Age and growth of juvenile lemon sharks (Negaprion brevirostris) at an insular nursery in the southern Caribbean
Rafael Tavares
A , Bradley M. Wetherbee B C E and Jon Paul Rodriguez D
+ Author Affiliations
- Author Affiliations
A Centro para la Investigación de Tiburones (CIT), Avenida Don Bosco, Quinta ABC, No. 10, La Florida 1050, Distrito Capital, Caracas, Venezuela.
B Department of Biological Sciences, University of Rhode Island, Kingston, RI 02881, USA.
C Guy Harvey Research Institute, Nova Southeastern University, Dania Beach, FL 33064, USA.
D Instituto Venezolano de Investigaciones Científicas (IVIC), Avenida Panamericana kilómetro 11, San Antonio de los Altos 1204, Estado Miranda, Venezuela.
E Corresponding author. Email: wetherbee@uri.edu
Marine and Freshwater Research 72(2) 163-172 https://doi.org/10.1071/MF20070
Submitted: 9 March 2020 Accepted: 9 April 2020 Published: 6 June 2020
Abstract
During the first few years of life, lemon sharks (Negaprion brevirostris) occupy discrete nursery areas in small numbers (<100). Biotic and abiotic features vary among nursery areas, resulting in young sharks experiencing a range of physical and biological conditions that, in turn, influence life-history characteristics such as growth and mortality and are, therefore, directly related to population structure and ability to withstand fishing pressure. In the present study, we used tag and recapture data to estimate growth rates and construct size at age models for lemon sharks at Los Roques, Venezuela. Annual growth rates of lemon sharks were comparable to those in other nursery areas, but considerably higher than those reported for the well studied nursery at Bimini, Bahamas. Growth rate increased with age during the first 4 years of life for lemon sharks at Los Roques, while they occupied the nursery area. Comparison of growth rates of lemon sharks among geographically separate nursery areas showed no obvious relationships between growth rate and latitude or temperature. For species with broad geographical distributions, consideration of variability of life-history characteristics such as growth is important for accurate stock assessment and effective large-scale management of populations.
Additional keywords: life-history traits, Los Roques, tag and recapture.
References
Akaike, H. (1981). Likelihood of a model and information criteria. Journal of Econometrics 16, 3–14.| Likelihood of a model and information criteria.Crossref | GoogleScholarGoogle Scholar |
Ashe, J. L., Feldheim, K. A., Fields, A. T., Reyier, E. A., Brooks, E. J., O’Connell, M. T., Skomal, G., Gruber, S. H., and Chapman, D. D. (2015). Local population structure and context-dependent isolation by distance in a large coastal shark. Marine Ecology Progress Series 520, 203–216.
| Local population structure and context-dependent isolation by distance in a large coastal shark.Crossref | GoogleScholarGoogle Scholar |
Barker, M. J., Gruber, S. H., Newman, S. P., and Schluessel, V. (2005). Spatial and ontogenetic variation in growth of nursery-bound juvenile lemon sharks, Negaprion brevirostris: a comparison of two age-assessing techniques. Environmental Biology of Fishes 72, 343–355.
| Spatial and ontogenetic variation in growth of nursery-bound juvenile lemon sharks, Negaprion brevirostris: a comparison of two age-assessing techniques.Crossref | GoogleScholarGoogle Scholar |
Bhattacharya, C. G. (1967). A simple method of resolution of a distribution into Gaussian components. Biometrics 23, 115–135.
| A simple method of resolution of a distribution into Gaussian components.Crossref | GoogleScholarGoogle Scholar | 6050463PubMed |
Bradley, D., Conklin, E., Papastamatiou, Y. P., McCauley, D. J., Pollock, K., Kendall, B. E., Gaines, S. D., and Caselle, J. E. (2017). Growth and life history variability of the grey reef shark (Carcharhinus amblyrhynchos) across its range. PLoS One 12, e0172370.
| Growth and life history variability of the grey reef shark (Carcharhinus amblyrhynchos) across its range.Crossref | GoogleScholarGoogle Scholar | 28207874PubMed |
Carlson, J. K., and Baremore, I. E. (2003). Changes in biological parameters of Atlantic sharpnose shark Rhizoprionodon terranovae in the Gulf of Mexico: evidence for density-dependent growth and maturity? Marine and Freshwater Research 54, 227–234.
| Changes in biological parameters of Atlantic sharpnose shark Rhizoprionodon terranovae in the Gulf of Mexico: evidence for density-dependent growth and maturity?Crossref | GoogleScholarGoogle Scholar |
Castro, J. I. (1993). The shark nursery of Bulls Bay, South Carolina, with a review of the shark nurseries of the southeastern coast of the United States. Environmental Biology of Fishes 38, 37–48.
| The shark nursery of Bulls Bay, South Carolina, with a review of the shark nurseries of the southeastern coast of the United States.Crossref | GoogleScholarGoogle Scholar |
Cervigón, F. (1992). ‘Las Dependencias Federales.’ (Editorial ExLibris: Caracas, Venezuela.)
Chapman, D. D., Babcock, E. A., Gruber, S. H., DiBattista, J. D., Franks, B. R., Kessel, S. A., Guttridge, T., Pikitch, E. K., and Feldheim, K. A. (2009). Long-term natal site-fidelity by immature lemon sharks (Negaprion brevirostris) at a subtropical island. Molecular Ecology 18, 3500–3507.
| Long-term natal site-fidelity by immature lemon sharks (Negaprion brevirostris) at a subtropical island.Crossref | GoogleScholarGoogle Scholar | 19659480PubMed |
Clark, T. D., and Seymour, R. S. (2006). Cardiorespiratory physiology and swimming energetics of a high-energy-demand teleost, the yellowtail kingfish (Seriola lalandi). The Journal of Experimental Biology 209, 3940–3951.
| Cardiorespiratory physiology and swimming energetics of a high-energy-demand teleost, the yellowtail kingfish (Seriola lalandi).Crossref | GoogleScholarGoogle Scholar | 16985209PubMed |
Compagno, L. J. V. (1984). ‘Sharks of the World: an Annotated and Illustrated Catalogue of Shark Species Known to Date.’ FAO Fisheries Synopsis, 125. (FAO: Rome, Italy.)
Cortés, E., Brooks, E. N., and Gedamke, T. (2012). Population dynamics, demography and stock assessment. In ‘Biology of Sharks and Their Relatives’. (Eds J. A. Musick and M. R. Heithaus.) pp. 453–486. (CRC Press: New York, NY, USA.)
Dawkins, R., and Krebs, J. R. (1979). Arms races between and within species. Proceedings of the Royal Society of London. Series B, Biological Sciences 205, 489–511.
| Arms races between and within species.Crossref | GoogleScholarGoogle Scholar |
DiBattista, J. D., Feldheim, K. A., Gruber, S. H., and Hendry, A. P. (2007). When bigger is not better: selection against large size, high condition and fast growth in juvenile lemon sharks. Journal of Evolutionary Biology 20, 201–212.
| When bigger is not better: selection against large size, high condition and fast growth in juvenile lemon sharks.Crossref | GoogleScholarGoogle Scholar | 17210013PubMed |
Feldheim, K. A., Gruber, S. H., and Ashley, M. V. (2001). Population genetic structure of the lemon shark (Negaprion brevirostris) in the western Atlantic: DNA microsatellite variation. Molecular Ecology 10, 295–303.
| Population genetic structure of the lemon shark (Negaprion brevirostris) in the western Atlantic: DNA microsatellite variation.Crossref | GoogleScholarGoogle Scholar | 11298946PubMed |
Feldheim, K. A., Gruber, S. H., and Ashley, M. V. (2002). The breeding biology of lemon sharks at a tropical nursery lagoon. Proceedings of the Royal Society B. Biological Sciences 269, 1655–1661.
| The breeding biology of lemon sharks at a tropical nursery lagoon.Crossref | GoogleScholarGoogle Scholar |
Francis, R. I. C. C. (1988). Maximum likelihood estimation of growth and growth variability from tagging data. New Zealand Journal of Marine and Freshwater Research 22, 43–51.
| Maximum likelihood estimation of growth and growth variability from tagging data.Crossref | GoogleScholarGoogle Scholar |
Freitas, R. H. A., Rosa, R. S., Gruber, S. H., and Wetherbee, B. M. (2006). Early growth and juvenile population structure of lemon sharks, Negaprion brevirostris, in the Atol das Rocas Biological Reserve, off north-east Brazil. Journal of Fish Biology 68, 1319–1332.
| Early growth and juvenile population structure of lemon sharks, Negaprion brevirostris, in the Atol das Rocas Biological Reserve, off north-east Brazil.Crossref | GoogleScholarGoogle Scholar |
Gayanilo, F. C., Sparre, P., and Pauly, D. (2005). ‘The FAO-ICLARM Stock Assessment Tools II (FiSAT II).’ FAO Computerized Information Series 8. (FAO: Rome, Italy.)
Goldman, K. J., Natanson, L. J., and Cailliet, G. M. (2012). Assessing the age and growth of chondrichthyan fishes. In ‘Biology of Sharks and Their Relatives’. (Eds J. A. Musick and M. R. Heithaus.) pp. 423–451. (CRC Press: New York, NY, USA.)
Gruber, S. H., Nelson, D. R., and Morrissey, J. F. (1988). Patterns of activity and space utilization of juvenile lemon sharks, Negaprion brevirostris, in a shallow Bahamian lagoon. Bulletin of Marine Science 43, 61–76.
Gruber, S. H., de Marignac, J. R. C., and Hoenig, J. M. (2001). Survival of juvenile lemon sharks at Bimini, Bahamas, estimated by mark–depletion experiments. Transactions of the American Fisheries Society 130, 376–384.
| Survival of juvenile lemon sharks at Bimini, Bahamas, estimated by mark–depletion experiments.Crossref | GoogleScholarGoogle Scholar |
Guttridge, T. L., Gruber, S. H., Franks, B. R., Kessel, S. T., Gledhill, K. S., Uphill, J., Krause, J., and Sims, D. W. (2012). Deep danger: intra-specific predation risk influences habitat use and aggregation formation of juvenile lemon sharks Negaprion brevirostris. Marine Ecology Progress Series 445, 279–291.
| Deep danger: intra-specific predation risk influences habitat use and aggregation formation of juvenile lemon sharks Negaprion brevirostris.Crossref | GoogleScholarGoogle Scholar |
Henderson, A. C., McClellan, K., and Calosso, M. (2010). Preliminary assessment of a possible lemon shark nursery in the Turks & Caicos Islands, British West Indies. Caribbean Journal of Science 46, 29–38.
| Preliminary assessment of a possible lemon shark nursery in the Turks & Caicos Islands, British West Indies.Crossref | GoogleScholarGoogle Scholar |
Hoenig, J. M., and Gruber, S. H. (1990). Life-history patterns in the elasmobranchs: implications for fisheries management. In ‘Elasmobranchs as Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of the Fisheries’. Technical Report NMFS 90. (Eds H. L. Pratt Jr., S. H. Gruber, and T. Taniuchi.) pp. 1–16. (NOAA: Washington, DC, USA.)
Jennings, D. E., Gruber, S. H., Franks, B. R., Kessel, S. T., and Robertson, A. L. (2008). Effects of large-scale anthropogenic development on juvenile lemon shark (Negaprion brevirostris) populations of Bimini, Bahamas. Environmental Biology of Fishes 83, 369–377.
| Effects of large-scale anthropogenic development on juvenile lemon shark (Negaprion brevirostris) populations of Bimini, Bahamas.Crossref | GoogleScholarGoogle Scholar |
Kessel, S. T., Hansell, A. C., Gruber, S. H., Guttridge, T. L., Hussey, N. E., and Perkins, R. G. (2016). Three decades of longlining in Bimini, Bahamas, reveals long-term trends in lemon shark Negaprion brevirostris (Carcharhinidae) catch per unit effort. Journal of Fish Biology 88, 2144–2156.
| Three decades of longlining in Bimini, Bahamas, reveals long-term trends in lemon shark Negaprion brevirostris (Carcharhinidae) catch per unit effort.Crossref | GoogleScholarGoogle Scholar | 27245624PubMed |
Laake, J. (2013). ‘RMark: an R Interface for Analysis of Capture–Recapture Data with MARK.’ (Alaska Fisheries Science Center, NMFS-NOAA, US Department of Commerce: Seattle, WA, USA.)
Lombardi-Carlson, L., Cortes, E., Parsons, G., and Manire, C. (2003). Latitudinal variation in life-history traits of bonnethead sharks, Sphyrna tiburo (Carcharhiniformes: Sphyrnidae) from the eastern Gulf of Mexico. Marine and Freshwater Research 54, 875–883.
| Latitudinal variation in life-history traits of bonnethead sharks, Sphyrna tiburo (Carcharhiniformes: Sphyrnidae) from the eastern Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Manire, C. A., and Gruber, S. H. (1991). Effect of M-type dart tags on field growth of juvenile lemon sharks. Transactions of the American Fisheries Society 120, 776–780.
| Effect of M-type dart tags on field growth of juvenile lemon sharks.Crossref | GoogleScholarGoogle Scholar |
Manire, C. A., and Gruber, S. H. (1993). A preliminary estimate of natural mortality of age-0 lemon sharks, Negaprion brevirostris. In ‘Conservation Biology of Elasmobranchs’. Technical Report NMFS 115. (Ed. S. Branstetter.) pp. 65–71. (NOAA: Washington, DC, USA.)
Morrissey, J. F., and Gruber, S. H. (1993). Habitat selection by juvenile lemon sharks, Negaprion brevirostris. Environmental Biology of Fishes 38, 311–319.
| Habitat selection by juvenile lemon sharks, Negaprion brevirostris.Crossref | GoogleScholarGoogle Scholar |
Murchie, K. J., Schwager, E., Cooke, S. J., Danylchuk, A. J., Danylchuk, S. E., Goldberg, T. L., Suski, C. D., and Philipp, D. P. (2010). Spatial ecology of juvenile lemon sharks (Negaprion brevirostris) in tidal creeks and coastal waters of Eleuthera, The Bahamas. Environmental Biology of Fishes 89, 95–104.
| Spatial ecology of juvenile lemon sharks (Negaprion brevirostris) in tidal creeks and coastal waters of Eleuthera, The Bahamas.Crossref | GoogleScholarGoogle Scholar |
Newman, S. P., Handy, R. D., and Gruber, S. H. (2010). Diet and prey preference of juvenile lemon sharks, Negaprion brevirostris. Marine Ecology Progress Series 398, 221–234.
| Diet and prey preference of juvenile lemon sharks, Negaprion brevirostris.Crossref | GoogleScholarGoogle Scholar |
Oliveira, P. G. V., de Oliveira, D. S., Pinheiro, P. B., Hazin, F. H., Carvalho, F. C., Veras, D. P., and Silva, M. B. (2011). Population structure and growth of young lemon shark, Negaprion brevirostris (Poey, 1868), at the Atol das Rocas Biological Reserve, Brazil. Journal of Integrated Coastal Zone Management 11, 389–395.
| Population structure and growth of young lemon shark, Negaprion brevirostris (Poey, 1868), at the Atol das Rocas Biological Reserve, Brazil.Crossref | GoogleScholarGoogle Scholar |
R Development Core Team (2016). A language and environment for statistical computing, ver. 3.5.0. (R Foundation for Statistical Computing.) Available at http://www.R-project.org [verified 2 September 2019].
Reyier, E., Adams, D., and Lowers, R. (2008). First evidence of a high density nursery ground for the lemon shark, Negaprion brevirostris, near Cape Canaveral, Florida. Florida Scientist 71, 134–148.
Ricker, W. E. (1979). Growth rates and models. Fish Physiology 8, 677–743.
| Growth rates and models.Crossref | GoogleScholarGoogle Scholar |
Sundström, L. F. (2015). Negaprion brevirostris: the IUCN red list of threatened species 2015, e.T39380A81769233
Tavares, R. (2005). Abundance and distribution of sharks in Los Roques Archipelago National Park and other Venezuelan oceanic islands, 1997–1998. Ciencias Marinas 31, 441–454.
| Abundance and distribution of sharks in Los Roques Archipelago National Park and other Venezuelan oceanic islands, 1997–1998.Crossref | GoogleScholarGoogle Scholar |
Tavares, R. (2008). Occurrence, diet and growth of juvenile blacktip sharks, Carcharhinus limbatus, from Los Roques Archipelago National Park, Venezuela. Caribbean Journal of Science 44, 291–302.
| Occurrence, diet and growth of juvenile blacktip sharks, Carcharhinus limbatus, from Los Roques Archipelago National Park, Venezuela.Crossref | GoogleScholarGoogle Scholar |
Tavares, R. (2009). Fishery biology of the Caribbean reef sharks, Carcharhinus perezi (Poey, 1876), in a Caribbean insular platform: Los Roques Archipelago National Park, Venezuela. Pan-American Journal of Aquatic Sciences 4, 500–512.
Tavares, R., Rodriguez, J. P., and Morales, M. (2016). Nursery area and size structure of the lemon shark population, Negaprion brevirostris (Poey, 1868), in Los Roques Archipelago National Park, Venezuela. Universitas Scientiarum 21, 33–52.
| Nursery area and size structure of the lemon shark population, Negaprion brevirostris (Poey, 1868), in Los Roques Archipelago National Park, Venezuela.Crossref | GoogleScholarGoogle Scholar |
Wetherbee, B. M., Gruber, S. H., and Rosa, R. (2007). Movement patterns of juvenile lemon sharks Negaprion brevirostris within Atol das Rocas, Brazil: a nursery characterized by tidal extremes. Marine Ecology Progress Series 343, 283–293.
| Movement patterns of juvenile lemon sharks Negaprion brevirostris within Atol das Rocas, Brazil: a nursery characterized by tidal extremes.Crossref | GoogleScholarGoogle Scholar |
White, E. R., Nagy, J. D., and Gruber, S. H. (2014). Modeling the population dynamics of lemon sharks. Biology Direct 9, 23.
| Modeling the population dynamics of lemon sharks.Crossref | GoogleScholarGoogle Scholar | 25403640PubMed |
Zar, J. (1996). ‘Biostatistical Analysis.’ (Prentice Hall: Upper Saddle River, NJ, USA.)
