Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Macroalgal resource use differences across age and size classes in the dominant temperate herbivorous fish Aplodactylus lophodon (Aplodactylidae)

B. A. Yiu A B E , D. J. Booth A , A. M. Fowler A C and D. A. Feary D
+ Author Affiliations
- Author Affiliations

A School of Life Sciences, Building 4, Level 6, University of Technology Sydney, NSW 2007, Australia.

B GreenCollar, 37 George Street, The Rocks, NSW 2000, Australia.

C New South Wales Department of Primary Industries, Sydney Institute of Marine Science, Mosman, NSW 2088, Australia.

D MRAG Ltd, 18 Queen Street, London, W1J 5PN, UK.

E Corresponding author. Email: bevan.yiu@gmail.com

Marine and Freshwater Research 70(4) 531-540 https://doi.org/10.1071/MF18086
Submitted: 6 March 2018  Accepted: 31 August 2018   Published: 12 November 2018

Abstract

Herbivorous fishes comprise a substantial proportion of temperate fish communities, although there is little understanding of their trophic resource use and whether this changes throughout post-settlement ontogeny. With increasing loss of macroalgal forests, understanding how temperate fishes use macroalgae will be vital in predicting future effects on temperate fish biodiversity. The Australian rock cale (Aplodactylus lophodon) is one of the most abundant herbivorous fish inhabiting shallow temperate south-eastern Australian reefs. We examined gastrointestinal contents throughout ontogeny and demonstrated that this species maintains a herbivorous diet through all life stages. Differences in algal taxa consumed were apparent through ontogeny, with the juvenile diet dominated by filamentous red and green algae and the adult diet dominated by brown and calcareous red algae. Relative gut length increased through ontogeny, potentially facilitating dietary transition to less digestible algae, but no concurrent increase in jaw power was observed. The results highlight the diversity of trophic resource use in a temperate marine herbivore, but the near-complete dominance of dietary algae throughout ontogeny indicates the reliance on primary producers across all life stages. Given the importance of fucoid resources in the adult diet, any loss of macroalgal forests within south-eastern Australia may affect foraging success and persistence.

Additional keywords: herbivory, morphology, ontogeny, trophic.


References

Andrew, N. L., and Jones, G. P. (1990). Patch formation by herbivorous fish in a temperate Australian kelp forest. Oecologia 85, 57–68.
Patch formation by herbivorous fish in a temperate Australian kelp forest.Crossref | GoogleScholarGoogle Scholar |

Behrens, M. D., and Lafferty, K. D. (2007). Temperature and diet effects on omnivorous fish performance: implications for the latitudinal diversity gradient in herbivorous fishes. Canadian Journal of Fisheries and Aquatic Sciences 64, 867–873.
Temperature and diet effects on omnivorous fish performance: implications for the latitudinal diversity gradient in herbivorous fishes.Crossref | GoogleScholarGoogle Scholar |

Benavides, A. G., Cancino, J. M., and Ojeda, F. P. (1994). Ontogenetic changes in gut dimensions and macroalgal digestibility in the marine herbivorous fish, Aplodactylus punctatus. Functional Ecology 8, 46–51.
Ontogenetic changes in gut dimensions and macroalgal digestibility in the marine herbivorous fish, Aplodactylus punctatus.Crossref | GoogleScholarGoogle Scholar |

Buckle, E. C., and Booth, D. (2009). Ontogeny of space and diet of two temperate damselfish species, Parma microlepis and Parma unifasciata. Marine Biology 156, 1497–1505.
Ontogeny of space and diet of two temperate damselfish species, Parma microlepis and Parma unifasciata.Crossref | GoogleScholarGoogle Scholar |

Campbell, S. (2001). Ammonium requirements of fast-growing ephemeral macroalgae in a nutrient-enriched marine embayment (Port Phillip Bay, Australia). Marine Ecology Progress Series 209, 99–107.
Ammonium requirements of fast-growing ephemeral macroalgae in a nutrient-enriched marine embayment (Port Phillip Bay, Australia).Crossref | GoogleScholarGoogle Scholar |

Choat, J. H., and Clements, K. D. (1992). Diet in Odacid and Aplodactylid fishes from Australia and New Zealand. Australian Journal of Marine and Freshwater Research 43, 1451–1459.
Diet in Odacid and Aplodactylid fishes from Australia and New Zealand.Crossref | GoogleScholarGoogle Scholar |

Clarke, K., and Warwick, R. (2001). ‘Changes in Marine Communities: An Approach to Statistical Analysis and Interpretation.’ (PRIMER-E: Plymouth, UK.)

Clements, K. D., and Choat, J. H. (1993). Influence of season, ontogeny and tide on the diet of the temperate marine herbivorous fish Odax pullus (Odacidae). Marine Biology 117, 213–220.
Influence of season, ontogeny and tide on the diet of the temperate marine herbivorous fish Odax pullus (Odacidae).Crossref | GoogleScholarGoogle Scholar |

Clements, K. D., and Zemke-White, W. L. (2008). Diet of subtropical herbivorous fishes in northeastern New Zealand. New Zealand Journal of Marine and Freshwater Research 42, 47–55.
Diet of subtropical herbivorous fishes in northeastern New Zealand.Crossref | GoogleScholarGoogle Scholar |

Clements, K., Gleeson, P. V., and Slaytor, M. B. (1994). Short-chain fatty acid metabolism in temperate herbivorous fish. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 164, 372–377.
Short-chain fatty acid metabolism in temperate herbivorous fish.Crossref | GoogleScholarGoogle Scholar |

Clements, K. D., Raubenheimer, D., and Choat, J. H. (2009). Nutritional ecology of marine herbivorous fishes: ten years on. Functional Ecology 23, 79–92.
Nutritional ecology of marine herbivorous fishes: ten years on.Crossref | GoogleScholarGoogle Scholar |

Coleman, M. A., Kelaher, B. P., Steinberg, P. D., and Millar, A. J. (2008). Absence of a large brown macroalga on urbanised rocky reefs around Sydney, Australia and evidence of historical decline. Journal of Phycology 44, 897–901.
Absence of a large brown macroalga on urbanised rocky reefs around Sydney, Australia and evidence of historical decline.Crossref | GoogleScholarGoogle Scholar |

Day, R. D., German, D. P., and Tibbetts, I. R. (2011). Why can’t young fish eat plants? Neither digestive enzymes nor gut development preclude herbivory in the young of a stomachless marine herbivorous fish. Comparative Biochemistry and Physiology – B. Biochemical and Molecular Biology 158, 23–29.
Why can’t young fish eat plants? Neither digestive enzymes nor gut development preclude herbivory in the young of a stomachless marine herbivorous fish.Crossref | GoogleScholarGoogle Scholar |

Elliott, J. P., and Bellwood, D. R. (2003). Alimentary tract morphology and diet in three coral reef fish families. Journal of Fish Biology 63, 1598–1609.
Alimentary tract morphology and diet in three coral reef fish families.Crossref | GoogleScholarGoogle Scholar |

Erickson, A. A., Paul, V. J., Van Alstyne, K. L., and Kwiatkowski, L. M. (2006). Palatability of macroalgae that use different types of chemical defenses. Journal of Chemical Ecology 32, 1883–1895.
Palatability of macroalgae that use different types of chemical defenses.Crossref | GoogleScholarGoogle Scholar |

Filbee-Dexter, K., and Scheibling, R. E. (2014). Sea urchin barrens as alternative stable states of collapsed kelp ecosystems. Marine Ecology Progress Series 495, 1–25.
Sea urchin barrens as alternative stable states of collapsed kelp ecosystems.Crossref | GoogleScholarGoogle Scholar |

Filbee-Dexter, K., and Wernberg, T. (2018). Rise of Turfs: a new battlefront for globally declining kelp forests. Bioscience 68, 64–76.
Rise of Turfs: a new battlefront for globally declining kelp forests.Crossref | GoogleScholarGoogle Scholar |

Floeter, S. R., Behrens, M. D., Ferreira, C. E. L., Paddack, M. J., and Horn, M. H. (2005). Geographical gradients of marine herbivorous fishes: patterns and processes. Marine Biology 147, 1435–1447.
Geographical gradients of marine herbivorous fishes: patterns and processes.Crossref | GoogleScholarGoogle Scholar |

German, D. P., and Horn, M. H. (2006). Gut length and mass in herbivorous and carnivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects. Marine Biology 148, 1123–1134.
Gut length and mass in herbivorous and carnivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects.Crossref | GoogleScholarGoogle Scholar |

Gray, C. A., Ives, M. C., Macbeth, W. G., and Kendall, B. W. (2010). Variation in growth, mortality, length and age compositions of harvested populations of the herbivorous fish Girella tricuspidata. Journal of Fish Biology 76, 880–899.
Variation in growth, mortality, length and age compositions of harvested populations of the herbivorous fish Girella tricuspidata.Crossref | GoogleScholarGoogle Scholar |

Horn, M. H. (1989). Biology of marine herbivorous fishes. Oceanography and Marine Biology – an Annual Review 27, 167–272.

Kramer, D. L., and Bryant, M. J. (1995). Intestine length in the fishes of a tropical stream: 2. Relationships to diet – the long and short of a convoluted issue. Environmental Biology of Fishes 42, 129–141.
Intestine length in the fishes of a tropical stream: 2. Relationships to diet – the long and short of a convoluted issue.Crossref | GoogleScholarGoogle Scholar |

Krumhansl, K. A., Okamoto, D. K., Rassweiler, A., Novak, M., Bolton, J. J., Cavanaugh, K. C., Connell, S. D., Johnson, C. R., Konar, B., Ling, S. D., Micheli, F., Norderhaug, K. M., Pérez-Matus, A., Sousa-Pinto, I., Reed, D. C., Salomon, A. K., Shears, N. T., Wernberg, T., Anderson, R. J., Barrett, N. S., Buschmann, A. H., Carr, M. H., Caselle, J. E., Derrien-Courtel, S., Edgar, G. J., Edwards, M., Estes, J. A., Goodwin, C., Kenner, M. C., Kushner, D. J., Moy, F. E., Nunn, J., Steneck, R. S., Vásquez, J., Watson, J., Witman, J. D., and Byrnes, J. E. K. (2016). Global patterns of kelp forest change over the past half-century. Proceedings of the National Academy of Sciences of the United States of America 113, 13785–13790.
Global patterns of kelp forest change over the past half-century.Crossref | GoogleScholarGoogle Scholar |

Lees, K., Pitois, S., Scott, C., and Frid, C. (2006). Characterizing regime shifts in the marine environment. Fish and Fisheries 7, 104–127.
Characterizing regime shifts in the marine environment.Crossref | GoogleScholarGoogle Scholar |

Lewis, S. M. (1985). Herbivory on coral reefs: algal susceptibility to herbivorous fishes. Oecologia 65, 370–375.
Herbivory on coral reefs: algal susceptibility to herbivorous fishes.Crossref | GoogleScholarGoogle Scholar |

Lilley, S. A., and Schiel, D. R. (2006). Community effects following the deletion of a habitat-forming alga from rocky marine shores. Oecologia 148, 672–681.
Community effects following the deletion of a habitat-forming alga from rocky marine shores.Crossref | GoogleScholarGoogle Scholar |

Ling, S. D. (2008). Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state. Oecologia 156, 883–894.
Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state.Crossref | GoogleScholarGoogle Scholar |

May, V., and Larkum, A. W. D. (1981). A subtidal transect in Jervis Bay, New South Wales. Australian Journal of Ecology 6, 439–457.
A subtidal transect in Jervis Bay, New South Wales.Crossref | GoogleScholarGoogle Scholar |

Montgomery, W. L., and Gerking, S. D. (1980). Marine macroalgae as foods for fishes: an evaluation of potential food quality. Environmental Biology of Fishes 5, 143–153.
Marine macroalgae as foods for fishes: an evaluation of potential food quality.Crossref | GoogleScholarGoogle Scholar |

Moran, D., and Clements, K. D. (2002). Diet and endogenous carbohydrases in the temperate marine herbivorous fish Kyphosus sydneyanus. Journal of Fish Biology 60, 1190–1203.
Diet and endogenous carbohydrases in the temperate marine herbivorous fish Kyphosus sydneyanus.Crossref | GoogleScholarGoogle Scholar |

Neira, J., Miskiewicz, G., and Trnski, T. (1998). ‘Larvae of Temperate Australian Fishes: Laboratory Guide for Larval Fish Identification.’ (University of Western Australia Press: Perth, WA, Australia.)

Pérez-Matus, A., Carrasco, S. A., Gelcich, S., Fernandez, M., and Wieters, E. A. (2017). Exploring the effects of fishing pressure and upwelling intensity over subtidal kelp forest communities in central Chile. Ecosphere 8, e01808.
Exploring the effects of fishing pressure and upwelling intensity over subtidal kelp forest communities in central Chile.Crossref | GoogleScholarGoogle Scholar |

Pillans, R. D., Franklin, C. E., and Tibbetts, I. R. (2004). Food choice in Siganus fuscescens: influence of macrophyte nutrient content and availability. Journal of Fish Biology 64, 297–309.
Food choice in Siganus fuscescens: influence of macrophyte nutrient content and availability.Crossref | GoogleScholarGoogle Scholar |

Rimmer, D. W. (1986). Changes in diet and the development of microbial digestion in juvenile buffalo bream, Kyphosus cornelii. Marine Biology 92, 443–448.
Changes in diet and the development of microbial digestion in juvenile buffalo bream, Kyphosus cornelii.Crossref | GoogleScholarGoogle Scholar |

Schiel, D. R., and Lilley, S. A. (2007). Gradients of disturbance to an algal canopy and the modification of an intertidal community. Marine Ecology Progress Series 339, 1–11.
Gradients of disturbance to an algal canopy and the modification of an intertidal community.Crossref | GoogleScholarGoogle Scholar |

Schiel, D. R., and Lilley, S. A. (2011). Impacts and negative feedbacks in community recovery over eight years following removal of habitat-forming macroalgae. Journal of Experimental Marine Biology and Ecology 407, 108–115.
Impacts and negative feedbacks in community recovery over eight years following removal of habitat-forming macroalgae.Crossref | GoogleScholarGoogle Scholar |

Seeto, G. S., Veivers, P. C., Clements, K. D., and Slaytor, M. (1996). Carbohydrate utilisation by microbial symbionts in the marine herbivorous fishes Odax cyanomelas and Crinodus lophodon. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 165, 571–579.
Carbohydrate utilisation by microbial symbionts in the marine herbivorous fishes Odax cyanomelas and Crinodus lophodon.Crossref | GoogleScholarGoogle Scholar |

Shears, N. T., and Babcock, R. C. (2003). Continuing trophic cascade effects after 25 years of no-take marine reserve protection. Marine Ecology Progress Series 246, 1–16.
Continuing trophic cascade effects after 25 years of no-take marine reserve protection.Crossref | GoogleScholarGoogle Scholar |

Skea, G. L., Mountfort, D. O., and Clements, K. D. (2005). Gut carbohydrases from the New Zealand marine herbivorous fishes Kyphosus sydneyanus (Kyphosidae), Aplodactylus arctidens (Aplodactylidae) and Odax pullus (Labridae). Comparative Biochemistry and Physiology – B. Biochemistry & Molecular Biology 140, 259–269.
Gut carbohydrases from the New Zealand marine herbivorous fishes Kyphosus sydneyanus (Kyphosidae), Aplodactylus arctidens (Aplodactylidae) and Odax pullus (Labridae).Crossref | GoogleScholarGoogle Scholar |

Smit, A. J., Brearley, A., Hyndes, G. A., Lavery, P. S., and Walker, D. I. (2006). δ15N and δ13C analysis of a Posidonia sinuosa seagrass bed. Aquatic Botany 84, 277–282.
δ15N and δ13C analysis of a Posidonia sinuosa seagrass bed.Crossref | GoogleScholarGoogle Scholar |

Steinberg, P. D., Edyvane, K., Denys, R., Birdsey, R., and Vanaltena, I. A. (1991). Lack of avoidance of phenolic-rich brown-algae by tropical herbivorous fishes. Marine Biology 109, 335–343.
Lack of avoidance of phenolic-rich brown-algae by tropical herbivorous fishes.Crossref | GoogleScholarGoogle Scholar |

Steneck, R. S., Graham, M. H., Bourque, B. J., Corbett, D., Erlandson, J. M., Estes, J. A., and Tegner, M. J. (2002). Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental Conservation 29, 436–459.
Kelp forest ecosystems: biodiversity, stability, resilience and future.Crossref | GoogleScholarGoogle Scholar |

Tait, L. W., and Schiel, D. R. (2011). Legacy effects of canopy disturbance on ecosystem functioning in macroalgal assemblages. PLoS One 6, e26986.
Legacy effects of canopy disturbance on ecosystem functioning in macroalgal assemblages.Crossref | GoogleScholarGoogle Scholar |

Taylor, D. A., and Schiel, D. R. (2010). Algal populations controlled by fish herbivory across a wave dominated exposure gradient on southern temperate shores. Ecology 91, 201–211.
Algal populations controlled by fish herbivory across a wave dominated exposure gradient on southern temperate shores.Crossref | GoogleScholarGoogle Scholar |

Trip, E. D. L., Raubenheimer, D., Clements, K. D., and Choat, J. H. (2011). Reproductive demography of a temperate protogynous and herbivorous fish, Odax pullus (Labridae, Odacini). Marine and Freshwater Research 62, 176–186.

Underwood, A. J., Kingsford, M. J., and Andrew, N. L. (1991). Patterns in shallow subtidal marine assemblages along the coast of New South Wales. Australian Journal of Ecology 16, 231–249.
Patterns in shallow subtidal marine assemblages along the coast of New South Wales.Crossref | GoogleScholarGoogle Scholar |

Vergés, A., Steinberg, P. D., Hay, M. E., Poore, A. G. B., Campbell, A. H., Ballesteros, E., Heck, K. L., Booth, D. J., Coleman, M. A., Feary, D. A., Figueira, W., Langlois, T., Marzinelli, E. M., Mizerek, T., Mumby, P. J., Nakamura, Y., Roughan, M., van Sebille, E., Gupta, A. S., Smale, D. A., Tomas, F., Wernberg, T., and Wilson, S. K. (2014). The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proceedings of the Royal Society of London – B. Biological Sciences 281, 20140846.
The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts.Crossref | GoogleScholarGoogle Scholar |

Vergés, A., Doropoulos, C., Malcolm, H. A., Skye, M., Garcia-Pizá, M., Marzinelli, E. M., Campbell, A. H., Ballesteros, E., Hoey, A. S., Vila-Concejo, A., Bozec, Y.-M., and Steinberg, P. D. (2016). Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp. Proceedings of the National Academy of Sciences of the United States of America 113, 13791–13796.
Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp.Crossref | GoogleScholarGoogle Scholar |

Wainwright, P., and Bellwood, D. (2002). Ecomorphology of feeding in coral reef fishes. In ‘Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem’. (Ed. P. Sale.) pp. 33–56. (Academic Press: Cambridge, MA, USA.)

Wernberg, T., Bennett, S., Babcock, R. C., de Bettignies, T., Cure, K., Depczynski, M., Dufois, F., Fromont, J., Fulton, C. J., Hovey, R. K., Harvey, E. S., Holmes, T. H., Kendrick, G. A., Radford, B., Santana-Garcon, J., Saunders, B. J., Smale, D. A., Thomsen, M. S., Tuckett, C. A., Tuya, F., Vanderklift, M. A., and Wilson, S. (2016). Climate-driven regime shift of a temperate marine ecosystem. Science 353, 169–172.
Climate-driven regime shift of a temperate marine ecosystem.Crossref | GoogleScholarGoogle Scholar |

Westneat, M. W. (2003). A biomechanical model for analysis of muscle force, power output and lower jaw motion in fishes. Journal of Theoretical Biology 223, 269–281.
A biomechanical model for analysis of muscle force, power output and lower jaw motion in fishes.Crossref | GoogleScholarGoogle Scholar |

Westneat, M. W. (2004). Evolution of levers and linkages in the feeding mechanisms of fishes. Integrative and Comparative Biology 44, 378–389.
Evolution of levers and linkages in the feeding mechanisms of fishes.Crossref | GoogleScholarGoogle Scholar |

Yiu, B. (2012). Spatial patterns in the diet and growth of the herbivorous fish, Aplodactylus lophodon, across the NSW coastline. B.Sc.(Hons) Thesis, University of Technology Sydney, Sydney, NSW, Australia.