Investigations of Δ 14C, δ 13C, and δ 15N in vertebrae of white shark (Carcharodon carcharias) from the eastern North Pacific Ocean

The white shark, Carcharodon carcharias, has a complex life history that is characterized by large scale movements and a highly variable diet. Estimates of age and growth for the white shark from the eastern North Pacific Ocean indicate they have a slow growth rate and a relatively high longevity. Age, growth, and longevity estimates useful for stock assessment and fishery models, however, require some form of validation. By counting vertebral growth band pairs, ages can be estimated, but because not all sharks deposit annual growth bands and many are not easily discernable, it is necessary to validate growth band periodicity with an independent method. Radiocarbon (¹⁴C) age validation uses the discrete ¹⁴C signal produced from thermonuclear testing in the 1950s and 1960s that is retained in skeletal structures as a time-specific marker. Growth band pairs in vertebrae, estimated as annual and spanning the 1930s to 1990s, were analyzed for Δ¹⁴C and stable carbon and nitrogen isotopes (δ¹³C and δ¹⁵N). The aim of this study was to evaluate the utility of ¹⁴C age validation for a wide-ranging species with a complex life history and to use stable isotope measurements in vertebrae as a means of resolving complexity introduced into the ¹⁴C chronology by ontogenetic shifts in diet and habitat. Stable isotopes provided useful trophic position information; however, validation of age estimates was confounded by what may have been some combination of the dietary source of carbon to the vertebrae, large-scale movement patterns, and steep ¹⁴C gradients with depth in the eastern North Pacific Ocean.     

Comparative morphology of the electrosensory system of the epaulette shark Hemiscyllium ocellatum and brown-banded bamboo shark Chiloscyllium punctatum

We compared the electrosensory system of two benthic elasmobranchs Hemiscyllium ocellatum and Chiloscyllium punctatum. The distribution of the ampullary pores on the head was similar for both species, with a higher density of pores anteriorly and a lower density posteriorly, although C. punctatum generally possessed larger pores. Ampullary canals of the mandibular cluster were quasi-sinusoidal in H. ocellatum, a shape previously found in benthic rays only, whereas ampullary canals in C. punctatum were of a linear morphology as reported for many shark and ray species previously. The ampullae proper were of the lobular type, as occurs in most galean sharks. Chiloscyllium punctatum had six sensory chambers compared with the five per ampulla in H. ocellatum, which were generally smaller than those of C. punctatum. The sensory epithelium comprised flattened receptor cells, compared with the usual pear-shaped receptor cells encountered in other elasmobranchs and their apically nucleated supportive cells did not protrude markedly into the ampullary lumen, unlike those in benthic rays.     

A critical appraisal of marginal increment analysis for assessing temporal periodicity in band formation among tropical sharks

Marginal increment ratio (MIR) analyses were conducted as part of age and growth studies on three coastal/semi-oceanic species, the smalltail shark, Carcharhinus porosus, daggernose shark, Isogomphodon oxyrhynchus and the night shark C. signatus, and two ubiquitous oceanic species, blue shark, Prionace glauca, and whitetip shark, C. longimanus, collected in equatorial areas off Brazil with the aim of establishing the interspecific temporal nature of vertebral band formation. Monthly variations in marginal bands were analyzed using mean MIR on the entire sample as the standard method for all species. Reasons for the inconclusive results regarding these species are critically appraised with respect to three main sources of bias that are associated with marginal increment analysis (MIA). Bias due to insufficient sample sizes may have hampered the analysis for I. oxyrhynchus and C. longimanus due to movements from shallow waters to seamounts for the former species and to extensive migrations for the latter. Bias due to data collection over too long a period is thought to have influenced monthly mean MIR for C. porosus and P. glauca. For the latter, individuals from different age groups lay down rings at different times, making band deposition inconsistent between individuals. Finally, bias due to births occurring over too long a period was the prevalent cause for confounding MIR values among I. oxyrhynchus and C. signatus species, whose birth period lasts several months and leads to different ages within the same cohort. Other approaches used for MIA in C. signatus and P.␣glauca led to distinct times of band formation by age-groups when compared to MIR applied on the entire sample. For the daggernose shark, delays in events related to the reproductive cycle from one year to the next were also found to confound MIR. Requirements for the use of MIR implying a band width that displays a sinusoidal cycle when temporally plotted (month or season) were not fulfilled for any of these species. The method has been of little utility for detecting the periodicity of band deposition among sharks from the tropics. This emphasizes the need for supplying information on the temporal periodicity of pair deposition based on other methods.     

Age and growth of the sandbar shark, Carcharhinus plumbeus, in Hawaiian waters through vertebral analysis

Age and growth estimates were determined for the sandbar shark, Carcharhinus plumbeus, from Oahu, Hawaii in the central Pacific Ocean. Age estimates were obtained through vertebral centra analysis of 187 sharks. We verified our age estimates through marginal increment analysis of centra and oxytetracycline marking methods of at liberty sandbar sharks. Sizes of sampled sharks ranged from 46 to 147 cm pre-caudal length. Four growth models were fitted to length-at-age data; two forms of the von Bertalanffy growth model, the Gompertz growth model, and a logistic growth model. Males and females exhibited statistically significant differences in growth, indicating that females grow slower and attain larger sizes than males. Growth parameter estimates revealed slower growth rates than previously estimated (based on captive specimens) for Hawaiian sandbar sharks. The von Bertalanffy growth model using empirical length-at-birth provided the best biological and statistical fit to the data. This model gave parameter estimates of L _∞ = 138.5 cm PCL and k = 0.12 year⁻¹ for males and L _∞ = 152.8 cm PCL, k = 0.10 year⁻¹ for females. Male and female sandbar sharks mature at approximately 8 and 10 years of age, respectively.     

Long‐term sperm storage in the brownbanded bamboo shark Chiloscyllium punctatum

This study investigated the birth of a brownbanded bamboo shark Chiloscyllium punctatum at the Steinhart Aquarium. Genetic analyses suggest this is the longest documented case of sperm storage for any species of shark (45 months).     

Turning maneuvers in sharks: Predicting body curvature from axial morphology

Given the diversity of vertebral morphologies among fishes, it is tempting to propose causal links between axial morphology and body curvature. We propose that shape and size of the vertebrae, intervertebral joints, and the body will more accurately predict differences in body curvature during swimming rather than a single meristic such as total vertebral number alone. We examined the correlation between morphological features and maximum body curvature seen during routine turns in five species of shark: Triakis semifasciata, Heterodontus francisci, Chiloscyllium plagiosum, Chiloscyllium punctatum, and Hemiscyllium ocellatum. We quantified overall body curvature using three different metrics. From a separate group of size‐matched individuals, we measured 16 morphological features from precaudal vertebrae and the body. As predicted, a larger pool of morphological features yielded a more robust prediction of maximal body curvature than vertebral number alone. Stepwise linear regression showed that up to 11 features were significant predictors of the three measures of body curvature, yielding highly significant multiple regressions with r² values of 0.523, 0.537, and 0.584. The second moment of area of the centrum was always the best predictor, followed by either centrum length or transverse height. Ranking as the fifth most important variable in three different models, the body's total length, fineness ratio, and width were the most important non‐vertebral morphologies. Without considering the effects of muscle activity, these correlations suggest a dominant role for the vertebral column in providing the passive mechanical properties of the body that control, in part, body curvature during swimming. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

No apparent negative tagging effects after 13 years at liberty for lemon shark,Negaprion brevirostris implanted with acoustic transmitter

An intact and uncompromised internal acoustic transmitter was non-lethally recovered from a lemon shark Negaprion brevirostris, after 13 years at liberty. The shark, first tagged at an estimated age of 2 years old near South Bimini, Bahamas in 2004, was recaptured in 2017 with a total length of 264 cm. The tagged shark displayed typical growth rate, pregnancy, natal homing and pupping behaviour of other individuals in this population. This observation provides important evidence regarding the effects from long-term retention of implanted acoustic transmitters in a carcharhinid shark.     

Analysis of variability in vertebral morphology and growth ring counts in two Carcharhinid sharks

Inter- and intra-regional variations in vertebrae morphology and growth increment counts (band counts) were analyzed for two carcharhinid shark species, Carcharhinus plumbeus (n = 10) and C. limbatus (n = 11). Five sequential vertebrae were removed from the cervical region, above the branchial chamber and posterior to the chondrocrainium, and thoracic region, below the first dorsal fin. Dorsal–ventral height, medial–lateral breadth, and caudal–cranial length were measured for each sampled vertebra. Results indicate no significant difference in vertebral morphology within a sampled region of the vertebral column. However, a significant difference in vertebral morphology was noted between regions for both shark species, with thoracic vertebrae consistently larger than cervical vertebrae. A sub-set of three vertebrae was taken from each sampled region of each shark for sectioning and counting of growth increments. Analyses of growth increment counts by two readers indicated no significant difference in band counts within and between sampled regions.     

Periodicity of the growth-band formation in vertebrae of juvenile scalloped hammerhead shark Sphyrna lewini from the Mexican Pacific Ocean

The age of 296 juvenile scalloped hammerhead sharks Sphyrna lewini caught by several fisheries in the Mexican Pacific Ocean from March 2007 to September 2017 were estimated from growth band counts in thin-sectioned vertebrae. Marginal-increment analysis (MIA) and centrum-edge analysis (CEA) were used to verify the periodicity of formation of the growth bands, whereas elemental profiles obtained from LA-ICP-MS transect scans in vertebrae of 15 juveniles were used as an alternative approach to verify the age of the species for the first time. Age estimates ranged from 0 to 10+ years (42–158.7 cm total length; L_T). The index of average percentage error (I_APE 3.6%), CV (5.2%), bias plots and Bowker's tests of symmetry showed precise and low-biased age estimation. Both MIA and CEA indicated that in the vertebrae of juveniles of S. lewini a single translucent growth band was formed during winter (November–March) and an opaque band during summer (July–September), a period of faster growth, apparently correlated with a higher sea surface temperature. Peaks in vertebral P and Mn content spatially corresponded with the annual banding pattern in most of the samples, displaying 1.19 and 0.88 peaks per opaque band, respectively, which closely matched the annual deposition rate observed in this study. Although the periodicity of growth band formation needs to be verified for all sizes and ages representing the population of the species in the region, this demonstration of the annual formation of the growth bands in the vertebrae of juveniles should lead to a re-estimation of the growth parameters and productivity of the population to ensure that it is harvested at sustainable levels.     

Viscosity and optical activity of chondroitin sulfate C

Chondroitin sulfate C (CSC), isolated from shark vertebral mucoprotein, has a molecular weight of 0.2 × 10⁴–5.5 × 10⁴ in both NaCl and CaCl₂ solutions. Optical rotatory dispersion and circular dichroism of CSC reveal a strong, negative, optically active band near 210 mμ, arising from the carboxylate and N-acetyl groups. Results of similar studies of glucuronic acid and N-acetyl-D -galactosamine suggest that the N-acetyl group contributes more to the rotations of CSC than does the carboxylate group, but the acidification of the carboxylate groups largely accounts for the change in magnitude and position of the circular dichroic bands of CSC at low pH.     

Vertebral Bomb Radiocarbon Suggests Extreme Longevity in White Sharks

Conservation and management efforts for white sharks (Carcharodon carcharias) remain hampered by a lack of basic demographic information including age and growth rates. Sharks are typically aged by counting growth bands sequentially deposited in their vertebrae, but the assumption of annual deposition of these band pairs requires testing. We compared radiocarbon (Δ¹⁴C) values in vertebrae from four female and four male white sharks from the northwestern Atlantic Ocean (NWA) with reference chronologies documenting the marine uptake of ¹⁴C produced by atmospheric testing of thermonuclear devices to generate the first radiocarbon age estimates for adult white sharks. Age estimates were up to 40 years old for the largest female (fork length [FL]: 526 cm) and 73 years old for the largest male (FL: 493 cm). Our results dramatically extend the maximum age and longevity of white sharks compared to earlier studies, hint at possible sexual dimorphism in growth rates, and raise concerns that white shark populations are considerably more sensitive to human-induced mortality than previously thought.     

Growth forms and age estimation of treeline species

The correct evaluation of the age of small tree individuals is of great importance in ecological studies, and can be performed if growth units are identifiable even under strong environmental constraints. We aimed to assess the reliability of age evaluation of small individuals of four species commonly occurring at the treeline in the Alps and the Apennines (N Italy), Picea abies, Pinus cembra, Larix decidua and Fagus sylvatica. A total of 224 individuals were sampled along an altitudinal gradient up to the treeline. For each species, we assessed the growth architecture and the appearance of annual growth units; for each individual, age and evaluation uncertainty were estimated. To verify the estimation a core or a cross-section was obtained. The estimated age was compared with the tree-ring age through linear regression and reduced chi square test, and the estimation accuracy was evaluated as function of tree age, dimension and environmental parameters. A good estimation was possible for all species, even when loss of vertical growth occurred. The highest error occurred for Larix, the lowest for Pinus; the error was generally correlated with tree age and dimension, and was affected by altitude and geomorphology. Good reduced chi square values were reached considering only the youngest individuals for Fagus and Picea and the smallest for Fagus and Larix; the uncertainty was generally underestimated for Pinus. Even though reliable age estimation could be obtained, a realistic and species-specific evaluation of the estimation uncertainties is necessary to assess estimation accuracy for ecological studies.     

Age and Growth of the Whiskery Shark, Furgaleus macki, from Southwestern Australia

Age and growth of the whiskery shark, Furgaleus macki, from southwestern Australia were examined using vertebral ageing and tag-recapture data. The readability of bands on the vertebral centra varied markedly between individuals. Four readers were used to make band counts, with the most experienced reader having the lowest index of average percent error and the highest level of agreement with final counts. Marginal increment analysis indicated that opaque bands form in January. With parturition occurring from August to October, size data suggests that the first band is probably formed 15–17 months after birth. The age at maturity was estimated to be 4.5 years for males, and 6.5 years for females. The oldest male was 10.5 years, and oldest female was 11.5 years. Von Bertalanffy growth parameters for males were L =121.5cm fork length, K=0.423 year^–1, t ₀=–0.472 years, were L =120.7cm fork length, K=0.369 year^–1, t ₀=–0.544 years for females, and were L =118.1cm fork length, K=0.420 year^–1, t ₀=–0.491 years for combined sexes. Data from a tag recapture study were analysed using a maximum likelihood method to verify the estimates of growth parameters from vertebral ageing. Von Bertalanffy growth parameters from the tag recapture study were L =128.2cm fork length, K=0.288 year^–1, t ₀=–0.654 years. The two methods of estimating growth parameters produced similar results, with rapid growth until approximately 5 years of age, after which there was little increase in length.     

New information on age and growth in length of Micromesistius australis,Norman 1937 (Pisces,Gadidae), in the South-West Atlantic

Summary Sagittal otoliths were used for age determination in 1121 specimens of Micromesistius australis, caught in waters of the South-West Atlantic during the cruises made by the ships Walther Herwig and Shinkai Maru in agreement with the Argentine Republic, during the years 1978 and 1978/1979, respectively. The interpretation of growth rings required the otoliths to undergo a paraffin wax embedding and cutting technique. The relations otolith length-fish length and fish length-half otolith width were linear. Thus, back calculations, when necessary, were made by a simple extrapolation. Numbers of males and females were nearly equal, resulting in a sex ratio of 1:1.09. Length frequencies and age distributions were calculated for each sex separately. A significant difference in growth between sexes was found, curves for each were derived. A linear, regression was made and the Von Bertalanffy equation estimated as: Lt=56.90 [1-e^{-0.1983 (t+1.84)}], in males, and Lt=60.08 [1-e^{-0.1769 (t+2.07)}] in females, with Lt in cm and t in years. For estimation of these equation parameters age groups 2–16 years in males and 2–22 years in females were taken into account. All theoretical Lt values and almost all observed lengths for females were greater than those of males in corresponding age groups. Previously published observations about M. australis on this subject, are not in agreement or only in partial accord with present results. These are discussed. Original photographs of otolith cross sections illustrating age determination methods are presented for the first time in age and growth studies of this species.     

Gap-phase dynamics and coexistence of a long-lived pioneer and shade-tolerant tree species in the canopy of an old-growth coastal temperate rain forest of Chiloé Island, Chile

Aim A major question with regard to the ecology of temperate rain forests in south‐central Chile is how pioneer and shade‐tolerant tree species coexist in old‐growth forests. We explored the correspondence between tree regeneration dynamics and life‐history traits to explain the coexistence of these two functional types in stands apparently representing a non‐equilibrium mixture. Location This study was conducted in northern Chiloé Island, Chile (41.6° S, 73.9° W) in a temperate coastal rain forest with no evidence of stand disruption by human impact. Methods We assessed stand structure by sampling all stems within two 50 × 20 m and four 5 × 100 m plots. A 600‐m long transect, with 20 uniformly spaced sampling points, was used to quantify seedling and sapling densities, obtain increment cores, and randomly select 10 tree‐fall gaps. We used tree‐ring analysis to assess establishment periods and to relate the influences of disturbances to the regeneration dynamics of the main canopy species. Results Canopy emergent tree species were the long‐lived pioneer Eucryphia cordifolia and the shade‐tolerant Aextoxicon punctatum. Shade‐tolerant species such as Laureliopsis philippiana and several species of Myrtaceae occupied the main canopy. The stem diameter distribution for E. cordifolia was distinctly unimodal, while for A. punctatum it was multi‐modal, with all age classes represented. Myrtaceae accounted for most of the small trees. Most tree seedlings and saplings occurred beneath canopy gaps. Based on tree‐ring counts, the largest individuals of A. punctatum and E. cordifolia had minimum ages estimated to be > 350 years and > 286 years, respectively. Shade‐tolerant Myrtaceae species and L. philippiana had shorter life spans (< 200 years). Most growth releases, regardless of tree species, were moderate and have occurred continuously since 1750. Main conclusions We suggest that this coastal forest has remained largely free of stand‐disrupting disturbances for at least 450 years, without substantial changes in canopy composition. Release patterns are consistent with this hypothesis and suggest that the disturbance regime is dominated by individual tree‐fall gaps, with sporadic multiple tree falls. Long life spans, maximum height and differences in shade tolerance provide a basis for understanding the long‐term coexistence of pioneer and shade‐tolerant tree species in this coastal, old‐growth rain forest, despite the rarity of major disturbances.     

Estimation of growth parameters from published data for several Mediterranean fishes

Two sets of von Bertalanffy growth parameter (VBGP) estimates are provided for several Mediterranean fish stocks. All estimates are based on the non‐linear least square regression and accompanied by uncertainty measures (i.e. standard errors). The first set consists of growth parameters estimated from 73 published length‐at‐age data with no previous VBGP estimations; in this case, fitting was possible for 30 length‐at‐age sets, corresponding to 22 species, two estimates of which (Mycteroperca rubra and Myctophum punctatum) are the first for the Mediterranean. The second set refers to the re‐estimation of VBGPs from 69 published length‐at‐age data with available original VBGP estimates derived from linear methods (i.e. Ford‐Walford, von Bertalanffy and Gulland‐Holt plots); in this case, fitting was possible for 50 sets. Overall VBGP estimation was not possible for 43 and 19 cases for the first and second sets, respectively. This was because either (a) <4 mean length‐at‐age data were available, or (b) fitting was not possible because of an exponential or a very slow linear increase of length with age, or (c) estimates were unrealistic (i.e. L_max/L_∞ < 0.7) mainly because of unrealistic length‐at‐ages and/or insufficient sampling of older individuals. These estimations and re‐estimations enrich the available data on growth parameters of Mediterranean fishes, both in terms of quantity and quality of information.     

Comparison of otolith and scale readings for age and growth estimation of common dentex Dentex dentex

Three methods of age estimation were compared for Dentex dentex. Based on sectioned otoliths, scales appeared to be relevant only up to 5 years and whole otoliths up to 12 years. The maximum estimated age was 36 years, which constitutes to date the oldest age reported.