Journal of Fish Biology (2016) doi:10.1111/jfb.12943, available online at wileyonlinelibrary.com
BRIEF COMMUNICATION Using genetic inference to re-evaluate the minimum longevity of the lemon shark Negaprion brevirostris J. L. Brooks*†‡, T. L. Guttridge*, B. R. Franks§, R. D. Grubbs‖, D. D. Chapman¶, S. H. Gruber***, J. D. Dibattista†† and K. A. Feldheim§§ *Bimini Biological Field Station Foundation, South Bimini, Bahamas, †Fish Ecology and Conservation Physiology Lab., Carleton Technology and Training Centre, Carleton University, 1125 Colonel By Drive, Ottawa, ON, K1S 5B6 Canada, §Department of Biology, Florida Southern College, Lakeland, FL 33801, U.S.A., ‖FSU Coastal and Marine Laboratory, 3618 Coastal Highway 98, St Teresa, FL 32358-2702, U.S.A., ¶School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY 11794-5000, U.S.A., **Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, 4600 Rickenbacker Causeway, Miami, FL 33149, U.S.A., ††Department of Environment and Agriculture, Curtin University, P. O. Box U1987, Perth, WA 6845, Australia and §§Pritzker Laboratory for Molecular Systematics and Evolution, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL 60605, U.S.A. (Received 4 July 2015, Accepted 8 February 2016) A combination of mark–recapture and genetic sampling was used to extend the minimum longevity of an elasmobranch species and the life span estimate of the lemon shark Negaprion brevirostris was increased conservatively from 20⋅2 to 37 years. This increase in longevity means higher vulnerability and a longer recovery time from exploitation. © 2016 The Fisheries Society of the British Isles
Key words: fishery management; genetic pedigree; life span; mark–recapture; natural mortality.
Accurately modelling population dynamics is impossible without an understanding of how quickly individuals are naturally removed from the population, and how many offspring they produce over a lifetime, both of which are influenced by life span (Hoenig, 1983). Life spans of long-lived fishes are often underestimated, which has implications for calculating natural mortality rates and intrinsic rebound potentials and can lead to mismanagement of stocks (Cailliet & Andrews, 2008). If a species is longer lived than originally modelled, for example, lifetime fecundity is underestimated, but instantaneous rates of natural mortality are overestimated. Across shark species, population productivity is negatively correlated with maximum reproductive age (Smith et al., 1998); therefore, an increase in the known maximum age within a population suggests the stock is actually more vulnerable to overexploitation. ‡Author to whom correspondence should be addressed. Tel.: +1 613 600 5895; email:
[email protected]
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J . L . B R O O K S E T A L.
Several methods for validating age have been developed and applied to sharks and batoids (Campana, 2001). Traditional age determination techniques involve analysing growth rings in vertebral centra, dorsal fin spines and caudal thorns (Brown & Gruber, 1988; Cailliet et al., 2006). Considerable variability, however, exists in calcification patterns, and thus the utility of ageing techniques, within and among taxonomic groups of elasmobranchs (Goldman, 2005). The precision (verification) and accuracy (validation) of ageing techniques should be assessed in all studies (Cailliet et al., 2006) using determinate methods such as mark–recapture of known-age or chemically tagged fishes or dating using lead:radium or bomb radiocarbon, or through indeterminate methods such as marginal increment analysis (Beamish & McFarlane, 1983; Brown & Gruber, 1988; Campana, 2001). Age estimation of older sharks using band pairs is also less accurate due to a decrease in somatic growth, leading to a decrease in the rate of deposition of vertebral material (Francis et al., 2007; Andrews et al., 2011; Hamady et al., 2014). Many original life span estimates have been re-evaluated using bomb radiocarbon methods and have often been revised upwards substantially (Campana, 2001; Cailliet & Andrews, 2008). The lemon shark Negaprion brevirostris (Poey 1868) is a large coastal shark that is found on both sides of the Atlantic Ocean and the eastern Pacific Ocean, where it is exploited by recreational and commercial fisheries (Compagno, 1984; Carlson et al., 2012; Shiffman & Hammerschlag, 2014). Brown & Gruber (1988) used vertebral centra to age 110 N. brevirostris in Florida, U.S.A., and Bimini, Bahamas. Annual band deposition on the vertebrae was validated through mark–recapture of chemically tagged individuals. Of the 110 animals aged, the oldest estimated was 20⋅2 years for a 226 cm pre-caudal length (LPC ) male. The study suffered, as many do, from low sample sizes and hence the growth curve did not form an asymptote. Hoenig & Gruber (1990) estimated that the theoretical maximum age for N. brevirostris was 26 years since the largest specimens from the Brown & Gruber (1988) study were considerably smaller than the maximum reported size. It was hypothesized that the maximum longevity for N. brevirostris had been largely underestimated and could be extended using previously documented age at maturity (Brown & Gruber, 1988), and an extensive genetic pedigree of offspring within the nurseries (Feldheim et al., 2014). Adult female N. brevirostris were aged in one of the two ways: parental genotype reconstruction or parental genotype reconstruction combined with tag–recapture. Parental genotype reconstruction involved exhaustively sampling 0 to 3 year old N. brevirostris at Bimini (25∘ 44′ N; 79∘ 18′ W), Bahamas, every year since 1993 (Feldheim et al., 2014). Sampling occurred each June using monofilament gillnets (180 m length, 2 m height) set perpendicular from shore. All captured N. brevirostris were measured (cm) for LPC , fork length (LF ) and total length (LT ), sex determined and tagged with a passive integrated transponder tag (PIT, Destron Fearing; www.destronfearing.com). See Gruber et al. (2001) for a full description of methods. A small piece of fin was removed and stored in 20% DMSO solution for genetic analysis. Individuals were released alive after a brief holding period of no more than 7 days (Feldheim et al., 2014). DNA from all N. brevirostris were genotyped at 11 polymorphic microsatellite markers followed by sibship and parental genotype reconstruction (for detailed methods, see Feldheim et al., 2002, 2014; Wang, 2004; DiBattista et al., 2008). Genetic profiling of N. brevirostris from 20 consecutive cohorts (1993–2012) showed that certain females faithfully gave birth at this site for nearly two decades (Feldheim et al., 2014). This enabled estimation of minimum
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12943
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E X T E N D I N G L O N G E V I T Y O F N E G A P R I O N B R E V I RO S T R I S
Table I. Female Negaprion brevirostris first and last year detected in Bimini, Bahamas, either as a physical capture or inferred genetically via their sampled pups. Minimum age is calculated by adding the approximate age at first parturition of 14 years (Brown & Gruber, 1988) Shark ID B-female 12 B-female 15 B-female 16 B-female 36 B-female 49 B-female 4 A4D11 B-female 1 B-female 8 B-female 10 B-female 5 B-female 18 B-female 119 B-female 19 B-female 105 B-female Mama B-female 27 B-female 34556 B-female 26
First year detected
Last year detected
Minimum age (years)
1989 1992 1991 1995 1995 1996 1997 1990 1992 1997 1991 1999 2000 1993 2001 1991 1995 1995 1996
2012 2015 2010 2013 2013 2014 2015 2007 2008 2013 2006 2013 2014 2006 2013 2001 2003 2003 2004
37 35 33 32 32 32 32 31 30 30 29 28 28 27 26 24 22 22 22
age of these individuals, with the conservative assumption being made that their first genetically confirmed litter in Bimini was their first litter. Brown & Gruber (1988) estimated age of maturity of 12⋅7 years with first parturition at 14 years, which was concordant with direct observations of philopatric females of known age first returning to Bimini for parturition (Feldheim et al., 2014). This study, therefore, conservatively estimated the age of 19 females that gave birth multiple times at Bimini by assuming that they were age 14 years the first year any of their offspring were sampled, and died the last year any of their offspring were sampled. Tag–recapture was also used to directly estimate age of one tagged female. Gravid females are annually targeted for capture in late March and April, as they enter the Bimini Lagoon as part of an ongoing study of natal philopatry. Individuals were either captured by closely following the N. brevirostris from a skiff in shallow water (
