Cited by 436Insect-Plant Interactions and ControlAvian ecology and behaviorForest Insect Ecology and Management

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Insectivorous Birds Increase Growth of White Oak through Consumption of Leaf-Chewing Insects

Marquis, Robert J., Whelan, Christopher J.·1994·Ecology

DOI 10.2307/1941605

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Abstract

We examined the indirect effects of insectivorous birds on plant growth through consumption of leaf—chewing insects in a Missouri Ozark deciduous forest. Over a period of 2 yr, we compared insect numbers, leaf damage, and resultant plant growth for control saplings of white oak (Quercus alba), vs. saplings that we caged to limit access by insectivorous birds but not herbivorous insects. In a third treatment, we sprayed insecticide on young white oak trees to determine the impact of the insect herbivores on plant growth in the presence of birds. The total number of insects encountered on plants inside of cages was twice that on control plants for both years. Insecticide spray reduced herbivore numbers substantially but did not eliminate them. As a result of the treatments, cage plants suffered 25% leaf area loss, control plants 13%, and spray plants 6% at the end of the first season (34, 24, and 9%, respectively, for the 2nd yr). As a result of the differences in damage, cage plants produced one—third less total aboveground biomass compared to insecticide—treated plants, with control plants producing intermediate value. Differences in biomass production were due mainly to decreased leaf biomass, which in turn was associated with decreased leaf size in subsequent years as a result to high damage during the previous year. This is the first terrestrial ecosystem study to demonstrate a significant impact of insectivorous birds on plant growth. Our results suggest that over the long term observed declines in North American populations of insectivorous birds may reduce forest productivity because of potentially higher numbers of leaf—chewing insects and the concomitant negative effect on plant growth.

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Kozlov, M. V., Lanta, V., Zverev, V., & Zvereva, E. L. (2015) · Global Ecology and Biogeography · doi:10.1111/geb.12347 · Cited by 134
INDUCED DEFENSE IN WHITE OAK: EFFECTS ON HERBIVORES AND CONSEQUENCES FOR THE PLANT
Wold, E. N., & Marquis, R. J. (1997) · Ecology · doi:10.1890/0012-9658(1997)078[1356:idiwoe]2.0.co;2 · Cited by 132
Self-citation
BOTTOM-UP AND TOP-DOWN FORCES IN TIDE POOLS: TEST OF A FOOD CHAIN MODEL IN AN INTERTIDAL COMMUNITY
Nielsen, K. J. (2001) · Ecological Monographs · doi:10.1890/0012-9615(2001)071[0187:buatdf]2.0.co;2 · Cited by 136
Bird Predation and Vegetation Structure Affecting Spruce-Living Arthropods in a Temperate Forest
Gunnarsson, B. (1996) · Journal of Animal Ecology · doi:10.2307/5885 · Cited by 124
An invasive plant–fungal mutualism reduces arthropod diversity
Rudgers, J. A., & Clay, K. (2008) · Ecology Letters · doi:10.1111/j.1461-0248.2008.01201.x · Cited by 125
Diversification of tree stands as a means to manage pests and diseases in boreal forests: myth or reality?
Koricheva, J., Vehviläinen, H., Riihimäki, J., Ruohomäki, K., Kaitaniemi, P., & Ranta, H. (2006) · Canadian Journal of Forest Research · doi:10.1139/x05-172 · Cited by 121
Volatile Emissions from Alnus glutionosa Induced by Herbivory are Quantitatively Related to the Extent of Damage
Copolovici, L. O., Kännaste, A., Remmel, T., Vislap, V., & Niinemets, Ü. (2010) · Journal of Chemical Ecology · doi:10.1007/s10886-010-9897-9 · Cited by 119
“Herbivorous larvae, such as geometrids, cause considerable damage to deciduous trees, ranging from the consumption of a notable percentage of total leaf area (Marquis and Whelan, 1994; Martel and Mauffette, 1997) to complete defoliation in extreme cases (Wesolowski and Rowinski, 2006; van Asch and Visser, 2007).”
Background
Tritrophic interactions: willows, herbivorous insects and insectivorous birds
Sipura, M. (1999) · Oecologia · doi:10.1007/s004420050960 · Cited by 116
Past and Current Attempts to Evaluate the Role of Birds as Predators of Insect Pests in Temperate Agriculture
Kirk, D. A., Evenden, M., & Mineau, P. (1996) · Springer eBooks · doi:10.1007/978-1-4615-5881-1_5 · Cited by 107
EXPERIMENTAL TEST IN LOWLAND TROPICAL FOREST SHOWS TOP-DOWN EFFECTS THROUGH FOUR TROPHIC LEVELS
Letourneau, D. K., & Dyer, L. A. (1998) · Ecology · doi:10.1890/0012-9658(1998)079[1678:etiltf]2.0.co;2 · Cited by 109
Impacts of major predators on tropical agroforest arthropods: comparisons within and across taxa
Philpott, S., Greenberg, R., Bichier, P., & Perfecto, I. (2004) · Oecologia · doi:10.1007/s00442-004-1561-z · Cited by 112
“Ants and birds are taxonomically important predators of arthropods in natural and agricultural settings (Way and Khoo 1992; Marquis and Whelan 1994; Perfecto and Castiñeiras 1998; Greenberg et al. 2000; Schmitz et al. 2000; Sanz 2001; Mols and Visser 2002; Van Bael et al. 2003), and likely differentially affect prey b…”
Background
Ecological Sustainability of Birds in Boreal Forests
Niemi, G. J., Hanowski, J. M., Helle, P., Howe, R. W., Mönkkönen, M., Venier, L., & Welsh, D. A. (1998) · Conservation Ecology · doi:10.5751/es-00079-020217 · Cited by 105
Plant defenses and population fluctuations of forest defoliators : mechanism-based scenarios
Haukioja, E. (2005) · Annales Zoologici Fennici · Cited by 104
Does Food Web Complexity Eliminate Trophic‐Level Dynamics?
Hairston, N. G., & Hairston, N. G. (1997) · The American Naturalist · doi:10.1086/286035 · Cited by 104
Top-Down Control of Herbivory by Birds and Bats in the Canopy of Temperate Broad-Leaved Oaks (Quercus robur)
Böhm, S. M., Wells, K., & Kalko, E. K. V. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017857 · Cited by 104
“ecosystem functioning and deliver base-line data for the prediction of effects of environmental changes on ecosystem services relevant for forest primary productivity [12].”
Background
The Effects of habitat area, vegetation structure and insect richness on breeding bird populations in Beijing urban parks
Huang, Y., Zhao, Y., Li, S., & von Gadow, K. (2015) · Urban forestry & urban greening · doi:10.1016/j.ufug.2015.09.010 · Cited by 103
Relative strengths of top-down and bottom-up forces in a tropical forest community
Dyer, L. A., & Letourneau, D. K. (1999) · Oecologia · doi:10.1007/s004420050785 · Cited by 101
“mechanism for ``why the world is green,'' prompted many theoretical and empirical studies on the eects of top-down and bottom-up forces on community structure (e.g., Murdoch 1966; Menge and Sutherland 1976; Fretwell 1977, 1987; White 1978; Oksanen et al. 1981; Spiller and Schoener 1990; Hunter and Price 1992; Menge 1…”
Background
TRITROPHIC EFFECTS OF BIRDS AND ANTS ON A CANOPY FOOD WEB, TREE GROWTH, AND PHYTOCHEMISTRY
Mooney, K. A. (2007) · Ecology · doi:10.1890/06-1095.1 · Cited by 101
“Key words: ant–aphid mutualism; Cinara; emergent property; Formica podzolica; indirect effect; multiple predator effect; negative-biased interaction; phloem monoterpenes; Pinus ponderosa; positive-biased interaction; tritrophic interaction; trophic cascade.”
Background
Tritrophic Interactions at a Community Level: Effects of Host Plant Species Quality on Bird Predation of Caterpillars
Singer, M. S., Farkas, T. E., Skorik, C., & Mooney, K. A. (2012) · The American Naturalist · doi:10.1086/664080 · Cited by 100
“…was counted, 10 intact leaves were collected from each branch and measured with a leaf area meter (Li-Cor, Lincoln, NE), and total leaf areas for each sampling branch were calculated as the average leaf area for each branch multiplied by the number of leaves sampled (Marquis and Whelan 1994).”
Method
FOOD WEB ARCHITECTURE AND POPULATION DYNAMICS: Theory and Empirical Evidence
Morin, P. J., & Lawler, S. (1995) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.es.26.110195.002445 · Cited by 101
Differences between understorey and canopy in herbivore community composition and leaf quality for two oak species in Missouri
Corff, J. L., & Marquis, R. J. (1999) · Ecological Entomology · doi:10.1046/j.1365-2311.1999.00174.x · Cited by 98
“Only leaf-chewing insects were included in the study due to low abundance of galling and sap-feeding species (Marquis & Whelan, 1994).”
BackgroundSelf-citation
Genetically-based plant resistance traits affect arthropods, fungi, and birds
Dickson, L. L., & Whitham, T. G. (1996) · Oecologia · doi:10.1007/bf00334568 · Cited by 97
A trophic cascade in a diverse arthropod community caused by a generalist arthropod predator
Moran, M. D., & Hurd, L. E. (1997) · Oecologia · doi:10.1007/s004420050360 · Cited by 97
“Others have examined the eects on a plant species of guilds of predators such as insectivorous birds (Altegrim 1989; Marquis and Whelan 1994), lizards (Spiller and Schoener 1990, 1994; Dial and Roughgarden 1995), and arthropods (Hartvigsen et al.”
BackgroundInfluential
Effects of Shade‐Tree Species and Crop Structure on the Winter Arthropod and Bird Communities in a Jamaican Shade Coffee Plantation1
Johnson, M. D. (2000) · Biotropica · doi:10.1111/j.1744-7429.2000.tb00456.x · Cited by 96
Causes and Implications of Species Restoration in Altered Ecosystems
Mladenoff, D. J., Haight, R. G., Sickley, T. A., & Wydeven, A. P. (1997) · BioScience · doi:10.2307/1313003 · Cited by 98
ASYMMETRICAL INTERACTIONS BETWEEN UNGULATES AND PHYTOPHAGOUS INSECTS: BEING DIFFERENT MATTERS
Gómez, J. M., & González‐Megías, A. (2002) · Ecology · doi:10.1890/0012-9658(2002)083[0203:aibuap]2.0.co;2 · Cited by 95
Plant Morphology and Recruitment of the Third Trophic Level: Subtle and Little-Recognized Defenses?
Marquis, R. J., & Whelan, C. J. (1996) · Oikos · doi:10.2307/3546260 · Cited by 95
Self-citation
OakContig DF 159.1, a reference library for studying differential gene expression in Quercus robur during controlled biotic interactions: use for quantitative transcriptomic profiling of oak roots in ectomycorrhizal symbiosis
Tarkka, M. T., Herrmann, S., Wubet, T., Feldhahn, L. M., Recht, S., Kurth, F., Mailänder, S., Bönn, M., Neef, M., Angay, O., et al. (2013) · New Phytologist · doi:10.1111/nph.12317 · Cited by 92
Multiple approaches to estimating the relative importanceof top-down and bottom-up forces on insect populations:Experiments, life tables, and time-series analysis
Hunter, M. D. (2001) · Basic and Applied Ecology · doi:10.1078/1439-1791-00068 · Cited by 92
Experimentally increased insectivorous bird density results in a reduction of caterpillar density and leaf damage to Pyrenean oak
Sanz, J. J. (2001) · Ecological Research · doi:10.1046/j.1440-1703.2001.00403.x · Cited by 90
“The present study confirms the suggestion given by Marquis & Whelan 1994) that forest management practices that promote the conservation of insectivorous birds are imperative for the maintenance of forest productivity.”
BackgroundResultInfluential
Predation of Artificial Ground Nests at Two Types of Edges in a Forest-Dominated Landscape
Fenske-Crawford, T. J., & Niemi, G. J. (1997) · Ornithological Applications · doi:10.2307/1370220 · Cited by 88
Effects of timber harvests on invertebrate biomass and avian nest success
Duguay, J. P., Wood, P. B., & Miller, G. W. (2000) · Cited by 88
Global impacts of climate change on avian functional diversity
Stewart, P. S., Voskamp, A., Santini, L., Biber, M. F., Devenish, A. J. M., Hof, C., Willis, S. G., & Tobias, J. A. (2022) · Ecology Letters · doi:10.1111/ele.13830 · Cited by 90
Impact of avian and arthropod predation on lepidopteran caterpillar densities and plant productivity in an ephemeral agroecosystem
Hooks, C. R. R., Pandey, R. R., & Johnson, M. W. (2003) · Ecological Entomology · doi:10.1046/j.1365-2311.2003.00544.x · Cited by 84
Heterospecific attraction affects community structure and migrant abundances in northern breeding bird communities
Mönkkönen, M., Helle, P., Niemi, G. J., & Montgomery, K. (1997) · Canadian Journal of Zoology · doi:10.1139/z97-842 · Cited by 84
Trophic cascades in a complex terrestrial community
Dyer, L. A., & Letourneau, D. K. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.9.5072 · Cited by 84
Bird predation on herbivorous insects: indirect effects on sugar maple saplings
Strong, A. M., Sherry, T. W., & Holmes, R. T. (2000) · Oecologia · doi:10.1007/s004420000467 · Cited by 83
INVASIVE PREY IMPACTS THE ABUNDANCE AND DISTRIBUTION OF NATIVE PREDATORS
Barber, N. A., Marquis, R. J., & Tori, W. (2008) · Ecology · doi:10.1890/08-0395.1 · Cited by 83
“Insectivorous birds can have important effects, both directly on insect prey (Holmes et al. 1979) and indirectly on plants by consuming herbivorous insects (Marquis and Whelan 1994, Van Bael et al. 2008).”
BackgroundSelf-citation
Can forest trees compensate for stress-generated growth losses by induced production of volatile compounds?
Holopainen, J. K. (2011) · Tree Physiology · doi:10.1093/treephys/tpr111 · Cited by 85
Conservation in temperate forests: what do we need to know and do?
Ehrlich, P. R. (1996) · Forest Ecology and Management · doi:10.1016/s0378-1127(96)03746-2 · Cited by 82
Herbivore diet breadth mediates the cascading effects of carnivores in food webs
Singer, M. S., Lichter‐Marck, I. H., Farkas, T. E., Aaron, E., Whitney, K. D., & Mooney, K. A. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1401949111 · Cited by 79
“7. Beckerman AP, Uriarte M, Schmitz OJ (1997) Experimental evidence for a behavior-”
Background
Leaf quality, predators, and stochastic processes in the assembly of a diverse herbivore community.
Barber, N., & Marquis, R. (2011) · Ecology · doi:10.1890/10-0125.1 · Cited by 72
“The overall weak impacts of bird predation are surprising considering the strong direct effects of birds documented in this (Marquis and Whelan 1994) and other systems (Van Bael et al. 2008, Mooney et al. 2010).”
BackgroundSelf-citation
The Coffee Agroecosystem in the Neotropics: Combining Ecological and Economic Goals
Vandermeer, J. H. (2002) · CRC Press eBooks · doi:10.1201/9781420039887-9 · Cited by 79
The Importance of Species: Perspectives on Expendability and Triage
McPhearson, T. (2003) · Integrative and Comparative Biology · doi:10.1093/icb/43.4.603 · Cited by 79

Authors: Marquis, R. J., & Whelan, C. J.
ORCID: Marquis, Robert J.
Whelan, Christopher J.
Venue: Ecology
Publisher: Wiley
Published: 1994-10
Volume: 75
Issue: 7
Pages: 2007-2014
ISSN: 0012-9658 (ISSN-L)
DOI: 10.2307/1941605
OpenAlex: W2042570348
Cited by: 436
References: 38
Citations by year: 2026: 5 · 2025: 7 · 2024: 6 · 2023: 10 · 2022: 10 · 2021: 3 · 2020: 13 · 2019: 9 · 2018: 10 · 2017: 29 · 2016: 13 · 2015: 22 · 2014: 13 · 2013: 23 · 2012: 20
FWCI: 23.10
Type: journal article
Language: en
Open access: closed
Licence: doi.wiley.com/10.1002/tdm_license_1.1 (tdm, 7640 d)
Locations: Ecology (publishedVersion)
Topics: Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
Physical Sciences › Environmental Science › Ecology › Avian ecology and behavior
Physical Sciences › Environmental Science › Ecology › Forest Insect Ecology and Management
Keywords: insectivorous birds, Quercus alba, leaf-chewing insects, herbivory, plant growth, indirect effects, bird population decline, forest productivity, leaf damage, aboveground biomass, insecticide effects, deciduous forest, Missouri Ozarks

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Insectivorous Birds Increase Growth of White Oak through Consumption of Leaf-Chewing Insects

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