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Frontiers in Ecology and the Environment 12

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Frontiers in Ecology and the Environment 12 Sea-levelTHE rise ECOLOGICAL and tidal marsh ecosystems` SOCIETY OF AMERICA FrontiersFrontiers inin EcologyEcology andand thethe EnvironmentEnvironment Issue No 7 Volume 12 September 2014 Whales as ecosystem engineers Conserving mobile species Assessing environmental security in China esa REVIEWS REVIEWS REVIEWS Whales as marine ecosystem engineers Joe Roman1*, James A Estes2, Lyne Morissette3, Craig Smith4, Daniel Costa2, James McCarthy5, JB Nation6, Stephen Nicol7, Andrew Pershing8,9, and Victor Smetacek10 Baleen and sperm whales, known collectively as the great whales, include the largest animals in the history of life on Earth. With high metabolic demands and large populations, whales probably had a strong influence on marine ecosystems before the advent of industrial whaling: as consumers of fish and invertebrates; as prey to other large-bodied predators; as reservoirs and vertical and horizontal vectors for nutrients; and as detrital sources of energy and habitat in the deep sea. The decline in great whale numbers, estimated to be at least 66% and perhaps as high as 90%, has likely altered the structure and function of the oceans, but recovery is possible and in many cases is already underway. Future changes in the structure and function of the world’s oceans can be expected with the restoration of great whale populations. Front Ecol Environ 2014; doi:10.1890/130220 here is mounting evidence that apex predators play emerging understanding of the ecological role of great Timportant roles in the workings of natural ecosys- whales, a group – largely defined by size and commercial tems (Estes et al. 2011; Smith et al. 2013). Ocean science history – that includes all baleen whales (Mysticeti) and has been slow to embrace this view for at least three the sperm whale (Physeter macrocephalus). The terms interrelated reasons: (1) following World War II, when whales and great whales are used interchangeably in this oceanographic research gained new impetus, most whale text. Even though the large body size, great historical populations had been depleted or were in steep decline, abundance, high metabolic demands, and broad global so that ocean scientists had little opportunity to study distribution of whales is well known, we propose that the oceans with natural stocks of large predators, especially ecological role of these animals has been undervalued great whales; (2) there are logistical and operational chal- because we have underestimated the degree to which the lenges in studying large mobile animals on the high seas, depletion of great whales caused by a worldwide commer- with manipulative experiments being all but impossible cial harvest has altered marine ecosystems. (Bowen 1997); and (3) the prevailing focus of ocean sci- The earliest records of commercial whaling date from ence has been on bottom-up controls, such as resource approximately 1000 CE, when the Basque people began limitation and physical factors such as temperature hunting North Atlantic right whales (Eubalaena glacialis). In (Baum and Worm 2009). This review synthesizes our the millennium that followed, whaling systematically depleted coastal whale species, followed by reductions of pelagic species as well (Tønnessen and Johnsen 1982). In a nutshell: Although the overall level of reduction is still debated, • Commercial whaling dramatically reduced the biomass and experts agree that tens of millions of whales were killed dur- abundance of great whales and, until recently, we have lacked ing the thousand-year period of commercial whaling. the ability to study and directly observe the functional roles Estimates of numerical declines range from 66% to 90% of of whales in marine ecosystems • Whales facilitate the transfer of nutrients by releasing fecal populations, and total whale biomass may have been plumes near the surface after feeding at depth and by moving reduced by an estimated 85% (Branch and Williams 2006; nutrients from highly productive, high-latitude feeding areas Christensen 2006). For many species, population reductions to low-latitude calving areas were even more extreme: blue whales (Balaenoptera muscu- • Whale carcasses sequester carbon to the deep sea, where they lus), for example, have been reduced to 1% of their historical provide habitat and food for many endemic invertebrates • The continued recovery of great whales may help to buffer numbers in the Southern Hemisphere (Christensen 2006). marine ecosystems from destabilizing stresses and could lead Analyses of genetic diversity suggest that historical popula- to higher rates of productivity in locations where whales tions of several species, including North Atlantic humpback aggregate to feed and give birth whales (Megaptera novaeangliae) and fin whales (Balae- noptera physalus), in addition to Pacific gray whales (Eschrichtius robustus), were larger than previously supposed 1Gund Institute for Ecological Economics, University of Vermont, (Roman and Palumbi 2003; Alter et al. 2007; Ruegg et al. Burlington, VT *([email protected]); 2Department of Ecology 2013). This genetic approach indicates that the depletion of and Evolutionary Biology, University of California, Santa Cruz, the great whales may be in the range of 90% or greater. Santa Cruz, CA; 3M Expertise Marine, Sainte-Luce, Canada; Whales were once almost exclusively valued as goods to 4Department of Oceanography, University of Hawaii at Manoa, be removed from the ocean: for meat, oil (fuel, lubrica- Honolulu, HI (continued on last page) tion, and the manufacture of nitroglycerine), baleen (or © The Ecological Society of America www.frontiersinecology.org Whales as ecosystem engineers J Roman et al. Whale pump Prey whales as consumers is consider- 6 able; for instance, an estimated 15 65% (range 53–86%) of the North –1 yr 4 Pacific Ocean’s primary produc- 4 10 10 tion was required to sustain the ϫ large whale populations prior to 2 5 pressure Predation Tons N Tons commercial whaling (Croll et al. 2006). There is evidence that T Wu J Roman whales were similarly abundant Sediment suspension Whale falls elsewhere, so this calculation may 200 8 have applied to temperate oceans –1 160 6 yr generally. Lacking whales, this 3 10 –1 120 productivity is now shunted to yr ϫ 3 4 m other species and food-web path- 8 80 10 Tons C Tons ways, though arguably primary 2 40 production may have been higher in the past because of whale- F Nicklin M Rothman induced recycling and upper- Figure 1. Examples of the influence of whales on diverse ecosystem functions. Black bars ocean retention of nutrients represent estimated pre-whaling contributions; gray bars show contributions from currently (Roman and McCarthy 2010). estimated populations. Data for gray whales (Eschrichtius robustus) (“Sediment suspension”), Although as an endotherm a “Whale pump” (N released at the surface in the Gulf of Maine), and “Whale falls” (C exported whale’s total metabolic rate is to sea floor) are from original sources (Alter et al. 2007; Pershing et al. 2010; Roman and high, one consequence of its McCarthy 2010). Predation pressure is measured as the biomass of killer whales per unit immense size is a low mass-specific biomass of available marine mammal prey, calculated from estimates of abundance for all metabolic rate relative to smaller available marine mammal prey, including great whales, small cetaceans, pinnipeds, and sea animals. The amount of food otters for the North Pacific Ocean and Bering Sea before and after industrial whaling (Pfister and required to sustain one blue whale DeMaster 2006) and assuming that killer whale numbers have remained the same. As a result of could support seven smaller minke these changes in abundance, the risk of predation has increased for great whales and prey whales (Balaenoptera acutorostrata) availability has declined for killer whales. Although standard errors are not available for these or 1500 penguins, but the higher estimates, there is uncertainty in the number of whales before and after commercial exploitation metabolic rates of these smaller and the contribution of N and C for the whale-pump and whale-fall calculations. animals would limit their collec- tive biomass to just 50% or 8%, whalebone, prized for its flexibility and strength), and respectively, of a blue whale’s biomass. With primary pro- spermaceti (a waxy substance found in the head cavities duction held constant, reducing baleen whale popula- of sperm whales that was used in candles, ointments, and tions lowers the potential for marine ecosystems to retain industrial lubricants). They are now increasingly valued carbon (C), both in living biomass and in carcasses that for the many ecosystem services they provide. Great sink to the ocean floor (Pershing et al. 2010). whales can exert major trophic influences on marine As major predators in many marine ecosystems, whales ecosystems and also act as ecosystem engineers (Jones and can influence the ecological and evolutionary dynamics of Gutierrez 2007), influencing material fluxes and species prey populations, with effects propagating through food diversity and causing physical changes to the ocean envi- webs and biogeochemical cycles, such as the transport of ronment (Table 1). These functions will become increas- nitrogen (N) and iron (Fe). Predation by baleen whales, ingly relevant to ocean restoration and management as for example, may have been an important evolutionary great whale populations continue to recover in the post- force on Calanus copepods in the Arctic, selecting for whaling era (Magera et al. 2013; Roman et al. 2013). shorter life spans, smaller size, and higher growth rates; In this paper, we describe and discuss four mechanisms now that whales are functionally extinct in much of this or ecological pathways by which whales influence marine region, selection is favoring longer-lived, larger copepod ecosystems – as consumers, prey, detritus, and nutrient species (Berge et al. 2011). The near-extirpation of whales vectors (Figure 1) – and identify the associated ecosystem from the Southern Ocean in the 20th century may have services. released other krill predators, such as penguins and Antarctic fur seals (Arctocephalus gazella), from competi- n Whales as consumers tion (Ballance et al.
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