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Herbivore responses to nutrient enrichment and landscape heterogeneity in a mangrove ecosystem

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Abstract

Complex gradients in forest structure across the landscape of offshore mangrove islands in Belize are associated with nutrient deficiency and flooding. While nutrient availability can affect many ecological processes, here we investigate how N and P enrichment interact with forest structure in three distinct zones (fringe, transition, dwarf) to alter patterns of herbivory as a function of folivory, loss of yield, and tissue mining. The effects of nutrient addition and zone varied by functional feeding group or specific herbivore. Folivory ranged from 0 to 0.4% leaf area damaged per month, but rates did not vary by either nutrient enrichment or zone. Leaf lifetime damage ranged from 3 to 10% of the total leaf area and was caused primarily by the omnivorous tree crab Aratus pisonii. We detected two distinct spatial scales of response by A. pisonii that were unrelated to nutrient treatment, i.e., most feeding damage occurred in the fringe zone and crabs fed primarily on the oldest leaves in the canopy. Loss of yield caused by the bud moth Ecdytolopha sp. varied by zone but not by nutrient treatment. A periderm-mining Marmara sp. responded positively to nutrient enrichment and closely mirrored the growth response by Rhizophora mangle across the tree height gradient. In contrast, a leaf-mining Marmara sp. was controlled by parasitoids and predators that killed >89% of its larvae. Thus, nutrient availability altered patterns of herbivory of some but not all mangrove herbivores. These findings support the hypothesis that landscape heterogeneity of the biotic and abiotic environment has species-specific effects on community structure and trophic interactions. Predicting how herbivores respond to nutrient over-enrichment in mangrove ecosystems also requires an assessment of habitat heterogeneity coupled with feeding strategies and species-specific behavior measured on multiple scales of response.

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References

  • Alongi DM, Boto KG, Robertson AI (1992) Nitrogen and phosphorus cycles. In: Robertson AI, Alongi DM (eds) Tropical mangrove ecosystems. American Geophysical Union, Washington, D.C., pp 251–292

    Google Scholar 

  • Bazzaz FA, Chiariello NR, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37:58–67

    Article  Google Scholar 

  • Beever III JW, Simberloff D, King LL (1979) Herbivory and predation by the mangrove tree crab Aratus pisonii. Oecologia 43:317–328

    Article  Google Scholar 

  • Boto KG, Wellington JT (1983) Phosphorus and nitrogen nutritional status of a northern Australian mangrove forest. Mar Ecol Prog Ser 11:63–69

    Google Scholar 

  • Burrows DW (2003) The role of insect herbivory on the mangroves Avicennia marina and Rhizophora stylosa. PhD dissertation, James Cook University, Townsville

  • Chen R, Twilley RR (1999) Patterns of mangrove forest structure and soil nutrient dynamics along the shark river estuary, Florida. Estuaries 22:955–970

    Article  Google Scholar 

  • Cintròn G, Lugo AE, Martinez R (1985) Structural and functional properties of mangrove forests. In: D’Arcy WG, Correa MD (eds) The botany and natural history of Panama. Missouri Botanical Garden, St Louis, Mo., pp 53–66

    Google Scholar 

  • Clay RE, Andersen AN (1996) Ant fauna of a mangrove community in the Australian seasonal tropics, with particular reference to zonation. Aust J Zool 44:521–533

    Article  Google Scholar 

  • Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335

    Article  Google Scholar 

  • Coley PD, Bryant JP, Chapin III FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

    Article  PubMed  CAS  Google Scholar 

  • Condit R, Pitman N, Leigh Jr EG, Chave J, Terborgh J, Foster RB, Nuñez P, Aguilar S, Valencia R, Villa G, Muller-Landau HC, Losos E, Hubbell SP (2002) Beta-diversity in tropical forest trees. Science 295:666–669

    Article  PubMed  CAS  Google Scholar 

  • Cornell HV, Hawkins BA, Hochberg ME (1998) Towards an empirically based theory of herbivore demography. Ecol Entomol 23:340–349

    Article  Google Scholar 

  • Cyr H, Pace ML (1993) Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. Nature 361:148–150

    Article  Google Scholar 

  • Denno RF, Fagan WF (2003) Might nitrogen limitation promote omnivory among carnivorous arthropods. Ecology 84:2522–2531

    Article  Google Scholar 

  • Downing JA, Osenberg CW, Sarnelle O (1999) Meta-analysis of marine nutrient-enrichment experiments: variation in the magnitude of nutrient limitation. Ecology 80:1157–1167

    Google Scholar 

  • Erickson AA, Saltis M, Bell SS, Dawes CJ (2003) Herbivore feeding preferences as measured by leaf damage and stomatal ingestion: a mangrove crab example. J Exp Mar Biol Ecol 289:123–138

    Article  Google Scholar 

  • Farnsworth EJ (1998) Issues of spatial, taxonomic and temporal scale in delineating links between mangrove diversity and ecosystem function. Glob Ecol Biogeogr 7:15–25

    Article  Google Scholar 

  • Farnsworth EJ, Ellison AM (1991) Patterns of herbivory in Belizean mangrove swamps. Biotropica 23:555–567

    Article  Google Scholar 

  • Farnsworth EJ, Ellison AM (1993) Dynamics of herbivory in Belizean mangal. J Trop Ecol 9:435–455

    Article  Google Scholar 

  • Feller IC (1995) Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecol Monogr 65:477–505

    Article  Google Scholar 

  • Feller IC (2002) The role of herbivory by wood-boring insects in mangrove ecosystems in Belize. Oikos 97:167–176

    Article  Google Scholar 

  • Feller IC, Mathis WN (1997) Primary herbivory by wood-boring insects along a tree-height architectural gradient of Rhizophora mangle L. in Belizean mangrove swamps. Biotropica 29:440–451

    Article  Google Scholar 

  • Feller IC, McKee KL (1999) Light-gap creation in a Belizean red-mangrove forest by a wood-boring insect. Biotropica 31:607–617

    Article  Google Scholar 

  • Feller IC, Lovelock CE, McKee KL (2007) Nutrient addition differentially affects ecological processes of Avicennia germinans in nitrogen versus phosphorus limited mangrove ecosystems. Ecosystems (in press)

  • Feller IC, McKee KL, Whigham DF, O’Neill JP (2003) Nitrogen versus phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry 62:145–175

    Article  CAS  Google Scholar 

  • Feller IC, Whigham DF, O’Neill JP, McKee KL (1999) Effects of nutrient enrichment on within-stand nutrient cycling in mangrove ecosystems in Belize. Ecology 80:2193–2205

    Google Scholar 

  • Forkner RE, Hunter MD (2000) What goes up must come down? Nutrient addition and predation pressure on oak herbivores. Ecology 81:1588–1600

    Google Scholar 

  • Forrester GE, Dudley TL, Grimm NB (1999) Trophic interactions in open systems: effects of predators and nutrients on stream food chains. Limnol Oceanogr 44:1187–1197

    Article  Google Scholar 

  • Fraser LH, Grime JP (1998) Top-down control and its effect on the biomass and composition of three grasses at high and low soil fertility in outdoor microcosms. Oecologia 113:239–246

    Article  Google Scholar 

  • Fraser LH (1998) Top-down versus bottom-up control influenced by productivity in a north Derbyshire, UK, dale. Oikos 81:99–108

    Article  Google Scholar 

  • Fukui A (2001) Indirect interactions mediated by leaf shelters in animal-plant communities. Popul Ecol 43:31–40

    Article  Google Scholar 

  • Gill AM, Tomlinson PB (1969) Studies on the growth of red mangrove (Rhizophora mangle L.). 1. Habit and general morphology. Biotropica 1:1–9

    Article  Google Scholar 

  • Golley FB, McGinnis JT, Clements RG, Child GI, Duever MJ (1975) Mineral cycling in a tropical moist forest ecosystem. University of Georgia Press, Ga.

  • Goranson CE, Ho K, Pennings SC (2004) Environmental gradients and herbivore feeding preferences in coastal salt marshes. Oecologia 140:591–600

    Article  PubMed  Google Scholar 

  • Hochuli DF (2001) Insect herbivory and ontogeny: How do growth and development influence feeding behaviour, morphology and host use? Aust Ecol 26:563–570

    Article  Google Scholar 

  • Holmer M, Andersen FØ, Holmboe N, Kristensen E, Thongtham N (1999) Transformation and exchange processes in the Bang rong mangrove forest-seagrass bed system, Thailand: seasonal variations in benthic primary production and nutrient dynamics. Aquat Microb Ecol 20:203–212

    Google Scholar 

  • Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732

    Google Scholar 

  • Landsberg J, Ohmart C (1989) Levels of insect defoliation in forests: patterns and concepts. Trends Ecol Evol 4:96–100

    Article  Google Scholar 

  • Lovelock CE, Feller IC, McKee KL, Engelbrecht BMJ, Ball MC (2004) The effect of nutrient enrichment on growth, photosynthesis and hydraulic conductance of dwarf mangroves in Panamá. Funct Ecol 18:25–33

    Article  Google Scholar 

  • Lovett GM, Jones CG, Turner MG, Weathers KC (2005) Ecosystem function in heterogeneous landscapes. Springer, New York

    Google Scholar 

  • Lugo AE (1997) Old-growth mangrove forests in the United States. Conserv Biol 11:11–20

    Article  Google Scholar 

  • Lugo AE, Snedaker SC (1974) The ecology of mangroves. Annu Rev Ecol Syst 5:39–64

    Article  Google Scholar 

  • Macintyre IG, Toscano MA, Bond GB (2004) Modern sedimentary environments, Twin Cays, Belize, Central America. Atoll Res Bull 509:12

    Google Scholar 

  • McKee KL (1993) Soil physiochemical patterns and mangrove species distribution: reciprocal effects. J Ecol 81:477–487

    Article  Google Scholar 

  • McKee KL (1995) Seedling recruitment patterns in a Belizean mangrove forest: effects of establishment ability and physico-chemical factors. Oecologia 101:448–460

    Article  Google Scholar 

  • McKee KL, Cahoon C, Feller IC (in press) Caribbean mangroves adjust to rising sea-level through biotic controls on soil elevation change. Glob Ecol Biogeogr

  • McKee KL, Feller IC, Popp M, Wanek W (2002) Mangrove isotopic fractionation (δ15N and δ13C) across a nitrogen versus phosphorus limitation gradient. Ecology 83:1065–1075

    Google Scholar 

  • McKeon CS, Feller IC (2004) The supratidal fauna of Twin Cays, Belize. Atoll Res Bull 526:22

    Google Scholar 

  • Moon DC, Stiling P (2002) The influence of species identity and herbivore feeding mode on top-down and bottom-up effects in a saltmarsh system. Oecologia 133:243–253

    Article  Google Scholar 

  • Morin PJ (2000) Biodiversity’s ups and downs. Nature 406:263–264

    Article  CAS  Google Scholar 

  • National Research Council (NRC) (2001) Grand challenges in environmental science. National Academy Press, Washington, D.C.

    Google Scholar 

  • Odum WE, EJ Heald (1975) The detritus-based food web of an estuarine mangrove community. In: Cronin LE(ed) Estuarine research. Academic Press, New York, pp 265–286

    Google Scholar 

  • Onuf CP, Teal JM, Valiela I (1977) Interactions of nutrients, plant growth and herbivory in a mangrove ecosystem. Ecology 58:514–526

    Article  Google Scholar 

  • Pedigo LP, Hutchins SH, Higley LG (1986) Economic injury levels in theory and practice. Annu Rev Entomol 31:341–368

    Article  Google Scholar 

  • Peterson RKD, LG Higley (2000) Biotic stress and yield loss. CRC, Boca Raton, Fla.

  • Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316

    Article  Google Scholar 

  • Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251

    Article  Google Scholar 

  • Risley LS, Crossley Jr DA (1988) Herbivore-caused greenfall in the southern Appalachians. Ecology 69:1118–1127

    Article  Google Scholar 

  • Rodriguez W, Feller IC (2004) Mangrove landscape characterization and change in Twin Cays, Belize using aerial photography and IKONOS satellite data. Atoll Res Bull 513:22

    Google Scholar 

  • Rützler K, Goodbody I, Diaz MC, Feller IC, Macintyre IG (2004) The aquatic environment of Twin Cays, Belize. Atoll Res Bull 512:31

    Google Scholar 

  • Schade J, Kyle M, Hobbie S, Fagan W, Elser JJ (2003) Stoichiometric tracking of soil nutrients by a desert insect herbivore. Ecol Lett 6:96–101

    Article  Google Scholar 

  • Silver WL, Scatena FN, Johnson AH, Siccama TG, Sanchez MJ (1994) Nutrient availability in a montane wet tropical forest: spatial patterns and methodological considerations. Plant Soil 164:129–145

    Article  CAS  Google Scholar 

  • Sollins P (1998) Factors influencing species composition in tropical lowland rain forest: does soil matter? Ecology 79:23–30

    Article  Google Scholar 

  • Stiling P, Rossi AM (1997) Experimental manipulations of top-down and bottom-up factors in a tri-trophic system. Ecology 78:1602–1606

    Google Scholar 

  • Stiling P, Moon DC (2005) Quality or quantity: the direct and indirect effects of host plants on herbivores and their natural enemies. Oecologia 142:413–420

    Article  PubMed  Google Scholar 

  • Thies C, Steffan-Dewenter I, Tscharntke T (2003) Effects of landscape context on herbivory and parasitism at different spatial scales. Oikos 101:18–25

    Article  Google Scholar 

  • Valiela I, Rutecki D, Fox S (2004) Salt marshes: biological controls of food webs in a diminishing environment. J Exp Mar Biol Ecol 300:131–159

    Article  Google Scholar 

  • WagnerDL, Loose JL, Fitzgerald TD, De Benedictis JA, Davis DR (2000) A hidden past: the hypermetamorphic development of Marmara arbutiella (Lepidoptera: Gracillariidae). Ann Entomol Soc Am 93:59–64

    Article  Google Scholar 

  • Warner GF (1967) The life-history of the mangrove tree crab, Aratus pisonii. J Zool 153:321–335

    Article  Google Scholar 

  • Wiens JA (1989) Spatial scaling in ecology. Funct Ecol 3:385–397

    Article  Google Scholar 

  • Wiens JA, Schooley RL, Weeks RD Jr (1997) Patchy landscapes and animal movements: do beetles percolate? Oikos 78:257–264

    Article  Google Scholar 

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Acknowledgements

We thank the following: the Government of Belize for permission to use study sites at Twin Cays; Don Davis and Marc Epstein for identification of Lepidoptera; Claudette DeCourley and Rachel Borgatti for assistance in the field; and Rainer Feller for image analyses. Financial support was provided by the National Science Foundation DEB-9981535 and the Caribbean Coral Reef Ecosystems Program (contribution no. 799).

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  1. Smithsonian Environmental Research Center, 647 Contees Wharf Road, Edgewater, MD, 21037, USA

    Ilka C. Feller & Anne Chamberlain

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  1. Ilka C. Feller
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  2. Anne Chamberlain
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Correspondence to Ilka C. Feller.

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Communicated by Marilyn Ball.

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Feller, I., Chamberlain, A. Herbivore responses to nutrient enrichment and landscape heterogeneity in a mangrove ecosystem. Oecologia 153, 607–616 (2007). https://doi.org/10.1007/s00442-007-0760-9

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