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Ecological Effects of Marine Mammals
Ecological Effects of Marine Mammals
The use of relatively short broadband echolocation signals by whistling dolphins is probably the most important factor in the dolphin’s good discrimination capabilities. The broad frequency range of hearing extending over 10 octaves and the good peak sensitivity of 30–40 dB re 1 mPa are certainly contributing factors in the dolphin’s echolocation capabilities. Another feature of the dolphin’s auditory system that contributes to its good echolocation capabilities is the extremely rapid response of its auditory nervous system. The auditory nervous system of the dolphin probably responds faster than that of any other animal if the relative dimensions of the auditory system are taken into account. Finally, dolphins are extremely mobile and can investigate objects at different aspects and angles to maximize the amount of echo information from objects and thus enhance their echolocation capabilities.
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Purves, P. E., and Pilleri, G. (1983). “Echolocation in Whales and Dolphins.” Academic Press, London. Ridgway, S. H. (1983). Dolphin hearing and sound production in health and illness. In “Hearing and Other Senses: Presentations in Honor of E. G. Wever” (R. R. Fay, and G. Gourevitch, eds), pp. 247–296. Amphora Press, Gronton.
Ecological Effects of Marine Mammals JAMES A. ESTES
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Aroyan, J. L. (2001). Three-dimensional modeling of hearing in Delphinus delphis. J. Acoust. Soc. Am. 110, 3305–3318. Au, W. W. L. (1993). “The Sonar of Dolphins.” Springer-Verlag, New York. Au, W. W. L., and Benoit-Bird, K. J. (2003). Automatic gain control in the echolocation system of dolphin. Nature 423, 861–863. Au, W. W. L., and Würsig, B. (2004). Echolocation signals of dusky dolphins (Lagenorhynchus obscurus) in Kaikoura, New Zealand. J. Acous. Soc. Am. 115, 2307–2313. Au, W. W. L., Kastelein, R. A., Rippe, T., and Schooneman, N. M. (1999). Transmission beam pattern and echolocation signals of a harbor porpoise (Phocoena phocoena). J. Acoust. Soc. Am. 106, 3699–3705. Bullock, T. H., Grinnell, A. D., Ikezono, E., Kameda, K., Katsuki, Y., Nomoto, M., Sato, O., Suga, N., and Yanagisawa, K. (1968). Electrophysiological studies of the central auditory mechanisms in cetaceans. J. Compar. Physiol. A. 59, 117–156. Cranford, T. W. (1988). The anatomy of acoustic structures in the spinner dolphin forehead as shown by X-ray computed tomography and computer graphics. In “Animal Sonar: Processes and Performance” (P. E. Nactigall, and P. W. B. Moore, eds), pp. 67–77. Plenum Publishing, New York. Cranford, T. W., Van Bonn, W. G., Chaplin, M. S., Carr, J. A., Kamolnick, T. A., Carder, D. A., and Ridgway, S. H. (1997). Visualizing dolphin sonar signal generation using high-speed video endoscopy. J. Acoust. Soc. Am. 102, 3123. Kastelein, R. A., Au, W. W. L., Rippe, T., and Schooneman, N. M. (1999). Target detection by an echolocating harbor porpoise (Phocoena phocoena). J. Acoust. Soc. Am. 105, 2493–2498. Li, S., Wang, D., Wang, K., and Akamatsu, T. (2006). Sonar gain control in echolocating finless porpoises (Neophocaena phocaenoides) in open waters. J. Acoust. Soc. Am. 120, 1803–1806. MacBride, A. F. (1956). Evidence for echolocation in cetaceans. Deep Sea Res. 3, 153–154. Møhl, B., Au, W. W. L., Pawloski, J. L., and Nachtigall, P. E. (1999). Dolphin hearing: relative hearing as a function of point of application of a contact sound source in the jaw and head region. J. Acoust. Soc. Am. 105, 3421–3424. Norris, K. S. (1968). The echolocation of marine mammals. In “The Biology of Marine Mammals” (H. T. Andersen, ed.), pp. 391–423. Academic Press, New York. Norris, K. S., Prescott, J. H., Asa-Dorian, P. V., and Perkins, P. (1961). An experimental demonstration of echo-location behavior in the porpoise, Tursiops truncatus. Biol. Bull. 120, 163–176.
tors
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here are two ways in which marine mammals and their ecosystems can interact. One encompasses the effects of the ecosystem on marine mammals; the other, the effects of marine mammals on their ecosystems (Fig. 1). Ocean scientists in general and marine mammalogists in particular often consider their worlds from the former perspective. However, the latter perspective should also be of interest for two main reasons. First, there is a large and growing body of evidence from diverse ecosystems for the ecological importance of large vertebrate consumers, including several marine mammal species (Pace et al., 1999; Shurin et al., 2002). And second, significant ecological effects of marine mammals are implied from their great abundance, high trophic status, high metabolic rates, and the resulting fact that some of these consumers co-opt significant proportions of their ecosystem’s primary production (Estes et al., 2006). Many marine mammal species have been depleted through overexploitation for protein, oil, and other products. A few others have increased dramatically in recent years due to protection from human harassment or perhaps other factors. If marine mammals are important drivers of ecosystem structure and function, the ecological effects resulting from these changes in their abundance could be substantial. It follows that the structure and function of future world oceans may depend critically on the way in which the distribution and abundance of marine mammals are managed.
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Ocean ecosystems
Figure 1 Cartoon drawing illustrating the various interactions between marine mammals and their ecosystems.
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Ecological Effects of Marine Mammals
I. Conceptualizing and Understanding Interaction Web Processes A. The Nature of Species Interactions
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Before considering the ecological roles of marine mammals in marine ecosystems, it is important to reflect on the diverse ways in which species interact with one another and how these processes can be understood. The influence of any one species on another can be categorized broadly as positive, negative, or neutral. The most ubiquitous and important species interactions probably are those that occur between consumers and their prey. Consumers are fueled by the things they eat and thus the influences of prey on their consumers are usually positive. Prey are killed by the things that eat them and thus the influences of consumers on their prey are usually negative. Competitive interactions between any two species are defined by reciprocal negativity. These interactions can be weak or strong, symmetrical or asymmetric, and manifested through exploitation of a shared resource or behavioral interference. Mutualisms are defined by reciprocal positive relationships. Like competitive interactions, these can be weak or strong, symmetrical or asymmetric. Unlike competitive interactions, mutualisms take many forms.
B. Bottom-Up vs Top-Down Forcing Bottom-up forcing occurs when the distribution and abundance of species are influenced by production and the efficiency of energy transfer upward through the food web. Top-down forcing occurs when the distribution and abundance of species are influenced by the impacts of consumers on their prey (Hunter and Price, 1992). These processes are not mutually exclusive nor do they act independently from one another. Bottom-up effects are ubiquitous in nature whereas top-down effects may not be. The important questions for this chapter are whether or not top-down forcing processes influence the structure and organization of marine mammaldominated ecosystems and if so, the relative degree to which variation in bottom-up vs top-down forcing is responsible for changes in the distribution and abundance of marine mammals and their prey.
states arise within similar species assemblages because the transition vectors (i.e., the forces that drive population change following a perturbation) are commonly strongly non-linear and the pathways of historical context are highly unpredictable. Given this well-known feature of ecosystem dynamics on the one hand and the fact that so many marine mammal populations and their ecosystems have been extensively perturbed by various human-induced influences on the other, there is strong likelihood that the recovery of these systems will lead to alternate states.
II. Approaches to Understanding While the distribution and abundance of species are relatively easy to observe and measure, species interactions are invisible and therefore difficult to grasp. Two approaches (philosophies) have been employed in efforts to observe and measure the strength of species interactions.
A. Perturbation Approaches Perturbation-based approaches derive from the assumption that species interactions maintain ecosystems in equilibrium or quasiequilibrium states, and thus that the interaction web pathways and their strengths can be observed and measured from responses to single species perturbations. Perturbation experiments have been done in three general ways. One of these is through purposeful manipulations, ideally conducted in a controlled and replicated manner. Properly executed over adequate scales of space and time, experiments of this nature provide the least equivocal evidence for species interactions. Most marine mammals cannot be purposefully manipulated for logistic, ethical, and legal reasons. Thus natural experiments based on fortuitous perturbations is another approach that has been used to understand the ecological roles of these and other large, mobile species. Yet another approach is to use historical records to infer the nature of species interactions through the retrospective analysis of patterns of covariation in the abundance of species over time. The scales of such historical analyses have varied from decades or centuries in the case of records obtained by modern humans, to millions of years for those based on the geological record.
C. Direct Vs Indirect Effects Species may interact with one another directly or indirectly. The direct effects of one species on another are those that occur in the absence of intervening species. Indirect effects, in contrast, include one or more intervening species. The indirect effect of predators on lower trophic status species through top-down forcing is known as a trophic cascade (Paine, 1980). It is important to recognize that for any community of species there are vastly more potential indirect than direct interactions (Estes, 2005).
D. Alternate Stable States Contrary to a widely held view that underlies much of natural resource management and conservation, the same assemblage of species in similar physical settings does not necessarily organize itself in a single manner. In fact, there is growing evidence for alternate stable-state systems, among which the nature of species interactions and the abundances and distributions of species can differ substantially (Scheffer et al., 2001). There are numerous specific causes for this seemingly peculiar feature of ecosystem behavior (Doak et al., 2008). Cultural differences in foraging behavior can develop among individuals within a species as the result of serendipitous events that may be entirely lost to specific explanation. In general, alternate stable
B. Constructionist Approaches Finding informative perturbations and using them to answer specific questions can be challenging. An alternative approach to understanding species interactions is to construct model interaction webs from information on species distributions, abundances, diets, metabolic rates, life histories, behaviors, etc., and then to observe how the model system responds to perturbations of interest. The Ecopath/ Ecosim/Ecospace family of mass balance models is one well-known example of this approach (Pauly et al., 2000), although the coupling of energetics and demography to estimate the strength of both bottom-up and top-down trophic effects and a variety of other methods have also been used. By and large, these constructionist approaches are more useful in evaluating the plausibility of particular hypotheses than in predicting population or ecosystem change.
III. Case Studies A. Otters Sea (Enhydra lutris) otters and the nearshore habitats in which they live provide the clearest and most compelling evidence for the ecological effects of a marine mammal. One reason for the utility of
Ecological Effects of Marine Mammals
this particular system is that the Pacific maritime fur trade perturbed sea otter populations in such a way that their ecological effects could be observed on appropriate scales of space and time. Another helpful attribute is that many of the key species in the sea otter’s coastal ecosystem are easy to observe, measure, and experimentally manipulate. Studies built around the decline and recovery of sea otters have shown that they limit the size, abundance, and distribution of their benthic invertebrate prey in both soft-sediment and rocky-reef habitats. These and other studies have further demonstrated that the control of herbivorous sea urchins by sea otter predation helps to maintain kelp forests on shallow reefs across much of the North Pacific Ocean (Estes and Duggins, 1995). This trophic cascade from otters to sea urchins to kelp indirectly affects other species and ecosystem processes through increased production, the creation of three-dimensional habitat (the kelp forest), and reduced water flow. The interactions resulting from sea otter predation may have exerted strong selective influences on various other species (Steinberg et al., 1995; Estes et al., 2005). North American otters also have important ecosystem-level effects, which are founded on a characteristic high latitude sea-to-land production gradient. By foraging at sea and defecating at traditional landbased sprainting sites, North American otters vector nutrients from the sea to the land, thereby increasing secondary production, altering plant species composition, and generating habitat heterogeneity across coastal landscapes. In areas where sea otters and North American otters coexist, sea otters may enhance the effects of North American otters by increasing production and fish abundance in the coastal marine ecosystem. The direct and indirect effects of sea otters and North American otters are discussed in the chapter on OTTERS, MARINE.
B. Sirenians Like sea otters, sirenians live in coastal marine systems where many of the species with which they interact can be observed and manipulated. Because sirenians are exclusively herbivores, their direct impacts are on aquatic plant assemblages. Dugongs (Dugong dugon) in the tropical southwest Pacific Ocean provide the clearest evidence for the ecological effects of sirenians. Foraging dugongs uproot seagrasses, reducing their overall biomass, and creating heterogeneous habitats. These effects are clearly evident in seagrass meadows and have even been used to determine the presence or absence of dugongs in particular areas. By generating organic detritus, disturbing the substrate, and suspending sediments, dugong foraging has numerous effects on seagrass species composition and succession, as well as on associated species of invertebrates and fishes. The intensity of dugong foraging on seagrass meadows varies seasonally in Western Australia because of changes in dugong habitat utilization in response to the risk of tiger shark (Galeocerdo cuvier) predation. When large tiger sharks are present during the warm season, dugongs tend to forsake the shallower seagrass-dominated habitats in favor of deeper channels where presumably they are better able to avoid shark attacks. Dugongs also change the way they feed in seagrass meadows (more cropping and less substrate excavation) when sharks are abundant. Large sharks therefore reduce the overall impact of dugong foraging in seagrass-dominated systems. Although the kelp-eating Steller’s sea cow (Hydrodamalis gigas) has been extinct for 250 years, the possible role of this species as an herbivore in kelp forest ecosystems is the subject of long-standing interest and speculation. Grazing sea cows may have created light
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gaps in the surface canopy-forming kelps, thereby increasing benthic illumination and releasing the competitively subordinate under story kelps from light limitation. Steller’s sea cows are believed by most experts to have succumbed to extinction from direct human exploitation. However, others have argued that sea cows may only have been able to persist through an indirect asymmetric mutualism with sea otters, and thus that the sea cow’s demise may have been caused or at least facilitated by kelp forest collapses resulting from human overexploitation of sea otters. Because manatees (Trichechus spp.) tend to inhabit highly turbid tropical rivers and streams, relatively little is known of their effects in these systems.
C. Pinnipeds The ecological effects of pinnipeds are poorly known, due in part to the perspective from which they have been studied and in part to the absence of opportunity. With several notable exceptions, the interactions between pinnipeds and their prey have commonly been viewed from a bottom-up perspective. Furthermore, the areas of the ocean where pinnipeds feed are intrinsically more difficult to study than those described above for marine otters and sirenians. Despite these limiting perspectives and the limited opportunities for empirically based studies, there are reasons to suspect that pinnipeds are strong interactors in some ecosystems. Pinnipeds have relatively high field metabolic rates and live at high population densities compared with terrestrial carnivores of comparable body size. Pinniped foraging ranges are often limited by distance from shore, thus concentrating their potential ecological effects in relatively narrow bands of coastal habitat. The most compelling case study of a consumer-induced effect by pinnipeds involves harbor seals (Phoca vitulina) trapped in the lakes of eastern Canada. As freshwater lakes were formed following the retreating Pleistocene ice sheet, harbor seals survived in some of these but not others, thus providing the opportunity to contrast lake systems with and without seals. Such contrasts suggest that seal predation affected the size, species composition, and life history patterns of salmonids (Power and Gregoire, 1978). Smaller scale studies have been done on the influences of benthic feeding walruses in the western Arctic. Walruses not only reduce prey biomass, they create pits in the substrate that accumulate detritus, thus facilitating a detritivore-based food web. The only other substantive efforts to document the ecological effects of pinnipeds come from constructionist approaches, most of which have focused on competition between pinnipeds and fisheries. The distribution, abundance, and behavior of several pinniped species may be influenced by the realization or risk of predation. Various recent population declines have been attributed to predation by sharks and killer whales (Orcinus orca). Striking behavioral contrasts in the reaction of pagophilic (ice-associated) pinnipeds to humans between the Northern (fright reactions) and Southern Hemispheres (generally tame) are purportedly due in large measure to the differential risk of predation from polar bears (Ursus maritimus) and humans in the Northern Hemisphere.
D. Cetaceans The potential influence of cetaceans on marine ecosystems is intriguing because of the antiquity of cetacean evolution, the diversity of foraging modes employed by various mysticetes and odontocetes, and because cetaceans comprise far more consumer biomass
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Ecological Effects of Marine Mammals
than other marine mammal groups (Estes et al., 2006). This latter feature suggests not only large effects of cetaceans on their associated ecosystems, but a release from any such effects following the overexploitation of whales by industrial whaling. As is generally true for pinnipeds, the ecological effects of small cetaceans are mostly unexplored, for likely the same reasons. The great whales are thought to be ecologically important because of their influences as predators, as prey, and as detritus (Fig. 1).
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1. As Predators Gray whale (Eschrichtius robustus) foraging on the Bering Sea shelf probably provides the clearest example of consumer-induced effects by a large cetacean. Gray whales consume various epibenthic and infaunal invertebrates, in the process re-suspending large quantities of sediment and nutrients. Gray whale feeding pits contain 50% less invertebrate biomass, and a fauna dominated more by free-living scavenger amphipods compared with the tube-building amphipods and polychaetes that characterize unexploited sites. The rate of sediment re-suspension from gray whale feeding is substantial, equaling or exceeding the rate of sediment input from the major rivers that enter the Bering Sea. This latter process must have a wide range of influences on marine fishes, birds, and mammals in the highly productive Bering Sea Ecosystem. Other consumer-induced effects by great whales are known or suspected. The depletion of once abundant krill-feeding mysticetes by industrial whaling in the Southern Ocean purportedly led to more abundant krill, in turn resulting in improved body condition, earlier reproduction, and population increases by other krill-feeding species, including the smaller-bodied mysticetes and odontocetes, penguins, and various pinnipeds. Similar kinds of effects likely occurred in squid-based food webs following the reduction of sperm whales. Time series analyses further suggest that predatory fishes and piscivorous or semi-piscivorous whales once competed for what may have been a jointly limiting forage-fish prey base in both the North Atlantic and North Pacific Oceans. 2. As Prey Because of their large size, great abundance, and high energy density, the great whales represent a valuable nutritional resource for both human and animal consumers. At least one large predator, the killer whale, is known to attack and consume great whales. These behemoths therefore were quite possibly an important prey resource for killer whales, especially prior to industrial whaling. Modern industrial whaling may have facilitated this interaction by dispatching the living whales, advertising their locations through the sounds produced by exploding harpoons and preventing the carcasses from sinking by injecting them with gas, thereby greatly extending the periods of time carcasses were available on the ocean’s surface to scavenging by killer whales. The reduction of great whales through industrial whaling and the sudden elimination of harvested carcasses as a food resource for killer whales at the end of the industrial whaling era, may have caused transient killer whales to expand their diets to include smaller marine mammal species, ultimately resulting in population declines of some of these. Although there are numerous records of attacks by killer whales on various great whales, and living whales commonly have rake marks on their flukes from failed killer whale attacks, the importance of consumer– prey interactions between killer whales and large whales is much contended. 3. As Detritus Dead whales that are not immediately consumed either wash ashore or sink to the sea floor. Although whale falls only constitute an estimated 0.3% of the particulate organic flux to the seafloor, these materials are highly concentrated so that the area in
the immediate vicinity of a fallen carcass receives the equivalent of several thousand years of organic carbon input in a single pulse. A diverse assemblage of species (approximately 370 in the North Pacific Ocean alone) utilizes these carcasses, some of which appear to be obligate associates of whale falls. Whale falls typically undergo a succession of stages upon reaching the sea floor. These include an initial mobile-scavenger stage, in which organisms like sleeper sharks (Somniosus spp.), hagfish, crabs, and amphipods remove flesh from the carcass; an enrichmentopportunist stage in which invertebrates and heterotrophic bacteria colonize the organic carbon-rich skeleton and surrounding sediments; a sulfophilic stage in which chemoautotrophic organisms exploit the sulfide emitting anaerobic decomposition of skeletal lipids; and a reef stage in which organisms exploit the physical structure of inorganic skeletal remains. Because the first three of these stages may require decades to run their course, the effects of whaling on deep sea assemblages are perhaps only now becoming manifest. Marine mammals in general and large whales in particular provide important nutritional resources to various terrestrial vertebrates, including bears, foxes, eagles, and condors. The demise of the California condor (Gymnogyps californianus) may have been facilitated by the whaling-induced reduction in stranded carcasses.
IV. Density-Mediated Vs Trait-Mediated Effects The aforementioned examples all are of what have been referred to as density-mediated effects, or those for which the interaction strength is determined by mass–energy relationships between consumers and prey. Consumers can also influence their ecosystems through trait-mediated effects or behavioral responses to the risk of being eaten. Trait-mediated effects have been referred to under the rubric of “the ecology of fear.” Although the study of trait-mediated effects is still in its infancy, various and sundry examples illustrate their potential importance to the dynamics of consumer–prey interactions involving marine mammals (Box 1). Density- and trait-mediated effects usually are complementary rather than antagonistic, with trait-mediated effects likely being the more important of the two in some instances.
V. Future Directions Although marine mammals clearly can have important and farreaching effects on marine ecosystems, at this juncture the support for this contention comes mostly from theory, analogy with other species and ecosystems, and a smattering of case studies (Bowen, 1997). What might scientists do to better understand the ecological roles of marine mammals in the sea? One useful approach would be to document associated changes in the ecosystem as marine mammal populations grow or decline, keeping in mind and controlling for the potentially confounding influences of other environmental factors. Another potentially useful approach would be to use theory and interdisciplinary synthesis to better define the limits of ecosystem behavior. Modeling approaches involving demography, energetics, and behavior could be used to answer such important questions as whether killer whale/marine mammal assemblages are sustainable without killer whale predation on great whales, and if marine mammal population changes are more sensitive to bottom-up or top-down forcing. These latter approaches cannot provide definitive answers, but they can establish the plausibility of hypothesized processes,
Ecology, Overview
which is an important step in the search. Finally, marine mammalogists should continue to expand their conceptual visions and conduct their research in the company of interdisciplinary collaborators.
Box 1 Trait-mediated effects of consumers on their prey may complement density-mediated effects, establishing qualitatively new pathways of important species interactions and even exceeding or overriding the more traditionally understood density-mediated effects in some systems (Wirsing et al., in press). The following select examples illustrate the range of known or suspected trait-mediated effects in marine mammaldominated systems. ● Great whale migrations from high-latitude foraging areas to low-latitude breeding and calving sites were once thought to function primarily as a means of energy conservation through reduced heat loss in the warmer tropical or subtropical oceans. Subsequent analyses, and the fact that not all large whales migrate toward the equator to reproduce, cast doubt on this explanation. An alternative (and still contended) hypothesis is that large whales migrate to low-productivity tropical waters to reduce the risk of predation by killer whales on the highly vulnerable newborn calves. ● Dugongs spend more time feeding in shallow seagrass meadows during the cool seasons, when large sharks are rare, than during the warm seasons when large sharks are relatively abundant. This behavioral response to the risk of attack by sharks reduces the intensity of disturbance and herbivory by dugongs just as though they were actually being eaten by the predator. ● As sea otters re-colonized long unoccupied habitats in British Columbia, they foraged on the abundant red sea urchins (Strongylocentrotus franciscanus) in kelpdeforested ecosystems that had developed in their absence. The damaged urchin tests and other uneaten remains were dropped to the seafloor where they elicited a flight response by healthy conspecifics. Kelps re-colonized areas from which the urchins had fled just as though they had been directly removed by sea otter predation.
See Also the Following Articles Biogeography ■ Distribution ■ Ecology, Overview ■ Habitat Use
References Bowen, W. D. (1997). The role of marine mammals in aquatic ecosystems. Mar. Ecol. Prog. Ser. 158, 267–274. Doak, D. F. et al. (14 authors) (2008). Understanding and predicting ecological dynamics: Are major surprises inevitable? Ecology: 89, 952–961. Estes, J. A. (2005). Carnivory and trophic connectivity in kelp forests. In “Large Carnivores and the Conservation of Biodiversity” (J. C. Ray, K. H. Redford, R. S. Steneck, and J. Berger, eds), pp. 61–81. Island Press, Washington, DC. Estes, J. A., and Duggins, D. O. (1995). Sea otters and kelp forests in Alaska: Generality and variation in a community ecological paradigm. Ecol. Monogr. 65, 75–100.
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Estes, J. A., Lindberg, D. R., and Wray, C. (2005). Evolution of large body size in abalones (Haliotis): Patterns and implications. Paleobiology 31, 591–606. Estes, J. A., DeMaster, D. P., Brownell, R. L., Jr., Doak, D. F., and Williams, T. M. (2006). Retrospection and review. In “Whales, Whaling and Ocean Ecosystems” (J. A. Estes, D. P. DeMaster, D. F. Doak, T. M. Williams, and R. L. Brownell, Jr., eds), pp. 388– 393. University of California Press, Berkeley, CA. Hunter, M. D., and Price, P. W. (1992). Playing chutes and ladders: Heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73, 724–732. Pace, M. L., Cole, J. J., Carpenter, S. R., and Kitchell, J. G. (1999). Trophic cascades revealed in diverse ecosystems. Trends Ecol. Evol. 14, 483–488. Paine, R. T. (1980). Food webs: Linkage, interaction strength, and community infrastructure. J. Anim. Ecol. 49, 667–685. Pauly, D., Christensen, V., and Walters, C. (2000). Ecopath, Ecosim, and Ecospace as tools for evaluating ecosystem impact of fisheries. ICES J. Mar. Sci. 57, 697–706. Polis, G.E., Power, M.E. and Huxel, G.R. (eds), (2004). Food Webs at the Landscape Level. University of Chicago Press, Chicago, IL. Power, G., and Gregoire, J. (1978). Predation by fresh water seals on the fish community of Lower Seal Lake, Quebec. J. Fish. Res. Board Can. 35, 844–850. Scheffer, M., Carpenter, S., Foley, J. A., Folke, C., and Walker, B. (2001). Catastrophic shifts in ecosystems. Nature 413, 591–596. Shurin, J. B., et al. (8 authors) (2002). A cross-ecosystem comparison of the strength of trophic cascades. Ecol. Lett. 5, 785–791. Steinberg, P. D., Estes, J. A., and Winter, F. C. (1995). Evolutionary consequences of food chain length in kelp forest communities. Proc. Natl. Acad. Sci. USA 92, 8145–8148. Wirsing, A. A., Heithaus, M. R., Frid, A., and Dill, A. M. (2008). Seascapes of fear: Evaluating sublethal predator effects experienced and generated by marine mammals. Mar. Mamm. Sci. 24, 1–15. Wootton, J. T., and Emmerson, M. (2005). Measurement of interaction strength in nature. Ann. Rev. Ecol. Evolution Syst. 36, 419–444.
Ecology, Overview BERND WÜRSIG
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arine mammals have entered just about all ocean habitats, and several mighty rivers and inshore seas as well. Only the deep abyss is foreign to them, but—remarkably— elephant seals (Mirounga spp.), sperm whales (Physeter macrocephalus), and several other toothed whales can “easily” dive to depths that exceed 1000 m, where it is cold and dark and where the pressure is 100 times and more what we experience on land. Perhaps just as remarkable is the fact that some of these divers, the pinnipeds, are also able to live on land, where they mate, give birth, and molt. Morphologic, physiologic, and behavioral adaptations to the environments of marine mammals are largely driven by their food and the habitats of their prey. Although there are various ways that ecological adaptations can be divided, this article does so by several broad-based general habitat types: open ocean, semipelagic, coastal, and riverine feeding and breeding habitats and—for pinnipeds and the polar bear (Ursus maritimus)—their obligatory stint on land to breed.
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The use of relatively short broadband echolocation signals by whistling dolphins is probably the most important factor in the dolphin’s good discrimination capabilities. The broad frequency range of hearing extending over 10 octaves and the good peak sensitivity of 30–40 dB re 1 mPa are certainly contributing factors in the dolphin’s echolocation capabilities. Another feature of the dolphin’s auditory system that contributes to its good echolocation capabilities is the extremely rapid response of its auditory nervous system. The auditory nervous system of the dolphin probably responds faster than that of any other animal if the relative dimensions of the auditory system are taken into account. Finally, dolphins are extremely mobile and can investigate objects at different aspects and angles to maximize the amount of echo information from objects and thus enhance their echolocation capabilities.
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Purves, P. E., and Pilleri, G. (1983). “Echolocation in Whales and Dolphins.” Academic Press, London. Ridgway, S. H. (1983). Dolphin hearing and sound production in health and illness. In “Hearing and Other Senses: Presentations in Honor of E. G. Wever” (R. R. Fay, and G. Gourevitch, eds), pp. 247–296. Amphora Press, Gronton.
Ecological Effects of Marine Mammals JAMES A. ESTES
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Aroyan, J. L. (2001). Three-dimensional modeling of hearing in Delphinus delphis. J. Acoust. Soc. Am. 110, 3305–3318. Au, W. W. L. (1993). “The Sonar of Dolphins.” Springer-Verlag, New York. Au, W. W. L., and Benoit-Bird, K. J. (2003). Automatic gain control in the echolocation system of dolphin. Nature 423, 861–863. Au, W. W. L., and Würsig, B. (2004). Echolocation signals of dusky dolphins (Lagenorhynchus obscurus) in Kaikoura, New Zealand. J. Acous. Soc. Am. 115, 2307–2313. Au, W. W. L., Kastelein, R. A., Rippe, T., and Schooneman, N. M. (1999). Transmission beam pattern and echolocation signals of a harbor porpoise (Phocoena phocoena). J. Acoust. Soc. Am. 106, 3699–3705. Bullock, T. H., Grinnell, A. D., Ikezono, E., Kameda, K., Katsuki, Y., Nomoto, M., Sato, O., Suga, N., and Yanagisawa, K. (1968). Electrophysiological studies of the central auditory mechanisms in cetaceans. J. Compar. Physiol. A. 59, 117–156. Cranford, T. W. (1988). The anatomy of acoustic structures in the spinner dolphin forehead as shown by X-ray computed tomography and computer graphics. In “Animal Sonar: Processes and Performance” (P. E. Nactigall, and P. W. B. Moore, eds), pp. 67–77. Plenum Publishing, New York. Cranford, T. W., Van Bonn, W. G., Chaplin, M. S., Carr, J. A., Kamolnick, T. A., Carder, D. A., and Ridgway, S. H. (1997). Visualizing dolphin sonar signal generation using high-speed video endoscopy. J. Acoust. Soc. Am. 102, 3123. Kastelein, R. A., Au, W. W. L., Rippe, T., and Schooneman, N. M. (1999). Target detection by an echolocating harbor porpoise (Phocoena phocoena). J. Acoust. Soc. Am. 105, 2493–2498. Li, S., Wang, D., Wang, K., and Akamatsu, T. (2006). Sonar gain control in echolocating finless porpoises (Neophocaena phocaenoides) in open waters. J. Acoust. Soc. Am. 120, 1803–1806. MacBride, A. F. (1956). Evidence for echolocation in cetaceans. Deep Sea Res. 3, 153–154. Møhl, B., Au, W. W. L., Pawloski, J. L., and Nachtigall, P. E. (1999). Dolphin hearing: relative hearing as a function of point of application of a contact sound source in the jaw and head region. J. Acoust. Soc. Am. 105, 3421–3424. Norris, K. S. (1968). The echolocation of marine mammals. In “The Biology of Marine Mammals” (H. T. Andersen, ed.), pp. 391–423. Academic Press, New York. Norris, K. S., Prescott, J. H., Asa-Dorian, P. V., and Perkins, P. (1961). An experimental demonstration of echo-location behavior in the porpoise, Tursiops truncatus. Biol. Bull. 120, 163–176.
tors
References
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here are two ways in which marine mammals and their ecosystems can interact. One encompasses the effects of the ecosystem on marine mammals; the other, the effects of marine mammals on their ecosystems (Fig. 1). Ocean scientists in general and marine mammalogists in particular often consider their worlds from the former perspective. However, the latter perspective should also be of interest for two main reasons. First, there is a large and growing body of evidence from diverse ecosystems for the ecological importance of large vertebrate consumers, including several marine mammal species (Pace et al., 1999; Shurin et al., 2002). And second, significant ecological effects of marine mammals are implied from their great abundance, high trophic status, high metabolic rates, and the resulting fact that some of these consumers co-opt significant proportions of their ecosystem’s primary production (Estes et al., 2006). Many marine mammal species have been depleted through overexploitation for protein, oil, and other products. A few others have increased dramatically in recent years due to protection from human harassment or perhaps other factors. If marine mammals are important drivers of ecosystem structure and function, the ecological effects resulting from these changes in their abundance could be substantial. It follows that the structure and function of future world oceans may depend critically on the way in which the distribution and abundance of marine mammals are managed.
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Brain ■ Hearing ■ Song ■ Sound Production
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See Also the Following Articles
Ocean ecosystems
Figure 1 Cartoon drawing illustrating the various interactions between marine mammals and their ecosystems.
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Ecological Effects of Marine Mammals
I. Conceptualizing and Understanding Interaction Web Processes A. The Nature of Species Interactions
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Before considering the ecological roles of marine mammals in marine ecosystems, it is important to reflect on the diverse ways in which species interact with one another and how these processes can be understood. The influence of any one species on another can be categorized broadly as positive, negative, or neutral. The most ubiquitous and important species interactions probably are those that occur between consumers and their prey. Consumers are fueled by the things they eat and thus the influences of prey on their consumers are usually positive. Prey are killed by the things that eat them and thus the influences of consumers on their prey are usually negative. Competitive interactions between any two species are defined by reciprocal negativity. These interactions can be weak or strong, symmetrical or asymmetric, and manifested through exploitation of a shared resource or behavioral interference. Mutualisms are defined by reciprocal positive relationships. Like competitive interactions, these can be weak or strong, symmetrical or asymmetric. Unlike competitive interactions, mutualisms take many forms.
B. Bottom-Up vs Top-Down Forcing Bottom-up forcing occurs when the distribution and abundance of species are influenced by production and the efficiency of energy transfer upward through the food web. Top-down forcing occurs when the distribution and abundance of species are influenced by the impacts of consumers on their prey (Hunter and Price, 1992). These processes are not mutually exclusive nor do they act independently from one another. Bottom-up effects are ubiquitous in nature whereas top-down effects may not be. The important questions for this chapter are whether or not top-down forcing processes influence the structure and organization of marine mammaldominated ecosystems and if so, the relative degree to which variation in bottom-up vs top-down forcing is responsible for changes in the distribution and abundance of marine mammals and their prey.
states arise within similar species assemblages because the transition vectors (i.e., the forces that drive population change following a perturbation) are commonly strongly non-linear and the pathways of historical context are highly unpredictable. Given this well-known feature of ecosystem dynamics on the one hand and the fact that so many marine mammal populations and their ecosystems have been extensively perturbed by various human-induced influences on the other, there is strong likelihood that the recovery of these systems will lead to alternate states.
II. Approaches to Understanding While the distribution and abundance of species are relatively easy to observe and measure, species interactions are invisible and therefore difficult to grasp. Two approaches (philosophies) have been employed in efforts to observe and measure the strength of species interactions.
A. Perturbation Approaches Perturbation-based approaches derive from the assumption that species interactions maintain ecosystems in equilibrium or quasiequilibrium states, and thus that the interaction web pathways and their strengths can be observed and measured from responses to single species perturbations. Perturbation experiments have been done in three general ways. One of these is through purposeful manipulations, ideally conducted in a controlled and replicated manner. Properly executed over adequate scales of space and time, experiments of this nature provide the least equivocal evidence for species interactions. Most marine mammals cannot be purposefully manipulated for logistic, ethical, and legal reasons. Thus natural experiments based on fortuitous perturbations is another approach that has been used to understand the ecological roles of these and other large, mobile species. Yet another approach is to use historical records to infer the nature of species interactions through the retrospective analysis of patterns of covariation in the abundance of species over time. The scales of such historical analyses have varied from decades or centuries in the case of records obtained by modern humans, to millions of years for those based on the geological record.
C. Direct Vs Indirect Effects Species may interact with one another directly or indirectly. The direct effects of one species on another are those that occur in the absence of intervening species. Indirect effects, in contrast, include one or more intervening species. The indirect effect of predators on lower trophic status species through top-down forcing is known as a trophic cascade (Paine, 1980). It is important to recognize that for any community of species there are vastly more potential indirect than direct interactions (Estes, 2005).
D. Alternate Stable States Contrary to a widely held view that underlies much of natural resource management and conservation, the same assemblage of species in similar physical settings does not necessarily organize itself in a single manner. In fact, there is growing evidence for alternate stable-state systems, among which the nature of species interactions and the abundances and distributions of species can differ substantially (Scheffer et al., 2001). There are numerous specific causes for this seemingly peculiar feature of ecosystem behavior (Doak et al., 2008). Cultural differences in foraging behavior can develop among individuals within a species as the result of serendipitous events that may be entirely lost to specific explanation. In general, alternate stable
B. Constructionist Approaches Finding informative perturbations and using them to answer specific questions can be challenging. An alternative approach to understanding species interactions is to construct model interaction webs from information on species distributions, abundances, diets, metabolic rates, life histories, behaviors, etc., and then to observe how the model system responds to perturbations of interest. The Ecopath/ Ecosim/Ecospace family of mass balance models is one well-known example of this approach (Pauly et al., 2000), although the coupling of energetics and demography to estimate the strength of both bottom-up and top-down trophic effects and a variety of other methods have also been used. By and large, these constructionist approaches are more useful in evaluating the plausibility of particular hypotheses than in predicting population or ecosystem change.
III. Case Studies A. Otters Sea (Enhydra lutris) otters and the nearshore habitats in which they live provide the clearest and most compelling evidence for the ecological effects of a marine mammal. One reason for the utility of
Ecological Effects of Marine Mammals
this particular system is that the Pacific maritime fur trade perturbed sea otter populations in such a way that their ecological effects could be observed on appropriate scales of space and time. Another helpful attribute is that many of the key species in the sea otter’s coastal ecosystem are easy to observe, measure, and experimentally manipulate. Studies built around the decline and recovery of sea otters have shown that they limit the size, abundance, and distribution of their benthic invertebrate prey in both soft-sediment and rocky-reef habitats. These and other studies have further demonstrated that the control of herbivorous sea urchins by sea otter predation helps to maintain kelp forests on shallow reefs across much of the North Pacific Ocean (Estes and Duggins, 1995). This trophic cascade from otters to sea urchins to kelp indirectly affects other species and ecosystem processes through increased production, the creation of three-dimensional habitat (the kelp forest), and reduced water flow. The interactions resulting from sea otter predation may have exerted strong selective influences on various other species (Steinberg et al., 1995; Estes et al., 2005). North American otters also have important ecosystem-level effects, which are founded on a characteristic high latitude sea-to-land production gradient. By foraging at sea and defecating at traditional landbased sprainting sites, North American otters vector nutrients from the sea to the land, thereby increasing secondary production, altering plant species composition, and generating habitat heterogeneity across coastal landscapes. In areas where sea otters and North American otters coexist, sea otters may enhance the effects of North American otters by increasing production and fish abundance in the coastal marine ecosystem. The direct and indirect effects of sea otters and North American otters are discussed in the chapter on OTTERS, MARINE.
B. Sirenians Like sea otters, sirenians live in coastal marine systems where many of the species with which they interact can be observed and manipulated. Because sirenians are exclusively herbivores, their direct impacts are on aquatic plant assemblages. Dugongs (Dugong dugon) in the tropical southwest Pacific Ocean provide the clearest evidence for the ecological effects of sirenians. Foraging dugongs uproot seagrasses, reducing their overall biomass, and creating heterogeneous habitats. These effects are clearly evident in seagrass meadows and have even been used to determine the presence or absence of dugongs in particular areas. By generating organic detritus, disturbing the substrate, and suspending sediments, dugong foraging has numerous effects on seagrass species composition and succession, as well as on associated species of invertebrates and fishes. The intensity of dugong foraging on seagrass meadows varies seasonally in Western Australia because of changes in dugong habitat utilization in response to the risk of tiger shark (Galeocerdo cuvier) predation. When large tiger sharks are present during the warm season, dugongs tend to forsake the shallower seagrass-dominated habitats in favor of deeper channels where presumably they are better able to avoid shark attacks. Dugongs also change the way they feed in seagrass meadows (more cropping and less substrate excavation) when sharks are abundant. Large sharks therefore reduce the overall impact of dugong foraging in seagrass-dominated systems. Although the kelp-eating Steller’s sea cow (Hydrodamalis gigas) has been extinct for 250 years, the possible role of this species as an herbivore in kelp forest ecosystems is the subject of long-standing interest and speculation. Grazing sea cows may have created light
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gaps in the surface canopy-forming kelps, thereby increasing benthic illumination and releasing the competitively subordinate under story kelps from light limitation. Steller’s sea cows are believed by most experts to have succumbed to extinction from direct human exploitation. However, others have argued that sea cows may only have been able to persist through an indirect asymmetric mutualism with sea otters, and thus that the sea cow’s demise may have been caused or at least facilitated by kelp forest collapses resulting from human overexploitation of sea otters. Because manatees (Trichechus spp.) tend to inhabit highly turbid tropical rivers and streams, relatively little is known of their effects in these systems.
C. Pinnipeds The ecological effects of pinnipeds are poorly known, due in part to the perspective from which they have been studied and in part to the absence of opportunity. With several notable exceptions, the interactions between pinnipeds and their prey have commonly been viewed from a bottom-up perspective. Furthermore, the areas of the ocean where pinnipeds feed are intrinsically more difficult to study than those described above for marine otters and sirenians. Despite these limiting perspectives and the limited opportunities for empirically based studies, there are reasons to suspect that pinnipeds are strong interactors in some ecosystems. Pinnipeds have relatively high field metabolic rates and live at high population densities compared with terrestrial carnivores of comparable body size. Pinniped foraging ranges are often limited by distance from shore, thus concentrating their potential ecological effects in relatively narrow bands of coastal habitat. The most compelling case study of a consumer-induced effect by pinnipeds involves harbor seals (Phoca vitulina) trapped in the lakes of eastern Canada. As freshwater lakes were formed following the retreating Pleistocene ice sheet, harbor seals survived in some of these but not others, thus providing the opportunity to contrast lake systems with and without seals. Such contrasts suggest that seal predation affected the size, species composition, and life history patterns of salmonids (Power and Gregoire, 1978). Smaller scale studies have been done on the influences of benthic feeding walruses in the western Arctic. Walruses not only reduce prey biomass, they create pits in the substrate that accumulate detritus, thus facilitating a detritivore-based food web. The only other substantive efforts to document the ecological effects of pinnipeds come from constructionist approaches, most of which have focused on competition between pinnipeds and fisheries. The distribution, abundance, and behavior of several pinniped species may be influenced by the realization or risk of predation. Various recent population declines have been attributed to predation by sharks and killer whales (Orcinus orca). Striking behavioral contrasts in the reaction of pagophilic (ice-associated) pinnipeds to humans between the Northern (fright reactions) and Southern Hemispheres (generally tame) are purportedly due in large measure to the differential risk of predation from polar bears (Ursus maritimus) and humans in the Northern Hemisphere.
D. Cetaceans The potential influence of cetaceans on marine ecosystems is intriguing because of the antiquity of cetacean evolution, the diversity of foraging modes employed by various mysticetes and odontocetes, and because cetaceans comprise far more consumer biomass
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than other marine mammal groups (Estes et al., 2006). This latter feature suggests not only large effects of cetaceans on their associated ecosystems, but a release from any such effects following the overexploitation of whales by industrial whaling. As is generally true for pinnipeds, the ecological effects of small cetaceans are mostly unexplored, for likely the same reasons. The great whales are thought to be ecologically important because of their influences as predators, as prey, and as detritus (Fig. 1).
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1. As Predators Gray whale (Eschrichtius robustus) foraging on the Bering Sea shelf probably provides the clearest example of consumer-induced effects by a large cetacean. Gray whales consume various epibenthic and infaunal invertebrates, in the process re-suspending large quantities of sediment and nutrients. Gray whale feeding pits contain 50% less invertebrate biomass, and a fauna dominated more by free-living scavenger amphipods compared with the tube-building amphipods and polychaetes that characterize unexploited sites. The rate of sediment re-suspension from gray whale feeding is substantial, equaling or exceeding the rate of sediment input from the major rivers that enter the Bering Sea. This latter process must have a wide range of influences on marine fishes, birds, and mammals in the highly productive Bering Sea Ecosystem. Other consumer-induced effects by great whales are known or suspected. The depletion of once abundant krill-feeding mysticetes by industrial whaling in the Southern Ocean purportedly led to more abundant krill, in turn resulting in improved body condition, earlier reproduction, and population increases by other krill-feeding species, including the smaller-bodied mysticetes and odontocetes, penguins, and various pinnipeds. Similar kinds of effects likely occurred in squid-based food webs following the reduction of sperm whales. Time series analyses further suggest that predatory fishes and piscivorous or semi-piscivorous whales once competed for what may have been a jointly limiting forage-fish prey base in both the North Atlantic and North Pacific Oceans. 2. As Prey Because of their large size, great abundance, and high energy density, the great whales represent a valuable nutritional resource for both human and animal consumers. At least one large predator, the killer whale, is known to attack and consume great whales. These behemoths therefore were quite possibly an important prey resource for killer whales, especially prior to industrial whaling. Modern industrial whaling may have facilitated this interaction by dispatching the living whales, advertising their locations through the sounds produced by exploding harpoons and preventing the carcasses from sinking by injecting them with gas, thereby greatly extending the periods of time carcasses were available on the ocean’s surface to scavenging by killer whales. The reduction of great whales through industrial whaling and the sudden elimination of harvested carcasses as a food resource for killer whales at the end of the industrial whaling era, may have caused transient killer whales to expand their diets to include smaller marine mammal species, ultimately resulting in population declines of some of these. Although there are numerous records of attacks by killer whales on various great whales, and living whales commonly have rake marks on their flukes from failed killer whale attacks, the importance of consumer– prey interactions between killer whales and large whales is much contended. 3. As Detritus Dead whales that are not immediately consumed either wash ashore or sink to the sea floor. Although whale falls only constitute an estimated 0.3% of the particulate organic flux to the seafloor, these materials are highly concentrated so that the area in
the immediate vicinity of a fallen carcass receives the equivalent of several thousand years of organic carbon input in a single pulse. A diverse assemblage of species (approximately 370 in the North Pacific Ocean alone) utilizes these carcasses, some of which appear to be obligate associates of whale falls. Whale falls typically undergo a succession of stages upon reaching the sea floor. These include an initial mobile-scavenger stage, in which organisms like sleeper sharks (Somniosus spp.), hagfish, crabs, and amphipods remove flesh from the carcass; an enrichmentopportunist stage in which invertebrates and heterotrophic bacteria colonize the organic carbon-rich skeleton and surrounding sediments; a sulfophilic stage in which chemoautotrophic organisms exploit the sulfide emitting anaerobic decomposition of skeletal lipids; and a reef stage in which organisms exploit the physical structure of inorganic skeletal remains. Because the first three of these stages may require decades to run their course, the effects of whaling on deep sea assemblages are perhaps only now becoming manifest. Marine mammals in general and large whales in particular provide important nutritional resources to various terrestrial vertebrates, including bears, foxes, eagles, and condors. The demise of the California condor (Gymnogyps californianus) may have been facilitated by the whaling-induced reduction in stranded carcasses.
IV. Density-Mediated Vs Trait-Mediated Effects The aforementioned examples all are of what have been referred to as density-mediated effects, or those for which the interaction strength is determined by mass–energy relationships between consumers and prey. Consumers can also influence their ecosystems through trait-mediated effects or behavioral responses to the risk of being eaten. Trait-mediated effects have been referred to under the rubric of “the ecology of fear.” Although the study of trait-mediated effects is still in its infancy, various and sundry examples illustrate their potential importance to the dynamics of consumer–prey interactions involving marine mammals (Box 1). Density- and trait-mediated effects usually are complementary rather than antagonistic, with trait-mediated effects likely being the more important of the two in some instances.
V. Future Directions Although marine mammals clearly can have important and farreaching effects on marine ecosystems, at this juncture the support for this contention comes mostly from theory, analogy with other species and ecosystems, and a smattering of case studies (Bowen, 1997). What might scientists do to better understand the ecological roles of marine mammals in the sea? One useful approach would be to document associated changes in the ecosystem as marine mammal populations grow or decline, keeping in mind and controlling for the potentially confounding influences of other environmental factors. Another potentially useful approach would be to use theory and interdisciplinary synthesis to better define the limits of ecosystem behavior. Modeling approaches involving demography, energetics, and behavior could be used to answer such important questions as whether killer whale/marine mammal assemblages are sustainable without killer whale predation on great whales, and if marine mammal population changes are more sensitive to bottom-up or top-down forcing. These latter approaches cannot provide definitive answers, but they can establish the plausibility of hypothesized processes,
Ecology, Overview
which is an important step in the search. Finally, marine mammalogists should continue to expand their conceptual visions and conduct their research in the company of interdisciplinary collaborators.
Box 1 Trait-mediated effects of consumers on their prey may complement density-mediated effects, establishing qualitatively new pathways of important species interactions and even exceeding or overriding the more traditionally understood density-mediated effects in some systems (Wirsing et al., in press). The following select examples illustrate the range of known or suspected trait-mediated effects in marine mammaldominated systems. ● Great whale migrations from high-latitude foraging areas to low-latitude breeding and calving sites were once thought to function primarily as a means of energy conservation through reduced heat loss in the warmer tropical or subtropical oceans. Subsequent analyses, and the fact that not all large whales migrate toward the equator to reproduce, cast doubt on this explanation. An alternative (and still contended) hypothesis is that large whales migrate to low-productivity tropical waters to reduce the risk of predation by killer whales on the highly vulnerable newborn calves. ● Dugongs spend more time feeding in shallow seagrass meadows during the cool seasons, when large sharks are rare, than during the warm seasons when large sharks are relatively abundant. This behavioral response to the risk of attack by sharks reduces the intensity of disturbance and herbivory by dugongs just as though they were actually being eaten by the predator. ● As sea otters re-colonized long unoccupied habitats in British Columbia, they foraged on the abundant red sea urchins (Strongylocentrotus franciscanus) in kelpdeforested ecosystems that had developed in their absence. The damaged urchin tests and other uneaten remains were dropped to the seafloor where they elicited a flight response by healthy conspecifics. Kelps re-colonized areas from which the urchins had fled just as though they had been directly removed by sea otter predation.
See Also the Following Articles Biogeography ■ Distribution ■ Ecology, Overview ■ Habitat Use
References Bowen, W. D. (1997). The role of marine mammals in aquatic ecosystems. Mar. Ecol. Prog. Ser. 158, 267–274. Doak, D. F. et al. (14 authors) (2008). Understanding and predicting ecological dynamics: Are major surprises inevitable? Ecology: 89, 952–961. Estes, J. A. (2005). Carnivory and trophic connectivity in kelp forests. In “Large Carnivores and the Conservation of Biodiversity” (J. C. Ray, K. H. Redford, R. S. Steneck, and J. Berger, eds), pp. 61–81. Island Press, Washington, DC. Estes, J. A., and Duggins, D. O. (1995). Sea otters and kelp forests in Alaska: Generality and variation in a community ecological paradigm. Ecol. Monogr. 65, 75–100.
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Estes, J. A., Lindberg, D. R., and Wray, C. (2005). Evolution of large body size in abalones (Haliotis): Patterns and implications. Paleobiology 31, 591–606. Estes, J. A., DeMaster, D. P., Brownell, R. L., Jr., Doak, D. F., and Williams, T. M. (2006). Retrospection and review. In “Whales, Whaling and Ocean Ecosystems” (J. A. Estes, D. P. DeMaster, D. F. Doak, T. M. Williams, and R. L. Brownell, Jr., eds), pp. 388– 393. University of California Press, Berkeley, CA. Hunter, M. D., and Price, P. W. (1992). Playing chutes and ladders: Heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73, 724–732. Pace, M. L., Cole, J. J., Carpenter, S. R., and Kitchell, J. G. (1999). Trophic cascades revealed in diverse ecosystems. Trends Ecol. Evol. 14, 483–488. Paine, R. T. (1980). Food webs: Linkage, interaction strength, and community infrastructure. J. Anim. Ecol. 49, 667–685. Pauly, D., Christensen, V., and Walters, C. (2000). Ecopath, Ecosim, and Ecospace as tools for evaluating ecosystem impact of fisheries. ICES J. Mar. Sci. 57, 697–706. Polis, G.E., Power, M.E. and Huxel, G.R. (eds), (2004). Food Webs at the Landscape Level. University of Chicago Press, Chicago, IL. Power, G., and Gregoire, J. (1978). Predation by fresh water seals on the fish community of Lower Seal Lake, Quebec. J. Fish. Res. Board Can. 35, 844–850. Scheffer, M., Carpenter, S., Foley, J. A., Folke, C., and Walker, B. (2001). Catastrophic shifts in ecosystems. Nature 413, 591–596. Shurin, J. B., et al. (8 authors) (2002). A cross-ecosystem comparison of the strength of trophic cascades. Ecol. Lett. 5, 785–791. Steinberg, P. D., Estes, J. A., and Winter, F. C. (1995). Evolutionary consequences of food chain length in kelp forest communities. Proc. Natl. Acad. Sci. USA 92, 8145–8148. Wirsing, A. A., Heithaus, M. R., Frid, A., and Dill, A. M. (2008). Seascapes of fear: Evaluating sublethal predator effects experienced and generated by marine mammals. Mar. Mamm. Sci. 24, 1–15. Wootton, J. T., and Emmerson, M. (2005). Measurement of interaction strength in nature. Ann. Rev. Ecol. Evolution Syst. 36, 419–444.
Ecology, Overview BERND WÜRSIG
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arine mammals have entered just about all ocean habitats, and several mighty rivers and inshore seas as well. Only the deep abyss is foreign to them, but—remarkably— elephant seals (Mirounga spp.), sperm whales (Physeter macrocephalus), and several other toothed whales can “easily” dive to depths that exceed 1000 m, where it is cold and dark and where the pressure is 100 times and more what we experience on land. Perhaps just as remarkable is the fact that some of these divers, the pinnipeds, are also able to live on land, where they mate, give birth, and molt. Morphologic, physiologic, and behavioral adaptations to the environments of marine mammals are largely driven by their food and the habitats of their prey. Although there are various ways that ecological adaptations can be divided, this article does so by several broad-based general habitat types: open ocean, semipelagic, coastal, and riverine feeding and breeding habitats and—for pinnipeds and the polar bear (Ursus maritimus)—their obligatory stint on land to breed.
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