Assessment of radiometric dating for age validation of deep-water dogfish (Order: Squaliformes) finspines
Introduction
Age determination in chondrichthyans typically involves counting growth bands within calcified vertebral centra, however the vertebrae of most deep-water chondrichthyans are too poorly calcified to record visible growth bands (Cailliet et al., 1983). Alternatively, growth bands found on or within dorsal finspines can be used to age phalacanthous (finspine-bearing) species (Goldman et al., 2012). Models of finspine growth in squaliform sharks have been proposed by Holden and Meadows (1962) and Maisey (1979), showing that new material is added: (1) at the base of the spine, (2) along the lumen, and (3) at the base of the enamel cap (if present) as the spine grows distally (Fig. 1). Growth of the spine occurs throughout the life of the animal and these proposed zones of accretion have been verified with oxytetracycline (OTC) stain uptake in finspines of captive Heterodontus portusjacksoni (Tovar-Avila et al., 2008). Finspines are formed early during embryonic development and pups have substantial, protruding spines at the time of parturition (Maisey, 1979, Cotton, 2010). Since new spine growth is accreted subdermally at the base of the spine, the tip of the spine therefore represents material formed in utero and the base encompasses the newest spine growth formed near the time of death.
A number of recent studies have estimated ages of deep-water sharks using the dorsal finspines (e.g. Machado and Figueiredo, 2000, Clarke et al., 2002a, Clarke et al., 2002b, Irvine et al., 2006a, Irvine et al., 2006b, Cotton et al., 2011), yet age validation for deep-water species remains elusive. Regardless of the method or structure used for age determination, validation of the age estimates should be performed for each population of each species studied (Beamish and McFarlane, 1983). Age validation for Squalus acanthias, primarily a shelf-dwelling species, has been accomplished using a variety of methods, including OTC marking and bomb radiocarbon dating (Beamish and McFarlane, 1985, Campana et al., 2006). However, many of the commonly used methods of age validation may be impractical for deep-water species (Table 1). Innovative approaches are therefore needed and radiometric methods offer great promise and are suitable for validating age estimates of long-lived fishes (Burton et al., 1999, Andrews et al., 2009b).
Radiometric techniques used for age validation of teleosts and elasmobranchs has primarily involved lead–radium dating and bomb radiocarbon (14C) chronologies. Lead–radium dating of shark vertebrae has proven ineffective, likely due to variable uptake and reworking of radioisotopes within the vertebral centra (Welden et al., 1987). Fenton (2001) used lead–radium dating to age vertebrae of four species of coastal and deep-water sharks with inconclusive results. The author made no direct comparisons of radiometric age estimates to other structures (e.g. growth bands recorded in vertebrae or finspines), relying instead on size-at-age estimates derived from the literature. Conversely, lead–radium dating of fish otoliths has proven highly successful using the 210Pb:226Ra disequilibria method, which compares relative compositions of the radioisotope pair within the otolith core (Andrews et al., 1999a, Andrews et al., 1999b, Kastelle and Kimura, 2006). Additionally, lead–radium dating has been used in conjunction with bomb radiocarbon dating to yield concordant validation methods for age estimates derived from otoliths of teleosts (Andrews et al., 2002a, Andrews et al., 2005, Andrews et al., 2007, Andrews et al., 2012, Kerr et al., 2004). Because 226Ra is a calcium analog, it is incorporated into calcified structures and age of the calcified structure is determined by ingrowth of 210Pb as 226Ra decays (Burton et al., 1999). Using this technique, age validation may be achieved with relatively few samples (Welden et al., 1987), provided that the following three assumptions are upheld:
Assumption # 1 – Once formed, each growth band within the calcified structure must act as a closed system to the lead–radium decay series.
Assumption # 2 – There must be no significant exogenous uptake of 210Pb during growth band formation (the only source of 210Pb should come from ingrowth via the decay of 226Ra).
Assumption # 3 – Isotopic uptake is proportional to mass growth of the calcified structure (depending on the sampling design, see Andrews et al., 1999a).
Radiometric ageing methods may be adaptable for use on other hard parts, such as dorsal finspines of phalacanthous sharks. However, these methods might not be suitable for use on internal growth bands of finspines because canaliculi within the inner dentin layers might add or remove material, thus resulting in a violation of Assumption #1. More importantly, individual internal growth bands do not offer sufficient mass for radiometric analysis. By contrast, external spine material (outer dentin material and enamel) is avascular and is available in abundance near the spine tip and therefore may be more suitable for use with radiometric methods. In theory, radiometric analysis of the spine tip would determine the year that this material was formed and thus the age of the animal. This radiometric age might then be compared to the number of growth bands counted within a transverse section of the spine to determine whether band formation is correlated with age.
In this study we assessed the efficacy of lead–radium dating for age determination using dorsal finspines of deep-water sharks. Although Fenton (2001) assessed the 210Pb:226Ra disequilibria method for age determination of deep-water sharks using vertebral centra, our study represents the first attempt at radiometric age determination of deep-water sharks using dorsal finspines. The initial experimental approach employed the 210Pb:226Ra disequilibria method, but an alternate method using the decay of 210Pb was subsequently used due to a perceived violation of Assumption #2. Previous studies have relied on this alternate approach to radiometric age determination when exogenous uptake of 210Pb was determined (e.g. Benavides and Druffel, 1986, Andrews et al., 2002b, Andrews et al., 2009a). In those studies, age was determined by measuring the change in 210Pb activity between the earliest (birth) and latest (death) structural depositions. Age was then calculated from those activity levels using the law of radioactive decay (Andrews et al., 2002b).
Section snippets
Sample collection/preparation
Shark specimens were collected in July 2004 during the MAR-ECO expedition to the Mid-Atlantic Ridge according to the methods described in Fossen et al. (2008). Specimen collection data and information about the individual spine samples are listed in Table 2. Anterior (D1) and posterior (D2) dorsal finspines of Centroselachus crepidater and Centrophorus squamosus were collected and cleaned as described in Cotton (2010). Terminology used to describe finspine structure follows Clarke and Irvine
Theory
Analysis of the relatively stable parent isotope (226Ra) within the recently deposited material at the base of the spine, when compared to material from the spine tip, will indicate whether the spine is a closed system (Assumption #1) and whether the rate of isotopic uptake changes over the life of the individual (Assumption #3). Due to the long half-life of 226Ra, one would expect to find similar activity levels of this isotope in the spine tip and spine base, to provide a baseline for the
Results and discussion
In the pilot study of C. crepidater finspines, only the tips of the spines were examined because it was unclear how 210Pb would be processed in the finspine. Since the spine tips are formed in utero, it was thought that these early stage spine tips were likely to exclude any exogenous 210Pb, and that all the 210Pb present in the spine's tip would have originated from ingrowth from the parent isotope, 226Ra. Unfortunately, the source of 210Pb present in the spine tip was unknown due to the lack
Acknowledgements
The authors thank the MAR-ECO project (www.mar-eco.no), especially Odd Aksel Bergstad and Mike Vecchione, for facilitating cruise logistics. We also thank the captains and crews of the M/S Loran and M/V Green Reefer, as well as Jan Erik Dyb for assistance with sample collection and arrangement of transport to the USA. The authors appreciate the valuable comments provided on this manuscript by Jose Castro, Mike Vecchione and Tracey Sutton, as well as two anonymous reviewers. Partial funding was
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