, Volume 16, Issue 7, pp 1203–1215 | Cite as

Latitudinal Patterns of Herbivory in Mangrove Forests: Consequences of Nutrient Over-Enrichment

  • Ilka C. FellerEmail author
  • Anne H. Chamberlain
  • Cyril Piou
  • Samantha Chapman
  • Catherine E. Lovelock


Ecosystems in the tropics are predicted to have stronger responses to nutrient enrichment, greater diversity, and more intense biotic interactions than in temperate areas. Mangrove forests, which occur across a broad biogeographic range from warm temperate to tropical, provide a unique opportunity to test these hypotheses by investigating the responses of herbivores to nutrient enrichment in temperate versus tropical latitudes. Mangroves are complex intertidal ecosystems with spatial differences in structure and diversity along tidal gradients and are threatened globally by human activities including nutrient over-enrichment. In this study, we used long-term fertilization experiments at the Indian River Lagoon, FL; Twin Cays, Belize; and Bocas del Toro, Panamá to determine how increased nutrients impact herbivore abundance and herbivory of Rhizophora mangle at the tree, forest, and regional scales. At these locations, which span approximately 2185 km and 18.4º of latitude, we fertilized individual trees with one of three treatments (Control, +N, +P) in two zones (fringe, scrub) along transects perpendicular to the shoreline and measured their responses for 4 years. Herbivory was measured as folivory, loss of yield, and tissue mining. Although nutrient enrichment altered plant growth, leaf traits, and nutrient dynamics, these variables had little effect on folivory at any location. Our results did not support the prediction that herbivory and per capita consumption are greatest at the most tropical location. Instead, folivory was highest at the most temperate location and lowest at the intermediate location. Folivory was generally higher in the fringe than in the scrub zone, but the pattern varied by location, herbivore, and nutrient treatment. Folivory by a dominant herbivore, Aratus pisonii, decreased from the highest to the lowest latitude. Our data suggest that factors controlling population dynamics of A. pisonii cascade to the mangrove canopy, linking herbivory to crab densities.


Aratus pisonii Ecdytolopha herbivory loss of yield mangrove Marmara nitrogen phosphorus Rhizophora mangle latitude nutrient enrichment 



We thank the Smithsonian Marine Science Network for funding and the staffs of the Smithsonian Marine Station in Fort Pierce (SMS), the Smithsonian Marine Field Station in Belize (CCRE), and the Smithsonian Marine Laboratory in Bocas del Toro, Panamá for logistical and field support. This material is based upon work supported by the National Science Foundation (DEB9981535, EF1065821) and the Australian Research Council (DP0879354 and DP0986179). We also thank the governments of Belize and Panamá for permission to use study sites at Twin Cays and Bocas del Toro. This is CCRE Contribution No. 936 and SMS Contribution No. 906.

Supplementary material

10021_2013_9678_MOESM1_ESM.docx (57 kb)
Supplementary material 1 (DOCX 56 kb)
10021_2013_9678_MOESM2_ESM.tif (2 mb)
Figure B1. The three study sites used in this study span a latitudinal gradient of more than 18° in the Atlantic-East Pacific Region from the Indian River Lagoon (IRL), Florida to Twin Cays, Belize, and to Bocas del Toro, Panamá. Supplementary material 2 (TIFF 2058 kb)
10021_2013_9678_MOESM3_ESM.tif (332 kb)
Figure B2. Mangrove forests at each of our study sites were dominated by Rhizophora mangle and were characterized by distinctive tree-height gradient with tall trees fringing the shoreline and stunted scrub trees in the interior. Supplementary material 3 (TIFF 331 kb)


  1. Adams JM, Zhang Y. 2009. Is there more insect folivory in warmer temperate climates? A latitudinal comparison of insect folivory in eastern North America. J Ecol 97:933–40.CrossRefGoogle Scholar
  2. Andrews NR, Hughes L. 2005. Herbivore damage along a latitudinal gradient: relative impacts of different feeding guilds. Oikos 108:176–82.CrossRefGoogle Scholar
  3. Beever JW, Simberloff D, King LL. 1979. Herbivory and predation by the mangrove tree crab Aratus pisonii. Oecologia 43:317–28.CrossRefGoogle Scholar
  4. Cannicci S, Burrows D, Fratini S, Smith TJIII, Offenberg J, Dahdouh-Guebas F. 2008. Faunal impact on vegetation structure and ecosystem function in mangrove forests: a review. Aquat Bot 89:186–200.CrossRefGoogle Scholar
  5. Chapman VJ. 1984. Mangrove biogeography. In: Por FD, Dor I, Eds. Hydrobiology of the Mangal: the ecosystem of the Mangrove forests. The Hague: Dr. W. Junk Publishers. p 15–24.Google Scholar
  6. Corredor JE, Howarth RW, Twilley RR, Morell JM. 1999. Nitrogen cycling and anthropogenic impact in the tropical interamerican seas. Biogeochemistry 46:163–78.Google Scholar
  7. del-Val E, Armesto JJ. 2010. Seedling mortality and herbivory damage in subtropical and temperate populations: testing the hypothesis of higher herbivore pressure toward the tropics. Biotropica 42:174–9.CrossRefGoogle Scholar
  8. Downing JA, Osenberg CW, Sarnelle O. 1999. Meta-analysis of marine nutrient-enrichment experiments: variation in the magnitude of nutrient limitation. Ecology 80:1157–67.CrossRefGoogle Scholar
  9. Duke NC. 1992. Mangrove floristics and biogeography. In: Robertson AI, Alongi DM, Eds. Tropical mangrove ecosystems. Coastal and Estuarine Studies 41. Washington, DC: American Geophysical Union. p 63–100.CrossRefGoogle Scholar
  10. Dyer LA, Singer MS, Lill JT, Stireman JO, Gentry GL, Marquis RJ, Ricklefs RE, Greeney HF, Wagner DL, Morais HC, Diniz IR, Kursar TA, Coley PD. 2007. Host specificity of Lepidoptera in tropical and temperate forests. Nature 448:696–9.PubMedCrossRefGoogle Scholar
  11. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JY, Seabloom EW, Shurin JB, Smith JE. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater marine and terrestrial ecosystems. Ecol Lett 10:1135–42.PubMedCrossRefGoogle Scholar
  12. 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 289:123–38.CrossRefGoogle Scholar
  13. Erickson AA, Feller IC, Paul VJ, Kwiatkowski LM, Lee W. 2008. Selection of an omnivorous diet by the mangrove tree crab Aratus pisonii. J Sea Res 59:59–69.CrossRefGoogle Scholar
  14. Farnsworth EJ, Ellison AM. 1997. Global patterns of pre-dispersal propagule predation in mangrove forests. Biotropica 29:318–30.CrossRefGoogle Scholar
  15. Feller IC. 1995. Effects of nutrient enrichment on growth and herbivory in dwarf red mangrove (Rhizophora mangle). Ecol Monogr 65:477–505.CrossRefGoogle Scholar
  16. Feller IC. 2002. The role of herbivory by wood-boring insects in mangrove ecosystems in Belize. Oikos 97:167–76.CrossRefGoogle Scholar
  17. Feller IC, Chamberlain AH. 2007. Herbivore responses to nutrient enrichment and landscape heterogeneity in a mangrove ecosystem. Oecologia 153:607–16.PubMedCrossRefGoogle Scholar
  18. Feller IC, Lovelock CE, McKee KL. 2007. Nutrient addition differentially affects ecological processes of Avicennia germinans in nitrogen vs. phosphorus limited mangrove ecosystems. Ecosystems 10:347–59.CrossRefGoogle Scholar
  19. Feller IC, Lovelock CE, Piou C. 2009. Growth and nutrient conservation in Rhizophora mangle in response to fertilization along latitudinal and tidal gradients. Smithson Contrib Mar Sci 38:345–58.Google Scholar
  20. Grime JP, Campbell BD. 1991. Growth rate habitat productivity and plant strategy as predictors of stress response. In: Mooney HA et al., Eds. Response of plants to multiple stresses. San Diego: Academic Press. p 143–61.CrossRefGoogle Scholar
  21. Gruner DS, Smith JE, Seabloom EW, Sandin SA, Ngai JT, Hillebrand H, Harpole WS, Elser JJ, Cleland EE, Bracken JES, Borer ET, Bolker BM. 2008. A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecol Lett 11:740–55.PubMedCrossRefGoogle Scholar
  22. Hallam A, Read J. 2006. Do tropical species invest more in anti-herbivore defence than temperate species? A test in Eucryphia (Cunoniaceae) in eastern Australia. J Trop Biol 22:41–51.Google Scholar
  23. Hillebrand H. 2004. On the generality of the latitudinal diversity gradient. Am Nat 163:192–211.PubMedCrossRefGoogle Scholar
  24. Krauss KW, Lovelock CE, McKee KL, López-Hoffman L, Ewe SML, Sousa WP. 2008. Environmental drivers in mangrove establishment and early development: a review. Aquat Bot 89:105–27.CrossRefGoogle Scholar
  25. Lovelock CE, Feller IC, McKee KL, Thompson R. 2005. Forest structure of the extensive Caribbean mangrove forests of Bocas del Toro Panama. Carib J Sci 41:456–64.Google Scholar
  26. Lovelock CE, Feller IC, Ball MC, Engelbrecht BMJ, Ewe ML. 2006. Differences in plant function in phosphorus and nitrogen limited mangrove ecosystems. New Phytol 172:514–22.PubMedCrossRefGoogle Scholar
  27. Lovelock CE, Feller IC, Ball MC, Ellis J, Schwarz AM, Sorrell B. 2007. Growth rate hypothesis vs geochemical hypothesis for variation in plant nutrients over latitude: a test using mangroves. Ecol Lett 10:1154–63.PubMedCrossRefGoogle Scholar
  28. Lugo AE, Snedaker SC. 1974. The ecology of mangroves. Annu Rev Ecol Syst 5:39–64.CrossRefGoogle Scholar
  29. MacArthur RH. 1972. Geographical ecology: patterns in the distribution of species. New York: Harper and Row.Google Scholar
  30. Mattson WJ. 1980. Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–61.CrossRefGoogle Scholar
  31. McKee KL, Cahoon D, Feller IC. 2007. Caribbean mangroves adjust to rising sea-level through biotic controls on soil elevation change. Glob Ecol Biogeogr 16:546–56.CrossRefGoogle Scholar
  32. Novotny V, Drozd P, Miller SE, Kulfan M, Janda M, Basset Y, Weiblen GD. 2006. Why are there so many species of herbivorous insects in tropical rainforests? Science 313:1115–18.PubMedCrossRefGoogle Scholar
  33. Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. 2009. Vegan: Community ecology package.
  34. Olmos F, Silva e Silva RS, Prado A. 2001. Breeding season diet of scarlet ibises and little blue herons in a Brazilian mangrove swamp. Waterbirds 24:50–7.Google Scholar
  35. Onuf CP, Teal JM, Valiela I. 1977. Interactions of nutrients plant growth and herbivory in a mangrove ecosystem. Ecology 58:514–26.CrossRefGoogle Scholar
  36. Pennings SC, Silliman BR. 2005. Linking biogeography and community ecology: latitudinal variation in plant–herbivore interaction strength. Ecology 86:2310–19.CrossRefGoogle Scholar
  37. Pennings SC, Zimmer M, Dias N, Sprung M, Davé N, Ho CK, Kunza A, McFarlin C, Mews M, Pfauder A, Salgado CS. 2007. Latitudinal variation in plant–herbivore interactions in European salt marshes. Oikos 116:543–6.Google Scholar
  38. Pennings SC, Ho CK, Salgado CS, Więski K, Davé D, Kunza AE, Wason EL. 2009. Latitudinal variation in herbivore pressure in Atlantic Coast salt marshes. Ecology 90:183–95.PubMedCrossRefGoogle Scholar
  39. Petersen RKD, Higley LG. 2001. Biotic stress and yield loss. Boca Raton: CRC Press.Google Scholar
  40. R Development Core Team. 2009. R: A Language and Environment for Statistical Computing.Google Scholar
  41. Reich PB, Oleksyn J. 2004. Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101:11001–6.PubMedCrossRefGoogle Scholar
  42. Rivera-Monroy VH, Twilley RR, Bone D, Childers DL, Coronado-Molina C, Feller IC, Herrera-Silveira J, Jaffe R, Mancera E, Rejmankova E, Salisbury JE, Weil E. 2004. A biogeochemical conceptual framework to develop long term ecological research and sustain coastal management in the wider Caribbean Region. Bioscience 54:843–56.CrossRefGoogle Scholar
  43. Salgado CS, Pennings SC. 2005. Latitudinal variation in palatability of salt-marsh plants: are differences constitutive? Ecology 86:1571–9.CrossRefGoogle Scholar
  44. Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Roy K. 2009. Is there a latitudinal gradient in the importance of biotic interactions? Annu Rev Ecol Evol Syst 40:245–69.CrossRefGoogle Scholar
  45. Schowalter TD, Hargrove WW, Crossley DA, Jr. 1986. Herbivory in forested ecosystems. Annu Rev Entomol 31:177–96.Google Scholar
  46. Tomlinson PB. 1986. The botany of mangroves. Cambridge: Cambridge University Press.Google Scholar
  47. Vazquez E, Stevens RD. 2004. The latitudinal gradient in niche breadth: concepts and evidence. Am Nat 164:E1–19.PubMedCrossRefGoogle Scholar
  48. Venables WN, Ripley BD. 2002. Modern applied statistics with S. New York: Springer.CrossRefGoogle Scholar
  49. Warner GF. 1967. Life history of the mangrove tree crab Aratus pisonii. J Zool 153:321–35.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Ilka C. Feller
    • 1
    Email author
  • Anne H. Chamberlain
    • 1
  • Cyril Piou
    • 2
  • Samantha Chapman
    • 1
    • 3
  • Catherine E. Lovelock
    • 1
    • 4
  1. 1.Smithsonian Environmental Research CenterEdgewaterUSA
  2. 2.French Agricultural Research Centre for International Development CIRADUPR Bioagresseurs analyse et maîtrise du risqueMontpellierFrance
  3. 3.Department of BiologyVillanova UniversityVillanovaUSA
  4. 4.School of Biological SciencesUniversity of QueenslandSt. LuciaAustralia

Personalised recommendations