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Cascading top-down effects of changing oceanic predator abundances
Open accessAbstract
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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Reef Shark Science – Key Questions and Future Directions
Heupel, M. R., Papastamatiou, Y. P., Espinoza, M., Green, M. E., & Simpfendorfer, C. A. (2019) · Frontiers in Marine Science · doi:10.3389/fmars.2019.00012 · Cited by 63
“, marine protected areas), and other factors as the equivalent of experimental manipulation (Baum and Worm, 2009).”
BackgroundMethodFeeding requirements of white sharks may be higher than originally thought
Semmens, J. M., Payne, N. L., Huveneers, C. P. M., SIMS, D. W., & Bruce, B. D. (2013) · Scientific Reports · doi:10.1038/srep01471 · Cited by 60
Anderson, A. B., Bonaldo, R. M., Barneche, D. R., Hackradt, C. W., Félix‐Hackradt, F. C., García‐Charton, J. A., & Floeter, S. R. (2014) · Marine Ecology Progress Series · doi:10.3354/meps11032 · Cited by 60
“Reductions in the biomass and abundance of top predators may trigger potentially irreversible cascade effects that destabilize food webs in the marine environment (Dulvy et al. 2004, Heithaus et al. 2008, Baum & Worm 2009).”
BackgroundKiller whales redistribute white shark foraging pressure on seals
Jorgensen, S. J., Anderson, S. D., Ferretti, F., Tietz, J. R., Chapple, T. K., Kanive, P. E., Bradley, R. W., Moxley, J. H., & Block, B. A. (2019) · Scientific Reports · doi:10.1038/s41598-019-39356-2 · Cited by 66
Bender, M. G., Floeter, S. R., MAYER, F. P., Vila-Nova, D. A., Longo, G. O., Hanazaki, N., Carvalho‐Filho, A., & Ferreira, C. E. L. (2013) · Oryx · doi:10.1017/s003060531100144x · Cited by 59
“This also seems to be the case for many marine fi shes (Morris et al., 2000 ; Myers et al., 2007 ; Baum & Worm, 2009 ), including Brazilian macrocarnivores, which is the most threatened trophic group, many of them being large bodied (Supplementary Table S 1 ).”
Clua, É., Chauvet, C., Read, T. C., Werry, J. M., & Lee, S. Y. (2013) · Marine and Freshwater Behaviour and Physiology · doi:10.1080/10236244.2013.773127 · Cited by 59
“…2013 Vol. 46, No. 1, 1–20, http://dx.doi.org/10.1080/10236244.2013.773127 2013 Taylor & Francis ine ecosystems has been documented by recent analyses of the detrimental cascading effects that follow their decline (Stevens et al. 2000; Heithaus et al. 2007; Myers et al. 2007; Baum and Worm 2009).”
BackgroundInfluentialStige, L. C., Dalpadado, P., Orlova, E. L., Boulay, A.-C., Durant, J. M., Ottersen, G., & Stenseth, N. C. (2013) · Progress In Oceanography · doi:10.1016/j.pocean.2013.09.006 · Cited by 59
“There is thus still little evidence for top-down effects on zooplankton (Baum and Worm, 2009), with exceptions including studies from the Baltic Sea (Casini et al.”
BackgroundResultNavia, A. F., Cruz‐Escalona, V. H., Giraldo, A., & Barausse, A. (2016) · Ecological Modelling · doi:10.1016/j.ecolmodel.2016.02.009 · Cited by 57
Houssard, P., Lorrain, A., Tremblay-Boyer, L., Allain, V., Graham, B. S., Menkès, C. E., Pethybridge, H., Couturier, L. I. E., Point, D., Leroy, B. M., et al. (2017) · Progress In Oceanography · doi:10.1016/j.pocean.2017.04.008 · Cited by 59
Temporal Variation in Trophic Cascades
Piovia‐Scott, J., Yang, L. H., & Wright, A. N. (2017) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-121415-032246 · Cited by 61
Predicting and Detecting Reciprocity between Indirect Ecological Interactions and Evolution
Estes, J. A., Brashares, J. S., & Power, M. E. (2013) · The American Naturalist · doi:10.1086/668120 · Cited by 58
How have fisheries affected parasite communities?
Wood, C. L., & Lafferty, K. D. (2014) · Parasitology · doi:10.1017/s003118201400002x · Cited by 58
What is at stake? Status and threats to South China Sea marine fisheries
Teh, L., Witter, A., Cheung, W. W. L., Sumaila, U. R., & Yin, X. (2016) · AMBIO · doi:10.1007/s13280-016-0819-0 · Cited by 58
Payne, N. L., Snelling, E. P., Fitzpatrick, R., Seymour, J., Courtney, R. L., Barnett, A., Watanabe, Y. Y., SIMS, D. W., Squire, L., & Semmens, J. M. (2015) · Methods in Ecology and Evolution · doi:10.1111/2041-210x.12358 · Cited by 61
“…of energy flux between trophic levels and is therefore a central parameter underpinning predator–prey interactions, and the cascading effects of changing population abundances in high (i.e. top-down; Heithaus et al. 2008; Baum & Worm 2009) and low (bottom-up; Ware &Thomson 2005) trophic positions.”
BackgroundReef fish structure and distribution in a south-western Atlantic Ocean tropical island
Pinheiro, H. T., Ferreira, C. E. L., Joyeux, J., Santos, R. G. D., & Horta, P. A. (2011) · Journal of Fish Biology · doi:10.1111/j.1095-8649.2011.03138.x · Cited by 58
“This expectation has been denied, however, for at least the last five decades, as industrial fishing and advances in fishing and navigation technology have opened up the last frontiers of the oceans (Myers & Worm, 2003; Ward & Myers, 2005; Baum & Worm, 2009).”
BackgroundChuang, P., Hung, T.-C., Chang, H.-A., Huang, C., & Shiao, J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0147290 · Cited by 57
River dolphins as indicators of ecosystem degradation in large tropical rivers
Gomez‐Salazar, C., Marta Coll, M., & Whitehead, H. (2012) · Ecological Indicators · doi:10.1016/j.ecolind.2012.02.034 · Cited by 58
“…of top predators is related to significant ecosystem transformations, including impacts on several trophic levels and changes in energy flows, marine resources’ removals from fisheries, and changes in the behavior of prey (Soulé et al., 2005; Heithaus et al., 2008; Baum and Worm, 2009).”
BackgroundResultInfluentialModelling the effects of fishing on the biomass of the world’s oceans from 1950 to 2006
Tremblay-Boyer, L., Gascuel, D., Watson, R. A., Christensen, V., & Pauly, D. F. (2011) · Marine Ecology Progress Series · doi:10.3354/meps09375 · Cited by 63
“…2 decades (Watson & Pauly 2001 The second method is based on the meta-analysis of data originating from a representative set of systems For instance, Baum & Worm (2009) summarized the effects and strength of top-down cascades from a set of locations distributed over the world’s oceans In this…”
InfluentialA history of the exploitation of the Ross Sea, Antarctica
Ainley, D. G. (2009) · Polar Record · doi:10.1017/s003224740999009x · Cited by 56
“…fishing and whaling, the Ross Sea neritic foodweb is expected to exhibit the sorts of trophic cascades that have been seen elsewhere as stocks of top trophic, long lived, slow to mature, and slow to reproduce minke whales and Antarctic toothfish are depleted (see review in Baum and Worm 2009).”
BackgroundEcosystem-based spatial planning and management of marine fisheries: Why and how?
Norse, E. A. (2010) · Bulletin of Marine Science · Cited by 56
Economic shocks in the fisheries sector and maritime piracy
Flückiger, M., & Ludwig, M. (2014) · Journal of Development Economics · doi:10.1016/j.jdeveco.2014.12.003 · Cited by 57
Bornatowski, H., Angelini, R., Marta Coll, M., Barreto, R. R. P., & de Amorim, A. F. (2017) · Reviews in Fish Biology and Fisheries · doi:10.1007/s11160-017-9492-z · Cited by 62
From diatoms to killer whales: impacts of pink salmon on North Pacific ecosystems
Ruggerone, G., Springer, A., van Vliet, G. V., Connors, B., Irvine, J., Shaul, L., Sloat, & Atlas, W. (2023) · Marine Ecology Progress Series · doi:10.3354/meps14402 · Cited by 44
“Although considerable progress has been made in identifying top-down effects in ocean ecosystems (e.g. Baum & Worm 2009), most inferences have been based on before−after comparisons of change following predator removals or additions.”
BackgroundComposition of cetacean communities worldwide shapes their contribution to ocean nutrient cycling
Gilbert, L., du Dot, T. J., Authier, M., Tiphaine Chouvelon, A., & Spitz, J. (2023) · Nature Communications · doi:10.1038/s41467-023-41532-y · Cited by 53
“Differences between the two groups are signi fi cant only in the Mediterranean Sea for N, P, Fe, Mn and Zn ( p ≤ 4.0 e − 4 , Supplementary Data 2).”
BackgroundInfluentialHammerschlag, N., Williams, L., Fallows, M., & Fallows, C. (2019) · Scientific Reports · doi:10.1038/s41598-018-37576-6 · Cited by 53
Maureaud, A. A., Andersen, K. H., Zhang, L., & Lindegren, M. (2020) · Journal of Animal Ecology · doi:10.1111/1365-2656.13207 · Cited by 52
Sterling, E. J., Gómez, A., & Porzecanski, A. L. (2010) · BioEssays · doi:10.1002/bies.201000049 · Cited by 53
Navarro, J., Sáez‑Liante, R., Albo-Puigserver, M., Coll, M., & Palomera, I. (2017) · Deep Sea Research Part II Topical Studies in Oceanography · doi:10.1016/j.dsr2.2016.06.009 · Cited by 46
Luiz, O. J., Mendes, T. C., Barneche, D. R., Ferreira, C. G., Noguchi, R., Villaça, R. C., Rangel, C. A., Gasparini, J. L. R., & Ferreira, C. E. L. (2015) · Marine and Freshwater Research · doi:10.1071/mf14150 · Cited by 54
Effects of Fishing and Regional Species Pool on the Functional Diversity of Fish Communities
Martins, G. M., Arenas, F., Neto, A. I., & Jenkins, S. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044297 · Cited by 59
“Vulnerability to extinction is also predicted to increase with both body size and trophic level [4,30–33].”
BackgroundMolfese, C., Beare, D., & Hall-Spencer, J. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0101506 · Cited by 52
Gaichas, S., Aydin, K., & Francis, R. C. (2011) · Canadian Journal of Fisheries and Aquatic Sciences · doi:10.1139/f2011-080 · Cited by 52
López, S., Abarca, N. L., & Meléndez, R. (2013) · Tropical Conservation Science · doi:10.1177/194008291300600103 · Cited by 52
“Also, data to assess direct impacts of exploitation on these large sharks are limited, but consistently indicate that they have been driven to low levels of abundance [49,50].”
BackgroundCould Seals Prevent Cod Recovery in the Baltic Sea?
MacKenzie, B. R., Eero, M., & Ojaveer, H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018998 · Cited by 51
Halting Regime Shifts in Floristically Intact Tropical Forests Deprived of Their Frugivores
Brodie, J. F., & Aslan, C. E. (2011) · Restoration Ecology · doi:10.1111/j.1526-100x.2011.00833.x · Cited by 51
“This process resembles the ecosystem regime shifts that have been observed in many habitat types following extirpation of key predators with resulting cascading effects on herbivore and plant populations (e.g. Croll et al. 2005; Baum & Worm 2009).”
BackgroundInfluentialSea ice phenology and primary productivity pulses shape breeding success in Arctic seabirds
Ramı́rez, F., Tarroux, A., Hovinen, J. E. H., Navarro, J., Afán, I., Forero, M. G., & Descamps, S. (2017) · Scientific Reports · doi:10.1038/s41598-017-04775-6 · Cited by 57
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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