Comparative Population Structure of Two Edible Indo-Pacific Coral Reef Sea Cucumbers (Echinodermata: Holothuroidea)

Bull Mar Sci. 90(1):359–378. 2014 research paper http://dx.doi.org/10.5343/bms.2013.1001 Comparative population structure of two edible Indo-Pacific coral reef sea cucumbers (Echinodermata: Holothuroidea) 1 Hawai‘i Institute of Marine Derek J Skillings 1, 2 * Biology, School of Ocean and 1, 3 Earth Science and Technology, Christopher E Bird University of Hawai‘i at Mānoa, Robert J Toonen 1 P.O. Box 1346, Kaneohe, Hawaii 96744. 2 Department of Biology, ABSTRACT.—Echinoderms are the targets of considerable University of Hawai‘i at Mānoa, global artisanal and commercial fisheries, but efforts to 2450 Campus Road, Honolulu, Hawaii 96822. effectively manage them suffer from poor understanding of population demographics and connectivity. Here we report 3 Marine Biology Program, population genetic data (mitochondrial COI sequence) for Department of Life Sciences, two congeneric sea cucumbers, Holothuria atra (Jaeger, Texas A & M University–Corpus Christi, 6300 Ocean Drive, 1833) and Holothuria whitmaei (Bell, 1887), throughout Corpus Christi, Texas 78412. the Hawaiian Archipelago and Johnston Atoll to inform resource management. These two species share a wide range * Corresponding Author: Current Address: Philosophy Program, across the Indo-Pacific region, and are the most ubiquitous The Graduate Center, CUNY, species on Hawaiian coral reefs. Both species have roughly 365 Fifth Ave., Rm. 7113, New similar haplotype diversity (h = 0.88 for H. atra, 0.83 for York, New York 10016. Email: H. whitmaei), but the nucleotide diversity (π = 0.0087 and <[email protected]>. 0.0067, respectively) and effective number of alleles (AE = 8.3 and 5.9, respectively) were both lower for H. whitmaei. Regardless of the metric of population differentiation used, H. atra shows evidence for restricted gene flow relative to the congeneric H. whitmaei; global ΦST was 0.165 with 12.65% of variation in analysis of molecular variance is distributed among groups for H. atra, whereas global ΦST was −0.006 and 100% of the variation is within the three groups (Main Hawaiian Islands, Northwestern Hawaiian Islands, Johnston Atoll) for H. whitmaei. These data contribute to the growing body of literature cautioning against the extrapolation of single-species exemplar studies to management and highlight that even for such broadly-distributed species, local-scale Date Submitted: 3 January, 2013. management is justified because migration between the Date Accepted: 30 May, 2013. Main and Northwestern Hawaiian islands does not occur Available Online: 14 January, 2014. within ecologically relevant time frames. The Hawaiian Archipelago stretches >2500 km, and consists of two regions: the Main Hawaiian Islands (MHI), which are populated high volcanic islands; and the Northwestern Hawaiian Islands (NWHI), which are an uninhabited string of tiny islands, atolls, shoals, and banks. Owing to their isolation, the NWHI coral reefs are among the healthiest and most extensive remaining in the world (Pandolfi et al. 2003, Halpern et al. 2008). The reefs of the NWHI represent one of the few remaining undamaged coral reef ecosystems with abundant and large apex predators and an extremely high proportion of endemic species across many taxa (Friedlander and DeMartini 2002, DeMartini and Friedlander 2004), and little human impact Bulletin of Marine Science 359 © 2014 Rosenstiel School of Marine & Atmospheric Science of OA the University of Miami Open access content 360 Bulletin of Marine Science. Vol 90, No 1. 2014 compared to the heavily populated MHI (Halpern et al. 2008, Selkoe et al. 2008, Selkoe et al. 2009). In contrast, coral reefs in the MHI are under considerable an- thropogenic pressure from 1.29 million residents (with >900,000 of those living on the island of Oahu) and more than seven million tourists visiting the state each year. The Hawaiian Archipelago also lies at the periphery of the tropical Central Pacific and is one of the most isolated island chains in the world, making it biogeographi- cally partitioned from the rest of the Pacific islands (reviewed by Ziegler 2002, Briggs and Bowen 2012). This isolation results in one of the highest proportions of ende- mism in the world (e.g., Briggs 1974, Kay 1980, Grigg 1983, reviewed by Ziegler 2002, Eldredge and Evenhuis 2003). Though there are many examples of pan-Pacific coral reef organisms in Hawaii, the isolation of the Hawaiian Archipelago is thought to limit larval exchange sufficiently that colonization is rare (Hourigan and Reese 1987, Kay and Palumbi 1987, Jokiel and Martinelli 1992). For example, Kay (1984) estimated that western Pacific marine species successfully colonize the Hawaiian Archipelago about once every 13,000 yrs. Unlike the terrestrial fauna, however, the Hawaiian marine fauna contains a large proportion of endemics that are differenti- ated, but not diversified, from their Indo–West Pacific roots (Hourigan and Reese 1987, Jokiel 1987, Kay and Palumbi 1987, Ziegler 2002). Johnston Atoll, the nearest emergent piece of land, is believed to be a stepping-stone into Hawaii. Simulations of larval dispersal indicate that larvae from Johnston atoll can reach French Frigate Shoals or Kauai within about a month along two separate larval corridors (Kobayashi 2006, Kobayashi and Polovina 2006). Proxies for dispersal, such as pelagic larval duration (PLD) and geographic range, have generally been used as rules of thumb in the absence of a detailed understanding of connectivity for most marine species. Additionally, intuitive expectations of larval dispersal potential as a function of PLD are often not upheld in comparative analyses of the existing literature (e.g., Weersing and Toonen 2009, Riginos et al. 2011, Selkoe and Toonen 2011, Mercer et al. 2013). Realized dispersal distance is typically less than potential dispersal distance because of factors such as larval swimming, larval settling preferences, larval mortality, or the presence of biophysical or biogeographi- cal barriers (Shanks et al. 2003, Severance and Karl 2006, Dawson and Hamner 2008). Barriers that limit dispersal between marine populations include obvious geographical features such as land masses, i.e., the Isthmus of Panama (Bermingham and Lessios 1993), but also more subtle factors such as currents and oceanographic regimes, i.e., the Mona Passage between Hispaniola and Puerto Rico (Dawson 2001, Barber et al. 2002, Sotka et al. 2004, Baums et al. 2006, White et al. 2010). Echinoderms play a major role in structuring several marine ecosystems, and many are described as “keystone species” because of their profound influence on benthic communities (e.g., Paine 1969, Power et al. 1996, Lessios et al. 2001, reviewed by Uthicke et al. 2009). In addition to their important ecosystem functions, numerous echinoderm species are also the target of artisanal or commercial fishing, particu- larly the sea urchins and sea cucumbers (Sloan 1984, Conand 1990, Sala et al. 1998, Purcell 2010). Stocks of the most valuable species are severely depleted throughout the Pacific with fishers continually moving to more remote locations and harvesting less valuable species (Conand 1990, Uthicke 2004, Purcell et al. 2011). The lollyfish, Holothuria atra (Jaeger, 1833), and the black teatfish, Holothuria whitmaei (Bell, 1887), are two common shallow-water tropical sea cucumbers in the Indo-Pacific waters that extend into the Hawaiian Archipelago, where they are locally Skillings et al.: Comparative population structure in two sea cucumbers 361 known as loli (Clark and Rowe 1971, Conand 1994, Uthicke et al. 2001, Uthicke and Benzie 2003). Both species perform vital ecosystem services on coral reefs such as sediment bioturbation. (Bonham and Held 1963, Uthicke 1999, Purcell 2010). There is an active fishery for both species in many regions of the Pacific; H. atra is a low value species, whereas H. whitmaei is a high value species and heavily overfished in much of its range (Uthicke and Benzie 2000a, Uthicke et al. 2004). There is no regu- lated sea cucumber fishery in Hawaii, but anecdotal evidence suggests that H. whitmaei is harvested. The authors have found H. whitmaei and H. atra to be common, and occasionally in high densities, in the protected Northwest Hawaiian Islands, which is unpopulated by humans. Holothuria atra is common in the populated Main Hawaiian Islands, whereas H. whitmaei is fairly uncommon and usually only found in isolated or difficult to access locations (DJS, CEB, RJT pers obs). Prepared and dried sea cucumber flesh—visually unidentifiable to the species level—can also -oc casionally be found for sale in Honolulu markets (DJS, CEB, RJT pers obs). Echinoderms are described as a boom-bust phylum in which populations go through marked natural population cycles (Uthicke et al. 2009). Generally, holo- thurians are further characterized by limited adult mobility, late maturity, density- dependent reproduction and low rates of recruitment (Uthicke and Benzie 2000b, Uthicke and Purcell 2004, Uthicke et al. 2004). Furthermore, the boom-bust nature of many echinoderm populations has important implications for connectivity in evolutionary time-frames where biological attributes can drive population structure to a greater extent than oceanographic processes as hypothesized in the Tripneustes sea urchins (Lessios et al. 2003). Together, these characteristics make H. atra and H. whitmaei ideal organisms to examine levels of connectivity and historical population dynamics to inform management and to test hypotheses about population connectivity

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