Insectivorous Birds Increase Growth of White Oak through Consumption of Leaf-Chewing Insects
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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The counter cascade of arthropod declines despite predator decreases conflicts with decades of research on trophic dynamics and with studies documenting the major impact of anoles, frogs, and birds on arthropod abundance.
“This “counter cascade” conflicts with decades of research on trophic dynamics (44), as well as studies documenting the major impact of anoles, frogs, and birds on arthropod abundance (45, 46).”
From Climate-driven declines in arthropod abundance restructure a rainforest food web (2018) · cites this paper as [46]
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BackgroundInfluentialFOLIAGE STRUCTURE INFLUENCES FORAGING OF INSECTIVOROUS FOREST BIRDS: AN EXPERIMENTAL STUDY
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Amo, L., Jansen, J. J., van Dam, N. M., Dicke, M., & Visser, M. E. (2013) · Ecology Letters · doi:10.1111/ele.12177 · Cited by 166 · see citing works
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BackgroundVegetation dynamics of predator‐free land‐bridge islands
Terborgh, J., Feeley, K. J., Silman, M. R., Núñez, P., & Balukjian, B. (2006) · Journal of Ecology · doi:10.1111/j.1365-2745.2006.01106.x · Cited by 159 · see citing works
“The matter is trivially simple in principle, but in practice, the challenge of experimentally creating predator-free environments in which herbivores can increase without constraint has proven almost insurmountable (Marquis & Whelan 1994; Schmitz et al. 2000; Sinclair et al. 2000).”
BackgroundFood Web Effects of Prey Size Refugia: Variable Interactions and Alternative Stable Equilibria
Chase, J. M. (1999) · The American Naturalist · doi:10.1086/303260 · Cited by 165 · see citing works
ATTENUATION OF TOP-DOWN AND BOTTOM-UP FORCES IN A COMPLEX TERRESTRIAL COMMUNITY
Gruner, D. S. (2004) · Ecology · doi:10.1890/04-0020 · Cited by 154 · see citing works
“…vertebrate predators can have large impacts on species-rich arthropod communities with indirect effects propagated to primary producers (e.g., Marquis and Whelan 1994, Van Bael et al. 2003), but top-down factors are often contingent on strong bottom-up influences (e.g., Sipura 1999, Ritchie…”
BackgroundInfluentialSTILING, P. D., & Moon, D. C. (2004) · Oecologia · doi:10.1007/s00442-004-1739-4 · Cited by 152 · see citing works
“…and bottom-up effects, adding to the volume of literature, which suggests that both effects are common in terrestrial (Gomez and Zamora 1994; Marquis and Whelan 1994; Dial and Roughgarden 1995; Letourneau and Dyer 1998; Dyer and Letourneau 1999; Forkner and Hunter 2000; Parry et al. 2003;…”
BackgroundConserving nature at regional and continental scales—a scientific program for North America
Soulé, M. E., & Terborgh, J. (1999) · BioScience · doi:10.2307/1313572 · Cited by 151 · see citing works
Top‐Down Cascade from a Bitrophic Predator in an Old‐Field Community
Moran, M. D., Rooney, T. P., & Hurd, L. E. (1996) · Ecology · doi:10.2307/2265715 · Cited by 139 · see citing works
“Other top-down studies have shown effects of vertebrate predators on plant growth and reproduction (Altegrim 1989, Spiller and Schoener 1990, 1994, Marquis and Whelan 1994, McLaren and Peterson 1994, Dial and Roughgarden 1995).”
BackgroundGoodale, E., Sridhar, H., Sieving, K. E., Bangal, P., Z., G. J. C., Farine, D. R., Heymann, E. W., Jones, H. H., Krams, I. A., Martínez, A. E., et al. (2020) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12591 · Cited by 141 · see citing works
“…example, the dominance of MSGs among insectivorous birds, and the enhanced foraging efficiency in MSGs, could have indirect positive effects on sympatric species via greater plant productivity generated by herbivorous insect population regulation (e.g. Marquis & Whelan, 1994; Vidal & Murphy, 2018).”
BackgroundTri‐trophic interactions: bridging species, communities and ecosystems
Abdala‐Roberts, L., Puentes, A., Finke, D. L., Marquis, R. J., Montserrat, M., Poelman, E. H., Rasmann, S., Sentis, A., van Dam, N. M., Wimp, G. M., et al. (2019) · Ecology Letters · doi:10.1111/ele.13392 · Cited by 140 · see citing works
“For instance, the many studies of arthropod TTIs within forest ecosystems have been limited to manipulations of saplings (e.g. Marquis & Whelan 1994) or individual tree branches (e.g. Mooney 2007), thus providing inference with respect to individual tree species but not to the larger…”
BackgroundSelf-citationPopulation Abundance and Ecosystem Service Provision: The Case of Birds
Gaston, K. J., Cox, D. T. C., Canavelli, S. B., Garcı́a, D., Hughes, B., Maas, B., Martínez, D., OGADA, D. L., & Inger, R. (2018) · BioScience · doi:10.1093/biosci/biy005 · Cited by 144 · see citing works
Gabbe, A. P., Robinson, S. K., & Brawn, J. D. (2002) · Conservation Biology · doi:10.1046/j.1523-1739.2002.00460.x · Cited by 138 · see citing works
“As a vital component of ecosystems, birds are important seed dispersers ( Willson 1986), pollinators ( Brown & Hopkins 1996), and predators of insects ( Holmes 1990; Marquis & Whelan 1994 ); they should not be overlooked in habitat restoration projects.”
BackgroundCarson, W. P., & Root, R. B. (1999) · Oecologia · doi:10.1007/s004420050928 · Cited by 138 · see citing works
“…of these top-down e ects is at least partly due to predators and parasitoids reducing the abundance of insect herbivores (e.g., Holmes et al. 1979; Strong et al. 1984; Spiller and Schoener 1990; Fowler et al. 1991; Bock et al. 1992; Marquis and Whelan 1994; Schmitz 1994; Schmitz et al. 1997).”
BackgroundKalka, M. B., & Kalko, E. K. V. (2005) · Journal of Tropical Ecology · doi:10.1017/s0266467405002920 · Cited by 137 · see citing works
“…of herbivorous insects on tropical forests has led to a corresponding appreciation of predators such as birds and insects, that control herbivore populations and thus reduce levels of herbivory (Atlegrim 1989, Greenberg et al. 2000, Marquis & Whelan 1994, Strong et al. 2000, Van Bael et al. 2003).”
BackgroundGlobal patterns in background losses of woody plant foliage to insects
Kozlov, M. V., Lanta, V., Zverev, V., & Zvereva, E. L. (2015) · Global Ecology and Biogeography · doi:10.1111/geb.12347 · Cited by 136 · see citing works
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 · see citing works
Self-citationBOTTOM-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 · see citing works
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 · see citing works
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 122 · see citing works
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 · see citing works
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 · see citing works
“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).”
BackgroundTritrophic interactions: willows, herbivorous insects and insectivorous birds
Sipura, M. (1999) · Oecologia · doi:10.1007/s004420050960 · Cited by 116 · see citing works
Kirk, D. A., Evenden, M., & Mineau, P. (1996) · Springer eBooks · doi:10.1007/978-1-4615-5881-1_5 · Cited by 107 · see citing works
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 · see citing works
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 · see citing works
“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…”
BackgroundEcological 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 · see citing works
Plant defenses and population fluctuations of forest defoliators : mechanism-based scenarios
Haukioja, E. (2005) · Annales Zoologici Fennici · Cited by 104 · see citing works
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 · see citing works
Böhm, S. M., Wells, K., & Kalko, E. K. V. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017857 · Cited by 104 · see citing works
“ecosystem functioning and deliver base-line data for the prediction of effects of environmental changes on ecosystem services relevant for forest primary productivity [12].”
BackgroundHuang, Y., Zhao, Y., Li, S., & von Gadow, K. (2015) · Urban forestry & urban greening · doi:10.1016/j.ufug.2015.09.010 · Cited by 103 · see citing works
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 · see citing works
“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…”
BackgroundTRITROPHIC 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 · see citing works
“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.”
BackgroundSinger, M. S., Farkas, T. E., Skorik, C., & Mooney, K. A. (2012) · The American Naturalist · doi:10.1086/664080 · Cited by 100 · see citing works
“…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).”
MethodFood 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 111 · see citing works
Corff, J. L., & Marquis, R. J. (1999) · Ecological Entomology · doi:10.1046/j.1365-2311.1999.00174.x · Cited by 98 · see citing works
“Only leaf-chewing insects were included in the study due to low abundance of galling and sap-feeding species (Marquis & Whelan, 1994).”
BackgroundSelf-citationGenetically-based plant resistance traits affect arthropods, fungi, and birds
Dickson, L. L., & Whitham, T. G. (1996) · Oecologia · doi:10.1007/bf00334568 · Cited by 97 · see citing works
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 · see citing works
“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.”
BackgroundInfluentialJohnson, M. D. (2000) · Biotropica · doi:10.1111/j.1744-7429.2000.tb00456.x · Cited by 96 · see citing works
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 96 · see citing works
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 · see citing works
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 · see citing works
Self-citationTarkka, 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 · see citing works
Hunter, M. D. (2001) · Basic and Applied Ecology · doi:10.1078/1439-1791-00068 · Cited by 92 · see citing works
Sanz, J. J. (2001) · Ecological Research · doi:10.1046/j.1440-1703.2001.00403.x · Cited by 90 · see citing works
“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.”
BackgroundResultInfluentialPredation 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 · see citing works
Effects of timber harvests on invertebrate biomass and avian nest success
Duguay, J. P., Wood, P. B., & Miller, G. W. (2000) · Cited by 88 · see citing works
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 84 · see citing works
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 · see citing works
Mönkkönen, M., Helle, P., Niemi, G. J., & Montgomery, K. (1997) · Canadian Journal of Zoology · doi:10.1139/z97-842 · Cited by 84 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
“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-citationHolopainen, J. K. (2011) · Tree Physiology · doi:10.1093/treephys/tpr111 · Cited by 83 · see citing works
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 · see citing works
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 · see citing works
“7. Beckerman AP, Uriarte M, Schmitz OJ (1997) Experimental evidence for a behavior-”
BackgroundLeaf 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 · see citing works
“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-citationThe 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 · see citing works
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 · see citing works
- Authors
- Marquis, R. J., & Whelan, C. J.
- Venue
- Ecology
- Publisher
- Wiley
- Published
- 1994-10
- Volume
- 75
- Issue
- 7
- Pages
- 2007-2014
- ISSN
- 0012-9658 (ISSN-L)
- 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
- 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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