Oecologia

, Volume 167, Issue 4, pp 1141–1149 | Cite as

Effects of manipulated herbivore inputs on nutrient flux and decomposition in a tropical rainforest in Puerto Rico

  • T. D. Schowalter
  • S. J. Fonte
  • J. Geaghan
  • J. Wang
Ecosystem ecology - Original Paper

Abstract

Forest canopy herbivores are known to increase rates of nutrient fluxes to the forest floor in a number of temperate and boreal forests, but few studies have measured effects of herbivore-enhanced nutrient fluxes in tropical forests. We simulated herbivore-induced fluxes in a tropical rainforest in Puerto Rico by augmenting greenfall (fresh foliage fragments), frassfall (insect feces), and throughfall (precipitation enriched with foliar leachates) in replicated experimental plots on the forest floor. Background rates of greenfall and frassfall were measured monthly using litterfall collectors and augmented by adding 10× greenfall or 10× frassfall to designated plots. Throughfall fluxes of NH4, NO3 and PO4 (but not water) were doubled in treatment plots, based on published rates of fluxes of these nutrients in throughfall. Control plots received only background flux rates for these compounds but the same minimum amount of distilled water. We evaluated treatment effects as changes in flux rates for NO3, NH4 and PO4, measured as decomposition rate of leaf litter in litterbags and as adsorption in ion-exchange resin bags at the litter–soil interface. Frass addition significantly increased NO3 and NH4 fluxes, and frass and throughfall additions significantly reduced decay rate, compared to controls. Reduced decay rate suggests that nitrogen flux was sufficient to inhibit microbial decomposition activity. Our treatments represented fluxes expected from low–moderate herbivore outbreaks and demonstrated that herbivores, at these outbreak levels, increase ecosystem-level N and P fluxes by >30% in this tropical rainforest.

Keywords

Herbivory Decomposition Nutrient flux Litterfall Puerto Rico 

Notes

Acknowledgments

N.V.L. Brokaw, S.K. Chapman and M.D. Lowman provided helpful comments on the manuscript. H. Bruce Rinker assisted with litterbag processing. M.D. Hunter, Institute of Ecology Analytical Chemistry Laboratory, University of Georgia analyzed nutrients in the resin bags. Q. Qi assisted with statistical analyses. This research was supported by NSF Grant DEB-9815133, subcontract to Oregon State University, the Luquillo Experimental Forest LTER Site, and the Louisiana State University Agricultural Center. This manuscript is published with approval of the Director of the Louisiana Agricultural Experiment Station, as manuscript number 7316.

References

  1. Belovsky GE, Slade JB (2000) Insect herbivory accelerates nutrient cycling and increases plant production. Proc Natl Acad Sci USA 97:14412–14417PubMedCrossRefGoogle Scholar
  2. Binkley D, Matson P (1983) Ion exchange resin bag method for assessing forest soil nitrogen availability. Soil Sci Soc Am 47:1050–1052CrossRefGoogle Scholar
  3. Binkley D, Aber J, Pastor J, Nadelhoffer K (1986) Nitrogen availability in some Wisconsin forests: comparisons of resin bags and on-site incubations. Biol Fert Soils 2:77–82CrossRefGoogle Scholar
  4. Chapman SK, Hart SC, Cobb NS, Whitham TG, Koch GW (2003) Insect herbivory increases litter quality and decomposition: an extension of the acceleration hypothesis. Ecology 84:2867–2876CrossRefGoogle Scholar
  5. Christenson LM, Lovett GM, Mitchell MJ, Groffman PM (2002) The fate of nitrogen in gypsy moth frass deposited to an oak forest floor. Oecologia 131:444–452CrossRefGoogle Scholar
  6. Classen AT, Hart SC, Whitham TG, Cobb NS, Koch GW (2005) Insect infestations linked to changes in microclimate: important climate change implications. Soil Sci Soc Am 69:2049–2057CrossRefGoogle Scholar
  7. Coleman DC, Crossley DA Jr, Hendrix PF (2004) Fundamentals of soil ecology. Elsevier, San DiegoGoogle Scholar
  8. Coley PD, Aide TM (1991) Comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant–animal interactions: evolutionary ecology in tropical and temperate regions. Wiley, New York, pp 25–49Google Scholar
  9. Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335CrossRefGoogle Scholar
  10. Cuevas E, Lugo AE (1998) Dynamics of organic matter and nutrient return from litterfall in stands of ten tropical tree plantation species. For Ecol Manag 112:263–279CrossRefGoogle Scholar
  11. Distefano JF, Gholtz HL (1986) A proposed use of ion exchange resins to measure nitrogen mineralization and nitrification in intact soil cores. Commun Soil Sci Plant Anal 17:989–998CrossRefGoogle Scholar
  12. Edmisten J (1970) Soil studies in the El Verde rain forest. In: Odum HT, Pigeon RF (eds) A tropical rain forest. US Atomic Energy Commission, Oak Ridge, pp H-79–H-87Google Scholar
  13. Enriquez S, Duarte CM, Sand-Jensen K (1993) Patterns in decomposition rates among photosynthetic organisms: the importance of detritus C:N:P content. Oecologia 94:457–471CrossRefGoogle Scholar
  14. Fonte SJ, Schowalter TD (2004) Decomposition of greenfall vs. senescent foliage in a tropical forest ecosystem in Puerto Rico. Biotropica 36:474–482Google Scholar
  15. Fonte SJ, Schowalter TD (2005) The influence of a neotropical herbivore (Lamponius portoricensis) on nutrient cycling and soil processes. Oecologia 146:423–431PubMedCrossRefGoogle Scholar
  16. Frost CJ, Hunter MD (2004) Insect canopy herbivory and frass deposition affect soil nutrient dynamics and export in oak mesocosms. Ecology 85:3335–3347CrossRefGoogle Scholar
  17. Frost CJ, Hunter MD (2007) Recycling of nitrogen in herbivore feces: plant recovery, herbivore assimilation, soil retention, and leaching losses. Oecologia 151:42–53PubMedCrossRefGoogle Scholar
  18. Frost CJ, Hunter MD (2008) Insect herbivores and their frass affect Quercus rubra leaf quality and initial stages of subsequent decomposition. Oikos 117:13–22CrossRefGoogle Scholar
  19. Greenberg AE, Clesceri LS, Eaton AD (1992) Standard methods for the examination of water and wastewater, 18th edn. American Public Health Association, Washington, DC, pp 4-91–4-92Google Scholar
  20. Herbert DA, Fownes JH, Vitousek PM (1999) Hurricane damage to a Hawaiian forest: nutrient supply rate affects resistance and resilience. Ecology 80:908–920CrossRefGoogle Scholar
  21. Hobbie SE (2005) Contrasting effects of substrate and fertilizer nitrogen on the early stages of litter decomposition. Ecosystems 8:644–656CrossRefGoogle Scholar
  22. Hollinger DY (1986) Herbivory and the cycling of nitrogen and phosphorus in isolated California oak trees. Oecologia 70:291–297CrossRefGoogle Scholar
  23. Hunt HW, Ingham ER, Coleman DC, Elliott ET, Reid CPP (1988) Nitrogen limitation of production and decomposition in prairie, mountain meadow, and pine forest. Ecology 69:1009–1016CrossRefGoogle Scholar
  24. Hunter MD, Linnen CR, Reynolds BC (2003) Effects of endemic densities of canopy herbivores on nutrient dynamics along a gradient in elevation in the southern Appalachians. Pedobiologia 47:231–244CrossRefGoogle Scholar
  25. Kimmins JP (1972) Relative contributions of leaching, litter-fall and defoliation by Neodiprion sertifer (Hymenoptera) to the removal of cesium-134 from red pine. Oikos 23:226–234CrossRefGoogle Scholar
  26. Kolb TE, Dodds KA, Clancy KM (1999) Effect of western spruce budworm defoliation on the physiology and growth of potted Douglas-fir seedlings. For Sci 45:280–291Google Scholar
  27. Lawrence WT Jr (1996) Plants: the food base. In: Reagan DP, Waide JB (eds) The food web of a tropical rain forest. University of Chicago Press, Chicago, pp 15–51Google Scholar
  28. le Mellec A, Habermann M, Michalzik B (2009) Canopy herbivory altering C to N ratios and soil input patterns of different organic matter fractions in a Scots pine forest. Plant Soil 325:255–262CrossRefGoogle Scholar
  29. Lodge DJ (1996) Microorganisms. In: Reagan DP, Waide JB (eds) The food web of a tropical rain forest. University of Chicago Press, Chicago, pp 53–108Google Scholar
  30. Lodge DJ, Scatena FN, Asbury CE, Sanchez MJ (1991) Fine litterfall and related nutrient inputs resulting from hurricane Hugo in subtropical wet and lower montane rain forests of Puerto Rico. Biotropica 23:336–342CrossRefGoogle Scholar
  31. Lodge DJ, McDowell WH, Macy J, Ward SK, Leisso R, Claudio-Campos K, Kuhnert K (2008) Distribution and role of mat-forming saprobic basidiomycetes in a tropical forest. In: Boddy L, Frankland JC (eds) Ecology of saprobic basidiomycetes. Elsevier, Amsterdam, pp 195–208Google Scholar
  32. Lovett GM, Ruesink AE (1995) Carbon and nitrogen mineralization from decomposing gypsy moth frass. Oecologia 104:133–138CrossRefGoogle Scholar
  33. Lowman MD (1984) An assessment of techniques for measuring herbivory: is rainforest defoliation more intense than we thought? Biotropica 16:264–268CrossRefGoogle Scholar
  34. Marschner H (1995) The mineral nutrition of higher plants, 2nd edn. Academic, San DiegoGoogle Scholar
  35. Mattson WJ, Haack RA (1987) The role of drought in outbreaks of plant-eating insects. Bioscience 37:110–118CrossRefGoogle Scholar
  36. McDowell WH (1998) Internal nutrient fluxes in a Puerto Rican rain forest. J Trop Ecol 14:521–536CrossRefGoogle Scholar
  37. McDowell WH, Estrada-Pinto A (1988) Rainfall at El Verde Field Station, 1964–1986. US Department of Energy, Technical Report CEER-T-228, Center for Energy and Environmental Research, San Juan, Puerto RicoGoogle Scholar
  38. McGroddy ME, Silver WL, de Oliveira RC Jr (2004) The effect of phosphorus availability on decomposition dynamics in a seasonal lowland Amazonian forest. Ecosystems 7:172–179CrossRefGoogle Scholar
  39. Mizutani M, Hijii N (2001) Mensuration of frass drop for evaluating arthropod biomass in canopies: a comparison among Cryptomeria japonica, Larix kaempferi, and deciduous broad-leaved trees. For Ecol Manag 154:327–335CrossRefGoogle Scholar
  40. Odum HT, Ruíz-Reyes J (1970) Holes in leaves and the grazing control mechanism. In: Odum HT, Pigeon RF (eds) A tropical rain forest. US Atomic Energy Commission, Oak Ridge, pp I-69–I-80Google Scholar
  41. Olson JS (1963) Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44:322–331CrossRefGoogle Scholar
  42. Ovington JD, Olson JS (1970) Biomass and chemical content of El Verde lower montane rain forest plants. In: Odum HT, Pigeon RF (eds) A tropical rain forest. US Atomic Energy Commission, Oak Ridge, H-53–H-77Google Scholar
  43. Prather CM (2010) Invertebrate consumer influences on ecosystem processes in a rainforest understory. PhD Dissertation, University of Notre Dame, South BendGoogle Scholar
  44. Reagan DP, Waide JB (eds) (1996) The food web of a tropical rain forest. University of Chicago Press, ChicagoGoogle Scholar
  45. Reynolds BC, Hunter MD (2001) Responses of soil respiration, soil nutrient, and litter decomposition to inputs from canopy herbivores. Soil Biol Biochem 33:1641–1652CrossRefGoogle Scholar
  46. Risley LS, Crossley DA Jr (1988) Herbivore-caused greenfall in the southern Appalachians. Ecology 69:1118–1127CrossRefGoogle Scholar
  47. Risley LS, Crossley DA Jr (1993) Contribution of herbivore-caused greenfall to litterfall nitrogen flux in several southern Appalachian forested watersheds. Am Midl Nat 129:67–74CrossRefGoogle Scholar
  48. SAS Institute (2004) SAS OnlineDoc® 9.1.3. SAS Institute, CaryGoogle Scholar
  49. Schowalter TD, Crossley DA Jr (1983) Forest canopy arthropods as sodium, potassium, magnesium and calcium pools in forests. For Ecol Manag 7:143–148CrossRefGoogle Scholar
  50. Schowalter TD, Ganio LM (1999) Invertebrate communities in a tropical rain forest canopy in Puerto Rico following Hurricane Hugo. Ecol Entomol 24:1–11CrossRefGoogle Scholar
  51. Schowalter TD, Ganio LM (2003) Diel, seasonal and disturbance-induced variation in invertebrate assemblages. In: Basset Y, Novotny V, Miller SE, Kitching RL (eds) Arthropods of tropical forests. Cambridge University Press, Cambridge, pp 315–328Google Scholar
  52. Schowalter TD, Sabin TE, Stafford SG, Sexton JM (1991) Phytophage effects on primary production, nutrient turnover, and litter decomposition of young Douglas-fir in Western Oregon. For Ecol Manag 42:229–243CrossRefGoogle Scholar
  53. Seastedt TR, Tate CM (1981) Decomposition rates and nutrient contents of arthropod remains in forest litter. Ecology 62:13–19CrossRefGoogle Scholar
  54. Seastedt TR, Crossley DA Jr, Hargrove WW (1983) The effects of low-level consumption by canopy arthropods on the growth and nutrient dynamics of black locust and red maple trees in the southern Appalachians. Ecology 64:1040–1048CrossRefGoogle Scholar
  55. 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 164:129–145CrossRefGoogle Scholar
  56. Throop HL, Holland EA, Parton WJ, Ojima DS, Keough CA (2004) Effects of nitrogen deposition and insect herbivory on patterns of ecosystem-level carbon and nitrogen dynamics: results from the CENTURY model. Glob Change Biol 10:1092–1105CrossRefGoogle Scholar
  57. Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120PubMedCrossRefGoogle Scholar
  58. Trumble JT, Kolodny-Hirsch DM, Ting IP (1993) Plant compensation for arthropod herbivory. Annu Rev Entomol 38:93–119CrossRefGoogle Scholar
  59. Van Bael SA, Aiello A, Valderrama A, Medianero E, Samaniego M, Wright SJ (2004) General herbivore outbreak following an El Niño-related drought in a lowland Panamanian forest. J Trop Ecol 20:625–633CrossRefGoogle Scholar
  60. Waide JB, Reagan DP (1996) The Rain Forest Setting. In: Reagan DP, Waide JB (eds) The food web of a tropical rain forest. University of Chicago Press, Chicago, pp 1–16Google Scholar
  61. Waldrop MP, Zak DR, Sinsabaugh L, Gallo M, Lauber C (2004) Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecol Appl 14:1172–1177CrossRefGoogle Scholar
  62. Whigham DF, Olmsted I, Cabrera E, Harmon ME (1991) The impact of hurricane Gilbert on trees, litterfall, and woody debris in a dry tropical forest in the northeastern Yucatan Peninsula. Biotropica 23:434–441CrossRefGoogle Scholar
  63. Wiegert RG (1970) Effects of ionizing radiation on leaf fall, decomposition, and litter microarthropods of a montane rain forest. In: Odum HT, Pigeon RF (eds) A tropical rain forest. US Atomic Energy Commission, Oak Ridge, H-89–H-100Google Scholar
  64. Wood TE, Lawrence D, Clark DA, Chazdon RL (2009) Rain forest nutrient cycling and productivity in response to large-scale litter manipulation. Ecology 90:109–121PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • T. D. Schowalter
    • 1
  • S. J. Fonte
    • 2
  • J. Geaghan
    • 3
  • J. Wang
    • 3
  1. 1.Department of EntomologyLouisiana State University Agricultural CenterBaton RougeUSA
  2. 2.Tropical Soil Biology and Fertility Program (Latin America and Caribbean Region), International Center for Tropical AgricultureCaliColombia
  3. 3.Department of Experimental StatisticsLouisiana State UniversityBaton RougeUSA

Personalised recommendations