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Cascading top-down effects of changing oceanic predator abundances
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1. Top-down control can be an important determinant of ecosystem structure and function, but in oceanic ecosystems, where cascading effects of predator depletions, recoveries, and invasions could be significant, such effects had rarely been demonstrated until recently. 2. Here we synthesize the evidence for oceanic top-down control that has emerged over the last decade, focusing on large, high trophic-level predators inhabiting continental shelves, seas, and the open ocean. 3. In these ecosystems, where controlled manipulations are largely infeasible, 'pseudo-experimental' analyses of predator-prey interactions that treat independent predator populations as 'replicates', and temporal or spatial contrasts in predator populations and climate as 'treatments', are increasingly employed to help disentangle predator effects from environmental variation and noise. 4. Substantial reductions in marine mammals, sharks, and piscivorous fishes have led to mesopredator and invertebrate predator increases. Conversely, abundant oceanic predators have suppressed prey abundances. Predation has also inhibited recovery of depleted species, sometimes through predator-prey role reversals. Trophic cascades have been initiated by oceanic predators linking to neritic food webs, but seem inconsistent in the pelagic realm with effects often attenuating at plankton. 5. Top-down control is not uniformly strong in the ocean, and appears contingent on the intensity and nature of perturbations to predator abundances. Predator diversity may dampen cascading effects except where nonselective fisheries deplete entire predator functional groups. In other cases, simultaneous exploitation of predator and prey can inhibit prey responses. Explicit consideration of anthropogenic modifications to oceanic foodwebs should help inform predictions about trophic control. 6. Synthesis and applications. Oceanic top-down control can have important socio-economic, conservation, and management implications as mesopredators and invertebrates assume dominance, and recovery of overexploited predators is impaired. Continued research aimed at integrating across trophic levels is needed to understand and forecast the ecosystem effects of changing oceanic predator abundances, the relative strength of top-down and bottom-up control, and interactions with intensifying anthropogenic stressors such as climate change.
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“Predator-prey relationships play an integral role as top-down ecological controls, influencing ecosystem function and stability [1,2,3].”
From Effects of Vegetation Structure on the Location of Lion Kill Sites in African Thicket (2016) · cites this paper as [1]
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Early-life exposure to climate change impairs tropical shark survival
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“Sharks occupy high trophic levels in marine habitats, and play a key role in the structure, function and health of marine ecosystems [10,11].”
BackgroundFilling historical data gaps to foster solutions in marine conservation
Thurstan, R. H., McClenachan, L., Crowder, L. B., Drew, J., Kittinger, J. N., Levin, P. S., Roberts, C. M., & Pandolfi, J. M. (2015) · Ocean & Coastal Management · doi:10.1016/j.ocecoaman.2015.04.019 · Cited by 124
Ballard, G., Jongsomjit, D., Veloz, S., & Ainley, D. G. (2011) · Biological Conservation · doi:10.1016/j.biocon.2011.11.017 · Cited by 123
“…levels, in turn potentially explained by the unusual (in today’s world) prevalence of their upper-level predators (Table A.1; Ainley et al., 2006; Baum and Worm, 2009; Smith et al., 2012), some of which have been shown to act together to deplete middle-trophic-level prey (smaller fish and…”
BackgroundRooker, J. R., Kitchens, L. L., Dance, M. A., Wells, R. J. D., Falterman, B. J., & Cornic, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076080 · Cited by 127
“Declines in the abundances of fishes in nearshore and offshore ecosystems have been shown to limit top-down regulation of marine food webs, often leading to reductions in ecosystems services [3–5].”
BackgroundPitcher, T. J., & Cheung, W. W. L. (2013) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2013.05.045 · Cited by 128
“A collapsed fishery means that the fish biomass does not contribute to the normal food web and other ecosystem services and processes (Worm et al., 2006; Baum and Worm, 2009).”
BackgroundOceanography and Marine Biology
Firth, L. B., Knights, A. M., Bridger, D., Evans, A. J., Mieszkowska, N., Moore, P. J., O’Connor, N. E., Sheehan, E. V., Thompson, R. C., & Hawkins, S. J. (2016) · CRC Press eBooks · doi:10.1201/9781315368597 · Cited by 137
Critical assessment and ramifications of a purported marine trophic cascade
Grubbs, R. D., Carlson, J. K., Romine, J. G., Curtis, T. H., McElroy, W. D., McCandless, C. T., Cotton, C., & Musick, J. A. (2016) · Scientific Reports · doi:10.1038/srep20970 · Cited by 119
A review of the impacts of fisheries on open-ocean ecosystems
Crespo, G. O., & Dunn, D. C. (2017) · ICES Journal of Marine Science · doi:10.1093/icesjms/fsx084 · Cited by 132
“Better understanding of these dynamics may help explain top-down trophic controls in open-ocean systems (Baum and Worm, 2009).”
BackgroundEcological risk assessment and its application to elasmobranch conservation and management
Gallagher, A. J., Kyne, P. M., & Hammerschlag, N. (2012) · Journal of Fish Biology · doi:10.1111/j.1095-8649.2012.03235.x · Cited by 121
“Overharvest can be especially detrimental to marine systems when the targeted species plays a keystone role in the ecosystem (Paine, 1966), such is the case with top oceanic predators (Stevens et al., 2000; Myers et al., 2007; Baum & Worm, 2009).”
BackgroundTracking seabirds to identify potential Marine Protected Areas in the tropical western Indian Ocean
Corre, M. L., Jaeger, A., Pinet, P., Kappes, M. A., Weimerskirch, H., Catry, T., Ramos, J. A., Russell, J. C., Shah, N. J., & Jaquemet, S. (2012) · Biological Conservation · doi:10.1016/j.biocon.2011.11.015 · Cited by 132
Hussey, N. E., McCann, H., Cliff, G., Dudley, S., Wintner, S. P., & Fisk, A. T. (2012) · CRC Press eBooks · doi:10.1201/b11532-5 · Cited by 121
Human Involvement in Food Webs
Strong, D. R., & Frank, K. T. (2010) · Annual Review of Environment and Resources · doi:10.1146/annurev-environ-031809-133103 · Cited by 118
“In the past few years, fisheries studies with a top-down point of departure have become more frequent (74).”
BackgroundFishing degrades size structure of coral reef fish communities
Robinson, J. P. W., Williams, I. D., Edwards, A. M., McPherson, J. M., Yeager, L. A., Vigliola, L., Brainard, R. E., & Baum, J. K. (2016) · Global Change Biology · doi:10.1111/gcb.13482 · Cited by 132
“Selective fishing of large consumers can produce trophic cascades (Bascompte et 77 al., 2005; Baum & Worm, 2009) and destabilize predator-prey dynamics (Britten et al., 78 2014), while sustained exploitation at lower trophic levels can collapse prey populations 79 (Essington et al., 2015).”
BackgroundSelf-citationBenchmarking global fisheries discards
Gilman, E. L., Roda, A. P., Huntington, T., Kennelly, S. J., Suuronen, P., Chaloupka, M. Y., & Medley, P. (2020) · Scientific Reports · doi:10.1038/s41598-020-71021-x · Cited by 117
Iverson, S. A., Gilchrist, H. G., Smith, P. A., Gaston, A. J., & Forbes, M. R. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.3128 · Cited by 123
“Rapid environmental changes affecting top predators are of particular relevance because behavioural changes on the part of predators have the potential to restructure food webs and lead to cascading ecological impacts on prey populations [6,8].”
BackgroundReisinger, R. R., Raymond, B., Hindell, M. A., Bester, M. N., Crawford, R. J. M., Davies, D., de Bruyn, P. J. N., Dilley, B. J., Kirkman, S. P., Makhado, A. B., et al. (2018) · Diversity and Distributions · doi:10.1111/ddi.12702 · Cited by 110
“Predators may also have significant top- down effects on ecosystems (Baum & Worm, 2009; Heithaus, Frid, Wirsing, & Worm, 2008).”
BackgroundSustained disruption of narwhal habitat use and behavior in the presence of Arctic killer whales
Breed, G. A., Matthews, C. J. D., Marcoux, M., Higdon, J. W., Leblanc, B., Petersen, S. D., Orr, J. R., Reinhart, N. R., & Ferguson, S. H. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1611707114 · Cited by 109
Barría, C., Marta Coll, M., & Navarro, J. (2015) · Marine Ecology Progress Series · doi:10.3354/meps11494 · Cited by 117
“The de - crease in population size of some elasmobranchs may initiate trophic cascades through top-down effects and modify marine communities and ecosystems dramatically (Baum & Worm 2009, Ferretti et al. 2010).”
BackgroundComparative feeding ecology of shortfin mako, blue and thresher sharks in the California Current
Preti, A., Soykan, C. U., Dewar, H., Wells, R. J. D., Spear, N., & Kohin, S. (2012) · Environmental Biology of Fishes · doi:10.1007/s10641-012-9980-x · Cited by 116
Bacterial predation in a marine host-associated microbiome
Welsh, R. M., Zaneveld, J., Rosales, S., Payet, J. P., Burkepile, D. E., & Thurber, R. L. V. (2015) · The ISME Journal · doi:10.1038/ismej.2015.219 · Cited by 103
“The mean relative abundance of Halobacteriovorax across all libraries was low (0.40%±0.04 SEM), similar to their abundances in estuarine systems (Pineiro et al., 2013) and as characteristic of predators across most ecosystems (Baum and Worm, 2009).”
BackgroundResultInfluentialEero, M., Vinther, M., Haslob, H., Huwer, B., Casini, M., Storr‐Paulsen, M., & Köster, F. (2012) · Conservation Letters · doi:10.1111/j.1755-263x.2012.00266.x · Cited by 110
“This is probably because declines in predator species have in many cases been followed by a pronounced increase in prey biomass (Myers and Worm 2003; Baum & Worm 2009), and food limitation for recovering predator populations is therefore not expected.”
BackgroundCascading ecological effects of eliminating fishery discards
Heath, M. R., Cook, R., Cameron, A. I., Morris, D. J., & Speirs, D. C. (2014) · Nature Communications · doi:10.1038/ncomms4893 · Cited by 105
Rooker, J. R., Simms, J. R., Wells, R. J. D., Holt, S. A., Holt, G. J., Graves, J. E., & Furey, N. B. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034180 · Cited by 105
“stability, and structure of marine ecosystems [8–10].”
Palm, H. W. (2011) · Springer eBooks · doi:10.1007/978-3-642-21396-0_12 · Cited by 105
“Bayoumy et al. (2008) showed conflicting evidence for the reaction of monogeneans to heavy metal concentrations in the Red Sea.”
BackgroundStable Isotope Analysis Challenges Wasp-Waist Food Web Assumptions in an Upwelling Pelagic Ecosystem
Madigan, D. J., Carlisle, A. B., Dewar, H., Snodgrass, O. E., Litvin, S. Y., Micheli, F., & Block, B. A. (2012) · Scientific Reports · doi:10.1038/srep00654 · Cited by 101
Vignaud, T., Maynard, J. A., Leblois, R., Meekan, M. G., Vázquez‐Juárez, R., Ramírez‐Macías, D., Pierce, S. J., Rowat, D. R. L., Berumen, M. L., Reddy, C. B., et al. (2014) · Molecular Ecology · doi:10.1111/mec.12754 · Cited by 100
“Conservation of these sharks is made challenging because of their slow growth, late maturation and resultant low rebound potential, which make them highly vulnerable to overexploitation, and because they move across political boundaries (Cort es 2000; Musick & Ellis 2005; Baum & Worm 2009).”
BackgroundKrone, R., Dederer, G., Kanstinger, P., Krämer, P., Schneider, C., & Schmalenbach, I. (2016) · Marine Environmental Research · doi:10.1016/j.marenvres.2016.11.011 · Cited by 102
Diet and trophic ecology of the tiger shark (Galeocerdo cuvier) from South African waters
Dicken, M. L., Hussey, N. E., Christiansen, H. M., Smale, M. J., Nkabi, N., Cliff, G., & Wintner, S. P. (2017) · PLoS ONE · doi:10.1371/journal.pone.0177897 · Cited by 100
“cuvier, and indeed any top predator, to better predict the ecological consequences of shark depletions or recoveries [1, 2, 3].”
BackgroundInfluentialClua, É., Buray, N., Legendre, P., Mourier, J., & Planes, S. (2011) · Marine and Freshwater Research · doi:10.1071/mf10163 · Cited by 101
Global variation in marine fish body size and its role in biodiversity–ecosystem functioning
Fisher, J., Frank, K. T., & Leggett, W. C. (2010) · Marine Ecology Progress Series · doi:10.3354/meps08601 · Cited by 104
“The most recent examples of exploitation-driven trophic cascades also come from the North Atlantic region (Frank et al. 2007, Baum & Worm 2009).”
BackgroundStatus of Marine Biodiversity in the Anthropocene
Luypaert, T., Hagan, J. G., McCarthy, M. L., & Poti, M. (2019) · Springer eBooks · doi:10.1007/978-3-030-20389-4_4 · Cited by 109
“The loss of top-down control following apex consumer decline is often followed by population increases of medium-sized vertebrate prey, known as mesopredator release (Baum and Worm 2009).”
BackgroundIndustrial fishing, no-take zones and endangered penguins
Pichegru, L., Ryan, P. G., van Eeden, R., Reid, T. A., Grémillet, D., & Wanless, R. M. (2011) · Biological Conservation · doi:10.1016/j.biocon.2011.12.013 · Cited by 109
Climate‐driven disparities among ecological interactions threaten kelp forest persistence
Provost, E. J., Kelaher, B. P., Dworjanyn, S. A., Russell, B. D., Connell, S. D., Ghedini, G., Gillanders, B. M., Figueira, W. F., & Coleman, M. A. (2016) · Global Change Biology · doi:10.1111/gcb.13414 · Cited by 104
“The resulting reduced top-down pressure from rock lobsters at 25 °C potentially leads to larger populations of urchins and, therefore, has indirect trophic consequences for kelp forests (Shears & Babcock, 2002; Baum & Worm, 2009).”
BackgroundEffects of Vegetation Structure on the Location of Lion Kill Sites in African Thicket
Davies, A. B., Tambling, C. J., Kerley, G. I. H., & Asner, G. P. (2016) · PLOS ONE · doi:10.1371/journal.pone.0149098 · Cited by 97
“Predator-prey relationships play an integral role as top-down ecological controls, influencing ecosystem function and stability [1,2,3].”
BackgroundJackson, J. B. C. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0278 · Cited by 102
“Overfishing of predators commonly allows unchecked increases of their former prey (Estes et al. 1998; Frank et al. 2005; Baum & Worm 2009).”
BackgroundDuffy, L. M., Kuhnert, P., Pethybridge, H., Young, J. W., Olson, R. J., Logan, J. M., Goñi, N., Romanov, E. V., Allain, V., Staudinger, M. D., et al. (2017) · Deep Sea Research Part II Topical Studies in Oceanography · doi:10.1016/j.dsr2.2017.03.003 · Cited by 103
A spatial regime shift from predator to prey dominance in a large coastal ecosystem
Eklöf, J., Sundblad, G., Erlandsson, M., Donadi, S., Hansen, J. P., Eriksson, B. K., & Bergström, U. (2020) · Communications Biology · doi:10.1038/s42003-020-01180-0 · Cited by 96
Trophic cascades in the western Ross Sea, Antarctica: revisited
Ainley, D. G., Ballard, G., Jones, R., Jongsomjit, D., Pierce, S. D., Smith, W., & Veloz, S. (2015) · Marine Ecology Progress Series · doi:10.3354/meps11394 · Cited by 100
“As the capacity for top-down forcing declines due to upper-level predator removal (e.g. Jackson et al. 2001, Myers & Worm 2003, Baum & Worm 2009, Estes et al. 2011, Cheung et al. 2013), and as changes associated with climate modification increase (e.g. Thomas et al. 2004, Ainley et al. 2010, Cheung…”
BackgroundBiological responses of sharks to ocean acidification
Rosa, R., Rummer, J. L., & Munday, P. L. (2017) · Biology Letters · doi:10.1098/rsbl.2016.0796 · Cited by 95
Metadata
- Authors
- Baum, J. K., & Worm, B.
- Affiliations
- Dalhousie University (CA)
- Corresponding author
- Baum, Julia K.
- Venue
- Journal of Animal Ecology
- Publisher
- Wiley
- Published
- 2009-06-04
- Volume
- 78
- Issue
- 4
- Pages
- 699-714
- ISSN
- 0021-8790 (ISSN-L)
- 1365-2656
- OpenAlex
- W2132556874
- Cited by
- 932
- References
- 134
- Citations by year
- 2026: 48 · 2025: 49 · 2024: 57 · 2023: 67 · 2022: 67 · 2021: 66 · 2020: 55 · 2019: 54 · 2018: 47 · 2017: 55 · 2016: 65 · 2015: 63 · 2014: 57 · 2013: 50 · 2012: 52
- FWCI
- 4.81
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Animal Ecology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Natural Sciences and Engineering Research Council of Canada
- Topics
- Life Sciences › Agricultural and Biological Sciences › Aquatic Science › Marine and fisheries research
- Physical Sciences › Environmental Science › Ecology › Marine animal studies overview
- Physical Sciences › Environmental Science › Ecology › Coral and Marine Ecosystems Studies
- Keywords
- top-down control, trophic cascades, predator abundance, marine mammals, sharks, piscivorous fish, mesopredator release, invertebrate predators, predator-prey interactions, role reversal, predator recovery, fisheries depletion, predator diversity, bottom-up control, food webs, climate change, marine conservation
- MeSH terms
- Animals, Oceans and Seas, Population Dynamics, Predatory Behavior, Time Factors, Food Chain
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