Use of bomb radiocarbon as a chronometer for age validation of shortfin mako (Isurus oxyrinchus)
Daniele Ardizzone Email address: dardizzone@mlml.calstate.edu

The shortfin mako (Isurus oxyrinchus) is a lamnoid shark that inhabits warm and temperate oceans of the world (Compagno 1998). The life history of this species is poorly known, and the lack of such information is a critical limiting factor for effective management (Cailliet et al. 1983). A review on the reproductive biology of the shortfin mako showed that their size at birth is approximately 70 cm total length (TL), litter size ranges between 4 and 25, predicted gestation lasts 15-18 months and length-at-maturity for females is reached at 2.73-2.98 m TL (Mollet et al. 2000). It is essential to obtain more detailed life history information to manage commercial and recreational fisheries and to prevent overexploitation of shark species such as the shortfin mako.

Sharks are vulnerable to overfishing because they have slow growth and low reproductive rates; typically, after a short rise, landings tend to decline rapidly (Holden 1973). Fisheries off the west coast of the United States mainly take juveniles and subadults of age 3 or less, of unknown proportion to the overall stock (Taylor and Bedford 2001). Exploitation of juveniles could lead to potential consequences at the population level, because insufficient individuals could reach reproductive maturity. Even though clear effects of exploitation have not been shown on this species in the Eastern North Pacific, it is important to protect the species critical life stages to assess proper fisheries management.

Since the late 1970s the shortfin mako has been one of the targets of a developing fishery that grew rapidly in Californian coastal waters. Landings increased from 12.4 metric tons in 1978 to over 187.8 in 1982, mainly through use of long drift gill nets (Cailliet and Bedford 1983). Reported catches peaked in 1982-83 at 19,500 fish and in the 1986-87 season at 13,500 fish (Hanan et al. 1993). Currently, shortfin mako sharks are caught by drift gillnets or hook-and-line, but the majority is taken as bycatch in the drift gillnet fishery for swordfish Xiphias gladius and thresher shark Alopias vulpinus. These bycatch landings ranged from 600,000 pounds in 1987 to less than 100,000 pounds in 1999 (Taylor and Bedford 2001). This species is also considered a prized game fish, and the sport fishery for shortfin mako has stabilized at a high level (Taylor and Bedford 2001). Currently, this species is not managed in the west coast of the United States and there are no quotas limiting catch.

Fishery management plans rely on accurate age determinations; if age estimations are not validated, errors in age determination could result in inaccurate mortality estimates, underestimation of strong year classes and longevity (Beamish and McFarlane 1983). Age estimates of bony fishes are commonly based on enumeration of growth increments in calcified structures like sagittal otoliths (Beamish and McFarlane 1987). Since sharks lack otoliths, vertebrae are used for estimates of age and growth because they are among the few structures that show periodic growth bands (Stevens 1975). A band is defined as a series of concentric marks composed of a group of rings (Cailliet et al. 1986).

Previous studies on age determination of shortfin mako have used techniques such as length-frequency analysis, X-radiography and silver nitrate impregnation to enhance the visibility of growth bands in vertebral centra (Cailliet et al. 1983; Pratt and Casey 1983). There is an ongoing issue on ageing of mako sharks, especially of the large size classes, due to different interpretations of the periodic deposition and difficulty of interpreting vertebral growth bands. Based on results obtained using temporal analysis of length-month information, tagging data and length-frequency analysis, Pratt and Casey (1983) concluded that two band pairs are formed on the vertebral centrum each year. Cailliet et al. (1983), on the other hand, assumed each pair of bands to be formed annually. Growth rates obtained by Pratt and Casey (1983) would be similar to Cailliet et al. (1983) if they assumed the formation of one band pair per year. Validation of these age estimates has yet to be determined.

In the last decade, a new technique has allowed for age validation of several fish species by measuring radiocarbon in calcified structures, such as otoliths, using accelerator mass spectrometry (Kalish 1995a; Kalish 1995b; Kalish et al. 1996; Kalish et al., 1997; Campana 1997; Campana and Jones 1998; Baker and Wilson 2001). Natural atmospheric 14C, occurring as 14CO2, results from nuclear reactions between cosmic ray neutrons and atmospheric nitrogen; the existing natural background radiocarbon levels are in part determined by the natural equilibrium between the production and disintegration of 14C (half-life of 5,730 ± 40 yrs) (Nydal et al. 1998). Between the early 1950’s and 1960’s, atmospheric thermonuclear testing produced and released large amounts of radiocarbon (14C) in the atmosphere. These tests, with strengths of 430 megatons over a period ranging from 1945 to 1980, increased dramatically the levels of atmospheric 14C (Nydal and Lövseth 1983). About two thirds of the total strength were released by the Soviet Union into the stratosphere in 1961 and 1962 at high latitudes (Nydal et al. 1998). The Test Ban Treaty, signed by the USA, Soviet Union and Great Britain on August 5, 1963 officially ended atmospheric testing for these nations, though France and China continued with smaller fission experiments until September 1974 and October 1980, respectively (Nydal et al. 1998).

As a consequence of these tests, radiocarbon entered the ocean through gas exchange with the atmosphere at the ocean surface (Watanabe et al. 1999). Radiocarbon (reported as 14C, the difference in the atom ratio of 14C:12C from pre-industrial radiocarbon levels, as measured in 19th century wood) surface water levels in the 1950’s ranged between –400/00 and 700/00, whereas in the 1970’s those values increased by 1600/00. Since then, there has been a slight but constant decrease.

The marked increase in radiocarbon levels in the dissolved inorganic carbon (DIC) of seawater was recorded in marine carbonates such as otoliths and reef-building corals (Druffel 1980). Records obtained from corals and otoliths and surface water databases can be used as a reference chronology to verify the synchrony with that of the fishes under study, because the accumulation of 14C in the hard organic parts of marine organisms occurs at a rate similar to corals living in the surrounding areas (Campana 1997; Campana and Jones 1998; Frantz et al. 2000). This technique has been used to validate longevity of at least eight bony fish species (Kalish 1993; 1995b; Kalish et al. 1996; Kalish et al. 1997; Campana 1997; Campana and Jones 1998; Baker and Wilson 2001, Kerr et al. In Prep.). In the first application of this methodology to cartilaginous fishes, Campana et al. (2002) validated the vertebral band ageing methodology for the porbeagle (Lamna nasus) aged up to 26 years. In the same study, a single shortfin mako vertebra was aged using the criteria for the porbeagle and then compared to the criteria as in Cailliet et al. (1983) and Pratt and Casey (1983). Samples of the first, last and two intermediate bands were assayed for radiocarbon with the results suggesting that those samples fit the porbeagle chronology when bands were counted as for the porbeagle, assuming one pair of bands formed each year. The same values showed instead a marked discrepancy when plotted against the curve for the porbeagle using the criteria in Pratt and Casey (1983), with two band pairs formed per year.

To provide a definitive growth function of the shortfin mako, more radiocarbon assays are required by sampling a larger number of vertebrae from animals of different age classes and locations, in which at least some of the growth bands were formed before 1965 (Campana et al. 2002). Once a chronology is obtained, it will be possible to validate the age estimates of all sizes for this species. The purpose of this study is to validate age and ageing methodology of the shortfin mako by measuring radiocarbon levels in growth bands from vertebrae obtained across different regions.

Materials and methods:

Vertebral samples from shortfin makos collected in the Western North Atlantic, Eastern North Pacific, South West Pacific and Western South Indian Ocean between 1950 and 1984 will be sectioned for age determination based upon band counts visible in transverse section. Each vertebra will be sectioned along the sagittal plane by using a Ray Tech® gem saw with two diamond blades separated by a 0.6 mm spacer at the NOAA Fisheries Northeast Fisheries Science Center, Narragansett Laboratory, Rhode Island. The resulting sections will be digitally photographed using a MTI® CCD 72 video camera mounted on a SZX9 Olympus® stereo microscope under reflected light, with a magnification ranging between 4X and 12X, according to the size of the vertebra. For larger vertebrae, an additional photograph at higher magnification will be taken to enhance the finer bands toward the edge. The sections will be then stored in 70% ethanol. Ages will be estimated by counting the number of band pairs on the images using Image Pro 4, ImageJ 1.29x and Adobe Photoshop 7.0 software. Each band pair consists of one opaque and one translucent band, corresponding to the light-dark pattern observed when observed against a dark background under reflected light.

Cores will be extracted from the first formed band (=1 year) and other individual growth bands visible in the corpus calcareum of each vertebral section using a New Wave Research® Micro-mill. Vertebral sections will be mounted onto the Micro-mill plate using double sided tape or wax to hold the sample onto the plate and cut along the boundary between two growth bands to isolate a solid piece composed of one opaque and one translucent band corresponding to the growth in one year. To minimize the contamination among cores, the drill bit will be rinsed in 70% EtOH between two coring events. The cores will be weighed to the nearest 0.1 mg and stored in sterile plastic cryo vials in preparation for radiocarbon assay by Accelerator Mass Spectrometry (AMS) at the Center for Mass Spectrometry, Lawrence Livermore National Laboratory, Livermore, California. Radiocarbon values from each band will be plotted against the corresponding estimated year of formation, and are expected to produce a sigmoidal curve similar to the ?14C signal observed in the marine environment.

The reference 14C chronologies obtained for the porbeagle by Campana et al. (2002) and for haddock Melanogrammus aeglefinus (Campana 1997) will be used as a benchmark for the northwest Atlantic samples, as well as those obtained for the arctic cod Gadus morhua (Kalish et al. 2001), the black drum Pogonia chromis (Campana and Jones 1996), the red snapper Lutjanus campechanus (Baker and Wilson 2001), Diploria strigosa and Diploria labyrinthiformis corals (Druffel 1989) and surface water samples (Nydal et al. 1998). For the northeast Pacific samples there are reference chronologies available from the yelloweye rockfish Sebastes ruberrimus in southeast Alaska region (Kerr et al. in prep.), from Pavona clavus coral in the Galapagos island (Druffel 1981, Druffel 1995; Guilderson and Schrag 1998), from Porites spp. heads collected in the tropical Pacific (Druffel 1987; Guilderson et al. 1998), rhodolith Lithothamnium crassiusculum from the southern Gulf of California (Frantz et al. 2000) and surface water samples (Nydal e al. 1994). For the Australian samples there are chronologies obtained for squirefish Pagrus auratus (Kalish 1993), redfish Centroberyx affinis (Kalish 1995b), the southern bluefin tuna Thunnus maccoyii (Kalish et al. 1996), the blue grenadier Macrunonus novazelandiae (Kalish et al. 1997), Tropical Pacific corals (Toggweiler et al. 1991; Druffel and Griffin 1993; Druffel 1995; Guilderson et al. 1998) and surface water samples (Nydal et al. 1998). For the South African samples there are available chronologies obtained for surface water samples (Vogel, pers. comm.; Nydal et al. 1998) Porites corals off the coast of South Africa (Cohen, pers. comm.) and off the coast of Kenya (Grumet et al. 2002a; Grumet et al. 2002b).

The radiocarbon values obtained from coring vertebral growth bands in shortfin mako are expected to match the radiocarbon values of reference chronologies for each region, thus validating the age estimates of the shortfin mako and clarifying how to interpret the periodic deposition of vertebral growth bands for this species. This will result in more accurate age and growth curves and therefore improved life history information, and consequently the ability to plan an accurate fisheries management strategy.

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