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Filter Feeding 363 FILTER FEEDING 363 of direct handouts of fish offered by people, and many species of likely drove the return of mammals to the ocean where they were odonotocetes remove either bait or fish from fishing lines. In the able to exploit highly productive coastal waters. With their return Bering Sea and off Southern Brazil, killer whales may damage over to the sea, marine mammals evolved a wide range of physiological 20% of the fish captured by longline fisheries. However, a number and morphological adaptations for feeding in water. Filter feeding of dolphin species from coastal (e.g., Tursiops truncatus, Sousa teu- is exhibited by baleen whales (Mysticeti) and three species of pinni- zii) and riverine (e.g., Orcaella brevirostris, Inia geoffrensis, P. ganget- peds (crabeater seals, Lobodon carcinophaga; leopard seals, Hydrurga ica) habitats also enhance coastal fisheries where both dolphins and leptonyx; and Antarctic fur seals, Arctocephalus gazella). Although fishermen take advantage of dolphin foraging. filter feeding is not found in terrestrial mammals, it has evolved Both the diversity of habitats in which marine mammals live and independently in multiple lineages of aquatic invertebrates and the flexibility of individuals have led to the wide variety of forag- vertebrates. ing tactics exhibited by the group. Further studies of these tactics In marine mammals, filter feeding facilitates the exploitation are still of great interest, especially systematic investigations of of extremely abundant, but small schooling fish and crustaceans the function and use of particular tactics and the circumstances in (e.g., krill or copepods) by capturing many individual prey items which they are employed. Such detailed studies will improve the in a single feeding event. This is useful in marine systems because ability to predict influences of anthropogenic changes to marine they have low standing biomass and high turnover of small-sized habitats and prey availability on marine mammals, and aid in efforts primary producers that respond rapidly to nutrient availability, and to conserve them. because marine ecosystems tend to be more patchy and ephem- eral than terrestrial systems due to spatial differences in physical See Also the Following Articles dynamics. Thus, the abundance and distribution of schooling fish F Behavior, Overview n Feeding Morphology n Filter Feeding n Tool and crustaceans reflects the spatial dynamics of marine primary Use production. Most marine mammals are primary carnivores and rely on these dense, patchily distributed aggregations of schooling prey. References The patchiness of prey means that filter feeding marine mammals Beck, B.B. (1980). “Animal Tool Behavior: The Use and Manufacture of must often travel long distances to locate prey, and annual migra- Tools by Animals”. Garland Press, New York. tions to seasonal feeding grounds is a hallmark of baleen whale life Boyd, I.L. (1997). The behavioural and physiological ecology of diving. history. Long distance migration across ocean basins is facilitated Trends Ecol. Evol. 12, 213–217. by the large body sizes of marine mammals, especially mysticetes, Frid, A., Heithaus, M.R., and Dill, L.M. (2006). Dangerous dive cycles and the proverbial ostrich. Oikos 116, 893–902. that provides low mass-specific metabolic rates and low cost of Giraldeau, L.A. (1988). The stable group and the determinants of transport (Croll et al., 2005). Thus, large body size buffers for the foraging group size. In “The Ecology of Social Behavior” (C.N. patchy and ephemeral distribution of marine prey because larger Slobodchikoff Ed.), pp. 33–53. Academic Press, New York. individuals can survive longer periods and travel longer distances Gross, M.R. (1996). Alternative reproductive strategies and tactics: between feeding events. However, a consequence of larger body size Diversity within sexes. Trends Ecol. Evol. 11, 92–98. is a higher absolute daily prey requirement. Kramer, D.L. (1988). The behavioral ecology of air breathing by aquatic Filter feeding allows individuals to capture and process large animals. Can. J. Zool. 66, 89–94. quantities of prey in a single mouth full, thus allowing them to Lima, S.L., and Dill, L.M. (1990). Behavioral decisions made under the acquire energy at high rates when small prey are at high densities risk of predation: A review and prospectus. Can. J. Zool. 68, 619–640. (Goldbogen et al., 2011). Large body size in mysticetes is associ- Mesterson-Gibbons, M., and Dugatkin, L.A. (1992). Cooperation among unrelated individuals: Evolutionary factors. Q. Rev. Biol. 67, ated with a relatively larger mouth enhancing intake capacity for 267–281. filter feeding (Goldbogen et al., 2010). The combination of large Packer, C., and Ruttan, L. (1988). The evolution of cooperative hunting. body size and filter feeding allows some marine mammals to exploit Am. Nat. 132, 159–198. extremely high densities of schooling prey that develop at high lati- Tregenza, T. (1995). Building on the ideal free distribution. Adv. Ecol. tudes during the spring and summer and in other areas of high pro- Res. 26, 253–307. ductivity. If resources are not available in the winter, large body size Wells, R.S., Boness, D.L., and Rathburn, G.B. (1999). Behavior. In provides an energy store for fasting in place or for long distance “Biology of Marine Mammals” (J.E. Reynolds and S. A. Rommel, migration without feeding (Brodie, 1975). Eds), pp. 324–422. Smithsonian Institution Press, Washington, DC. Due to this dependency on patchy but extremely productive food Wirsing, A.J., Heithaus, M.R., Frid, A., and Dill, L.M. (2008). Seascapes resources, it is hypothesized that filter feeding whales first evolved of fear: Methods for evaluating sublethal predator effects experi- enced and generated by marine mammals. Mar. Mamm. Sci. 24, 1–15. and radiated in the Southern Hemisphere during the Oligocene at the initiation of the Antarctic circumpolar current (ACC). It is generally agreed that the initiation of the ACC led to cooling of the Southern Oceans, increased nutrient availability, and thus increased FILTER FEEDING productivity. Although this increased productivity may have pro- vided a rich resource of zooplankton that could be effectively DONALD A. CROLL, BERNIE R. TERSHY, exploited through filter feeding, the discovery of a late Oligocene KELLY M. NEWTON, ASHA DE VOS, ELLIOTT HAZEN fossil archaic mysticete that was a nonfilter feeding predator casts AND JEREMY A. GOLDBOGEN doubt on the suggestion that the initial radiation of mysticetes was linked to the filter feeding (Fitzgerald, 2006). Present-day filter-feeding marine mammals concentrate forag- I. Filter Feeding and the Marine Environment ing in productive high-latitude and coastal upwelling regions, with A critical necessity for organisms is acquiring sufficient food the Southern Ocean recognized as one of the most important forag- for maintenance, growth, and reproduction. This search for food ing area for filter-feeding marine mammals. Indeed, prior to their 364 FILTER FEEDING exploitation by humans, some of the greatest densities of mysti- the dentition of crabeater and leopard seals. In both species elab- cetes occurred in highly productive waters of the Southern Ocean. orate cusps have developed on the postcanines in both the upper Crabeater seals, Antarctic fur seals, and leopard seals are also found and lower jaws (Fig. 1) (Berta and Sumich, 1999). Using suction primarily in the Southern Oceans where seasonally dense aggrega- as a potential engulfment mechanism (Hocking et al., 2013), the tions of krill develop (Berta and Sumich, 1999). mouth closes around a small group of prey (i.e., krill), water is fil- tered out through the cusps, trapping krill in the modified teeth. II. Diet, Filter-Feeding Structures, Little detailed information is available on the behavior used by fil- and Prey Capture ter-feeding pinnipeds to capture prey. However, data from Antarctic All filter-feeding species feed on prey that form dense aggrega- fur seals and crabeater seals indicate that they track the diel migra- tions (primarily pelagic schooling fish and crustaceans or densely tion of krill: shallow dives during night and deeper dives during day aggregated benthic amphipods). Two feeding adaptations have (Boyd and Croxall, 1992). evolved to allow the exploitation of these dense aggregations: baleen (mysticete whales) and modified dentition (seals). B. Mysticetes—Diet and Feeding Morphology Most mysticetes feed primarily on planktonic or micronec- A. Seals—Diet, Feeding Morphology, and Behavior tonic crustaceans (copepods and krill) and pelagic schooling fish. Unlike mysticetes, pinnipeds evolved in the Northern Gray whales, Eschrichtius robustus, however, feed primarily on ben- Hemisphere where krill was not likely an important component of thic gammarid amphipods. Right, Eubalaena spp., and bowhead, their diet, and adaptations for filter feeding are not as extensive in Balaena mysticetus, whales primarily feed on copepod crustaceans of F pinnipeds as in mysticetes. the genus Calanus. All rorquals feed on euphausiids (krill) to some Only three pinnipeds are thought to filter feed on small zoo- extent, and blue whales, Balaenoptera musculus, feed almost exclu- plankton: crabeater seals, leopard seals, and Antarctic fur seals sively upon euphausiids (see section on krill). The other rorquals (Riedman, 1990; Hocking et al., 2013). When presumably filter have a more varied diet that includes copepods (sei whales, B. bore- feeding, all the three species feed almost
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