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Stylet Elemental Signatures Indicate Population Structure in a Holobenthic Octopus Species, Octopus Pallidus

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Stylet Elemental Signatures Indicate Population Structure in a Holobenthic Octopus Species, Octopus Pallidus Vol. 371: 1–10, 2008 MARINE ECOLOGY PROGRESS SERIES Published November 19 doi: 10.3354/meps07722 Mar Ecol Prog Ser OPENPEN ACCESSCCESS FEATURE ARTICLE Stylet elemental signatures indicate population structure in a holobenthic octopus species, Octopus pallidus Zoë A. Doubleday1,*, Gretta T. Pecl1, Jayson M. Semmens1, Leonid Danyushevsky2 1Marine Research Laboratories, Tasmanian Aquaculture & Fisheries Institute, University of Tasmania, Private Bag 49, Hobart, Tasmania 7001, Australia 2Centre for Ore Deposit Research, University of Tasmania, Private Bag 79, Hobart, Tasmania 7001, Australia ABSTRACT: Targeted trace elemental analysis was used to investigate the population structure and disper- sal patterns of the holobenthic octopus species Octopus pallidus (Hoyle, 1885). Multi-elemental signatures within the pre-hatch region of the stylet (an internal ‘shell’) were used to determine the common origins and levels of connectivity of individuals collected from 5 locations in Tasmania. To determine whether hatchling elemental signatures could be used as tags for natal ori- gin, hatchling stylets from 3 of the 5 locations were also analysed. We analyzed 12 elements using laser ablation inductively-coupled plasma-mass spectrometry (LA- ICPMS). Of the 12 elements, 7 were excellent spatial discriminators. There was evidence of high-level struc- turing with distinct groupings between all sites (the 2 closest being 85 km apart) within the adult O. pallidus Octopus pallidus, a holobenthic species found in south-east population, suggesting that all adults had hatched in or Australia near their respective collection sites. The hatchling sig- Photo: Stephen Leporati natures showed significant spatial variation, and a high percentage of individuals could successfully be traced back to their collection locations. However, they could INTRODUCTION not be used to trace adults back to their natal site, due to significant differences in element concentrations in Population structure and connectivity determine the hatchling and adult stylets, which was likely the result spatial scale at which localised populations operate. of differences in Ca concentration. This study presents They may be predominantly self-recruiting, depend on the first insights into the population structure of a some exchange from neighbouring populations, or holobenthic octopus species using stylet elemental freely interbreed across the distributional range of signatures, which will have important implications for the species (Fowler et al. 2005). These parameters of the sustainable management of O. pallidus. marine populations, therefore, are key properties for KEY WORDS: Population structure · Octopus · Stylet determining the resilience of populations to harvest- elemental signatures · Laser ablation ing, and for the development of effective conservation and fisheries management strategies (Thorrold et al. Resale or republication not permitted without written consent of the publisher 2001, Gillanders 2002). However, reconstructing the *Email: [email protected] © Inter-Research 2008 · www.int-res.com 2 Mar Ecol Prog Ser 371: 1–10, 2008 dispersal patterns of marine species throughout their conducted on holobenthic octopus species, which also life history cycle, particularly the early stages, has constitute other, much larger fisheries, including the proved to be a continuing challenge (Jones et al. 2005, Octopus maya fishery in Mexico (Arreguín-Sánchez et Bradbury et al. 2008). Traditional tag-recapture meth- al. 2000) and Eledone cirrhosa fishery in the Medi- ods are often inadequate due to the small size, large terranean (Orsi Relini et al. 2006). number and high mortality rates of offspring (Gillan- There are no published studies on the targeted ele- ders 2005, Warner et al. 2005). Genetic markers can mental analysis of both juvenile and adult cephalo- be valuable for investigating levels of connectivity pod hard structures. However, targeted elemental ana- relevant to long-term intergenerational population lysis has been applied successfully to adult stylets of a changes (e.g. Shaw et al. 1999, Kassahn et al. 2003, merobenthic octopus species (Doubleday et al. 2008). Buresch et al. 2006); however, only a very low ex- Stylets are a pair of fine, cartilage-like rods embedded change rate is required to maintain genetic homo- within the mantle musculature. They are a little known geneity (Carvalho & Hauser 1994). structure unique to Octopoda and are thought to A more direct approach to the measurement of dis- represent a remnant shell (Bizikov 2004). Unlike octo- persal employs the analysis of natural elemental sig- pus statoliths, which lack concentric growth and age- natures within the hard bio-mineralised structures of related increments (Jackson 1994), stylets have distinct marine organisms, which can be influenced by the concentric regions, a visible pre-hatch region, and local physical and biological availability of various daily growth increments (Doubleday et al. 2006). elements in the seawater. Elemental signatures have This study utilises targeted elemental analysis of the advantage that all individuals within a population both hatchling and adult stylets to examine the popu- are ‘tagged’, regardless of size (Semmens et al. 2007), lation structure of the holobenthic octopus species and as they reflect the present movement patterns of Octopus pallidus. More specifically, we determine a population, they may reveal distinct sub-populations whether (1) elemental signatures from the pre-hatch that are otherwise genetically homogenous due to region of adult stylets can be used to examine popula- low-level mixing (Campana & Thorrold 2001, Arkhip- tion structure and dispersal patterns, (2) hatchling ele- kin et al. 2004). The development of targeted micro- mental signatures exhibit sufficient spatial variation to probe techniques, such as laser ablation inductively- act as tags for natal origin, (3) hatchling signatures are coupled plasma-mass spectrometry (LA-ICPMS), has stable over short time periods, and (4) adult signatures enabled the selective elemental analysis of specific, can be matched back to the hatchling signatures and temporally related regions within structures such as thus used to determine the natal origins of the adults. fish otoliths (Campana 1999), gastropod shells (Zacherl 2005), bivalve shells (Becker et al. 2005) and squid statoliths (Zumholz et al. 2007). Furthermore, MATERIALS AND METHODS elemental signatures from the pre-hatch region of an adult structure have been matched with signatures Collection of specimens. Octopus hatchlings were from equivalent juvenile structures, allowing the natal collected from 3 sites: Circular Head (CH) on the north origins of adults and dispersal trajectories of juveniles coast of Tasmania, and Mercury Passage (MP) and to be determined (e.g. Forrester & Swearer 2002, Northwest Bay (NWB) on the southeast coast of Tas- Hamer et al. 2005). mania, Australia (Table 1, Fig. 1). Unbaited octopus In spite of the ecological and increasing commercial pots attached to demersal longlines and set at depths significance of cephalopods, the population structure between 12 to 30 m were used to provide nesting habi- and dispersal patterns of most species are poorly tat for mature females. Pots were deployed for 3 to understood. For octopus, such studies are predomi- 5 mo and were checked regularly for egg broods. If nantly restricted to Octopus vulgaris, a merobenthic eggs were present, a PVC mesh bag was tied securely species with a planktonic larval stage, and are largely around the pot to aid hatchling collection and prevent based on genetics (e.g. Maltagliati et al. 2002, Oost- predation on the eggs. The pot was subsequently huizen et al. 2004). Octopus pallidus (Hoyle, 1885) is a checked every 2 to 4 wk. This procedure did not affect small species that growths up to a weight of 1 kg and the mother, as she did not feed or leave her ‘den’ dur- which is found in coastal southeast Australian waters ing egg development. The well developed benthic (Stranks 1996). The species is holobenthic and pro- hatchlings were collected as ‘near hatching’ eggs or duces large, well-developed benthic hatchlings that recently hatched individuals. To assess the temporal adopt an adult lifestyle immediately after hatching. O. short-term variation in hatchling elemental signatures, pallidus is currently harvested throughout Bass Strait, 2 additional batches of hatchlings were collected from Tasmania, with a current annual catch of 80 to 90 t NWB (Table 1), with collections spaced 4 to 6 wk apart. (Ziegler et al. 2007). No population-level research is All specimens were frozen (the –18°C) upon collection. Doubleday et al.: Population structure of a holobenthic octopus species 3 Table 1. Octopus pallidus. Details of sample collection. Adults were collected on mature) were assigned according to several days within the time period given. n.c.: no specimens collected ovary size and level of egg develop- ment, and Stage 5 was assigned to post- Sample site Collection date No. of Collection date No. of spawning females (Leporati et al. (hatchlings) hatchlings (adults) adults 2008). Octopuses ranged in weight West Flinders Island (WFI) n.c. 0 June 2006 17 from 280 to 1012 g, all males were mature and most females were either East Flinders Island (EFI) n.c. 0 April 2007 19 Stage 3 or 4. Northwest Bay (NWB) Collection 1 15 Nov 06 40 May – Sept 2007 8 Stylet preparation. Hatchling stylets Collection 2 14 Dec 06 33 were carefully removed from partially Collection
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