Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Intraspecific variability in reproductive patterns in the temperate hermaphrodite fish, Labrus bergylta

David Villegas-Ríos A B , Alexandre Alonso-Fernández A , Rosario Domínguez-Petit A and Fran Saborido-Rey A
+ Author Affiliations
- Author Affiliations

A Instituto de Investigaciones Marinas (IIM-CSIC), 36208, Vigo, Spain.

B Corresponding author. Email: villegas@iim.csic.es

Marine and Freshwater Research 64(12) 1156-1168 https://doi.org/10.1071/MF12362
Submitted: 27 December 2012  Accepted: 14 May 2013   Published: 14 October 2013

Abstract

For many fish populations reproductive patterns remain unknown, which often results in inadequate management strategies. Timing and intraspecific variability in the main reproductive traits of ballan wrasse (Labrus bergylta) were investigated based on microscopic analysis of gonads sampled from NW Spain in 2009–2012. This species displays two main body colour patterns, plain and spotted, which coexist in sympatry. Females spawned from January to April whereas spawning capable males were present almost year-round. Length at 50% maturity did not differ between colour patterns and was above the minimum catch size. Plain individuals attained the length and age at 50% sex change earlier than spotted individuals, which might be explained by differences in growth patterns, mortality rates or by an evolutionary genetic divergence between populations. Individuals with gonads infected by encysted trematode metacercariae were associated with an earlier timing of sex change, which represents one of the few examples of a possible parasitic influence on the sex allocation of its host. Our findings provide a framework for scientific-based management of this hermaphrodite fish.

Additional keywords: colour pattern, Galicia, hermaphroditism, Labrus bergylta, parasite infection, reproductive cycle, sex change, sexual maturity.


References

Afonso, P., Fontes, J., Holland, K., and Santos, R. (2009). Multi-scale patterns of habitat use in a highly mobile reef fish, the white trevally Pseudocaranx dentex, and their implications for marine reserve design. Marine Ecology Progress Series 381, 273–286.
Multi-scale patterns of habitat use in a highly mobile reef fish, the white trevally Pseudocaranx dentex, and their implications for marine reserve design.Crossref | GoogleScholarGoogle Scholar |

Ah-King, M., and Nylin, S. (2010). Sex in an evolutionary perspective: just another reaction norm. Evolutionary Biology 37, 234–246.
Sex in an evolutionary perspective: just another reaction norm.Crossref | GoogleScholarGoogle Scholar | 21170116PubMed |

Alonso-Fernández, A., Alós, J., Grau, A., Domínguez-Petit, R., and Saborido-Rey, F. (2011). The use of histological techniques to study the reproductive biology of the hermaphroditic mediterranean fishes Coris julis, Serranus scriba, and Diplodus annularis. Marine and Coastal Fisheries 3, 145–159.
The use of histological techniques to study the reproductive biology of the hermaphroditic mediterranean fishes Coris julis, Serranus scriba, and Diplodus annularis.Crossref | GoogleScholarGoogle Scholar |

Alonso-Fernández, A., Villegas-Ríos, D., Valdes-López, M., Oliveira-Domínguez, B., and Saborido-Rey, F. (in press). Histological assessment of the reproductive biology of Pollachius pollachius on the Galician shelf (NW Spain). Journal of the Marine Biological Association of the United Kingdom , .
Histological assessment of the reproductive biology of Pollachius pollachius on the Galician shelf (NW Spain).Crossref | GoogleScholarGoogle Scholar |

Alonzo, S. H., and Mangel, M. (2004). The effects of size-selective fisheries on the stock dynamics of and sperm limitation in sex-changing fish. Fishery Bulletin 102, 1–13.

Alonzo, S. H., and Mangel, M. (2005). Sex-change rules, stock dynamics, and the performance of spawning-per-recruit measures in protogynous stocks. Fishery Bulletin 103, 229–245.

Alonzo, S. H., Ish, T., Key, M., MacCall, A. D., and Mangel, M. (2008). The Importance of Incorporating Protogynous Sex Change Into Stock Assessments. Bulletin of Marine Science 83, 163–179.

Armsworth, P. R. (2001). Effects of fishing on a protogynous hermaphrodite. Canadian Journal of Fisheries and Aquatic Sciences 58, 568–578.
Effects of fishing on a protogynous hermaphrodite.Crossref | GoogleScholarGoogle Scholar |

Artüz, M. L. (2005). Age and growth of the ballan wrasse in the Sea of Marmara Labrus bergylta Ascanius 1767. Hidrobiologica 3, 17–21.

Bañon, R., Villegas-Ríos, D., Serrano, A., Mucientes, G., and Arronte, J. (2010). Marine fishes from Galicia (NW Spain): an updated checklist. Zootaxa 2667, 1–27.

Bentivegna, F., and Benedetto, F. (1993). Histological study on the gonochorism of Symphodus cinereus (Labridae). Cybium 17, 17–22.

Brown-Peterson, N. J., Wyanski, D. M., Saborido-Rey, F., Macewicz, B. J., and Lowerre-Barbieri, S. K. (2011). A standardized terminology for describing reproductive development in fishes. Marine and Coastal Fisheries 3, 52–70.
A standardized terminology for describing reproductive development in fishes.Crossref | GoogleScholarGoogle Scholar |

Charnov, E. L. (1982). ‘The Theory of Sex Allocation.’ (Princeton University Press: Princeton, NJ.)

Choat, J. H., Klanten, O. S., Van Herwerden, L., Robertson, D. R., and Clements, K. D. (2012). Patterns and processes in the evolutionary history of parrotfishes (family Labridae). Biological Journal of the Linnean Society. Linnean Society of London 107, 529–557.
Patterns and processes in the evolutionary history of parrotfishes (family Labridae).Crossref | GoogleScholarGoogle Scholar |

Collins, A. B., and McBride, R. S. (2011). Demographics by depth: spatially explicit life-history dynamics of a protogynous reef fish. Fishery Bulletin 109, 232–242.

Costello, M. J. (1991). Review of the biology of wrasse (Labridae:Pisces) in Northern Europe. Progress in Underwater Science 16, 29–51.

Coulson, P. G., Hesp, S. A., Hall, N. G., and Potter, I. C. (2009). The western blue groper (Achoerodus gouldii), a protogynous hermaphroditic labrid with exceptional longevity, late maturity, slow growth, and both late maturation and sex change. Fishery Bulletin 107, 57–75.

Cushing, D. H. (1969). The regularity of the spawning season of some fishes. ICES Journal of Marine Science 33, 81–92.
The regularity of the spawning season of some fishes.Crossref | GoogleScholarGoogle Scholar |

Dipper, F. A., and Pullin, R. S. V. (1979). Gonochorism and sex-inversion in British Labridae (Pisces). Journal of Zoology 187, 97–112.
Gonochorism and sex-inversion in British Labridae (Pisces).Crossref | GoogleScholarGoogle Scholar |

Dipper, F. A., Bridges, C. R., and Menz, A. (1977). Age, growth and feeding in the ballan wrasse Labrus bergylta Ascanius 1767. Journal of Fish Biology 11, 105–120.
Age, growth and feeding in the ballan wrasse Labrus bergylta Ascanius 1767.Crossref | GoogleScholarGoogle Scholar |

Fortier, L., Ponton, D., and Gilbert, M. (1995). The match/mismatch hypothesis and the feeding success of fish larvae in ice-covered southeastern Hudson Bay. Marine Ecology Progress Series 120, 11–27.
The match/mismatch hypothesis and the feeding success of fish larvae in ice-covered southeastern Hudson Bay.Crossref | GoogleScholarGoogle Scholar |

Fredensborg, B. L., and Poulin, R. (2006). Parasitism Shaping Host Life-History Evolution: Adaptive Responses in a Marine Gastropod to Infection by Trematodes. Journal of Animal Ecology 75, 44–53.
Parasitism Shaping Host Life-History Evolution: Adaptive Responses in a Marine Gastropod to Infection by Trematodes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28vnvVyrsg%3D%3D&md5=e467c8a76499ccb77b21a8ca43c02c41CAS | 16903042PubMed |

Froese, R., and Pauly, D. (2012). ‘FishBase.’ Version 08/12. Available at www.fishbase.org

Ghiselin, M. T. (1969). The evolution of hermaphroditism among animals. The Quarterly Review of Biology 44, 189–208.
The evolution of hermaphroditism among animals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE3c%2Fkt1Cjtg%3D%3D&md5=20fbcaa40d5d5b9e08621eccb2f714ecCAS | 4901396PubMed |

Grier, H. J., and Uribe-Aranzábal, M. C. (2009). The testis and spermatogenesis in teleosts. In ‘Reproductive Biology and Phylogeny of Fishes (Agnathans and Bony Fishes)’. Vol. 8A. (Ed. B. G. M. Jameson.) pp. 119–142. (Science Publishers: Enfield, NH.)

Gust, N. (2004). Variation in the population biology of protogynous coral reef fishes over tens of kilometres. Canadian Journal of Fisheries and Aquatic Sciences 61, 205–218.
Variation in the population biology of protogynous coral reef fishes over tens of kilometres.Crossref | GoogleScholarGoogle Scholar |

Hamilton, S. L., Caselle, J. E., Standish, J. D., Schroeder, D. M., Milton, S. L., Rosales-Casian, J. A., and Sosa-Nishizaki, O. (2007). Size-selective harvesting alters life histories of a temperate sex-changing fish. Ecological Applications 17, 2268–2280.
Size-selective harvesting alters life histories of a temperate sex-changing fish.Crossref | GoogleScholarGoogle Scholar | 18213967PubMed |

Hamilton, R., Adams, S., and Choat, J. (2008). Sexual development and reproductive demography of the green humphead parrotfish (Bolbometopon muricatum) in the Solomon Islands. Coral Reefs 27, 153–163.
Sexual development and reproductive demography of the green humphead parrotfish (Bolbometopon muricatum) in the Solomon Islands.Crossref | GoogleScholarGoogle Scholar |

Hamilton, S. L., Wilson, J. R., Ben-Horin, T., and Caselle, J. E. (2011). Utilizing spatial demographic and life history variation to optimize sustainable yield of a temperate sex-changing fish. PLoS ONE 6, e24580.
Utilizing spatial demographic and life history variation to optimize sustainable yield of a temperate sex-changing fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1entL3M&md5=f2e814921c10993c5aab7798cd43808aCAS | 21915353PubMed |

Hammerschlag-Peyer, C., and Layman, C. (2010). Intrapopulation variation in habitat use by two abundant coastal fish species. Marine Ecology Progress Series 415, 211–220.
Intrapopulation variation in habitat use by two abundant coastal fish species.Crossref | GoogleScholarGoogle Scholar |

Heins, D. C., and Baker, J. A. (2008). The stickleback Schistocephalus hostparasite system as a model for understanding the effect of a macroparasite on host reproduction. Behaviour 145, 625–645.
The stickleback Schistocephalus hostparasite system as a model for understanding the effect of a macroparasite on host reproduction.Crossref | GoogleScholarGoogle Scholar |

Heppell, S. S., Heppell, S. A., Coleman, F. C., and Koenig, C. C. (2006). Models to compare management options for a protogynous fish. Ecological Applications 16, 238–249.
Models to compare management options for a protogynous fish.Crossref | GoogleScholarGoogle Scholar | 16705976PubMed |

Kjesbu, O. S. (1994). Time of start of spawning in Atlantic cod (Gadus morhua) females in relation to vitellogenic oocyte diameter, temperature, fish length and condition. Journal of Fish Biology 45, 719–735.
Time of start of spawning in Atlantic cod (Gadus morhua) females in relation to vitellogenic oocyte diameter, temperature, fish length and condition.Crossref | GoogleScholarGoogle Scholar |

Kjesbu, O. S., Righton, D., Krüger-Johnsen, M., Thorsen, A., Michalsen, K., Fonn, M., and Witthames, P. R. (2010). Thermal dynamics of ovarian maturation in Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 67, 605–625.
Thermal dynamics of ovarian maturation in Atlantic cod (Gadus morhua).Crossref | GoogleScholarGoogle Scholar |

Kozlowski, J. (1992). Optimal allocation of resources to growth and reproduction: implications for age and size at maturity. Trends in Ecology & Evolution 7, 15–19.
Optimal allocation of resources to growth and reproduction: implications for age and size at maturity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itVKltQ%3D%3D&md5=80b2563607b9b3aeec1fcda12c83e690CAS |

Love, R. M. (1980). ‘The Chemical Biology of Fishes.’ Vol. 2. (Academic Press: London.)

Lowerre-Barbieri, S. K., Henderson, N., Llopiz, J., Walters, S., Bickford, J., and Muller, R. (2009). Defining a spawning population (spotted seatrout Cynoscion nebulosus) over temporal, spatial, and demographic scales. Marine Ecology Progress Series 394, 231–245.
Defining a spawning population (spotted seatrout Cynoscion nebulosus) over temporal, spatial, and demographic scales.Crossref | GoogleScholarGoogle Scholar |

Lowerre-Barbieri, S. K., Brown-Peterson, N. J., Murua, H., Tomkiewicz, J., Wyanski, D. M., and Saborido-Rey, F. (2011a). Emerging issues and methodological advances in fisheries reproductive biology. Marine and Coastal Fisheries 3, 32–51.
Emerging issues and methodological advances in fisheries reproductive biology.Crossref | GoogleScholarGoogle Scholar |

Lowerre-Barbieri, S. K., Ganias, K., Saborido-Rey, F., Murua, H., and Hunter, J. R. (2011b). Reproductive timing in marine fishes: variability, temporal scales, and methods. Marine and Coastal Fisheries 3, 71–91.
Reproductive timing in marine fishes: variability, temporal scales, and methods.Crossref | GoogleScholarGoogle Scholar |

Macnab, V., Scott, A., Katsiadaki, I., and Barber, I. (2011). Variation in the reproductive potential of Schistocephalus infected male sticklebacks is associated with 11-ketotestosterone titre. Hormones and Behavior 60, 371–379.
Variation in the reproductive potential of Schistocephalus infected male sticklebacks is associated with 11-ketotestosterone titre.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFarurnN&md5=35d22040548216c55e8356e08e15c5f7CAS | 21781969PubMed |

McBride, R. S., and Johnson, M. R. (2007). Sexual development and reproductive seasonality of hogfish (Labridae: Lachnolaimus maximus), an hermaphroditic reef fish. Journal of Fish Biology 71, 1270–1292.
Sexual development and reproductive seasonality of hogfish (Labridae: Lachnolaimus maximus), an hermaphroditic reef fish.Crossref | GoogleScholarGoogle Scholar |

McCormick, M. I., Ryen, C. A., Munday, P. L., and Walker, S. P. W. (2010). Differing mechanisms underlie sexual size-dimorphism in two populations of a sex-changing fish. PLoS ONE 5, e10616.
Differing mechanisms underlie sexual size-dimorphism in two populations of a sex-changing fish.Crossref | GoogleScholarGoogle Scholar | 20485547PubMed |

Morgan, M. J., Wright, P. J., and Rideout, R. M. (2013). Effect of age and temperature on spawning time in two gadoid species. Fisheries Research 138, 42–51.
Effect of age and temperature on spawning time in two gadoid species.Crossref | GoogleScholarGoogle Scholar |

Muncaster, S., Andersson, E., Kjesbu, O. S., Taranger, G. L., Skiftesvik, A. B., and Norberg, B. (2010). The reproductive cycle of female Ballan wrasse Labrus bergylta in high latitude, temperate waters. Journal of Fish Biology 77, 494–511.
| 1:STN:280:DC%2BC3cjktFOgtg%3D%3D&md5=a48ffd4bf0d7622dec3800765408533aCAS | 20701636PubMed |

Munday, P. L., Buston, P. M., and Warner, R. R. (2006). Diversity and flexibility of sex-change strategies in animals. Trends in Ecology & Evolution 21, 89–95.
Diversity and flexibility of sex-change strategies in animals.Crossref | GoogleScholarGoogle Scholar |

Muñoz, R. C., and Warner, R. R. (2003). A new version of the size-advantage hypothesis for sex change: Incorporating sperm competition and size-fecundity skew. American Naturalist 161, 749–761.
A new version of the size-advantage hypothesis for sex change: Incorporating sperm competition and size-fecundity skew.Crossref | GoogleScholarGoogle Scholar | 12858282PubMed |

Muñoz, R. C., and Warner, R. R. (2004). Testing a new version of the size-advantage hypothesis for sex change: Sperm competition and size-skew effects in the bucktooth parrotfish, Sparisoma radians. Behavioral Ecology 15, 129–136.
Testing a new version of the size-advantage hypothesis for sex change: Sperm competition and size-skew effects in the bucktooth parrotfish, Sparisoma radians.Crossref | GoogleScholarGoogle Scholar |

Murua, H., and Saborido-Rey, F. (2003). Female reproductive strategies of marine fish species of the North Atlantic. Journal of Northwest Atlantic Fishery Science 33, 23–31.

Nogueira, E., Pérez, F. F., and Ríos, A. F. (1997). Seasonal patterns and long-term trends in an estuarine upwelling ecosystem (Ria de Vigo, NW Spain). Estuarine, Coastal and Shelf Science 44, 285–300.
Seasonal patterns and long-term trends in an estuarine upwelling ecosystem (Ria de Vigo, NW Spain).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXivVyqs78%3D&md5=54956f265b7cac5d51c2f40b4676fb3aCAS |

Parpena, I. (1996). Parasites, infections and diseases of fishes in Africa: An update. FAO. CIFA Technical Paper 31, 130–199.

Pavlov, D. A., Emel’yanova, N. G. E., and Novikov, G. (2009) Reproductive dynamics. In ‘Fish Reproductive Biology: Implications for Assessment and Management’. (Eds. T. Jakobsen, M. J. Fogarty, B. A. Megrey and E. Moksness.) (Wiley-Blackwell: Chichester, UK.)

Porteiro, F., Barreiros, J. P., and Santos, R. S. (1996). Wrasses (Teleostei: Labridae) of the Azores. Archipelago: Life and Marine Sciences 14A, 23–40.

Puebla, O., Bermingham, E., Guichard, F., and Whiteman, E. (2007). Colour pattern as a single trait driving speciation in Hypoplectrus coral reef fishes? Proceedings of the Royal Society of London. Series B, Biological Sciences 274, 1265–1271.
Colour pattern as a single trait driving speciation in Hypoplectrus coral reef fishes?Crossref | GoogleScholarGoogle Scholar |

R Development Core Team (2011). R: a language and environment for statistical computing. R Foundation for Statistical Computing: Vienna, Austria. Available at http://www.R-project.org

Reñones, O., Grau, A., Mas, X., Riera, F., and Saborido-Rey, F. (2010). Reproductive pattern of an exploited dusky grouper Epinephelus marginatus (Lowe 1834) (Pisces: Serranidae) population in the western Mediterranean. Scientia Marina 74, 523–537.
Reproductive pattern of an exploited dusky grouper Epinephelus marginatus (Lowe 1834) (Pisces: Serranidae) population in the western Mediterranean.Crossref | GoogleScholarGoogle Scholar |

Reznick, D. A., Bryga, H., and Endler, J. A. (1990). Experimentally induced life-history evolution in a natural population. Nature 346, 357–359.
Experimentally induced life-history evolution in a natural population.Crossref | GoogleScholarGoogle Scholar |

Rideout, R. M., and Tomkiewicz, J. (2011). Skipped spawning in fishes: More common than you might think. Marine and Coastal Fisheries 3, 176–189.
Skipped spawning in fishes: More common than you might think.Crossref | GoogleScholarGoogle Scholar |

Saborido-Rey, F., and Junquera, S. (1998). Histological assessment of variations in sexual maturity of cod (Gadus morhua L.) at the Flemish Cap (north-west Atlantic). ICES Journal of Marine Science 55, 515–521.
Histological assessment of variations in sexual maturity of cod (Gadus morhua L.) at the Flemish Cap (north-west Atlantic).Crossref | GoogleScholarGoogle Scholar |

Sadovy, Y., and Domeier, M. L. (2005). Perplexing problems of sexual patterns in the fish genus Paralabrax (Serranidae, Serraninae). Journal of Zoology 267, 121–133.
Perplexing problems of sexual patterns in the fish genus Paralabrax (Serranidae, Serraninae).Crossref | GoogleScholarGoogle Scholar |

Sadovy, Y., and Liu, M. (2008). Functional hermaphroditism in teleosts. Fish and Fisheries 9, 1–43.
Functional hermaphroditism in teleosts.Crossref | GoogleScholarGoogle Scholar |

Sadovy, Y., and Shapiro, D. Y. (1987). Criteria for the diagnosis of hermaphroditism in fishes. Copeia 1987, 136–156.
Criteria for the diagnosis of hermaphroditism in fishes.Crossref | GoogleScholarGoogle Scholar |

Sattar, S. A., Jørgensen, C., and Fiksen, O. (2008). Fisheries-induced evolution of energy and sex allocation. Bulletin of Marine Science 83, 235–250.

Schärer, L., and Vizoso, D. B. (2003). Earlier sex change in infected individuals of the protogynous reef fish Thalassoma bifasciatum. Behavioral Ecology and Sociobiology 55, 137–143.
Earlier sex change in infected individuals of the protogynous reef fish Thalassoma bifasciatum.Crossref | GoogleScholarGoogle Scholar |

Shapiro, D. (1987). Differentiation and evolution of sex change in fishes. Bioscience 37, 490–497.
Differentiation and evolution of sex change in fishes.Crossref | GoogleScholarGoogle Scholar |

Sjolander, S., Larson, H., and Engstrom, J. (1972). On the reproductive behaviour of two labrid fishes, the ballan wrasse (Labrus bergylta) and Jago’s goldsinny (Ctenolabrus rupestris). Revue de Comportement Animal 6, 43–51.

Smith, J. M., Pierce, G. J., Zuur, A. F., and Boyle, P. R. (2005). Seasonal patterns of investment in reproductive and somatic tissues in the squid Loligo forbesi. Aquatic Living Resources 18, 341–351.
Seasonal patterns of investment in reproductive and somatic tissues in the squid Loligo forbesi.Crossref | GoogleScholarGoogle Scholar |

Stearns, S. C. (1992). ‘The Evolution of Life Histories.’ (Oxford University Press: New York.)

Talbot, C., Medeiros, M. V., and Davie, A. (2012). In vivo gender determination in captive ballan wrasse (Labrus bergylta Ascanius 1767). Final Report to the Scottish Salmon Producers Organisation 54.

Treasurer, J. W. (1994). The distribution, age and growth of wrasse (Labridae) in inshore waters of west Scotland. Journal of Fish Biology 44, 905–918.
The distribution, age and growth of wrasse (Labridae) in inshore waters of west Scotland.Crossref | GoogleScholarGoogle Scholar |

Trip, E. D. L., Clements, K. D., Raubenheimer, D., and Choat, J. H. (2011). Reproductive biology of an odacine labrid, Odax pullus. Journal of Fish Biology 78, 741–761.
Reproductive biology of an odacine labrid, Odax pullus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M3jtlCqtA%3D%3D&md5=ec339ecd62ac3ea9d3167e657e6c85f9CAS |

Trippel, E. A. (1995). Age at maturity as a stress indicator in fisheries. Bioscience 45, 759–771.
Age at maturity as a stress indicator in fisheries.Crossref | GoogleScholarGoogle Scholar |

Villegas-Ríos, D., Alós, J., March, D., Palmer, M., Mucientes, G., and Saborido-Rey, F. (2013). Home range and diel behaviour of the ballan wrasse, Labrus bergylta, determined by acoustic telemetry. Journal of Sea Research 80, 61–71.
Home range and diel behaviour of the ballan wrasse, Labrus bergylta, determined by acoustic telemetry.Crossref | GoogleScholarGoogle Scholar |

Villegas-Ríos, D., Alonso-Fernández, A., Fabeiro, M., Bañón, R., and Saborido-Rey, F. (2013). Demographic variation between colour patterns in a temperate protogynous hermaphrodite, the Ballan wrasse Labrus bergylta. PLOS ONE 8, .
Demographic variation between colour patterns in a temperate protogynous hermaphrodite, the Ballan wrasse Labrus bergylta.Crossref | GoogleScholarGoogle Scholar | 24058404PubMed |

Warner, R. R. (1988). Sex change and the size-advantage model. Trends in Ecology & Evolution 3, 133–136.
Sex change and the size-advantage model.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7gvFaksw%3D%3D&md5=35e7544ba24a4df1f26de13110e8f08cCAS |

Westneat, M. W., and Alfaro, M. E. (2005). Phylogenetic relationships and evolutionary history of the reef fish family Labridae. Molecular Phylogenetics and Evolution 36, 370–390.
Phylogenetic relationships and evolutionary history of the reef fish family Labridae.Crossref | GoogleScholarGoogle Scholar | 15955516PubMed |

Whitman, D.W., and Agrawal, A.A. (2009). What is phenotypic plasticity and why is it important? In ‘Phenotypic Plasticity of Insects’. (Eds D. W. Whitman and T. N. Ananthakrishnan.) pp. 1–63. (Science Publishers: Enfield, NH.)

Wood, S. N. (2000). Modelling and smoothing parameter estimation with multiple quadratic penalties. Journal of the Royal Statistical Society. Series B, Statistical Methodology 62, 413–428.
Modelling and smoothing parameter estimation with multiple quadratic penalties.Crossref | GoogleScholarGoogle Scholar |

Wood, S. N. (2011). Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society. Series B, Statistical Methodology 73, 3–36.
Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models.Crossref | GoogleScholarGoogle Scholar |

Wright, P. J., and Trippel, E. A. (2009). Fishery-induced demographic changes in the timing of spawning: consequences for reproductive success. Fish and Fisheries 10, 283–304.
Fishery-induced demographic changes in the timing of spawning: consequences for reproductive success.Crossref | GoogleScholarGoogle Scholar |

Zuur, A. F., Ieno, E. N., and Smith, G. M. (2007). ‘Analysing Ecological Data.’ (Springer: New York.)