A test of metabolic and consumptive responses to local and global perturbations: enhanced resources stimulate herbivores to counter expansion of weedy species
Chloe McSkimming A , Bayden D. Russell A C , Jason E. Tanner A B and Sean D. Connell A D
+ Author Affiliations
- Author Affiliations
A Southern Seas Ecology Laboratories, School of Biological Sciences and The Environmental Institute, University of Adelaide, SA 5005, Australia.
B SARDI Aquatic Sciences, PO Box 120, Henley Beach, SA 5022, Australia.
C Present address: Swire Institute of Marine Science and School of Biological Sciences, The University of Hong Kong, Hong Kong Special Administrative Region, P. R. China.
D Corresponding author. Email: sean.connell@adelaide.edu.au
Marine and Freshwater Research 67(1) 96-102 https://doi.org/10.1071/MF14266
Submitted: 3 September 2014 Accepted: 19 December 2014 Published: 22 June 2015
Abstract
The capacity of natural systems to resist environmental change underpins ecosystem stability, e.g. the persistence of kelp-dominated states which are sometimes displaced by subordinates or weedy species (i.e. algal turfs). Perturbation by resource enhancement at global (e.g. CO2 emissions) through local scales (e.g. nutrient pollution) increases the probability of turf domination, yet these same resources stimulate an increase in per capita consumption of turfs by herbivores. We test whether such resource perturbation can stimulate herbivores to absorb the additional productivity of turfs that cause kelp displacement. We tested the hypotheses that (1) elevated nitrogen (N) and carbon dioxide (CO2) not only stimulate an increase in consumptive rates, but also stimulate an increase in underlying metabolic rates of gastropod herbivores, so that (2) enhanced primary productivity is countered by herbivory. We reveal that elevated nitrogen and CO2 stimulated an elevation in rates of consumption in proportion to an increase in metabolic rate of grazers. Subsequently, grazers consumed proportionately greater cover of turfs to counter turf expansion. Resource enrichment, therefore, can stimulate metabolic and consumptive activity of herbivores to absorb the additional productivity of opportunistic species. Hence, the competitive potential of subordinates to displace community dominants may be checked by the very resources that otherwise drive instability.
Additional keywords: algal turfs, carbon dioxide, consumption, herbivory, nitrogen, nutrient, ocean acidification.
References
Beardall, J., and Raven, J. A. (2004). The potential effects of global climate change on microalgal photosynthesis, growth and ecology. Phycologia 43, 26–40.| The potential effects of global climate change on microalgal photosynthesis, growth and ecology.Crossref | GoogleScholarGoogle Scholar |
Bozinovic, F., and Novoa, F. F. (1997). Metabolic costs of rodents feeding on plant chemical defenses: a comparison between an herbivore and an omnivore. Comparative Biochemistry and Physiology. Part A, Physiology 117, 511–514.
| Metabolic costs of rodents feeding on plant chemical defenses: a comparison between an herbivore and an omnivore.Crossref | GoogleScholarGoogle Scholar |
Collins, M., Knutti, R., Arblaster, J., Dufresne, J., Fichefet, T., Friedlingstein, P., Gao, X., Gutowski, W., Johns, T., and Krinner, G. (2013). Long-term climate change: projections, commitments and irreversibility. In ‘Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change’. (Eds T. F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex and P. M. Midgley.) pp. 1029–1136. (Cambridge University Press: Cambridge, UK, and New York.)
Connell, S. D., and Irving, A. D. (2008). Integrating ecology with biogeography using landscape characteristics: a case study of subtidal habitat across continental Australia. Journal of Biogeography 35, 1608–1621.
| Integrating ecology with biogeography using landscape characteristics: a case study of subtidal habitat across continental Australia.Crossref | GoogleScholarGoogle Scholar |
Connell, S. D., and Russell, B. D. (2010). The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proceedings of the Royal Society of London – B. Biological Sciences 277, 1409–1415.
| The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests.Crossref | GoogleScholarGoogle Scholar |
Connell, S. D., Russell, B. D., Turner, D. J., Shepherd, A. J. S., Kildea, T. N., Miller, D., Airoldi, L., and Cheshire, A. (2008). Recovering a lost baseline: missing kelp forests from a metropolitan coast. Marine Ecology Progress Series 360, 63–72.
| Recovering a lost baseline: missing kelp forests from a metropolitan coast.Crossref | GoogleScholarGoogle Scholar |
Connell, S. D., Kroeker, K. J., Fabricius, K. E., Kline, D. I., and Russell, B. D. (2013). The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 368, 20120442.
| The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance.Crossref | GoogleScholarGoogle Scholar |
Connell, S. D., Foster, M. S., and Airoldi, L. (2014). What are algal turfs? Towards a better description of turfs. Marine Ecology Progress Series 495, 299–307.
| What are algal turfs? Towards a better description of turfs.Crossref | GoogleScholarGoogle Scholar |
Cruz‐Neto, A. P., and Bozinovic, F. (2004). The relationship between diet quality and basal metabolic rate in endotherms: insights from intraspecific analysis. Physiological and Biochemical Zoology 77, 877–889.
| The relationship between diet quality and basal metabolic rate in endotherms: insights from intraspecific analysis.Crossref | GoogleScholarGoogle Scholar | 15674763PubMed |
Cruz-Rivera, E., and Hay, M. E. (2000). Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 81, 201–219.
| Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers.Crossref | GoogleScholarGoogle Scholar |
Cummings, V., Hewitt, J., Van Rooyen, A., Currie, K., Beard, S., Thrush, S., Norkko, J., Barr, N., Heath, P., and Halliday, N. J. (2011). Ocean acidification at high latitudes: potential effects on functioning of the Antarctic bivalve Laternula elliptica. PLoS One 6, e16069.
| Ocean acidification at high latitudes: potential effects on functioning of the Antarctic bivalve Laternula elliptica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXosVOnuw%3D%3D&md5=00c0fe733e40800d71c074569bf5069cCAS | 21245932PubMed |
Diaz‐Pulido, G., Gouezo, M., Tilbrook, B., Dove, S., and Anthony, K. (2011). High CO2 enhances the competitive strength of seaweeds over corals. Ecology Letters 14, 156–162.
| High CO2 enhances the competitive strength of seaweeds over corals.Crossref | GoogleScholarGoogle Scholar | 21155961PubMed |
Dickson, A., and Millero, F. (1987). A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Research. Part A, Oceanographic Research Papers 34, 1733–1743.
| A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXotFGjsg%3D%3D&md5=b1cc49b40ecb701b98c1e0cda8cf8f69CAS |
Drummond, S., and Connell, S. D. (2005). Quantifying percentage cover of subtidal organisms on rocky coasts: a comparison of the costs and benefits of standard methods. Marine and Freshwater Research 56, 865–876.
| Quantifying percentage cover of subtidal organisms on rocky coasts: a comparison of the costs and benefits of standard methods.Crossref | GoogleScholarGoogle Scholar |
Falkenberg, L. J., Connell, S. D., and Russell, B. D. (2013a). Disrupting the effects of synergies between stressors: improved water quality dampens the effects of future CO2 on a marine habitat. Journal of Applied Ecology 50, 51–58.
| Disrupting the effects of synergies between stressors: improved water quality dampens the effects of future CO2 on a marine habitat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmslWju7s%3D&md5=78ce3227390f5d05129f329c9b23287eCAS |
Falkenberg, L. J., Russell, B. D., and Connell, S. D. (2013b). Contrasting resource limitations of marine primary producers: implications for competitive interactions under enriched CO2 and nutrient regimes. Oecologia 172, 575–583.
| Contrasting resource limitations of marine primary producers: implications for competitive interactions under enriched CO2 and nutrient regimes.Crossref | GoogleScholarGoogle Scholar | 23111809PubMed |
Falkenberg, L. J., Russell, B. D., and Connell, S. D. (2013c). Future herbivory: the indirect effects of enriched CO2 may rival its direct effects. Marine Ecology Progress Series 492, 85–95.
| Future herbivory: the indirect effects of enriched CO2 may rival its direct effects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFymtrzN&md5=0278b494b0b65fd099ceaa885fbbf0faCAS |
Falkenberg, L. J., Connell, S. D., and Russell, B. D. (2014). Herbivory mediates the expansion of an algal habitat under nutrient and CO2 enrichment. Marine Ecology Progress Series 497, 87–92.
| Herbivory mediates the expansion of an algal habitat under nutrient and CO2 enrichment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXnslCrtrw%3D&md5=3c2f88516fde938d23ef6f128f68cc45CAS |
Feely, R. A., Sabine, C. L., Lee, K., Berelson, W., Kleypas, J., Fabry, V. J., and Millero, F. J. (2004). Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305, 362–366.
| Impact of anthropogenic CO2 on the CaCO3 system in the oceans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXls1egsbY%3D&md5=c23d37a3efa3094bd080f05e6df316e6CAS | 15256664PubMed |
Ghedini, G., Russell, B. D., and Connell, S. D. (2015). Trophic compensation reinforces resistance: herbivory absorbs the increasing effects of compounded disturbances. Ecology Letters 18, 182–187.
| Trophic compensation reinforces resistance: herbivory absorbs the increasing effects of compounded disturbances.Crossref | GoogleScholarGoogle Scholar | 25581377PubMed |
Gorman, D., Russell, B. D., and Connell, S. D. (2009). Land-to-sea connectivity: linking human-derived terrestrial subsidies to subtidal habitat change on open rocky coasts. Ecological Applications 19, 1114–1126.
| Land-to-sea connectivity: linking human-derived terrestrial subsidies to subtidal habitat change on open rocky coasts.Crossref | GoogleScholarGoogle Scholar | 19688920PubMed |
Hein, M., Pedersen, M. F., and Sand-Jensen, K. (1995). Size-dependent nitrogen uptake in micro- and macroalgae. Marine Ecology Progress Series 118, 247–253.
| Size-dependent nitrogen uptake in micro- and macroalgae.Crossref | GoogleScholarGoogle Scholar |
Hurd, C. L., Hepburn, C. D., Currie, K. I., Raven, J. A., and Hunter, K. A. (2009). Testing the effects of ocean acidification on algal metabolism: considerations for experimental designs. Journal of Phycology 45, 1236–1251.
| Testing the effects of ocean acidification on algal metabolism: considerations for experimental designs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVSisb8%3D&md5=9e1a888329ffcbfa9e6a7ab4531701c9CAS |
Innes, A., and Houlihan, D. (1985). Aquatic and aerial oxygen consumption of cool temperate gastropods: a comparison with some mediterranean species. Comparative Biochemistry and Physiology. Part A, Physiology 82, 105–109.
| Aquatic and aerial oxygen consumption of cool temperate gastropods: a comparison with some mediterranean species.Crossref | GoogleScholarGoogle Scholar |
Koch, M., Bowes, G., Ross, C., and Zhang, X. H. (2013). Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology 19, 103–132.
| Climate change and ocean acidification effects on seagrasses and marine macroalgae.Crossref | GoogleScholarGoogle Scholar | 23504724PubMed |
Leclercq, N. C., Gattuso, J. P., and Jaubert, J. (2000). CO2 partial pressure controls the calcification rate of a coral community. Global Change Biology 6, 329–334.
| CO2 partial pressure controls the calcification rate of a coral community.Crossref | GoogleScholarGoogle Scholar |
Li, W., and Gao, K. (2012). A marine secondary producer respires and feeds more in a high CO2 ocean. Marine Pollution Bulletin 64, 699–703.
| A marine secondary producer respires and feeds more in a high CO2 ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvFWqsbw%3D&md5=6a3fd33f6bdb2175a3c686e7c8e57c5fCAS | 22364924PubMed |
Lilly, G. (1979). The influence of diet on the oxygen uptake of the sea urchins, Tripneustes ventricosus and Strongylocentrotus droebachiensis. Comparative Biochemistry and Physiology. Part A, Physiology 62, 463–469.
| The influence of diet on the oxygen uptake of the sea urchins, Tripneustes ventricosus and Strongylocentrotus droebachiensis.Crossref | GoogleScholarGoogle Scholar |
Lotze, H. K., Worm, B., and Sommer, U. (2001). Strong bottom-up and top-down control of early life stages of macroalgae. Limnology and Oceanography 46, 749–757.
| Strong bottom-up and top-down control of early life stages of macroalgae.Crossref | GoogleScholarGoogle Scholar |
McNab, B. K. (1986). The influence of food habits on the energetics of eutherian mammals. Ecological Monographs 56, 1–19.
| The influence of food habits on the energetics of eutherian mammals.Crossref | GoogleScholarGoogle Scholar |
Mehrbach, C., Culberson, C., Hawley, J., and Pytkowich, R. (1973). Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography 18, 897–907.
| Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXhtFansLk%3D&md5=a888b7315ad1246a7b53f2cf466d7b4cCAS |
Miller, M., Hay, M., Miller, S., Malone, D., Sotka, E., and Szmant, A. (1999). Effects of nutrients versus herbivores on reef algae: a new method for manipulating nutrients on coral reefs. Limnology and Oceanography 44, 1847–1861.
| Effects of nutrients versus herbivores on reef algae: a new method for manipulating nutrients on coral reefs.Crossref | GoogleScholarGoogle Scholar |
Neckles, H. A., Wetzel, R. L., and Orth, R. J. (1993). Relative effects of nutrient enrichment and grazing on epiphyte–macrophyte (Zostera marina L.) dynamics. Oecologia 93, 285–295.
| Relative effects of nutrient enrichment and grazing on epiphyte–macrophyte (Zostera marina L.) dynamics.Crossref | GoogleScholarGoogle Scholar |
O’Connor, M. I. (2009). Warming strengthens an herbivore–plant interaction. Ecology 90, 388–398.
| Warming strengthens an herbivore–plant interaction.Crossref | GoogleScholarGoogle Scholar | 19323223PubMed |
Raven, J. A., and Hurd, C. L. (2012). Ecophysiology of photosynthesis in macroalgae. Photosynthesis Research 113, 105–125.
| Ecophysiology of photosynthesis in macroalgae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1KmurzJ&md5=adeca623805bd1b79764a599ca2a16ebCAS | 22843100PubMed |
Rosen, D. A., and Trites, A. W. (1999). Metabolic effects of low‐energy diet on Steller sea lions, Eumetopias jubatus. Physiological and Biochemical Zoology 72, 723–731.
| Metabolic effects of low‐energy diet on Steller sea lions, Eumetopias jubatus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2Fnt1yrsg%3D%3D&md5=cb256f4f47849134d5393535ddff3726CAS | 10603336PubMed |
Russell, B. D., and Connell, S. D. (2005). A novel interaction between nutrients and grazers alters relative dominance of marine habitats. Marine Ecology Progress Series 289, 5–11.
| A novel interaction between nutrients and grazers alters relative dominance of marine habitats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlslCltbc%3D&md5=69730dcc35cec35ae28a34a16ac256a8CAS |
Russell, B. D., and Connell, S. D. (2007). Response of grazers to sudden nutrient pulses in oligotrophic versus eutrophic conditions. Marine Ecology Progress Series 349, 73–80.
| Response of grazers to sudden nutrient pulses in oligotrophic versus eutrophic conditions.Crossref | GoogleScholarGoogle Scholar |
Russell, B. D., Thompson, J. A. I., Falkenberg, L. J., and Connell, S. D. (2009). Synergistic effects of climate change and local stressors: CO2 and nutrient‐driven change in subtidal rocky habitats. Global Change Biology 15, 2153–2162.
| Synergistic effects of climate change and local stressors: CO2 and nutrient‐driven change in subtidal rocky habitats.Crossref | GoogleScholarGoogle Scholar |
Russell, B. D., Connell, S. D., Findlay, H. S., Tait, K., Widdicombe, S., and Mieszkowska, N. (2013). Ocean acidification and rising temperatures may increase biofilm primary productivity but decrease grazer consumption. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 368, 20120438.
| Ocean acidification and rising temperatures may increase biofilm primary productivity but decrease grazer consumption.Crossref | GoogleScholarGoogle Scholar |
Secor, S. M. (2009). Specific dynamic action: a review of the postprandial metabolic response. Journal of Comparative Physiology – B. Biochemical, Systemic, and Environmental Physiology 179, 1–56.
| Specific dynamic action: a review of the postprandial metabolic response.Crossref | GoogleScholarGoogle Scholar |
Siikavuopio, S. I., Mortensen, A., Dale, T., and Foss, A. (2007). Effects of carbon dioxide exposure on feed intake and gonad growth in green sea urchin, Strongylocentrotus droebachiensis. Aquaculture 266, 97–101.
| Effects of carbon dioxide exposure on feed intake and gonad growth in green sea urchin, Strongylocentrotus droebachiensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksleqtb4%3D&md5=2c25bbcbe8469a638c4ed908d5ac43d1CAS |
Sokolova, I. M., and Pörtner, H. O. (2003). Metabolic plasticity and critical temperatures for aerobic scope in a eurythermal marine invertebrate (Littorina saxatilis, Gastropoda: Littorinidae) from different latitudes. The Journal of Experimental Biology 206, 195–207.
| Metabolic plasticity and critical temperatures for aerobic scope in a eurythermal marine invertebrate (Littorina saxatilis, Gastropoda: Littorinidae) from different latitudes.Crossref | GoogleScholarGoogle Scholar | 12456709PubMed |
Stadtlander, T., Khalil, W., Focken, U., and Becker, K. (2013). Effects of low and medium levels of red alga Nori (Porphyra yezoensis Ueda) in the diets on growth, feed utilization and metabolism in intensively fed Nile tilapia, Oreochromis niloticus (L.). Aquaculture Nutrition 19, 64–73.
| Effects of low and medium levels of red alga Nori (Porphyra yezoensis Ueda) in the diets on growth, feed utilization and metabolism in intensively fed Nile tilapia, Oreochromis niloticus (L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXosVSlsg%3D%3D&md5=8506e0c72f72f7c532f67bd628909c12CAS |
Steneck, R., and Watling, L. (1982). Feeding capabilities and limitation of herbivorous molluscs: a functional group approach. Marine Biology 68, 299–319.
| Feeding capabilities and limitation of herbivorous molluscs: a functional group approach.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 |
Tilman, D., and Lehman, C. (2001). Human-caused environmental change: impacts on plant diversity and evolution. Proceedings of the National Academy of Sciences of the United States of America 98, 5433–5440.
| Human-caused environmental change: impacts on plant diversity and evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjs1Wgur4%3D&md5=9af98b4d6fa4515f74b82032d3615b24CAS | 11344290PubMed |
Underwood, A. J. (1980). The effects of grazing by gastropods and physical factors on the upper limits of distribution of intertidal macroalgae. Oecologia 46, 201–213.
| The effects of grazing by gastropods and physical factors on the upper limits of distribution of intertidal macroalgae.Crossref | GoogleScholarGoogle Scholar |
Vitousek, P. M., Aber, J. D., Howarth, R. W., Likens, G. E., Matson, P. A., Schindler, D. W., Schlesinger, W. H., and Tilman, D. G. (1997). Human alteration of the global nitrogen cycle: sources and consequences. Ecological Applications 7, 737–750.
Wallace, J. (1973). Feeding, starvation and metabolic rate in the shore crab Carcinus maenas. Marine Biology 20, 277–281.
| Feeding, starvation and metabolic rate in the shore crab Carcinus maenas.Crossref | GoogleScholarGoogle Scholar |
Wood, H. L., Spicer, J. I., and Widdicombe, S. (2008). Ocean acidification may increase calcification rates, but at a cost. Proceedings of the Royal Society of London – B. Biological Sciences 275, 1767–1773.
| Ocean acidification may increase calcification rates, but at a cost.Crossref | GoogleScholarGoogle Scholar |
Worm, B., and Lotze, H. K. (2006). Effects of eutrophication, grazing, and algal blooms on rocky shores. Limnology and Oceanography 51, 569–579.
| Effects of eutrophication, grazing, and algal blooms on rocky shores.Crossref | GoogleScholarGoogle Scholar |
Worm, B., Lotze, H., Boström, C., Engkvist, R., Labanauskas, V., and Sommer, U. (1999). Marine diversity shift linked to interactions among grazers, nutrients and propagule banks. Marine Ecology Progress Series 185, 309–314.
| Marine diversity shift linked to interactions among grazers, nutrients and propagule banks.Crossref | GoogleScholarGoogle Scholar |
Worm, B., Reusch, T., and Lotze, H. K. (2000). In situ nutrient enrichment: methods for marine benthic ecology. International Review of Hydrobiology 85, 359–375.
| In situ nutrient enrichment: methods for marine benthic ecology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjvFSnuro%3D&md5=80c42c4ac40db49c875da532ada589ddCAS |
