Abstract
Many species of sedentary marine invertebrates exhibit large spatial variation in their morphology, which allow them to occupy a broad geographic distribution and range of environmental conditions. However, the detection of differences in morphology amongst variable environments cannot determine whether these differences represent a plastic response to the local environment, or whether morphology is genetically fixed. We used a reciprocal transplant experiment to test whether ‘stunted’ blacklip abalone (Haliotis rubra) are the result of a plastic response to the environment or fixed genetic trait. Furthermore, we related environmental factors, that affect food availability (density of abalone, water movement, algal cover and reef topography), to differences in growth and morphology. Morphological plasticity was confirmed as the mechanism causing morphological variation in H. rubra. Individuals transplanted to sites with ‘non-stunted’ H. rubra grew significantly faster when compared to stunted controls, whilst individuals transplanted to stunted sites grew significantly slower compared to non-stunted controls. The growth response was greater for individuals transplanted from ‘non-stunted’ to ‘stunted’ sites, suggesting that the environmental stressors in morphologically ‘stunted’ habitat are stronger compared to locations of faster growing morphology. We propose that these differences are related to resource availability whereby low algal cover and topographic simplicity results in stunted populations, whereas high algal abundance and topographic complexity results in non-stunted populations.
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References
Bell EC, Denny MW (1994) Quantifying wave exposure—a simple device for recording maximum velocity and results of its use at several field sites. J Exp Mar Biol Ecol 181:9–29. doi:https://doi.org/10.1016/0022-0981(94)90101-5
Breen PA, Adkins BE (1982) Observations of abalone populations on the north coast of British Columbia, July 1980. Department of Fisheries and Oceans Resource Services Branch, 1633, Nanaimo, British Columbia
Brown LD (1991) Genetic-variation and population-structure in the blacklip abalone, Haliotis rubra. Aust J Mar Freshw Res 42:77–90. doi:https://doi.org/10.1071/MF9910077
Conod N, Bartlett JP, Evans BS, Elliott NG (2002) Comparison of mitochondrial and nuclear DNA analyses of population structure in the blacklip abalone Haliotis rubra leach. Mar Freshw Res 53:711–718. doi:https://doi.org/10.1071/MF01197
Day RW, Fleming AE (1992) The determinants and measurement of abalone growth. In: Shepherd SA, Tegner MJ, Guzman Del Proo SA (eds) Abalone of the world: biology, fisheries and culture. Fishing News Books, Oxford, pp 141–168
Day RW, Quinn GP (1989) Comparisons of treatments after an analysis of variance in ecology. Ecol Monogr 59:433–463. doi:https://doi.org/10.2307/1943075
Dixon CD, Day RW (2004) Growth responses in emergent greenlip abalone to density reductions and translocations. J Shellfish Res 23:1223–1228
Donovan DA, Taylor HH (2008) Metabolic consequences of living in a wave-swept environment: effects of simulated wave forces on oxygen consumption, heart rate, and activity of the shell adductor muscle of the abalone Haliotis iris. J Exp Mar Biol Ecol 354:231–240. doi:https://doi.org/10.1016/j.jembe.2007.11.011
Ebert TA (1996) Adaptive aspects of phenotypic plasticity in echinoderms. Oceanol Acta 19:347–355
Emmett B, Jamieson GS (1989) An experimental transplant of northern abalone, Haliotis kamtschatkana, in Barkley Sound, British Columbia. Fish Bull (Wash DC) 87:95–104
Etter RJ (1996) The effect of wave action, prey type, and foraging time on growth of the predatory snail Nucella lapillus (L). J Exp Mar Biol Ecol 196:341–356. doi:https://doi.org/10.1016/0022-0981(95)00139-5
Fowler-Walker MJ, Wernberg T, Connell SD (2006) Differences in kelp morphology between wave sheltered and exposed localities: morphologically plastic or fixed traits? Mar Biol (Berl) 148:755–767. doi:https://doi.org/10.1007/s00227-005-0125-z
Guest MA, Nichols PD, Frusher SD, Hirst AJ (2007) Evidence of abalone (Haliotis rubra) diet from combined fatty acid and stable isotope analyses. Mar Biol (Berl) 153:579–588. doi:https://doi.org/10.1007/s00227-007-0831-9
Huang BX, Peakall R, Hanna PJ (2000) Analysis of genetic structure of blacklip abalone (Haliotis rubra) populations using RAPD, minisatellite and microsatellite markers. Mar Biol (Berl) 136:207–216. doi:https://doi.org/10.1007/s002270050678
Johannesson K, Kautsky N, Tedengren M (1990) Genotypic and phenotypic differences between Baltic and North-sea populations of Mytilus edulis evaluated through reciprocal transplantations 2. Genetic-variation. Mar Ecol Prog Ser 59:211–219. doi:https://doi.org/10.3354/meps059211
Johnson MS, Black R (1998) Effects of habitat on growth and shape of contrasting phenotypes of Bembicium vittatum philippi in the Houtman Abrolhos islands, Western Australia. Hydrobiologia 378:95–103. doi:https://doi.org/10.1023/A:1003241722328
Johnson MS, Black R (2000) Associations with habitat versus geographic cohesiveness: size and shape of Bembicium vittatum philippi (Gastropoda: Littorinidae) in the Houtman Abrolhos islands. Biol J Linn Soc Lond 71:563–580. doi:https://doi.org/10.1111/j.1095-8312.2000.tb01275.x
Jokiel PL, Morrissey JI (1993) Water motion on coral reefs—evaluation of the clod card technique. Mar Ecol Prog Ser 93:175–181. doi:https://doi.org/10.3354/meps093175
Lively CM (1986) Predator-induced shell dimorphism in the acorn barnacle Chthamalus anisopoma. Evol Int J Org Evol 40:232–242. doi:https://doi.org/10.2307/2408804
Luttikhuizen PC, Drent J, van Delden W, Piersma T (2003) Spatially structured genetic variation in a broadcast spawning bivalve: quantitative vs. molecular traits. J Evol Biol 16:260–272. doi:https://doi.org/10.1046/j.1420-9101.2003.00510.x
McShane PE, Naylor JR (1995a) Density-independent growth of Haliotis iris Martyn (mollusca, gastropoda). J Exp Mar Biol Ecol 190:51–60. doi:https://doi.org/10.1016/0022-0981(95)00031-L
McShane PE, Naylor JR (1995b) Small-scale spatial variation in growth, size at maturity, and yield- and egg-per-recruit relations in the New Zealand abalone Haliotis iris. N Z J Mar Freshw Res 29:603–612
McShane PE, Black KP, Smith MG (1988a) Recruitment processes in Haliotis rubra (mollusca, gastropoda) and regional hydrodynamics in South-eastern Australia imply localized dispersal of larvae. J Exp Mar Biol Ecol 124:175–203. doi:https://doi.org/10.1016/0022-0981(88)90171-2
McShane PE, Smith MG, Beinssen KHH (1988b) Growth and morphometry in abalone (Haliotis rubra leach) from Victoria. Aust J Mar Freshw Res 39:161–166. doi:https://doi.org/10.1071/MF9880161
Miller JA, Shanks AL (2004) Evidence for limited larval dispersal in black rockfish (Sebastes melanops): implications for population structure and marine-reserve design. Can J Fish Aquat Sci 61:1723–1735. doi:https://doi.org/10.1139/f04-111
Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692. doi:https://doi.org/10.1016/j.tree.2005.08.002
Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158. doi:https://doi.org/10.1890/1051-0761(2003)013[0146:PGDCAT]2.0.CO;2
Prince JD (1991) A new technique for tagging abalone. Aust J Mar Freshw Res 42:101–106. doi:https://doi.org/10.1071/MF9910101
Prince JD (2005) Combating the tyranny of scale for haliotids: micro-management for microstocks. Bull Mar Sci 76:557–577
Prince JD, Sellers TL, Ford WB, Talbot SR (1988) Confirmation of a relationship between the localized abundance of breeding stock and recruitment for Haliotis rubra leach (mollusca, gastropoda). J Exp Mar Biol Ecol 122:91–104. doi:https://doi.org/10.1016/0022-0981(88)90178-5
Prince JD, Peeters H, Gorfine H, Day RW (2008) The novel use of harvest policies and rapid assessment to manage spatially complex abalone resources (genus Haliotis). Fish Res 94(3):330–338. doi:https://doi.org/10.1016/j.fishres.2008.07.016
Raimondi PT, Forde SE, Delph LF, Lively CM (2000) Processes structuring communities: evidence for trait-mediated indirect effects through induced polymorphisms. Oikos 91:353–361. doi:https://doi.org/10.1034/j.1600-0706.2000.910215.x
Robles C, Robb J (1993) Varied carnivore effects and the prevalence of intertidal algal turfs. J Exp Mar Biol Ecol 166:65–91. doi:https://doi.org/10.1016/0022-0981(93)90079-4
Saunders T, Mayfield S (2008) Predicting biological variation using a simple morphometric marker in the sedentary marine invertebrate Predicting biological variation using a simple morphometric marker in the sedentary marine invertebrate Haliotis rubra. Mar Ecol Prog Ser 366:75–89. doi:https://doi.org/10.3354/meps07563
Saunders T, Mayfield S, Hogg A (2008) A simple, cost-effective, morphometric marker for characterising abalone populations at multiple spatial scales. Mar Freshw Res 59:32–40. doi:https://doi.org/10.1071/MF07150
Saunders T, Mayfield S, Hogg A (2009) Using a simple morphometric marker to identify fine-scale management units for abalone fisheries. ICES J Mar Sci (Advanced Access published on January 12, 2009, doi:https://doi.org/10.1093/icesjms/fsn210)
Schiel DR (1993) Experimental evaluation of commercial scale enhancement of abalone Haliotis iris populations in New Zealand. Mar Ecol Prog Ser 97:167–181. doi:https://doi.org/10.3354/meps097167
Shepherd SA (1973) Studies on Southern Australian abalone (genus Haliotis) I. Ecology of five sympatric species. Aust J Mar Freshw Res 24:217–257. doi:https://doi.org/10.1071/MF9730217
Shepherd SA, Hearn WS (1983) Studies on Southern Australian abalone (genus Haliotis) IV. Growth of Haliotis laevigata and Haliotis rubra. Aust J Mar Freshw Res 34:461–475. doi:https://doi.org/10.1071/MF9830461
Shepherd SA, Clarke SM, Dalgetty A (1992) Studies on Southern Australian abalone (genus Haliotis) XIV. Growth of H. laevigata on Eyre Peninsula. J Malacolog Soc Aust 13:99–113
Steffani CN, Branch GM (2003) Growth rate, condition, and shell shape of Mytilus galloprovincialis: responses to wave exposure. Mar Ecol Prog Ser 246:197–209. doi:https://doi.org/10.3354/meps246197
Swain DP, Hutchings JA, Foote CJ (2005) Environmental and genetic influences on stock identification characters. In: Cadrin SX, Friedland KD, Waldmann JR (eds) Stock identification methods applications in fishery science. Elsevier Academic Press, London, pp 45–85
Tegner MJ (1992) Brood-stock transplants as an approach to abalone stock enhancement. In: Shepherd SA, Tegner MJ, Guzmán del Próo SA (eds) Abalone of the world: biology, fisheries and culture. Blackwell, Oxford, pp 461–473
Temby N, Miller K, Mundy C (2007) Evidence of genetic subdivision among populations of blacklip abalone (Haliotis rubra leach) in Tasmania. Mar Freshw Res 58:733–742. doi:https://doi.org/10.1071/MF07015
Trussell GC (1996) Phenotypic plasticity in an intertidal snail: the role of a common crab predator. Evolut Int J Org Evolut 50:448–454. doi:https://doi.org/10.2307/2410815
Wells FE, Mulvay P (1995) Good and bad fishing areas for Haliotis laevigata: a comparison of population parameters. Mar Freshw Res 46:591–598. doi:https://doi.org/10.1071/MF9950591
Worthington DG, Andrew NL, Hamer G (1995) Covariation between growth and morphology suggests alternative size limits for the blacklip abalone, Haliotis rubra, in New South Wales, Australia. Fish Bull (Wash DC) 93:551–561
Acknowledgments
We would like to thank Associate Professor Andy Davis, Dr. Tim Ward, Erin Sautter and Ian Carlson for commenting on previous drafts of this article. We would also like to thank Andrew Hogg for extensive assistance with field and laboratory work and Neal Chambers, Dan Gorman, Kylie Howard, Alan Jones and David Sturges for assistance with diving. SARDI aquatic sciences provided funds for this research.
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Communicated by M. Byrne.
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Saunders, T.M., Connell, S.D. & Mayfield, S. Differences in abalone growth and morphology between locations with high and low food availability: morphologically fixed or plastic traits?. Mar Biol 156, 1255–1263 (2009). https://doi.org/10.1007/s00227-009-1167-4
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DOI: https://doi.org/10.1007/s00227-009-1167-4