Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-28T00:49:11.728Z Has data issue: false hasContentIssue false
  • English
  • Français

Mammalian herbivores in Australia transport nutrients from terrestrial to marine ecosystems via mangroves

Published online by Cambridge University Press:  20 February 2014

Ruth Reef ,
Ilka C. Feller  and
Catherine E. Lovelock
Ruth Reef*
Affiliation:
School of Biological Sciences, The University of Queensland, St Lucia QLD 4072, Australia
Ilka C. Feller
Affiliation:
Smithsonian Environmental Research Center, POB 28 Edgewater, MD 21037, USA
Catherine E. Lovelock
Affiliation:
School of Biological Sciences, The University of Queensland, St Lucia QLD 4072, Australia
*
1 Corresponding author. Email: r.reef@uq.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract:

Nutrient subsidies from one ecosystem to another serve a critical link among ecosystems. The transfer of materials across the terrestrial-to-marine boundary is considered to be driven by hydrological connectivity, but animal movement can provide another pathway for nutrient transfers. In two separate studies we assessed the role mammals (bats and kangaroos) play in alleviating nutrient limitation in mangrove forests in Australia. At Lizard Island, we measured tree growth and foliar elemental and isotopic composition of trees growing within and outside a large flying fox roost. In Western Australia, we measured foliar elemental and isotopic composition of trees within two forests frequented by kangaroos that feed in spinifex grasslands and shelter in the shade of the mangroves. We compared those with mangroves from adjacent forests that are not frequented by kangaroos. We show that at both locations, the mangrove forest receives terrestrial nutrient subsidies through animal movement. At Lizard Island dominant mangrove species were significantly enriched in nitrogen within the bat roost, as evidenced by higher foliar N concentrations (by up to 150%), N:P and N:C ratios in trees within the roost compared with trees outside the roost. The isotopic signature of foliar N was significantly enriched in 15N by 1–3‰ within the roost, further suggesting that the source of the N enrichment was the bat roost. Growth rates of mangroves within the roost were nearly six times higher than trees outside the roost. In the arid coast of Western Australia, we show elevated foliar 15N abundance of up to 3‰ in mangroves where kangaroos shelter relative to trees where they do not. Thus, this study presents two examples for mammalian herbivore mediated localized transport of nutrients from terrestrial to marine ecosystems, consequently affecting mangrove tree growth, productivity and forest structure.

Keywords

elemental compositionflying foxkangaroosMacropus sppnutrient subsidyPteropus sprooststable isotopestree growthvector
Type
Research Article
Information
Journal of Tropical Ecology , Volume 30 , Issue 3 , May 2014 , pp. 179 - 188
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ALONGI, D. M. 1994. The role of bacteria in nutrient recycling in tropical mangrove and other coastal benthic ecosystems. Hydrobiologia 285:19–32.Google Scholar
ALONGI, D. M., TIRENDI, F. & GOLDRICK, A. 1996. Organic matter oxidation and sediment chemistry in mixed terrigenous-carbonate sands of Ningaloo Reef, Western Australia. Marine Chemistry 54:203–219.CrossRefGoogle Scholar
ALONGI, D. M., TIRENDI, F. & CLOUGH, B. F. 2000. Below-ground decomposition of organic matter in forests of the mangroves Rhizophora stylosa and Avicennia marina along the arid coast of Western Australia. Aquatic Botany 68:97–122.CrossRefGoogle Scholar
ANDERSON, W. B. & POLIS, G. A. 1998. Marine subsidies of island communities in the gulf of California: evidence from stable carbon and nitrogen isotopes. Oikos 81:75–80.CrossRefGoogle Scholar
BAISRE, J. A. & ARBOLEYA, Z. 2006. Going against the flow: effects of river damming in Cuban fisheries. Fisheries Research 81:283–292.CrossRefGoogle Scholar
BALL, M. C. & PIDSLEY, S. M. 1988. Seedling establishment of tropical mangrove species in relation to salinity. Pp. 123–134 in Larson, H., Hanley, R. & Michie, M. (eds.). Darwin Harbour: proceedings of a Workshop on Research and Management in Darwin Harbour. Australian National University Press, Canberra.Google Scholar
CEDERHOLM, C. J., KUNZE, M. D., MUROTA, T. & SIBATANI, A. 1999. Pacific salmon carcasses: essential contributions of nutrients and energy for aquatic and terrestrial ecosystems. Fisheries 24:6–15.2.0.CO;2>CrossRefGoogle Scholar
CHEN, R. & TWILLEY, R. 1999. Patterns of mangrove forest structure and soil nutrient dynamics along the Shark River estuary, Florida. Estuaries and Coasts 22:955–970.Google Scholar
CLOUGH, B. 1984. Growth and salt balance of the mangroves Avicennia marina (Forsk.) Vierh. and Rhizophora stylosa Griff. in relation to salinity. Functional Plant Biology 11:419–430.Google Scholar
DUNTON, K. H., WEINGARTNER, T. & CARMACK, E. C. 2006. The nearshore western Beaufort Sea ecosystem: circulation and importance of terrestrial carbon in arctic coastal food webs. Progress in Oceanography 71:362–378.Google Scholar
EVANS, J. 1989. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19.Google Scholar
EWEL, K. C., TWILLEY, R. R. & ONG, J. E. 1998. Different kinds of mangrove forests provide different goods and services. Global Ecology and Biogeography Letters 7:83–94.CrossRefGoogle Scholar
FAUNCE, C. H. & SERAFY, J. E. 2006. Mangroves as fish habitat: 50 years of field studies. Marine Ecology Progress Series 318:1–18.Google Scholar
FELLER, I. C. 1995. Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecological Monographs 65:477–505.CrossRefGoogle Scholar
FELLER, I. C. & CHAMBERLAIN, A. 2007. Herbivore responses to nutrient enrichment and landscape heterogeneity in a mangrove ecosystem. Oecologia 153:607–616.CrossRefGoogle Scholar
FELLER, I. C., LOVELOCK, C. E. & MCKEE, K. L. 2007. Nutrient addition differentially affects ecological processes of Avicennia germinans in nitrogen versus phosphorus limited mangrove ecosystems. Ecosystems 10:347–359.Google Scholar
FELLER, I. C., LOVELOCK, C. E. & PIOU, C. 2009. Growth and nutrient conservation in Rhizophora mangle in response to fertilization along latitudinal and tidal gradients. Smithsonian Contributions to the Marine Sciences 38:345–358.Google Scholar
FIELD, C. B., OSBORN, J. G., HOFFMAN, L. L., POLSENBERG, J. F., ACKERLY, D. D., BERRY, J. A., BJORKMAN, O., HELD, A., MATSON, P. A. & MOONEY, H. A. 1998. Mangrove biodiversity and ecosystem function. Global Ecology and Biogeography Letters 7:3–14.Google Scholar
FRY, B. & EWEL, K. C. 2003. Using stable isotopes in mangrove fisheries research – a review and outlook. Isotopes in Environmental and Health Studies 39:191–196.CrossRefGoogle ScholarPubMed
GENDE, S. M., EDWARDS, R. T., WILLSON, M. F. & WIPFLI, M. S. 2002. Pacific salmon in aquatic and terrestrial ecosystems. BioScience 52:917–928.CrossRefGoogle Scholar
GIARDINA, C. P., RYAN, M. G., BINKLEY, D. & FOWNES, J. H. 2003. Primary production and carbon allocation in relation to nutrient supply in a tropical experimental forest. Global Change Biology 9:1438–1450.CrossRefGoogle Scholar
GRAVEL, D., GUICHARD, F., LOREAU, M. & MOUQUET, N. 2010. Source and sink dynamics in meta-ecosystems. Ecology 91:2172–2184.Google Scholar
HALL, R. C. 1944. A vernier tree-growth band. Journal of Forestry 42:742–743.Google Scholar
HAYNES, B. E. & GOWER, S. T. 1995. Belowground carbon allocation in unfertilized and fertilized red pine plantations in northern Wisconsin. Tree Physiology 15:317–325.Google Scholar
HERRERA, L. G., OSORIO, J. & MANCINA, C. A. 2011. Ammonotely in a neotropical frugivorous bat as energy intake decreases. Journal of Experimental Biology 214:3775–3781.Google Scholar
HOCKING, M. D. & REYNOLDS, J. D. 2011. Impacts of salmon on riparian plant diversity. Science 331:1609–1612.Google Scholar
HUTCHINGS, P. A. & RECHER, H. F. 1983. The faunal communities of Australian mangroves. Pp. 103–110 in Teas, H. J. (ed.). Biology and ecology of mangroves. Dr W. Junk, The Hague.Google Scholar
ILES, J., KELLEWAY, J., KOBAYASHI, T., MAZUMDER, D., KNOWLES, L., PRIDDEL, D. & SAINTILAN, N. 2010. Grazing kangaroos act as local recyclers of energy on semiarid floodplains. Australian Journal of Zoology 58:145–149.Google Scholar
KOERSELMAN, W. & MEULEMAN, A. F. M. 1996. The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. Journal of Applied Ecology 33:1441–1450.Google Scholar
KRAUSS, K. W., LOVELOCK, C. E., MCKEE, K. L., LÓPEZ-HOFFMAN, L., EWE, S. M. L. & SOUSA, W. P. 2008. Environmental drivers in mangrove establishment and early development: a review. Aquatic Botany 89:105–127.Google Scholar
LONERAGAN, N. R. & BUNN, S. E. 1999. River flows and estuarine ecosystems: implications for coastal fisheries from a review and a case study of the Logan River, southeast Queensland. Australian Journal of Ecology 24:431–440.Google Scholar
LOREAU, M. & HOLT, R. D. 2004. Spatial flows and the regulation of ecosystems. American Naturalist 163:606–615.CrossRefGoogle ScholarPubMed
LOVELOCK, C. E., FELLER, I. C., MCKEE, K. L., ENGELBRECHT, B. M. J. & BALL, M. C. 2004. The effect of nutrient enrichment on growth, photosynthesis and hydraulic conductance of dwarf mangroves in Panama. Functional Ecology 18:25–33.Google Scholar
LOVELOCK, C. E., FELLER, I. C., ELLIS, J., SCHWARZ, A., HANCOCK, N., NICHOLS, P. & SORRELL, B. 2007. Mangrove growth in New Zealand estuaries: the role of nutrient enrichment at sites with contrasting rates of sedimentation. Oecologia 153:633–641.Google Scholar
MCKEE, K. L., MENDELSSOHN, I. A. & HESTER, M. W. 1988. Reexamination of pore water sulfide concentrations and redox potentials near the aerial roots of Rhizophora mangle and Avicennia germinans . American Journal of Botany 75:1352–1359.Google Scholar
MCKEE, K. L., CAHOON, D. R. & FELLER, I. C. 2007. Caribbean mangroves adjust to rising sea level through biotic controls on change in soil elevation. Global Ecology and Biogeography 16:545–556.Google Scholar
MENZEL, D. & CORWIN, N. 1965. The measurement of total phosphorus in seawater based on the liberation of organically bound fractions by persulfate oxidation. Limnology and Oceanography 10:280–282.Google Scholar
MEYER, J. L. & SCHULTZ, E. T. 1985. Migrating haemulid fishes as a source of nutrients and organic matter on coral reefs. Limnology and Oceanography 30:146–156.CrossRefGoogle Scholar
MUMBY, P. J., EDWARDS, A. J., ERNESTO ARIAS-GONZALEZ, J., LINDEMAN, K. C., BLACKWELL, P. G., GALL, A., GORCZYNSKA, M. I., HARBORNE, A. R., PESCOD, C. L., RENKEN, H., WABNITZ, C. C. & LLEWELLYN, G. 2004. Mangroves enhance the biomass of coral reef fish communities in the Caribbean. Nature 427:533–536.Google Scholar
NAGELKERKEN, I., BLABER, S. J. M., BOUILLON, S., GREEN, P., HAYWOOD, M., KIRTON, L. G., MEYNECKE, J. O., PAWLIK, J., PENROSE, H. M., SASEKUMAR, A. & SOMERFIELD, P. J. 2008. The habitat function of mangroves for terrestrial and marine fauna: a review. Aquatic Botany 89:155–185.Google Scholar
NAIDOO, G. 2009. Differential effects of nitrogen and phosphorus enrichment on growth of dwarf Avicennia marina mangroves. Aquatic Botany 90:184–190.Google Scholar
NAIMAN, R. J., BILBY, R. E., SCHINDLER, D. E. & HELFIELD, J. M. 2002. Pacific salmon, nutrients, and the dynamics of freshwater and riparian ecosystems. Ecosystems 5:399–417.Google Scholar
NATELHOFFER, K. J. & FRY, B. 1988. Controls on natural nitrogen-15 and carbon-13 abundances in forest soil organic matter. Soil Science Society of America Journal 52:1633–1640.CrossRefGoogle Scholar
NEWSOME, A. E. 1975. An ecological comparison of the two arid-zone kangaroos of Australia, and their anomalous prosperity since the introduction of ruminant stock to their environment. Quarterly Review of Biology 50:389–424.Google Scholar
ODUM, W. E., MCIVOR, C. C. & SMITH, T. J. 1982. The ecology of the mangroves of south Florida: a community profile. United States Fish and Wildlife Service, Office of Biological Services, Washington, DC. 144 pp.Google Scholar
ONUF, C. P., TEAL, J. M. & VALIELA, I. 1977. Interactions of nutrients, plant growth and herbivory in a mangrove ecosystem. Ecology 58:514–526.CrossRefGoogle Scholar
PAERL, H. W. 1997. Coastal eutrophication and harmful algal blooms: importance of atmospheric deposition and groundwater as “new” nitrogen and other nutrient sources. Limnology and Oceanography 42:1154–1165.Google Scholar
PALMER, C. & WOINARSKI, J. C. Z. 1999. Seasonal roosts and foraging movements of the black flying fox (Pteropus alecto) in the Northern Territory: resource tracking in a landscape mosaic. Wildlife Research 26:823–838.Google Scholar
PALMER, C., PRICE, O. & BACH, C. 2000. Foraging ecology of the black flying fox (Pteropus alecto) in the seasonal tropics of the Northern Territory, Australia. Wildlife Research 27:169–178.CrossRefGoogle Scholar
PASSIOURA, J. B., BALL, M. C. & KNIGHT, J. H. 1992. Mangroves may salinize the soil and in so doing limit their transpiration rate. Functional Ecology 6:476–481.CrossRefGoogle Scholar
PIERSON, E. D. & RAINEY, W. E. 1990. The biology of flying foxes of the genus Pteropus: a review. Pp. 1–17 in Wilson, D. E. & Graham, G. L. (eds.). Pacific Island Flying Foxes: Proceedings of International Conservation Conference. U.S. Fish and Wildlife Service, Washington, DC.Google Scholar
POLIS, G. A. & HURD, S. D. 1996. Linking marine and terrestrial food webs: allochthonous input from the ocean supports high secondary productivity on small islands and coastal land communities. American Naturalist 147:396–423.Google Scholar
POLIS, G. A., ANDERSON, W. B. & HOLT, R. D. 1997. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annual Review of Ecology and Systematics 28:289–316.Google Scholar
PROSKE, U. & HABERLE, S. G. 2012. Island ecosystem and biodiversity dynamics in northeastern Australia during the Holocene: unravelling short-term impacts and long-term drivers. The Holocene 22:1097–1111.Google Scholar
REEF, R., BALL, M. C., FELLER, I. C. & LOVELOCK, C. E. 2010a. Relationships among RNA:DNA ratio, growth and elemental stoichiometry in mangrove trees. Functional Ecology 24:1064–1072.Google Scholar
REEF, R., FELLER, I. C. & LOVELOCK, C. E. 2010b. Nutrition of mangroves. Tree Physiology 30:1148–1160.Google Scholar
REEF, R., BALL, M. C. & LOVELOCK, C. E. 2012. The impact of a locust plague on mangroves of the arid Western Australia coast. Journal of Tropical Ecology 28:307–311.Google Scholar
REES, S., OPDYKE, B., WILSON, P., KEITH FIFIELD, L. & LEVCHENKO, V. 2006. Holocene evolution of the granite based Lizard Island and MacGillivray Reef systems, Northern Great Barrier Reef. Coral Reefs 25:555–565.CrossRefGoogle Scholar
ROBERTSON, A. I. & DUKE, N. C. 1987. Insect herbivory on mangrove leaves in North Queensland. Australian Journal of Ecology 12:1–7.Google Scholar
ROBERTSON, A. I. & PHILLIPS, M. J. 1995. Mangroves as filters of shrimp pond effluent: predictions and biogeochemical research needs. Hydrobiologia 295:311–321.Google Scholar
ROSE, M. D. & POLIS, G. A. 1998. The distribution and abundance of coyotes: the effects of allochthonous food subsidies from the sea. Ecology 79:998–1007.Google Scholar
SMITH, T. J. 1987. Effects of light and intertidal position on seedling survival and growth in tropical tidal forests. Journal of Experimental Marine Biology and Ecology 110:133–146.Google Scholar
SMITH, V. H., TILMAN, G. D. & NEKOLA, J. C. 1999. Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environmental Pollution 100:179–196.Google Scholar
TIDEMANN, C. R., VARDON, M. J., LOUGHLAND, R. A. & BROCKLEHURST, P. J. 1999. Dry season camps of flying-foxes (Pteropus spp.) in Kakadu World Heritage Area, north Australia. Journal of Zoology 247:155–163.Google Scholar
VAN VELDHOVEN, P. P. & MANNAERTS, G. P. 1987. Inorganic and organic phosphate measurements in the nanomolar range. Analytical Biochemistry 161:45–48.Google Scholar
VARDON, M. J., BROCKLEHURST, P. S., WOINARSKI, J. C. Z., CUNNINGHAM, R. B., DONNELLY, C. F. & TIDEMANN, C. R. 2001. Seasonal habitat use by flying-foxes, Pteropus alecto and P. scapulatus (Megachiroptera), in monsoonal Australia. Journal of Zoology 253:523–535.CrossRefGoogle Scholar