Growth of female southern elephant seals Mirounga leonina at Macquarie Island
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1 Polar Biol (05) 28: DOI /s ORIGINAL PAPER Cameron M. Bell Æ Harry R. Burton Æ Mary-Anne Lea Mark A. Hindell Growth of female southern elephant seals Mirounga leonina at Macquarie Island Received: 11 May 04 / Revised: 6 April 04 / Accepted: 10 October 04 / Published online: 13 January 05 Ó Springer-Verlag 05 Abstract Body growth of 137 female southern elephant seals (Mirounga leonina) over 1 year of age was investigated at subantarctic Macquarie Island. An asymptotic straight line, snout tail body length of 2.57±0.03 m was estimated to be attained at 9 years of age, using a threeparameter Gompertz equation. A significant increase of approximately 0.1 m (5%) in mean body length of females between 1 and 10 years of age was estimated to have occurred between the s and 1990s at Macquarie Island. This is consistent with a reduction in both the rate of population decline and the age of onset of sexual maturity. Age determination using dental cementum layers and the importance of standardised measurements in pinniped growth studies are discussed. Introduction In excess of one million southern elephant seals (Mirounga leonina Linn. 1758) were harvested between the late 1700s and early 1900s in an uncontrolled manner at several locations in the Southern Ocean (Laws 1994). During the mid-1900s, studies were focused on elephant seal growth at both South Georgia and Macquarie Island to assist rational regulation of harvesting (Laws C. M. Bell Æ M.-A. Lea Æ M. A. Hindell Antarctic Wildlife Research Unit, School of Zoology, University of Tasmania, GPO Box , Hobart, TAS, 7001, Australia Present address: C. M. Bell (&) Department of Primary Industries,Water and Environment, 13 St John s Avenue, New Town, TAS, 7008, Australia Cameron.Bell@dpiwe.tas.gov.au Tel.: Fax: H. R. Burton Australian Antarctic Division, Channel Highway, Kingston, TAS, 7050, Australia 1953; Carrick et al. 1962a; Carrick and Ingham 1962). A further study at Macquarie Island investigated body compositional changes at different growth stages and related this to the growth of domesticated animals (Bryden 1969a). Only the South Georgia stock ultimately experienced regulated sealing as a result, continuing until the late 1960s (Laws 1994). Since commercial hunting of elephant seals ceased, serious declines have been detected in the southern Indian Ocean and Macquarie Island stocks (Hindell et al. 1994), whilst the South Georgia population has remained stable (Boyd et al. 1996). Differences in body growth have been noted between the South Georgia and Macquarie Island populations, with animals from the latter recorded as being slower growing, commencing breeding when older and being of smaller adult body size (Carrick et al. 1962a; Laws 1984). Although bodygrowth analysis will not reveal the cause(s) of the population decline, it is nevertheless a useful diagnostic tool. For example, body growth has been correlated with physiological condition of populations (Hanks 1981), population status (Calkins et al. 1998), prey abundance (Trites et al. 1992), nutritional status (Calkins et al. 1998) and carrying capacity (Fowler et al. 1992). The lifetime growth pattern of southern elephant seals is characterised by several notable features. Nursing pups undergo a pronounced dynamic change, trebling their body weight over a 23-day period (Carrick et al. 1962a), a large percentage of this increase resulting from deposition of adipose tissue in the form of subcutaneous blubber (Bryden 1969b). After losing 30% of body mass during a post-weaning fast and departing from the natal site (Arnbom et al. 1993), body mass increases by approximately 75%, but body length by relatively less during the first winter foraging bout (Bell et al. 1997a). Increased mass gain during this first foraging trip and juvenile survival are associated with accelerated growth early in life (Bell et al. 1997a; McMahon et al. 00). The growth of juvenile females continues over the next few years in a negative exponential pattern,
2 396 accelerating steadily from the beginning of the second year of life, to approximately 3 4 years (McLaren 1993), at which point males and virgin females are not easily distinguished (Carrick et al. 1962a). Annual increments in body mass and length of females then decline, with females reaching approximately 2.5 m body length and kg body weight at growth maturity (Ling et al. 1981; Fedak et al. 1994). In contrast, males undergo a double-sigmoid pattern of growth (McLaren 1993), with a secondary period of accelerating growth at 6 7 years of age, coinciding with puberty (Carrick et al. 1962a). At growth maturity, males weigh up to 3,700 kg (Ling et al. 1981) and measure up to approximately 6.0 m straightline body length (Laws 1953). The advantages of increased body size are closely associated with reproductive success (Boyd 00). Phocids have a critical body size that must be acquired to achieve sexual maturity (Laws 1956; Arnbom et al. 1994). It follows that accelerated growth, associated with abundant food resources for example (Stewart et al. 1984), will allow sexual maturity to be achieved earlier. The size of mothers also has an important influence on pup size at both birth and weaning (Arnbom et al. 1993, 1994). For adult males, a larger body size allows for greater deposition of energy stores for haul-out periods (McCann 1981), allowing longer haul-out periods (Modig 1996) and conferring dominance characteristics that also result in greater reproductive success. Larger males tend to be higher ranking and have a higher copulatory frequency (McCann 1981; Modig 1996). The objectives of this study were to (1) describe the body growth of females of the present Macquarie Island southern elephant seal population using standardised measurement techniques to allow future comparative growth studies; and (2) re-analyse data sets from earlier studies for temporal and spatial comparisons. Materials and methods Field work Two groups of female southern elephant seals were studied at Macquarie Island (54 30 S, E) between March 1994 and January 1996: 1. Juvenile females during the 1994 austral winter 2. Post-lactation and pre-moult females during the 1994 and 1995 breeding seasons. The subjects were a combination of known-age animals identified by hind-flipper tags and/or flank hot-iron brands (McMahon et al. 03) and individuals of unknown age. During the winter and pre-moult phases of the study, a daily search was made of the isthmus study area (Carrick et al. 1962b) for animals hauled out within the previous 24 h. In contrast, the breeding-season phase targeted females from harems in the isthmus study area at day 23 of lactation, coinciding with the average duration of the lactation period (Carrick et al. 1962a). These females had been selected and identified with paint marks at parturition. Most animals less than 2 years of age were physically restrained with a canvas headbag and sedated by intravenous administration of 0.9 mg kg 1 ketamine hydrochloride and 0.03 mg kg 1 diazepam (Slip et al. 1996). All other animals were sedated using a combination of tiletamine and zolazepam at a dose rate of 1 mg kg 1 (Baker et al. 1990), administered by remote intramuscular method (Ryding 1982). Mass was measured to the nearest kilogram by suspending the sedated seal in a stretcher from an aluminium tripod, using an electronic strain-gauge of 2,500 kg capacity (Measurement Systems International, Seattle, WA, USA). Straight-line snout tail length (STL) was measured with the animal in ventral recumbency using a glass fibre tape measure. Age determination Whilst sedated, the lower left incisor was extracted (Arnbom et al. 1992) and then stored in distilled water. After the teeth had been cleaned of connective and soft tissue, they were mounted in a commercial polyester resin and cut longitudinally (sagittal to the crown-root axis) with a diamond-edged circular saw. Soaking in acetone dissolved the remaining resin. Sections were immersed in a commercial rapid bone decalcifying agent (RDO Rapid Decalcifier, Apex Engineering Products Corporation, IL, USA) for 12 h and once decalcified, were washed in running tap water for 24 h and then soaked in 10% formalin for 48 h. Thin sections (35 lm) were cut with a freezing microtome and mounted on a glass slide. Dental cementum layers were counted by a single operator using a polarising light microscope, viewing the prepared sections at or near the root tip (Mansfield 1991; Arnbom et al. 1992; Stewart et al. 1996). One year was assumed to be represented by one translucent and one dark band, known as a growth layer group, GLG (McCann 1993). A standardised technique of repeat blind readings was used (McCann 1993): if the first three counts were consistent, this was assumed to be the age. Otherwise, a further two readings were made, and the mean and 95% confidence interval were estimated for all five counts. Those readings beyond the confidence interval were assumed to be reading errors and discarded. The median of the remaining counts was taken as the final age of the tooth. Growth data All growth data used in the analysis of the sedated Macquarie Island females were cross-sectional, i.e. no repeat measurements of individuals were included in the data set. The Macquarie Island data set collected in comprised body length measurements from both dead and live females (Carrick et al. 1962a). This data set was sub-sampled to exclude, from the analysis,
3 397 repeat measurements from the same individual (only data from the last resight was used) and the numerous visual estimates made by Carrick et al. (1962a). Some snout tail measurements from the 1955 to 1959 data set were made over the dorsal curvature (CSTL) and were reduced by 5% to provide an estimation of STL (Carrick et al. 1962a). Measurements of STL from dead females collected at Macquarie Island in by Bryden (1967) were used. Body lengths over the dorsal curvature of dead females from South Georgia ( ), many selected by sealers, were collected by Laws (1953). To be consistent with data presented by Carrick et al. (1962a), which were already converted from CSTL to STL by a factor of 5%, the South Georgia data were also converted using the same factor. Recent STL measurements from sedated females at South Georgia in were also analysed (Arnbom et al. 1994). Growth analysis A three-parameter Gompertz equation, STL ¼ Ae ð e kðt t 0 ÞÞ (Zullinger et al. 1984), was fitted to individual lengths and ages using a non-linear least-squares iterative procedure where STL is straight line snout tail length (metres) in ventral recumbency at age t (years); A is the asymptotic value for body length; k, t 0, and m are fixed constants; and e is the base of natural logarithms. Residuals for each fitted model were examined graphically to ensure there were no obvious trends. Age-specific body length for certain age ranges was also transformed by the natural logarithm and analysed by linear regression using the least-squares method. Simple power models were used to test the relationship between STL and age, and a t-test was utilised to examine differences in straight-line slopes and elevation (Zar 1984). Results Age determination Using dental cementum layers, age was estimated for 114 females (range 1 15 years). Teeth were also extracted under sedation from 12 known-age animals: six females (range 4 7 years of age) and six juvenile males (range 3 6 years of age). Five repeat blind counts of each known-age tooth resulted in only three (25%) being consistently aged correctly; the other nine teeth were estimated as being within ±2 years of the true age (TA). There was a significant positive relationship between TA and difference between TA and estimated age (EA): TA = 0.85(TA EA) ; F (1,10) =34.27, P<0.001, r 2 =0.77). That is, animals younger than 4.7 years of age were over-estimated and animals older than 4.7 years of age were under-estimated. Growth of southern elephant seals, Macquarie Island The sigmoidal increase in STL of 137 females between 1 and 15 years of age in is shown in Fig. 1. Dental cementum layers were used to age 83% (n=114) of these animals; the remaining 23 seals were of known age. The Gompertz growth curve fitted to the bodylength data (Fig. 1, Table 1) had an asymptote (±SE) of 2.57±0.03 m, attained at 9 years of age. Age determination was corrected for possible underestimation by a factor of 1 and 2 years; however, this did not alter the predicted asymptotic values (Table 2). Data from the two earlier Macquarie Island studies mostly comprised animals 1 10 years of age (Fig. 2). Asymptotic values (±SE) estimated by fitting Gompertz models for the and data sets were 2.64±0.17 m and 2.58±0. m, respectively (Table 1). Simple power models fitted to age specific body-length data of females 1 10 years of age from (1) the combined data sets of (Carrick et al. 1962a) and (Bryden 1967): STL=1.67(Age 0. ); r 2 =0.992, n=45; and (2) the present study: STL=1.81(Age 0.18 ); r 2 =0.995, n=124 revealed significantly positive relationships. When transformed to a logarithmic scale, there was no significant difference in slope between the two lines (t (2,166) =0.522, P>0.05); however, the regression line had a significantly higher elevation (t (2,166) =3.646, P<0.001) indicating an increase in mean body length of 0.11±0.02 m (5.2%) between the s and 1990s for females between 1 and 10 years of age. Repeating this analysis after excluding data from dead animals from the 1950s to 1960s indicated a significant increase (the regression line had a significantly higher elevation, t (2,145) =4.448, P<0.001) in mean body length of 0.12±0.02 m (5.6%) over the same time period. Comparison with South Georgia stock For the and South Georgia data sets, asymptotic values of 3.04±0.17 m and Fig. 1 Body length plotted against age for live female southern elephant seals at Macquarie Island, The fitted line is the Gompertz curve STL ¼ 2:57e ð e 0:65ðtþ0:23ÞÞ where t is the age (years) and STL is the straight line snout tail length (m). Solid diamonds represent known-age animals and open diamonds represent animals aged by counting dental cementum layers
4 398 Table 1 Estimated Gompertz model parameters (±SE) for age-specific body length (straight-line snout-tail, m) of female southern elephant seals, where A is the asymptotic value for body length (m); and k and t 0 are fixed constants Location Years A K t 0 N r 2 Source Macquarie Island ± ± ± Present study ± ± ± Bryden (1967) ± ± ± Carrick et al. (1962a) South Georgia ± ± ± Arnbom et al. (1994) ± ± ± Laws (1953) Table 2 Effect of data adjustment on predicted Gompertz growth model parameters (±SE) for age-specific body length of female southern elephant seals Site and source Data adjustment A K t 0 N r 2 South Georgia 5% conversion for CSTL 2.84± ± ± (Laws 1953) 10% conversion for CSTL 2.55± ± ± % conversion for CSTL plus 1 year 2.55± ± ± Macquarie Island Non-adjusted 2.64± ± ± (present study) a +1 year 2.64± ± ± year 2.64± ± ± A denotes the asymptotic value for body length (m), k and t 0 are fixed constants, and CSTL is the snout tail length measured over the dorsal curvature a Includes only animals of estimated age 2.84±0.05 m, respectively, were estimated using the fitted Gompertz models (Table 1). The data excluded animals less than 5 years of age, and the Fig. 2 Body length plotted against age for female southern elephant seals at a Macquarie Island (Carrick et al. (1962a), b Macquarie Island (Bryden 1967), c South Georgia (Laws 1953) and d South Georgia (Arnbom et al. 1994). Solid diamonds represent animals measured after death and open diamonds represent animals measured whilst alive. The fitted lines are Gompertz curves: (a) STL ¼ 2:58e ð e 0:36ðtþ1:30Þ Þ (b) STL ¼ 2:64e ð e 0:27ðtþ2:23Þ Þ (c) STL ¼ 2:84e ð e 0:26ðtþ4:12Þ Þ and (d) STL ¼ 3:04e ð e 0:08ðtþ12:56Þ Þ where t is the age (years) and STL is the straight line snout tail length (m) Gompertz model did not appear to asymptote prior to years of age (Fig. 2). Increasing the factor for converting CSTL to STL from 5 to 10% significantly altered the model parameters (Table 2), although adding 1 year did not alter the asymptotic body length significantly (Table 2). Discussion Age estimation of southern elephant seals has previously relied upon counts of dentine GLGs of canine teeth collected from dead individuals (Laws 1952). To over- (a) 3.50 Macquarie Island Macquarie Island (b) (c) 3.50 South Georgia South Georgia (d)
5 399 come the drawbacks associated with killing animals to collect teeth, Arnbom et al. (1992) developed a technique to remove incisor teeth from live southern elephant seals for the counting of cementum GLGs. Because the pulp cavity of incisor teeth closes at 5 6 years of age, cementum GLGs can be counted as they continue to be deposited indefinitely on the outer surface of the tooth (Arnbom et al. 1992; McCann 1993). In contrast, the pulp cavity of canine teeth remains open throughout life (McCann 1993). The tendency to overestimate the age of younger animals (<4.7 years of age) reported here could be related to variations in GLG counts. Brent et al. (1996) noted that false annuli may be present, whilst Mansfield (1991) and Klevezal et al. (1994) suggested that the innermost layers may be misinterpreted because they can be subdivided into one or more additional layers. Moreover, Klevezal et al. (1994) observed a transition from two GLGs being deposited per year to one deposited per year at 2 5 years of age in female northern elephant seals (M. angustirostris). Underestimation of the age of older age class individuals has also been recorded in grey seals (Brent et al. 1996). Outer GLGs of older teeth are generally more difficult to interpret because they become increasingly narrow with age, with accuracy appearing to be best in the middle range of years (3 6 years) when annuli are relatively wide and well defined (Mansfield 1991). Correcting the present Macquarie Island data for underestimation by both 1 and 2 years of age did not alter the predicted asymptotic value, however (Table 2). Similarly, no difference was noted in asymptotic value for the South Georgia data when 1 year was added to age estimates (Table 2). In contrast, the point of inflexion for growth curves would be expected to shift to the left when age is under-estimated. Although this has no effect on the asymptotic length, it would distort length estimates for younger age classes. Other factors may introduce bias when using dental layers for age determination, particularly when teeth of the same age can vary in structure (McCann 1993). There is less space between the dental layers of incisors than canine teeth, making reading of GLGs more difficult (Brent et al. 1996). Variation may also exist both in the age at which the first cementum layer is deposited (Payne 1978) and when in the year the new layer of cementum starts being deposited (Mansfield 1991). Although Lawson et al. (1992) found increasing reader accuracy to be associated with experience, Brent et al. (1996) noted similar accuracies for both least experienced and very experienced readers, and attributed this to the least experienced reader being trained and familiarised immediately before starting the work. Of paramount importance to growth studies is the ability to consistently undertake repeatable, accurate and standardised morphometric measurements. McLaren (1993) reviewed the array of different body-length measurements used for pinnipeds for which it is not possible to establish a general set of conversions. Although curvilinear body-length measurement has been used previously for southern elephant seals (Laws 1953; Carrick et al. 1962a; Condy 1980), confusion may exist when trying to convert this to a straight-line measurement. For example, the difference in estimated asymptote when using a STL conversion factor of 5 and 10% was 0.30 m (McLaren 1993; Table 2, present study). Although measurement of body mass has less associated variation, body length was used to measure growth in the present study to offset the seasonal fluctuations in physical condition resulting from blubber deposition (Laws 1953). Inaccuracies in individual measurements need to be accounted for when calculating average growth curves (Laws 1953). Tape measures constructed of metal or other non-stretch material should be used, as fabric tapes may stretch considerably (Bonner et al. 1993). Variations in surface substrate and positioning of neck may also result in length variations in elephant seals of up to 4% between repeat measurements (Bell et al. 1997b). Although Wiig and Gjertz (1996) suggested that tonus in immobilised animals may result in lower length estimates when compared with dead animals, this effect is yet to be quantified. Although the different sets of growth data considered here all describe the body length of individuals of successive age, the data are subjected to many sampling and processing biases (Table 3), making most comparisons between studies inappropriate. These inconsistencies and Table 3 Comparison of data sets analysed and potential sources of bias and error Study Years Sample size Body length measured Animals measured dead or alive Method of age determination Source of potential bias or error South Georgia Laws (1953) CSTL Dead Teeth Non-random selection by sealers Arnbom et al. (1994) STL Alive (sedated) Teeth Bias towards small and large females, only females greater than 5 years of age Macquarie Island Carrick STL/CSTL Dead/alive Teeth/known age 5% conversion factor for CSTL et al. (1962a) Bryden (1967) STL Dead Teeth Small sample size Present study STL Alive (sedated) Teeth/known age Body length was measured by either straight line snout tail length (STL) or snout tail length over the dorsal curvature (CSTL)
6 400 biases may make the estimated asymptotic body lengths misleading. A number of fundamental differences between the South Georgia and Macquarie data sets examined here precluded a reliable comparison (Table 3). For example, the South Georgia data set was biased towards the extreme size classes (Arnbom et al. 1994). Approximately 40% of animals in the South Georgia study were chosen by sealers, who presumably had a commercial selection bias towards large animals (Laws 1953). A non-uniform sampling distribution can affect the shape of a growth curve and result in unreliable size estimates of younger age classes (Leberg et al. 1989). Over-representation of larger or smaller individuals may be a universal problem in studies of marine mammals and difficult to completely avoid. For example, it is possible that smaller individuals of some species are more readily captured (McLaren 1993). Further, sigmoidal growth curves are suitable only when complete lifetime growth is being analysed and will be influenced by the age classes present. The South Georgia data precluded animals less than 5 years of age, whilst the present study included many animals in their first few years of life. Hence, the asymptotic model for the South Georgia data reported here (Table 1) is not reliable. Considering the field methods used and selection of animals, the temporal comparison for Macquarie Island is likely to be more reliable. The state (dead or alive) at the time of measurement made little difference in estimates of asymptotic body length in females 1 10 years of age, despite almost half (n=21) of the measurements included in the s data set being taken from dead animals (Bryden 1967; Carrick et al. 1962a; Table 3, present study). Some (25%) of the body lengths obtained in were based on a 5% conversion factor from curvature length. Acknowledging these potential sources of error with the historical data, the apparent increase in body size reported here is nevertheless consistent with a reduction in both the rate of population decline recorded since the mid-1980s at Macquarie Island (H. Burton, unpublished data) and the onset of sexual maturity from 5 to 6 years in the s to 4 years of age in the latter half of the 1990s (Carrick et al 1962a; Hindell 1991; McMahon et al. 03). Relative to a generation length of approximately 5 10 years (McCann 1985), the reported increase in asymptotic body length of the 1- to 10-year-old age classes has occurred over a relatively short period of time. This suggests that the growth rate of females is more likely to have been limited during the s at Macquarie Island by an external factor(s), such as prey availability (Hindell et al. 1994; Guinet et al. 1999; Pistorius et al. 1999), rather than genetics. Acknowledgements J. Russell, P. Davis, S. Thalmann, C. Baars, M. Maurice and C. 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