric Science of OA the University of Miami Open access content 332 Bulletin of Marine Science. Vol 90, No 1. 2014 the density and persistence of individuals at specific locales (MacArthur and Wilson 1963, Stacey and Taper 1992, Sale and Kritzer 2003). This fact is notably pertinent for benthic marine invertebrates living in remote island chains where isolated lo- cations are more likely connected through larval dispersal than adult movement. Unfortunately, the pelagic developmental period of most invertebrate larvae, coupled with a small size and often directed movement to either avoid or take advantage of the prevailing oceanographic currents, make larvae extremely difficult to track (reviewed by Levin 2006). The poor understanding of population connectivity in or- ganisms with a biphasic life cycle and pelagic larval development has confounded the management of these marine species (Carr et al. 2003, López-Duarte et al. 2012). An example of this is the Northwestern Hawaiian Islands (NWHI) lobster fishery, which began in 1976 and principally targeted the endemic Hawaiian spiny lobster, Panulirus marginatus (Quoy and Gaimard, 1825), as well as the scaly slipper lobster, Scyllarides squammosus (H. Milne-Edwards, 1837). The Hawaiian Archipelago consists of the Main Hawaiian Islands (MHI, Hawaii to Niihau), and the NWHI, a series of islands, reefs, seamounts, and atolls (hereafter referred to as banks) that extend approximately 2000 km across the subtropical Pacific (Fig. 1). From 1976 to 2000, this NWHI lobster fishery reported landings of spiny and slipper lobsters totaling 11 million individuals (table 1 in Schultz et al. 2011). Landings peaked within 7–9 yrs (1983–1985; DiNardo et al. 2001), during which time it was Hawaii’s most valuable demersal fishery (Polovina 1993). However, both reported landings (DiNardo et al. 2001) and catch per unit effort C( PUE; fig. 2 in O’Malley 2009) steadily declined over the next decade (1986–1995). Despite almost yearly stock assessments and a variety of management measures, the National Marine Fisheries Service (NMFS) ultimately closed the fishery in 2000 because of increasing uncertainty in population and stock assessment models, particularly with regard to spatial heterogeneity and the assumption of synchronous dynamics among bank-specific stocks B( otsford et al. 2002). Since the closure of the fishery, there has been no evidence of recovery of either species (O’Malley 2009, 2011). In 2006, the entire NWHI region was protected as the Papahānaumokuākea Marine National Monument (PMNM). The non- extraction nature of the PMNM ensures that lobster fishing will not likely resume in the NWHI. Extensive subsequent research has justified the concerns of NMFS lobster fish- ery managers. O’Malley presents evidence for both spatial and temporal differences in growth rates of P. marginatus (2009) and S. squammosus (2011) across the three primary banks targeted by the fishery (Necker Island, Maro Reef, and Gardner Pinnacles), and an additional location closed to fishing throughout most of the fish- ery’s duration (Laysan Island). The results of these studies indicate that both spiny and slipper lobsters at each of these islands or atolls are experiencing different envi- ronmental conditions and/or varied prey regimes (O’Malley et al. 2012). Less well known is whether lobsters at each of the islands and atolls in the Hawaiian Archipelago are genetically isolated populations that are locally adapting to these bank-specific dynamics, or if this is one single population with phenotypically plastic traits that vary from bank to bank. Quantitative estimates of population connectiv- ity are required to develop models that more accurately represent island/bank spe- cific population dynamics. Results from tagging studies indicate that adult lobsters do not traverse the deep-water channels between banks. Not one of approximately 85,000-tagged lobsters was recaptured on a different bank (O’Malley and Walsh Iacchei et al.: Comparative population structure in spiny lobsters 333 Figure 1. Map of lobster specimen collection locations and number of individuals of Panulirus marginatus (bold font) and Panulirus penicillatus (italicized font) sampled at each location. Due to low sample size, site/species combinations identified with an asterisk were not included in the pairwise population analysis, but were included in the overall analysis of genetic diversity, as well as in the median joining networks. The distinction between the Main Hawaiian Islands (MHI) and the Northwest Hawaiian Islands (NWHI) is also identified in the figure: note that the Papahānaumokuākea Marine National Monument (PMNM) encompasses all of the NWHI locations, but not the MHI sites. Map is courtesy of J Lecky and NOAA PMNM. Photo credit: Panulirus marginatus, in the upper right hand corner: N Silbiger; Panulirus penicillatus, in the lower left hand corner: T Lilley. 2013). On average, tagged adults of both P. marginatus and S. squammosus move <1 km from their initial tagging location, even after 5 yrs at liberty (O’Malley and Walsh 2013). Therefore, if the different islands and atolls are forming an effectively panmic- tic population or even a structured metapopulation, the gene flow between islands is maintained through the pelagic larval phase. Spiny and slipper lobsters have some of the longest larval durations of any taxa (6 mo to >1 yr, and 3–6 mo, respectively; Phillips et al. 2006, Lavalli and Spanier 2007). Such long pelagic durations make larval dispersal patterns extremely difficult to predict, but intuitively, species with larval durations of this length are expected to be effectively panmictic across broad geographic ranges (Shanks et al. 2003, Siegel et al. 2003). More recent analyses sug- gest only a weak relationship exists between larval duration and the degree of popu- lation structure across a species’ range (Shanks 2009, Weersing and Toonen 2009, Riginos et al. 2011, Selkoe and Toonen 2011). Accordingly, although many previous genetic studies on spiny lobsters have found high levels of gene flow across broad geo- graphic scales (Shaklee and Samollow 1984, Ovenden et al. 1992, Tolley et al. 2005,
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