Feeding preferences of herbivores in a relatively pristine subtropical seagrass ecosystem
Derek A. Burkholder A C , Michael R. Heithaus A and James W. Fourqurean A BA Department of Biological Sciences, Marine Program, Florida International University, Biscayne Bay Campus, North Miami, FL 33181, USA.
B Southeast Environmental Research Center, Florida International University, Miami, FL 33199, USA.
C Corresponding author. Email: derek.burkholder@fiu.edu
Marine and Freshwater Research 63(11) 1051-1058 https://doi.org/10.1071/MF12029
Submitted: 31 January 2012 Accepted: 1 August 2012 Published: 26 November 2012
Abstract
Understanding forage choice of herbivores is important for predicting the potential impacts of changes in their abundance. Such studies, however, are rare in ecosystems with intact populations of both megagrazers (sirenians, sea turtles) and fish grazers. We used feeding assays and nutrient analyses of seagrasses to determine whether forage choice of grazers in Shark Bay, Australia, are influenced by the quality of seagrasses. We found significant interspecific variation in removal rates of seagrasses across three habitats (shallow seagrass bank interior, shallow seagrass bank edge, deep), but we did not detect variation in gazing intensity among habitats. In general, grazers were more likely to consume fast-growing species with lower carbon : nitrogen (C : N) and carbon : phosphorus (C : P) ratios, than the slower-growing species that are dominant in the bay. Grazer choices were not, however, correlated with nutrient content within the tropical seagrasses. Slow-growing temperate seagrasses that experienced lower herbivory provide greater habitat value as a refuge for fishes and may facilitate fish grazing on tropical species. Further studies are needed, however, to more fully resolve the factors influencing grazer foraging preferences and the possibility that grazers mediate indirect interactions among seagrass species.
Additional keywords : Amphibolis, Cymodocea, diet selection, dugong, food choice, green turtle, Halodule, Halophila, Pelates, Posidonia.
References
Aragones, L. V., and Marsh, H. (2000). Impact of dugong grazing and turtle cropping on tropical seagrass communities. Pacific Conservation Biology 5, 277–288.Armitage, A. R., and Fourqurean, J. W. (2006). The short-term influence of herbivory near patch reefs varies between seagrass species. Journal of Experimental Marine Biology and Ecology 339, 65–74.
| The short-term influence of herbivory near patch reefs varies between seagrass species.Crossref | GoogleScholarGoogle Scholar |
Arnold, T. M., Tanner, C. E., and Hatch, W. I. (1995). Phenotypic variation in polyphenolic content of the tropical brown algae Lobophora variegata as a function of nitrogen availability. Marine Ecology Progress Series 123, 177–183.
| Phenotypic variation in polyphenolic content of the tropical brown algae Lobophora variegata as a function of nitrogen availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXosFeltLY%3D&md5=aef183c0c42f92ec6f46d44e98a2085cCAS |
Belicka, L. L., Burkholder, D. A., Fourqurean, J. W., Heithaus, M. R., Macko, S. A., and Jaffe, R. (2012). Stable isotope and fatty acid biomarkers of seagrass, epiphytic, and algal organic matter of consumers in a nearly pristine seagrass ecosystem. Marine and Freshwater Research 63, 1085–1097.
| Stable isotope and fatty acid biomarkers of seagrass, epiphytic, and algal organic matter of consumers in a nearly pristine seagrass ecosystem.Crossref | GoogleScholarGoogle Scholar |
Bjorndal, K. A. (1997). Foraging ecology and nutrition of sea turtles. In ‘The Biology of Sea Turtles’. (Eds P. L. Lutz and J. A. Musick.) pp. 199–231. (CRC Press: Boca Raton, FL.)
Boyer, K. E., Fong, P., Armitage, A. R., and Cohen, R. A. (2004). Elevated nutrient content of tropical macroalgae increases rates of herbivory in coral, seagrass, and mangrove habitats. Coral Reefs 23, 530–538.
Burkepile, D. E., and Hay, M. E. (2009). Nutrient versus herbivore control of macroalgal community development and coral growth on a Caribbean reef. Marine Ecology Progress Series 389, 71–84.
| Nutrient versus herbivore control of macroalgal community development and coral growth on a Caribbean reef.Crossref | GoogleScholarGoogle Scholar |
Burkholder, D. A., Heithaus, M. R., Thomson, J. A., and Fourqurean, J. W. (2011). Diversity in trophic interactions of green sea turtles Chelonia mydas on a relatively pristine coastal foraging ground. Marine Ecology Progress Series 439, 277–293.
| Diversity in trophic interactions of green sea turtles Chelonia mydas on a relatively pristine coastal foraging ground.Crossref | GoogleScholarGoogle Scholar |
Burkholder, D. A., Fourqurean, J. W., and Heithaus, M. R. (in press). Spatial pattern in seagrass stoichiometry indicates both N-limited and P-limited regions of an iconic P-limited subtropical bay. , .
| Spatial pattern in seagrass stoichiometry indicates both N-limited and P-limited regions of an iconic P-limited subtropical bay.Crossref | GoogleScholarGoogle Scholar |
de Iongh, H. H., Wenno, B. J., and Meelis, E. (1995). Seagrass distribution and seasonal biomass changes in relation to dugong grazing in the Moluccas, East Indonesia. Aquatic Botany 50, 1–19.
| Seagrass distribution and seasonal biomass changes in relation to dugong grazing in the Moluccas, East Indonesia.Crossref | GoogleScholarGoogle Scholar |
Duarte, C. M. (1991). Allometric scaling of seagrass form and productivity. Marine Ecology Progress Series 77, 289–300.
| Allometric scaling of seagrass form and productivity.Crossref | GoogleScholarGoogle Scholar |
Fourqurean, J. W., Zieman, J. C., and Powell, G. V. N. (1992). Phosphorus limitation of primary production in Florida Bay: evidence from C : N : P ratios of the dominant seagrass Thalassia testudinum. Limnology and Oceanography 37, 162–171.
| Phosphorus limitation of primary production in Florida Bay: evidence from C : N : P ratios of the dominant seagrass Thalassia testudinum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xktleitbs%3D&md5=5bee7e8b99f1608ecb2b3c8104e86969CAS |
Fourqurean, J. W., Boyer, J. N., Durako, M. J., Hefty, L. N., and Peterson, B. J. (2003). Forecasting responses of seagrass distributions to changing water quality using monitoring data. Ecological Applications 13, 474–489.
| Forecasting responses of seagrass distributions to changing water quality using monitoring data.Crossref | GoogleScholarGoogle Scholar |
Fourqurean, J. W., Escorcia, S. P., Anderson, W. T., and Zieman, J. C. (2005). Spatial and seasonal variability in elemental content, δ13C, and δ15N of Thalassia testudinum from south Florida and its implications for ecosystem studies. Estuaries 28, 447–461.
| Spatial and seasonal variability in elemental content, δ13C, and δ15N of Thalassia testudinum from south Florida and its implications for ecosystem studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpslSmtb4%3D&md5=54b07885f409bb5c9adb06a7285cdadfCAS |
Fourqurean, J. W., Manuel, S., Coates, K. A., Kenworthy, J. W., and Smith, S. R. (2010). Effects of excluding sea turtle herbivores from a seagrass bed: overgrazing may have led to loss of seagrass meadows in Bermuda. Marine Ecology Progress Series 419, 223–232.
| Effects of excluding sea turtle herbivores from a seagrass bed: overgrazing may have led to loss of seagrass meadows in Bermuda.Crossref | GoogleScholarGoogle Scholar |
Fritz, R., and Simms, E. (1992). ‘Plant Resistance to Herbivores and Pathogens: Ecology Evolution and Genetics.’ (University of Chicago Press: Chicago, IL.)
Goecker, M. E., Heck, K. L., and Valentine, J. F. (2005). Effects of nitrogen concentrations in turtlegrass Thalassia testudinum on consumption by the bucktooth parrotfish Sparisona radians. Marine Ecology Progress Series 286, 239–248.
| Effects of nitrogen concentrations in turtlegrass Thalassia testudinum on consumption by the bucktooth parrotfish Sparisona radians.Crossref | GoogleScholarGoogle Scholar |
Hagerman, A. E., Robbins, C. T., Weerasuriya, Y., Wilson, T. C., and McArthur, C. (1992). Tannin chemistry in relation to digestion. Journal of Range Management 45, 57–62.
| Tannin chemistry in relation to digestion.Crossref | GoogleScholarGoogle Scholar |
Hay, M. E., and Fenical, W. (1988). Marine plant–herbivore interactions: the ecology of chemical defense. Annual Review of Ecology and Systematics 19, 111–145.
| Marine plant–herbivore interactions: the ecology of chemical defense.Crossref | GoogleScholarGoogle Scholar |
Hay, M. E., Fenical, W., and Gustafson, K. (1987). Chemical defense against divers coral-reef herbivores. Ecology 68, 1581–1591.
| Chemical defense against divers coral-reef herbivores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhsVOis7o%3D&md5=2bd5726aacf337d9e7a903e2497d5658CAS |
Heck, K. L., and Valentine, J. F. (2007). The primacy of top-down effects in shallow benthic ecosystems. Estuaries and Coasts 30, 371–381.
| The primacy of top-down effects in shallow benthic ecosystems.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R. (2004). Fish communities of seagrass meadows and associated habitats in Shark Bay, Western Australia. Bulletin of Marine Science 75, 79–99.
Heithaus, M. R., Frid, A., Wirsing, A., Bejder, L., and Dill, L. M. (2005). The biology of green and loggerhead turtles under risk from tiger sharks at a foraging ground. Marine Ecology Progress Series 288, 285–294.
| The biology of green and loggerhead turtles under risk from tiger sharks at a foraging ground.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Frid, A., Wirsing, A. J., Dill, L. M., Fourqurean, J., Burkholder, D., Thomson, J., and Bejder, L. (2007a). State-dependent risk-taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem. Journal of Animal Ecology 76, 837–844.
| State-dependent risk-taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Wirsing, A. J., Frid, A., and Dill, L. M. (2007b). Species interactions and marine conservation: lessons from an undisturbed ecosystem. Israel Journal of Ecology and Evolution 53, 355–370.
| Species interactions and marine conservation: lessons from an undisturbed ecosystem.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Frid, A., Wirsing, A. J., and Worm, B. (2008). Predicting ecological consequences of marine top predator declines. Trends in Ecology & Evolution 23, 202–210.
| Predicting ecological consequences of marine top predator declines.Crossref | GoogleScholarGoogle Scholar |
Herbert, D. A., Perry, W. B., Cosby, B. J., and Fourqurean, J. W. (2011). Projected reorganization of Florida Bay seagrass communities in response to the increased freshwater inflow of Everglades restoration. Estuaries and Coasts 34, 973–992.
| Projected reorganization of Florida Bay seagrass communities in response to the increased freshwater inflow of Everglades restoration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsFartrk%3D&md5=5b35d95254c41084a23435b735a18468CAS |
Holt, R. D. (1977). Predation, apparent competition, and structure of prey communities. Theoretical Population Biology 12, 197–229.
| Predation, apparent competition, and structure of prey communities.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1c%2FlsFegsg%3D%3D&md5=0108e4ccc22a30843b4ffa0335b152c3CAS |
Jones, W. T., and Mangan, J. L. (1977). Complexes of the condensed tannins of sainfoin (Onobrychis vicifolia Scop.) with fraction 1 leaf protein and with submaxillay mucoprotein, and their reversal by polyethylene glycol and pH. Journal of the Science of Food and Agriculture 28, 126–136.
| Complexes of the condensed tannins of sainfoin (Onobrychis vicifolia Scop.) with fraction 1 leaf protein and with submaxillay mucoprotein, and their reversal by polyethylene glycol and pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXhvVyjtrs%3D&md5=ea62d6b068d423ecd60f9e0b5ac0a9a8CAS |
Jormalainen, V., Wikstrom, S. A., and Honkanen, T. (2008). Fouling mediates grazing: intertwining of resistances to multiple enemies in the brown alga Fucus vesiculosus. Oecologia 155, 559–569.
| Fouling mediates grazing: intertwining of resistances to multiple enemies in the brown alga Fucus vesiculosus.Crossref | GoogleScholarGoogle Scholar |
Karez, R., Engelbert, S., and Sommer, U. (2000). ‘Co-consumption’ and ‘protective coating’: two new proposed effects of epiphytes on their macroalgal hosts in mesograzer–epiphyte–host interactions. Marine Ecology Progress Series 205, 85–93.
| ‘Co-consumption’ and ‘protective coating’: two new proposed effects of epiphytes on their macroalgal hosts in mesograzer–epiphyte–host interactions.Crossref | GoogleScholarGoogle Scholar |
Kirsch, K. D., Valentine, J. F., and Heck, K. L. (2002). Parrotfish grazing on turtlegrass, Thalassia testudinum: evidence for the importance of seagrass consumption in food web dynamics of the Florida Keys National Marine Sanctuary. Marine Ecology Progress Series 227, 71–85.
| Parrotfish grazing on turtlegrass, Thalassia testudinum: evidence for the importance of seagrass consumption in food web dynamics of the Florida Keys National Marine Sanctuary.Crossref | GoogleScholarGoogle Scholar |
Lal, A., Arthur, R., Marbá, N., Lill, A. W. T., and Alcoverro, T. (2010). Implications of conserving an ecosystem modifier: increasing green turtle (Chelonia mydas) densities substantially alters seagrass meadows. Biological Conservation 143, 2730–2738.
| Implications of conserving an ecosystem modifier: increasing green turtle (Chelonia mydas) densities substantially alters seagrass meadows.Crossref | GoogleScholarGoogle Scholar |
Mariani, S., and Alcoverro, T. (1999). A multiple-choice feeding-preference experiment utilizing seagrasses with a natural population of herbivorous fishes. Marine Ecology Progress Series 189, 295–299.
| A multiple-choice feeding-preference experiment utilizing seagrasses with a natural population of herbivorous fishes.Crossref | GoogleScholarGoogle Scholar |
Masini, R. J., Anderson, P. K., and McComb, A. J. (2001). A halodule-dominated community in a subtropical embayment: physical environment, productivity, biomass, and impact of dugong grazing. Aquatic Botany 71, 179–197.
| A halodule-dominated community in a subtropical embayment: physical environment, productivity, biomass, and impact of dugong grazing.Crossref | GoogleScholarGoogle Scholar |
Matheson, R. E. J., Camp, D. K., Sogard, S. M., and Bjorgo, K. A. (1999). Changes in seagrass-associated fish and crustacean communities of Florida Bay mud banks: the effects of recent ecosystem changes? Estuaries 22, 534–551.
| Changes in seagrass-associated fish and crustacean communities of Florida Bay mud banks: the effects of recent ecosystem changes?Crossref | GoogleScholarGoogle Scholar |
McMillan, C. (1984). The condensed tannins (proanthocyanidins) in seagrasses. Aquatic Botany 20, 351–357.
| The condensed tannins (proanthocyanidins) in seagrasses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhtV2qs70%3D&md5=1cd5de4cdabe2c9292e7c4e43b65d3c9CAS |
Moran, K. L., and Bjorndal, K. A. (2005). Simulated green turtle grazing affects structure and productivity of seagrass pastures. Marine Ecology Progress Series 305, 235–247.
| Simulated green turtle grazing affects structure and productivity of seagrass pastures.Crossref | GoogleScholarGoogle Scholar |
Prado, P., and Heck, K. L. (2011). Seagrass selection by omnivorous and herbivorous consumers: determining factors. Marine Ecology Progress Series 429, 45–55.
| Seagrass selection by omnivorous and herbivorous consumers: determining factors.Crossref | GoogleScholarGoogle Scholar |
Preen, A. R. (1995). Impacts of dugong foraging on seagrass habitats: observational and experimental evidence for cultivation grazing. Marine Ecology Progress Series 124, 201–213.
| Impacts of dugong foraging on seagrass habitats: observational and experimental evidence for cultivation grazing.Crossref | GoogleScholarGoogle Scholar |
Preen, A. R., Marsh, H. D., Lawler, I. R., Prince, R. I., and Shepherd, R. (1997). Distribution and abundance of dugongs, turtles, dolphins and other megafauna in Shark Bay, Ningaloo Reef and Exmouth Gulf, Western Australia. Wildlife Research 24, 185–208.
| Distribution and abundance of dugongs, turtles, dolphins and other megafauna in Shark Bay, Ningaloo Reef and Exmouth Gulf, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Robbins, C. T., Hanley, T. A., Hagerman, A. E., Hjeljord, O., Baker, D. L., Schwartz, C. C., and Mautz, W. W. (1987). Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology 68, 98–107.
| 1:CAS:528:DyaL2sXhtlGmtrg%3D&md5=04d4ec6341868e43504d7d5752bd7d8bCAS |
Tomas, F., Turon, X., and Romero, J. (2005). Seasonal and small-scale spatial variability of herbivory pressure on the temperate seagrass Posidonia oceanica. Marine Ecology Progress Series 301, 95–107.
| Seasonal and small-scale spatial variability of herbivory pressure on the temperate seagrass Posidonia oceanica.Crossref | GoogleScholarGoogle Scholar |
Wahl, M., and Hay, M. E. (1995). Associational resistance and shared doom-effects of epibiosis on herbivory. Oecologia 102, 329–340.
| Associational resistance and shared doom-effects of epibiosis on herbivory.Crossref | GoogleScholarGoogle Scholar |
Walker, D. I., Kendrick, G. A., and McComb, A. J. (1988). The distribution of seagrass species in Shark Bay, Western Australia, with notes on their ecology. Aquatic Botany 30, 305–317.
| The distribution of seagrass species in Shark Bay, Western Australia, with notes on their ecology.Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., Heithaus, M. R., and Dill, L. M. (2007a). Fear factor: Do dugongs (Dugong dugon) trade food for safety from tiger sharks (Galeocerdo cuvier)? Oecologia 153, 1031–1040.
| Fear factor: Do dugongs (Dugong dugon) trade food for safety from tiger sharks (Galeocerdo cuvier)?Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., Heithaus, M. R., and Dill, L. M. (2007b). Living on the edge: dugongs prefer to forage in microhabitats that allow escape from rather than avoidance of predators. Animal Behaviour 74, 93–101.
| Living on the edge: dugongs prefer to forage in microhabitats that allow escape from rather than avoidance of predators.Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., Heithaus, M. R., and Dill, L. M. (2007c). Can you dig it? Use of excavation, a risky foraging tactic, by dugongs is sensitive to predation danger. Animal Behaviour 74, 1085–1091.
| Can you dig it? Use of excavation, a risky foraging tactic, by dugongs is sensitive to predation danger.Crossref | GoogleScholarGoogle Scholar |