Cited by 932Marine and fisheries researchMarine animal studies overviewCoral and Marine Ecosystems Studies

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Cascading top-down effects of changing oceanic predator abundances

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Baum, Julia K., Worm, Boris·2009·Journal of Animal Ecology

DOI 10.1111/j.1365-2656.2009.01531.x

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Abstract

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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BackgroundInfluential
Experimental demonstration of a trophic cascade in the Galápagos rocky subtidal: Effects of consumer identity and behavior
Witman, J. D., Smith, F., & Novak, M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0175705 · Cited by 16
Modeling the dynamic habitats of mobile pelagic predators (Makaira nigricans and Istiompax indica) in the eastern Pacific Ocean
Farchadi, N., Hinton, M. G., Thompson, A., & Yin, Z. (2019) · Marine Ecology Progress Series · doi:10.3354/meps12996 · Cited by 17
“This, combined with climate change, pollution, and other anthropogenic activities, can put unprecedented pressure on higher trophic level predators, such as tunas, billfishes, or sharks, which may cascade downward through the food web and affect ecosystem function- ality (Baum & Worm 2009).”
Background
High‐quality whole‐genome sequence of an abundant Holarctic odontocete, the harbour porpoise ( Phocoena phocoena )
Autenrieth, M., Hartmann, S. A., Lah, L., Roos, A. M., Dennis, A. B., & Tiedemann, R. (2018) · Molecular Ecology Resources · doi:10.1111/1755-0998.12932 · Cited by 17
Compensation masks trophic cascades in complex food webs
Fahimipour, A. K., Anderson, K. E., & Williams, R. J. (2017) · Theoretical Ecology · doi:10.1007/s12080-016-0326-8 · Cited by 16
“However results have been mixed, with studies reporting both strong (Frank et al, 2006, 2007; Baum and Worm, 2009) and weak or noisy (Borer et al, 2005; Fox, 2007) associations between diversity measures and cascade strengths.”
Result
Effects of predator presence and habitat complexity on reef fish communities in The Bahamas
Hensel, E., Allgeier, J. E., & Layman, C. A. (2019) · Marine Biology · doi:10.1007/s00227-019-3568-3 · Cited by 16
Dietary niche differentiation in a mesopredatory dasyatid assemblage
Elston, C., Cowley, P. D., von Brandis, R. G., & Fisk, A. T. (2020) · Marine Biology · doi:10.1007/s00227-020-03695-w · Cited by 16
“2008; Baum and Worm 2009).”
Background
Ecological responses to blue water MPAs
Gilman, E. L., Chaloupka, M. Y., Fitchett, M., Cantrell, D. L., & Merrifield, M. (2020) · PLoS ONE · doi:10.1371/journal.pone.0235129 · Cited by 16
Direct and Indirect Effects of Invasive vs. Native Ant-Hemipteran Mutualism: A Meta-Analysis That Supports the Mutualism Intensity Hypothesis
Wang, B., Lu, M., Peng, Y., & Segar, S. T. (2021) · Agronomy · doi:10.3390/agronomy11112323 · Cited by 16
“On the other hand, this may be due to other factors influencing interaction occurrence and strength [54,55], for example, the population density of interacting species, host plant status, the time of observations, and weather [56].”
Background
Novel Fish Predator Causes Sustained Changes in Its Prey Populations
Nurkse, K., Kotta, J., Szava‐Kovats, R., Herkül, K., Eschbaum, R., & Vetemaa, M. (2022) · Frontiers in Marine Science · doi:10.3389/fmars.2022.849878 · Cited by 16
“Top-down trophic cascades in various ecosystems have been illustrated mainly in literature through the removal of top predators from the ecosystems (Terborgh et al., 2001; Worm and Myers, 2003; Elmhagen and Rushton, 2007; Baum and Worm, 2009).”
Background
When descriptive ecology meets physiology: a study in a South Atlantic rhodolith bed
de Carvalho, V. F., Silva, J., Kerr, R., Anderson, A. B., Bastos, E., Cabral, D. Q., Gouvêa, L. P., Peres, L., Martins, C. D. L., Silveira-Andrade, V. M., et al. (2020) · Journal of the Marine Biological Association of the United Kingdom · doi:10.1017/s0025315420000284 · Cited by 16
“(1) Top-down control (Worm & Myers, 2003; Begon et al., 2006; Baum & Worm, 2009): population increase mediated by predators in the studied area over time (2015–2016).”
Background
Forest conversion to oil palm compresses food chain length in tropical streams
Wilkinson, C. L., Chua, K. W. J., Fiala, R., Liew, J. H., Kemp, V. A., Fikri, A. H., Ewers, R. M., Kratina, P., & Yeo, D. C. J. (2020) · Ecology · doi:10.1002/ecy.3199 · Cited by 18
Using marine reserves to manage impact of bottom trawl fisheries requires consideration of benthic food‐web interactions
van Denderen, P. D., Rijnsdorp, A. D., & van Kooten, T. (2016) · Ecological Applications · doi:10.1002/eap.1360 · Cited by 15
“There are a variety of studies that have shown top-down effects of benthivorous fish (and benthic invertebrate predators) on abundance of their benthic prey (Wilson 1991, Baum and Worm 2009).”
Background
Diets of Atlantic Sharpnose Shark (Rhizoprionodon terraenovae) and Bonnethead (Sphyrna tiburo) in the northern Gulf of Mexico
Harrington, T., Plumlee, J. D., Drymon, J. M., & Wells, D. J. (2016) · Gulf and Caribbean Research · doi:10.18785/gcr.2701.05 · Cited by 15
“Keywords: stomach contents, feeding ecology, coastal sharks IntroductIon Predators play a critical role in the structure and function of marine ecosystems (Baum and Worm 2009).”
Background
Temporal and spatial isotopic variability of marine prey species in south-eastern Australia: Potential implications for predator diet studies
Rodríguez‐Malagón, M. A., Speakman, C. N., Sutton, G. J., Angel, L. P., & Arnould, J. P. Y. (2021) · PLoS ONE · doi:10.1371/journal.pone.0259961 · Cited by 15
“Within marine environments, top predators play an important role as top-down controllers of prey species, nutrient cyclers and ecosystem engineers [23].”
Background
New technologies can support data collection on endangered shark species in the Mediterranean Sea
Bargnesi, F., Moro, S., Leone, A., Giovos, I., & Ferretti, F. (2022) · Marine Ecology Progress Series · doi:10.3354/meps14030 · Cited by 15
Ontogenetic shift in diet and trophic role of Raja clavata inferred by stable isotopes and stomach content analysis in the Sea of Marmara
Gül, G., & Demirel, N. (2022) · Journal of Fish Biology · doi:10.1111/jfb.15123 · Cited by 15
Invasive species control with apex predators: increasing presence of wolves is associated with reduced occurrence of the alien raccoon dog
Selonen, V., Brommer, J. E., Holopainen, S., Kauhala, K., Krüger, H., Poutanen, J., Väänänen, V., & Laaksonen, T. (2022) · Biological Invasions · doi:10.1007/s10530-022-02850-2 · Cited by 15
“The arrival of an alien mesopredator may increase competition between mesopredator species in the community (Baum and Worm 2009; Wallach et al. 2015).”
Background
Vulnerability to overfishing of fish stocks in the Amazon Basin
Pereira, D. V., Mereles, M. D. A., de Matos, O. F., Lopes, G. C. D. S., Conceição, K. G., & Freitas, C. E. D. C. (2023) · Fisheries Research · doi:10.1016/j.fishres.2023.106740 · Cited by 17
Multiple lines of evidence highlight the dire straits of yellowfin tuna in the Indian Ocean.
Heidrich, K. N., Meeuwig, J. J., Juan‐Jordá, M. J., Palomares, M. L. D., Pauly, D. F., Thompson, C. D. H., Friedlander, A. M., Sala, E., & Zeller, D. C. (2023) · Ocean & Coastal Management · doi:10.1016/j.ocecoaman.2023.106902 · Cited by 22
“Their overexploitation can have various ecological consequences, including impacts on trophic integrity (Baum and Worm, 2009), reduced ecosystem productivity (Sumaila et al., 2011), and diminished resilience to environmental change (Srinivasan et al., 2010; Ortu ˜ no Crespo & Dunn, 2017).”
Background
A global ecological signal of extinction risk in marine ray-finned fishes (class Actinopterygii)
Bak, T. M., Camp, R. J., Heim, N. A., McCauley, D. J., Payne, J. L., & Knope, M. L. (2023) · Cambridge Prisms Extinction · doi:10.1017/ext.2023.23 · Cited by 15
“Reductions in large predatory fishes driven by overfishing have been associated with increases in meso-predator and other prey abundances (Dulvy et al., 2004; Baum and Worm, 2009) as well as ecologically consequential changes in prey behavior (Madin et al., 2010).”
Latitudinal and ontogenetic variation in the diet of a pelagic mesopredator (Pomatomus saltatrix), assessed with a classification tree analysis
Schilling, H. T., Hughes, J. M., Smith, J. A., Everett, J. D., Stewart, J., & Suthers, I. M. (2017) · Marine Biology · doi:10.1007/s00227-017-3105-1 · Cited by 15
Links between fish abundance and ocean biogeochemistry as recorded in marine sediments
Kavanagh, L., & Galbraith, E. D. (2018) · PLoS ONE · doi:10.1371/journal.pone.0199420 · Cited by 15
“…potential mechanisms by which fish might influence biogeochem-istry, the provision of firm observational constraints is hampered by the spatio-temporal variability of ocean circulation and lower trophic level processes, the highly motile nature of fish, and confounding environmental changes [10].”
Spatial distribution, seasonal abundance and exploitation status of shark species in Kenyan coastal waters
Kiilu, B., Kaunda‐Arara, B., Oddenyo, R. M., Thoya, P. Z., & Njiru, J. (2019) · African Journal of Marine Science · doi:10.2989/1814232x.2019.1624614 · Cited by 15
“Sharks, as apex predators, are now widely acknowledged to play a key role in maintaining ecosystem health, diversity and stability (Heithaus et al. 2008; Baum and Worm 2009).”
Background
Evidence of nitrification associated with globally distributed pelagic jellyfish
Hubot, N. D., Giering, S. L. C., Füssel, J., Robidart, J. C., Birchill, A. J., Stinchcombe, M. C., Dumousseaud, C., & Lucas, C. H. (2021) · Limnology and Oceanography · doi:10.1002/lno.11736 · Cited by 15
“Overall, the complex interaction of jellyfish with the food web can have large impacts on ecosystem structure, function and resilience (Baum and Worm 2009).”
Background
Feeding ecology of the long finned pilot whale, Globicephala melas edwardii, in the southwestern Atlantic Ocean, determined by stable isotopes analysis
Becker, Y. A., Fioramonti, N. E., Dellabianca, N. A., & Riccialdelli, L. (2021) · Polar Biology · doi:10.1007/s00300-021-02908-2 · Cited by 15
Detection of the Largest Deep-Sea-Endemic Teleost Fish at Depths of Over 2,000 m Through a Combination of eDNA Metabarcoding and Baited Camera Observations
Fujiwara, Y., Tsuchida, S., Kawato, M., Masuda, K., Sakaguchi, S. O., Sado, T., Miya, M. U., & Yoshida, T. (2022) · Frontiers in Marine Science · doi:10.3389/fmars.2022.945758 · Cited by 15
Potential impacts of ocean warming on the trophic control of a threatened marine ecosystem
Yin, J., Zhang, C., Xue, Y. W., Ji, Y., Xu, B., & Ren, Y. (2023) · Progress In Oceanography · doi:10.1016/j.pocean.2023.102976 · Cited by 15
How detectable is predation in stage‐structured populations? Insights from a simulation‐testing analysis
Oken, K. L., & Essington, T. E. (2014) · Journal of Animal Ecology · doi:10.1111/1365-2656.12274 · Cited by 15
Environmentally‐mediated consumer control of algal proliferation in Florida springs
Liebowitz, D. M., Cohen, M. J., Heffernan, J. B., Korhnak, L. V., & Frazer, T. K. (2014) · Freshwater Biology · doi:10.1111/fwb.12403 · Cited by 15
Disentangling Habitat Concepts for Demersal Marine Fish Management
Elliott, S. A. M., Milligan, R., Heath, M. R., Turrell, W. R., & Bailey, D. M. (2016) · Oceanography and Marine Biology/Oceanography and marine biology - an annual review · doi:10.1201/9781315368597-4 · Cited by 15
Environment-driven changes in terrestrial habitat use and distribution of the Galapagos sea lion
Montero‐Serra, I., Páez‐Rosas, D., Murillo, J., Vegas-Vilarrúbia, T. E., Fietz, K., & Denkinger, J. (2013) · Endangered Species Research · doi:10.3354/esr00573 · Cited by 15
Humans and Sharks
Panoch, R., & Pearson, E. L. (2017) · Society and Animals · doi:10.1163/15685306-12341441 · Cited by 15
Modeling the population dynamics of lemon sharks
White, E. R., Nagy, J. D., & Gruber, S. H. (2014) · Biology Direct · doi:10.1186/1745-6150-9-23 · Cited by 15
“For example, as predators, sharks not only regulate their own prey populations but also those of species deeper in the food web [5,7-9] (see also [10] for a recent review).”
Background
Whistle Classification of Sympatric False Killer Whale Populations in Hawaiian Waters Yields Low Accuracy Rates
Barkley, Y. M., Oleson, E. M., Oswald, J. N., & Franklin, E. C. (2019) · Frontiers in Marine Science · doi:10.3389/fmars.2019.00645 · Cited by 14
“Changes to their abundance and distributions have cascading effects that affect complex interactions between multiple trophic levels within the oceanic food web (Heithaus et al., 2008; Baum and Worm, 2009; Estes et al., 2011; Kiszka et al., 2015).”
Background
Trophic strategies of three predatory pelagic fish coexisting in the north-western Mediterranean Sea over different time spans
Navarro, J., Albo‐Puigserver, M., Serra‐Marin, P. E., Sáez‐Liante, R., & Marta Coll, M. (2020) · Estuarine Coastal and Shelf Science · doi:10.1016/j.ecss.2020.107040 · Cited by 14
“Pelagic predators have top-down effects on marine communities, and thus a reduction in their populations could have important impacts on ecosystems (Baum and Worm, 2009; Ward and Myers, 2005).”
Background
The Relative Abundance and Occurrence of Sharks off Ocean Beaches of New South Wales, Australia
Monteforte, K. I., Butcher, P. A., Morris, S., & Kelaher, B. P. (2022) · Biology · doi:10.3390/biology11101456 · Cited by 14
Trophic cascades and climate change
Ripple, W. J., Whalen, D., Wolf, C., Cao, Y., Schulte, J. M., Swann, S., Woodrich, S. T., Newsome, T. M., Cairncross, R. J., & Wirsing, A. J. (2024) · Food Webs · doi:10.1016/j.fooweb.2024.e00362 · Cited by 17
Non-invasive methods characterise the world’s largest tiger shark aggregation in Fuvahmulah, Maldives
Vossgaetter, L., Dudeck, T., Crouch, J., Cope, M., Ivanova, T., Siyan, I., Niyaz, A., Riyaz, M., & Araújo, G. (2024) · Scientific Reports · doi:10.1038/s41598-024-73079-3 · Cited by 14
Transmitting species‐interaction data from animal‐borne transceivers through Service Argos using Bluetooth communication
Lidgard, D. C., Bowen, W. D., Jonsen, I. D., McConnell, B. J., Lovell, P., Webber, D. M., Stone, T., & Iverson, S. J. (2014) · Methods in Ecology and Evolution · doi:10.1111/2041-210x.12235 · Cited by 14
“However, in comparison to terrestrial and inter-tidal environments, our understanding of species interactions involvingmarine top predators is limited due to their wide-ranging and relatively inaccessible nature (Heithaus et al. 2008; Baum & Worm 2009).”
Background
Density-driven habitat use differences across fishing zones by predator fishes (Serranidae) in south-western Mediterranean rocky reefs
Hackradt, C. W., Félix‐Hackradt, F. C., Treviño-Otón, J., Pérez‐Ruzafa, Á., & García‐Charton, J. A. (2019) · Hydrobiologia · doi:10.1007/s10750-019-04135-7 · Cited by 14
Spatial trophic variability of a coastal apex predator, the giant trevally Caranx ignobilis, in the western Indian Ocean
Glass, J. R., Daly, R., Cowley, P. D., & Post, D. (2020) · Marine Ecology Progress Series · doi:10.3354/meps13305 · Cited by 14
Discovery of a colossal slickhead (Alepocephaliformes: Alepocephalidae): an active-swimming top predator in the deep waters of Suruga Bay, Japan
Fujiwara, Y., Kawato, M., Poulsen, J. Y., Ida, H., Chikaraishi, Y., Ohkouchi, N., OGURI, K., Gotoh, S., Ozawa, G., Tanaka, S., et al. (2021) · Scientific Reports · doi:10.1038/s41598-020-80203-6 · Cited by 14
Direct and indirect effects of marine protection: rockfish conservation areas as a case study
Cloutier, R. N. (2010) · Summit (Simon Fraser University) · Cited by 14
Non‐consumptive effects of avian predators on fish behavior and cascading indirect interactions in seagrasses
Hill, J. M., & Heck, K. L. (2014) · Oikos · doi:10.1111/oik.01774 · Cited by 14

Authors: Baum, J. K., & Worm, B.
Affiliations: Dalhousie University (CA)
Corresponding author: Baum, Julia K.
ORCID: Baum, Julia K.
Worm, Boris
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
DOI: 10.1111/j.1365-2656.2009.01531.x
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
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
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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Cascading top-down effects of changing oceanic predator abundances

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