Bomb radiocarbon dating calibrates beluga (Delphinapterus leucas) age estimates.

Abstract: The ages of many mammals are estimated by counting growth layers in tooth sections, yet validation of age estimation techniques using free-ranging mammals has been problematic. Contrary to age estimates for most other animals in which it is assumed that one bipartite growth increment forms annually, beluga whale (Delphinapterus leucas (Pallas, 1776)) age estimates have been calculated assuming that two growth layer groups (GLGs) form each year. Here we report the age validation for belugas based on date-specific incorporation of atomic bomb radiocarbon into tooth GLGs. Radiocarbon assays of dentinal layers formed in belugas harvested between 1895 and 2001 indicated that radiocarbon from atmospheric testing of nuclear weapons was incorporated into growing teeth and retained for the remaining life of the animal. Comparison of age determined by bomb radiocarbon with age determined by GLG counts indicated that GLGs form annually, not semiannually, and provide an accurate indicator of age for belugas up to at least 60 years old. Radiocarbon signatures of belugas were temporally and metabolically stable and were apparently derived more from the radiocarbon content of their prey than from water. Our understanding of many facets of beluga population dynamics is altered by the finding that this species lives twice as long as previously thought.

Resume : L'estimation de l'age chez de nombreux mammiferes se fait par l'enumeration des couches de croissance dans des coupes de dents, bien que la validation de cette technique d'estimation de l'age chez les mammiferes libres en nature pose des problemes. Contrairement a la plupart des autres animaux chez qui on presume de la formation d'un pas de croissance bipartite chaque annee, on calcule les estimations d'age chez le beluga (Delphinapterus leucas (Pallas, 1776)) en presupposant la formation de deux groupes de couches de croissance (GLG) chaque annee. Nous presentons la validation de la determination d'age chez les belugas d'apres l'incorporation a des dates precises du radiocarbone provenant de bombes atomiques dans les GLG des dents. Les dosages du radiocarbone dans les couches de dentine deposees chez des belugas captures entre 1895 et 2001 indiquent que le radiocarbone provenant des essais atmospheriques d'armes nucleaires s'incorpore dans les dents en croissance et y demenre pour le reste de la vie de l'animal. Une comparaison des ages determines par le radiocarbone et par les comptages de GLG montre que les GLG se forment une fois et non pas deux fois Fan et qu'ils sont des indicateurs fiables de l'age des belugas jusqu'a l'age d'au moins 60 ans. Les signatures de radiocarbone sont stables en fonction du temps et du metabolisme et elles proviennent apparemment plus du contenu en radiocarbone des proies que de celui de l'eau. Notre comprehension de plusieurs aspects de la dynamique de population des belugas se voit modifiee par la reevaluation de cette espece qui vit deux fois plus longtemps qu'on le croyait precedemment.

[Traduit par la Redaction]

Introduction

Accurate age estimates are fundamental to ecological investigations of rates of individual growth, rates of population change, or rates incorporated in species-specific life-history parameters. For example, management tools such as potential biological removal (Wade 1998) and population viability analysis (Morris and Doak 2002) rely on age-specific fecundity and survival rates to calculate safe harvest levels. Life-history studies that attempt to understand the evolutionary significance of lifetime behavior (Boness et al. 2002; Winemiller 2005) rely on the timing of important events such as sexual maturation. Even population responses to climate change can be age-specific (Coulson et al. 2001). Particularly in management decisions, erroneous age estimates can have disastrous effects (Campana 2001). For example, age underestimation resulted in overly optimistic estimates of productivity and hence serious overfishing of several marine fish stocks before the inaccurate ageing was recognized (Beamish and McFarlane 1995; Smith et al. 1995; Campana 1997, 2001).

Many species are aged by examining growth lines or bands in hard structures. Bivalve shells (Lutz and Rhoads 1980), coral skeletons (Dodge and Thomson 1974), tortoise scutes (Germano 1998) and fish otoliths (Secor et al. 1995), scales (Robillard and Marsden 1996), vertebrae (Brown and Gruber 1988), and fin rays (Cass and Beamish 1983) all record growth increments that have been used for age estimation. In mammals, teeth (both dentine and cementum) and bone (Johnston et al. 1987; Klevezal 1996) are the basic recording structures, although teeth show less restructuring than bone (Garlich-Miller et al. 1993; Klevezal 1996).

The beluga (Delphinapterus leucas (Pallas, 1776)) is a toothed whale that is exploited throughout much of its circumpolar range (Stewart and Stewart 1989). Population trajectories that serve as the basis for management decisions rely on some combination of age at maturation, age-specific fecundity, age-specific survival, and longevity (e.g., Butterworth et al. 2002; Innes and Stewart 2002). Beluga ages have been estimated routinely by counting growth layers or bands in longitudinal sections of the teeth. The term "growth layer group" (GLG) has been adopted by the International Whaling Commission (International Whaling Commission 1980) and by marine mammalogists in general to denote a repeated dyad of contrasting lines, with each pair of light and dark lines representing a growth period (International Whaling Commission 1980; Hohn 2002). The term "GLG" is functionally similar to the term "growth band" or "growth increment" used by those determining the ages of fish, reptiles, amphibians, and terrestrial mammals (Neville 1967; Secor et al. 1995). Here we use the marine mammalogy terminology, i.e., GLG.

In general, GLGs in odontocete teeth are interpreted as representing 1 year of growth, although some shorter term banding may occur (Klevezal 1996). However, the deposition rate of GLGs in belugas has been interpreted to be semiannual, with two GLGs representing 1 year of growth (Sergeant 1959). If two GLGs are deposited each year, then age is equivalent to one half the number of GLGs (GLG/2), compared with the more conventional interpretation for most animals that age = GLG/1. The assumption that belugas form two dentinal GLGs/year (Sergeant 1959) was based on previous studies of sperm whales (Physeter macrocephalus L., 1758) that concluded two GLGs were formed each year and the observation that the maximum number of GLGs seen in beluga teeth was about twice that apparent in long-finned pilot whale (Globicephala melas (Traill, 1809)) teeth. Subsequently, it has been acknowledged that sperm whales deposit only one GLG/year (International Whaling Commission 1980; Evans et al. 2002). Indeed, Sergeant (1981) noted there was no a priori justification to assume two GLGs were formed each year in belugas.

Efforts to reject either the 1 GLG/year or the 2 GLGs/year hypothesis in belugas have been equivocal at best. Allometric comparisons suggest annual, not semi-annual, deposition (Ohsumi 1979). The examination of teeth from wild-born belugas held in captivity has been inconclusive (Brodie 1982; Heide-Jorgensen et al. 1994; Hohn and Lockyer 2001). The use of tetracycline marks as a dated chemical marker in teeth is one method of calibrating age estimates (Johnston et al. 1987; Brodie et al. 1990) but has not been definitive for belugas (Hohn and Lockyer 2001).

The use of radiocarbon (14C) to validate beluga ages may resolve this impasse. The atmospheric testing of atomic bombs in the 1950s and 1960s resulted in a rapid and well-documented increase in radiocarbon in the world's oceans (Druffel and Linick 1978). The period of initial radiocarbon increase in marine carbonate structures such as corals, bivalves, and fish otoliths was almost synchronous around the world (Kalish 1993; Weidman and Jones 1993; Campana 1997), allowing the first appearance of the increase around 1958 to be used as a dated marker in growth bands of marine animals (Druffel and Linick 1978; Kalish 1993). A similar pattern of increase, lagged by several years owing to the incorporation of dietary carbon, has been documented in porbeagle shark (Lampa nasus (Bonnaterre, 1788)) vertebrae (Campana et al. 2002) and spiny dogfish (Squalus acanthias L., 1758) spines (Campana et al. 2006). Here we report the first radiocarbon assays of beluga whale teeth, using 14C as a dated chemical marker, to determine whether these teeth recorded and preserved a bomb radiocarbon pulse in growth layers formed during the 1960s. We use [[delta].sup.13]C assays to test the assumption that the primary source of carbon in belugas is dietary carbon rather than dissolved inorganic carbon (DIC), and we explore the impact of the differing age interpretations on life-history parameters of belugas.

Materials and methods

Nine beluga teeth were selected from archived material (Table 1). Three of the whales (gender unknown) were from archaeological sites on Somerset Island in the high Arctic (Elwin Bay, 72.53N, 90.93W; Port Leopold, 73.90N, 90.15W; Outridge et al. 2005) and lived their whole lives before atomic bombs. The year of death for these animals was approximated as the midpoint of the whaling activity at the site (Outridge et al. 2005). Five whales (all females) were killed between 1991 and 1997 by hunters living on southeast Baffin Island at Kimmirut (62.85N, 69.88W), Igaluit (63.75N, 68.55W), and Pangnirtung (66.12N, 65.68W), Nunavut. These whales were selected so that back-calculating from their year of death would place their birth date either before the period of atmospheric atomic bomb testing if age = GLG/1 or after bomb testing if age = GLG/2. A sixth, younger, beluga harvested in 2001, also at southeast Baffin Island, represented the recent period. Teeth were stored dry or in glycerin-alcohol-water (Pueck and Lowe 1975) until sectioning.

Belugas have homodont …