Abstract
A longstanding goal for ecologists is to understand the processes that maintain biological diversity in communities, yet few studies have investigated the combined effects of predators and resources on biodiversity in natural ecosystems. We fertilized nutrient limited plots and excluded insectivorous birds in a randomized block design, and examined the impacts on arthropods associated with the dominant tree in the Hawaiian Islands, Metrosideros polymorpha (Myrtaceae). After 33 months, the species load (per foliage mass) of herbivores and carnivores increased with fertilization, but rarified richness (standardized to abundance) did not change. Fertilization depressed species richness of arboreal detritivores, and carnivore richness dropped in caged, unfertilized plots, both because of the increased dominance of common, introduced species with treatments. Herbivore species abundance distributions were more equitable than other trophic levels following treatments, and fertilization added specialized native species without changing relativized species richness. Overall, bird removal and nutrient addition treatments on arthropod richness acted largely independently, but with countervailing influences that obscured distinct top-down and bottom-up effects on different trophic levels. This study demonstrates that species composition, biological invasions, and the individuality of species traits may complicate efforts to predict the interactive effects of resources and predation on species diversity in food webs.
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References
Abrams PA (1995) Monotonic or unimodal diversity–productivity gradients: what does competition theory predict?. Ecology 76:2019–2027
Anderson MJ (2000) DISTLM: a FORTRAN computer program to calculate a distance-based multivariate analysis for a linear model. Department of Statistics, University of Auckland, Auckland, New Zealand
Anderson MJ (2001a) Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci 58:626–639
Anderson MJ (2001b) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Anderson MJ (2003) CAP: a FORTRAN computer program for canonical analysis of principal coordinates. Department of Statistics, University of Auckland, Auckland, New Zealand
Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525
Baldwin PH (1953) Annual cycle, environment and evolution in the Hawaiian honeycreepers (Aves: Drepaniidae). Univ Calif Publ Zool 52:285–398
Basset Y, Springate ND, Aberlenc HP, Delvare G (1997) A review of methods for sampling arthropods in tree canopies. In: Stork NE, Adis J, Didham RK (eds) Canopy Arthropods. Chapman and Hall, London, pp 27–52
Basset Y, Novotný V, Miller SE, Kitching RL (2003) Arthropods of tropical forests: spatio-temporal dynamics and resource use in the canopy. Cambridge University Press, London
Cardinale BJ, Palmer MA, Ives AR, Brooks SS (2005) Diversity-productivity relationships in streams vary as a function of the natural disturbance regime. Ecology 86:716–726
Christiansen K, Bellinger P (1992) Insects of Hawaii, vol. 15: Collembola. University of Hawaii Press, Honolulu, Hawaii
Clarke KR (2001) PRIMER for Windows, Version 5.0. PRIMER-E, Plymouth, UK
Colwell RK (1997) Biota: the Biodiversity Database Manager, Version 1.0. Sinauer, Sunderland, Mass.
Cordell S, Goldstein G, Meinzer FC, Vitousek PM (2001) Morphological and physiological adjustment to N and P fertilization in nutrient-limited Metrosideros polymorpha canopy trees in Hawaii. Tree Physiol 21:43–50
Corn CA, Hiesey WM (1973) Altitudinal variation in Hawaiian Metrosideros. Am J Bot 60:991–1002
Cronin JT, Abrahamson WG (2001) Goldenrod stem galler preference and performance: effects of multiple herbivores and plant genotypes. Oecologia 127:87–96
Davis AJ, Lawton JH, Shorrocks B, Jenkinson LS (1998) Individualistic species responses invalidate simple physiological models of community dynamics under global environmental change. J Anim Ecol 67:600–612
Dawson JW, Stemmerman L (1999) Metrosideros Banks ex Gaertn. In: Wagner WL, Herbst DR, Sohmer SH (eds) Manual of the flowering plants of Hawaii, 2nd edn, vol 1. Bernice P Bishop Museum Press, Honolulu, HI, pp 964–970
De Angelis DL (1980) Energy flow, nutrient cycling, and ecosystem resilience. Ecology 61:764–771
Dickson LL, Whitham TG (1996) Genetically-based plant resistance traits affect arthropods, fungi, and birds. Oecologia 106:400–406
Duffy JE (2003) Biodiversity loss, trophic skew and ecosystem functioning. Ecol Lett 6:680–687
Dyer LA, Letourneau DK (2003) Top-down and bottom-up diversity cascades in detrital vs. living food webs. Ecol Lett 6:60–68
Fisher RA, Corbet AS, Williams CB (1943) The relation between the number of species and the number of individuals in a random sample of an animal population. J Anim Ecol 12:42–58
Foster JT (2005) Exotic bird invasion into forests of Hawaii: demography, competition, and seed dispersal. Dissertation, University of Illinois at Urbana-Champaign
Fretz JS (2000) Relationship of canopy arthropod prey to distribution and life history of the Hawai‘i ‘akepa. PhD Dissertation, University of Hawai‘i at Manoa, Honolulu, Hawaii
Fritz RS, Price PW (1988) Genetic variation among plants and insect community structure: willows and sawflies. Ecology 69:845–856
Giambelluca TW, Nullet MA, Schroeder TA (1986) Rainfall atlas of Hawaii. Department of Land and Natural Resources, State of Hawaii, Honolulu, HI, USA
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391
Gotelli NJ, Entsminger GL (2002) EcoSim: Null Models Software for Ecology, Version 7. Acquired Intelligence Inc. & Kesey-Bear, Burlington, VT
Gruner DS (2004a) Arthropods from ‘ōhi‘a lehua (Myrtaceae: Metrosideros polymorpha), with new records for the Hawaiian Islands. Bish Mus Occas Pap 78:33–52
Gruner DS (2004b) Attenuation of top-down and bottom-up forces in a complex terrestrial community. Ecology 85:3010–3022
Gruner DS (2005) Biotic resistance to an invasive spider conferred by insectivorous birds on the island of Hawai‘i. Biol Invasions 7:541–546
Gruner DS, Taylor AD, Forkner RE (2005) The effects of foliar pubescence and nutrient enrichment on arthropod communities of Metrosideros polymorpha (Myrtaceae). Ecol Entomol 30:428–443
Haddad NM, Haarstad J, Tilman D (2000) The effects of long-term nitrogen loading on grassland insect communities. Oecologia 124:73–84
Hare JD, Elle E (2002) Variable impact of diverse insect herbivores on dimorphic Datura wrightii. Ecology 83:2711–2720
Hillebrand H (2003) Opposing effects of grazing and nutrients on diversity. Oikos 100:592–600
Holt RD, Grover J, Tilman D (1994) Simple rules for interspecific dominance in systems with exploitative and apparent competition. Am Nat 144:741–771
Holt RD, Lawton JH (1994) The ecological consequences of shared natural enemies. Annu Rev Ecol Syst 25:495–520
Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton, NJ
Hurd LE, Wolf LL (1974) Stability in relation to nutrient enrichment in arthropod consumers of old-field successional ecosystems. Ecol Mono 44:465–482
Huston MA (1994) Biological diversity: the coexistence of species on changing landscapes. Cambridge University Press, Cambridge, UK
Hutchinson GE (1959) Homage to Santa Rosalia, or why are there so many kinds of animals? Am Nat 93:145–159
James SA, Puttock CF, Cordell S, Adams RP (2004) Morphological and genetic variation in Metrosideros polymorpha (Myrtaceae) on Hawaii. New Zeal J Bot 42:263–270
Jefferies RL, Maron JL (1997) The embarassment of riches: atmospheric deposition of nitrogen and community and ecosystem processes. Trends Ecol Evol 12:74–78
Johnson MD (2000) Evaluation of an arthropod sampling technique for measuring food availability for forest insectivorous birds. J Field Ornithol 71:88–109
Kajak A (1981) Analysis of the effect of mineral fertilization on the meadow spider community. Ekol Pol 29:313–326
Kirchner TB (1977) The effects of resource enrichment on the diversity of plants and arthropods in a shortgrass prairie. Ecology 58:1334–1344
Kneitel JM, Miller TE (2002) Resource and top-predator regulation in the pitcher plant (Sarracenia purpurea) inquiline community. Ecology 83:680–688
Kondoh M (2001) Unifying the relationships of species richness to productivity and disturbance. Proc R Soc Lond B 268:269–271
Leibold MA (1996) A graphical model of keystone predators in food webs: trophic regulation of abundance, incidence, and diversity patterns in communities. Am Nat 147:784–812
MacArthur RH (1969) Patterns of communities in the tropics. Biol J Linn Soc 1:19–30
Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, Princeton, NJ
Magurran AE, Henderson PA (2003) Explaining the excess of rare species in natural species abundance distributions. Nature 422:714–716
McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297
McCune B, Grace JB (2002) Analysis of Ecological Communities. MJM Software, Gleneden Beach, OR
Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757
Mittelbach GG, et al. (2001) What is the observed relationship between species richness and productivity? Ecology 82:2381–2396
Mittelbach GG, Scheiner SM, Steiner CF (2003) What is the observed relationship between species richness and productivity? Reply. Ecology 84:3390–3395
Naeem S, Hakansson K, Lawton JH, Crawley MJ, Thompson LJ (1996) Biodiversity and plant productivity in a model assemblage of plant species. Oikos 76:259–264
Nishida GM (ed) (2002) Hawaiian Terrestrial Arthropod Checklist, 4th edn. Bishop Museum Press, Honolulu, HI
Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75
Palacios-Vargas JG, Castaño-Meneses G (2003) Seasonality and community composition of springtails in Mexican forests. In: Basset Y, Novotný V, Miller SE, Kitching RL (eds) Arthropods of tropical forests: spatio-temporal dynamics and resource use in the canopy. Cambridge University Press, London, pp 159–169
Perkins RCL (1903) Vertebrata. In: Sharp D (ed) Fauna Hawaiiensis. Cambridge University Press, Cambridge, pp 365–466
Prestidge RA (1982) The influence of nitrogenous fertilizer on the grassland Auchenorrhyncha (Homoptera). J Appl Ecol 19:735–749
Preston FW (1962) The canonical distribution of commonness and rarity. Ecology 43:185–215; 410–432
Proulx M, Mazumder A (1998) Reversal of grazing impact on plant species richness in nutrient-poor vs. nutrient-rich ecosystems. Ecology 79:2581–2592
Raich JW, Russell AE, Crews TE, Farrington H, Vitousek PM (1996) Both nitrogen and phosphorus limit plant production on young Hawaiian lava flows. Biogeochemistry 32:1–14
Raich JW, Russell AE, Vitousek PM (1997) Primary productivity and ecosystem development along an elevational gradient on Mauna Loa, Hawaii. Ecology 78:707–721
Ralph CJ, Fancy SG (1994) Timing of breeding and molting in six species of Hawaiian honeycreepers. Condor 96:151–161
Rosenzweig ML, Abramsky Z (1993) How are diversity and productivity related? In: Ricklefs RE, Schluter D (eds) Species diversity in ecological communities: historical and geographical perspectives. University of Chicago Press, Chicago, IL, pp 52–65
Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, Cambridge, UK
Rypstra AL (1983) The importance of food and space in limiting web-spider densities; a test using field enclosures. Oecologia 59:312–316
SAS (2001) SAS for Windows, Version 8.02. SAS Institute, Cary, N.C.
Schoener TW, Spiller DA (1996) Devastation of prey diversity by experimentally introduced predators in the field. Nature 381:691–694
Scott JM, Mountainspring S, Ramsey FL, Kepler CB (1986) Stud Avian Biol, vol. 9: Forest bird communities of the Hawaiian Islands: their dynamics, ecology, and conservation. Cooper Ornithological Society, Los Angeles, Calif.
Sedlacek JD, Barrett GW, Shaw DR (1988) Effects of nutrient enrichment on the Auchenorrhyncha (Homoptera) in contrasting grassland communities. J Appl Ecol 25:537–550
Siemann E (1998) Experimental tests of effects of plant productivity and diversity on grassland arthropod diversity. Ecology 79:2057–2070
Sih A, Crowley P, Mcpeek M, Petranka J, Strohmeier K (1985) Predation, competition, and prey communities: a review of field experiments. Annu Rev Ecol Syst 16:269–311
Spiller DA, Schoener TW (1998) Lizards reduce spider species richness by excluding rare species. Ecology 79:503–516
Srivastava DS, Lawton JH (1998) Why more productive sites have more species: an experimental test of theory using tree-hole communities. Am Nat 152:510–529
Stein JD (1983) Insects infesting Acacia koa (Legumosae) and Metrosideros polymorpha (Myrtaceae) in Hawaii: an annotated list. Proc Hawaii Entomol Soc 24:305–316
Stemmermann RL (1983) Ecological studies of Hawaiian Metrosideros in a successional context. Pac Sci 37:361–373
Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1879
Stiling P, Rossi AM (1996) Complex effects of genotype and environment on insect herbivores and their enemies. Ecology 77:2212–2218
Stirling G, Wilsey B (2001) Empirical relationships between species richness, evenness, and proportional diversity. Am Nat 158:286–299
Strauss SY (1987) Direct and indirect effects of host-plant fertilization on an insect community. Ecology 68:1670–1678
Suding KN, et al. (2005) Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. Proc Natl Acad Sci USA 102:4387–4392
Swift SF, Goff ML (2001) Mite (Acari) communities associated with ‘ōhi‘a, Metrosideros polymorpha (Myrtaceae), at Homo O Nā Pali and Kui‘a natural area reserves on Kaua‘i Island, Hawaiian Islands. Pac Sci 55:23–40
Tilman D (1986) A consumer-resource approach to community structure. Am Zool 26:5–22
van Riper C, III, Scott JM (1979) Observations on distribution, diet, and breeding of the Hawaiian thrush. Condor 81:65–71
Vince SW, Valiela I, Teal JM (1981) An experimental study of the structure of herbivorous insect communities in a salt marsh. Ecology 62:1662–1678
Waide RB, et al. (1999) The relationship between productivity and species richness. Annu Rev Ecol Syst 30:257–300
Whittaker RJ, Heegaard E (2003) What is the observed relationship between species richness and productivity? Comment. Ecology 84:3384–3390
Worm B, Lotze HK, Hillebrand H, Sommer U (2002) Consumer versus resource control of species diversity and ecosystem functioning. Nature 417:848–851
Wright DH (1983) Species-energy theory: an extension of species-area theory. Oikos 41:496–506
Acknowledgements
We thank the Hawai‘i Division of Forestry and Wildlife for field research permits and access, and D. Foote and research staff at Hawai‘i Volcanoes National Park for logistical assistance and laboratory space. We are grateful to G. Bodner, R. Cabin, S. Cordell, L. Durand, N. Everett, D. Feinholz, P. Hart, S. Hight, R. Langston, P. Nilsson, and especially K. Heckmann, L. Wilson, S. McDaniel, and E. McDaniels for providing invaluable field assistance. The following people graciously assisted with arthropod identifications: K. Arakaki, M. Arnedo, M. Asche, J. Beatty, J. Garb, M. Gates, G. Gibson, R. Gillespie, J. Huber, E. Mockford, J. Noyes, D. Percy, D. Polhemus, D. Preston, A. Samuelson, C. Tauber, and A. Vandergast. We thank R. Kinzie, R. Forkner, J. Ewel, D. Strong, T. Crist, O. Schmitz and an anonymous reviewer for critical comments on the manuscript. D.S.G. received funding from training grants from the John D. and Catherine T. MacArthur Foundation and NSF DGE-9355055 & DUE-9979656 to the Center for Conservation Research and Training at the University of Hawai‘i at Mānoa, an E.P.A Science to Achieve Results (STAR) graduate fellowship, and research grants from Sigma Xi, the Hawai‘i Audubon Society, the Watson T. Yoshimoto Foundation, the ARCS Foundation, and the NSF DDIG program (DEB-0073055).
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Gruner, D.S., Taylor, A.D. Richness and species composition of arboreal arthropods affected by nutrients and predators: a press experiment. Oecologia 147, 714–724 (2006). https://doi.org/10.1007/s00442-005-0337-4
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DOI: https://doi.org/10.1007/s00442-005-0337-4