The Role of Marine Mammals in Marine Ecosystems. Lisa T. Ballance SIO 133 Marine Mammal Biology Spring 2013
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1 The Role of Marine Mammals in Marine Ecosystems Lisa T. Ballance SIO 133 Marine Mammal Biology Spring 2013
2 Preface: The Take-Home Message
3 Current Population Estimates Southern Hemisphere North Pacific North Atlantic Total Mean Body Mass (tons) Tons of Whale in the Ecosystem Humpback Whale 56,000 20,000 12,000 88, ,798,400 Right Whales 12, , ,000 Gray Whales 20, , ,000 Blue Whales 4,600 2,000 2,000 8, ,120 Fin Whales 15,000 11,000 37,000 62, ,622,600 Sei Whales 10,000 10,000 12,400 32, ,760 Bryde's Whales 50,000 39,000 5,000 94, ,240,800 Minke Whales 500,000 30, , , ,005,000 Bowhead Whales ,000 8,000 20, ,600,000 Sources: RL Brownell pers. comm.; synthesis by Hewitt and Lipsky 2009 ~15.7 million tons of whale in the world s marine ecosystems
4 This sheer tonnage implies that whales can play significant roles in marine ecosystems. Cetaceans in the California Current are estimated to consume ~12% of the ecosystem s net primary productivity (Barlow et al. 2008). Benthic feeding by gray whales provides habitat for benthic scavengers, prey for seabirds, and mixes sediment, with the potential to alter primary production (Oliver and Slattery 1985, Obst and Hunt 1990, Pilskaln et al. 1998). A decline of sperm whales in the tropical and subtropical Pacific may have resulted in a shift toward ecosystems dominated by squids and tunas (Essington 2006). Killer whales may have sequentially depleted marine mammal species in the Bering Sea (Springer et al. 2003). Whale carcasses support 350+ species and can be havens of deepsea biodiversity (Jones et al. 1998, Smith 2006).
5 The irony is that, although whales have become a symbol of the human capacity for greedy overharvest and a rallying point for environmental activists, we know surprisingly little about their ecological role. Total Number of Publications Number (%) Addressing Whale Ecology, Species Interactions, Effects on Ecosystem Processes Marine Ecology ( ) (0%) Marine Mammal Science ( ) 94 (focused on whales) 17 (18%) Kareiva et al. 2006
6 The Role of Whales in Southern Ocean Ecosystems Lisa T. Ballance, Robert L. Pitman, and Robert L. Brownell, Jr. Southwest Fisheries Science Center, NMFS, NOAA, U.S.A. Symposium on Living Whales in the Southern Ocean, Puerto Varas, Chile, March 2012
7 The Southern Ocean* Ecosystem *South of the Polar Front
8 * Whales and the Southern Ocean Ecosystem: A trophic interactions perspective Whales as Consumers Whales as Competitors Whales as Prey * = Cetaceans
9 Whales as Consumers The combination of great abundance, large body size, and endothermic metabolic demands make odontocete and mysticete whales some of the most voracious consumers in the oceans. As such, they have the potential to place extraordinary pressures on marine resources. (Williams 2006)
10 When we think of consumers in an ecosystem context, we ask questions like: What is eaten? How much? How does this consumption impact the ecosystem?
11 Krill E. superba, E. crystallorophias, T. macrura Krill-based ecosystem in about one quarter of the ~32 million sq. km of the Southern Ocean (Siegel & Loeb 1995) How much krill is consumed? Ingestion Rate/Day (1,000 kcal) No. Days Spent Feeding Total Krill Consumed Annually (millions of tons) % Krill in Estimated Abundance Mean Mass (tons) Diet Antarctic Blue Whales 2, , Fin Whales 15, , Sei Whales 20, , Humpback Whales 55, , Antarctic Minke Whales 500, Sources: RL Brownell pers. comm.; synthesis by Hewitt and Lipsky 2009
12 ~53.4 million tons krill consumed annually by 5 species of whales For some perspective, annually: 104, ,984 metric tons harvested: (SC-CAMLR 2011) 190 million tons consumed by baleen whales alone prior to commercial exploitation (Laws 1985) 250 million tons consumed by current populations of all krill predators (whales, birds, pinnipeds, fish, squid: Miller and Hampton 1989) Despite much careful attention, estimates of krill consumption are invariably associated with a great degree of uncertainty (e.g., Leaper and Lavigne 2007) How does this consumption impact the ecosystem?* *remember for later
13 Squid Sperm whales 10,000 males (Brownell, pers. comm.) Beaked whales 599,300 Ziphiid whales (almost all H. planifrons) in the Southern Ocean (Kasamatsu & Joyce 1995) H. planifrons the most abundant cetacean in the Southern Ocean? Killer whales? (Type B) How much squid is consumed?* How does this consumption impact the ecosystem?* Durban & Pitman, unpublished data *Big Unanswered Questions
14 Other Species Killer whales as consumers of: Fish, penguins, seals, whales
15 Fish - Ross Sea KWs Type C Krahn et al. 2008
16 Penguins Gerlache KWs Mini Type B Pitman & Durban 2010
17 Seals - Pack Ice KW Big Type B Pitman & Durban 2011
18 Whales Type A Pitman & Ensor 2003
19 How much of these species do killer whales consume? ~ 25,000 killer whales in the Southern Ocean (Branch & Butterworth 2001) Prey specialization (?) What is the distribution and abundance of KW ecotypes?* How does this consumption impact the ecosystem?* *Big Unanswered Questions
20 Whales as Competitors competition from any one species may profoundly affect the population dynamics and carrying capacity of another, either through its effect on their mutual resources or by direct interference. (Rickleffs 1990)
21 Competitive Release: The Krill Surplus Hypothesis > 2 million whales removed from Southern Hemisphere (Clapham and Baker 2006) Up to 150 million tons krill/yr unconsumed (Laws 1977) Theoretically could support addition of million penguins per year (Sladen 1964; Emison 1968) Growth in penguin populations attributed to krill surplus (Sladen 1964; Emison 1968; Conroy 1975; Croxall and Kirkwood 1979; Croxall et al. 1981; Laws 1985; Rootes 1988)
22 Antarctic Fur Seals: the best example of competitive release? Remarkable recovery from commercial exploitation at South Georgia Populations above pre-exploitation levels? Boyd 1993 South Georgia Hodgson and Johnston 1997 Range expansion to Signy, South Orkneys, due to population increase Numbers 78-94% > than during past 6570 (±60) radiocarbon years exceeding range of natural variability
23 Competition for krill is occurring. At Anvers Island, there are significant relationships between humpback whale abundance, the sizefrequency distribution of krill targeted by Adélie Penguins, and penguin foraging success ( ). Humpback whales and Adélie Penguins appear to target and share similar spatio-temporal prey resources. Friedlander et al. 2008
24 This competition can result in changes in abundance (of predators and prey). Antarctic Fur Seal At Bird Island, South Georgia, Antarctic fur seals and Macaroni Penguins exploit the same size and population of krill Macaroni Penguin % krill in fur seal diet > in penguin diet Penguin population declining Interpretation Predators reaching K Competition for krill is occurring Fur seals are outcompeting penguins Antarctic Fur Seal Macaroni Penguin Barlow et al. 2002
25 Large Medium Small Competition can result in niche partitioning. Fin Minke Humpback Near the South Shetland Islands baleen whales show a krill size-dependent relationship with krill abundance hotspots Krill Hotspots Whale Hotspots Santora et al. 2010
26 More on competition Clapham, Phillip J., and R. L. Brownell The potential for interspecific competition in baleen whales. REPORT-INTERNATIONAL WHALING COMMISSION 46:
27 Whales as Prey The ecological role of large whales as prey is the most controversial of the three potential food web pathways (Estes et al. 2006)
28 Whales are prey for killer whales.. or humans.
29 Killer whale predation may drive: Baleen whale migration (Corkeron & Connor 1999) Trophic cascades: prey switching due to loss of large whales (Branch & Williams 2006)
30 Sequential megafaunal collapse in the north Pacific ocean: an ongoing legacy of industrial whaling? Springer, Estes, vanvliet, Williams, Doak, Danner, Forney, & Pfister 2003
31 Background Abrupt decline of western stock of Steller sea lions (Eumetopias jubatus) across northern North Pacific and southern Bering Sea Widely attributed to nutritional limitation due to a) climate regime shift, and/or b) competition with fisheries However Adults and pups have better body condition, reduced foraging effort and field metabolic rates relative to other SSL stocks Abundance and trends in abundance of SSL prey incongruent with hypothesis of prey limitation as driver of SSL decline Abundance of seabird populations feeding on SSL prey species stable or increasing over same time period
32 An alternative hypothesis: killer whale predation as the cause of SSL decline Evidence: Precipitous declines in abundance of multiple marine mammal species in the north Pacific since 1980s (northern fur seal, harbor seal, sea otter) Incidental mortality from fisheries and intentional harvesting (1960s-70s) initial cause, but not continued decline Killer whales were likely responsible for sea otter decline (Estes et al. 1998) Why the sudden and dramatic change in predator-prey relationships?
33 Sequential megafaunal collapse: i) killer whales are predators of large whales Killer whales attack and consume all species of great whales Scars from KW teeth indicate attacks are common 20-40% of individuals in some species typical >60% of individuals in Southern Ocean sperm whales Migration of baleen whales proposed as an evolutionary response to KW predation Failure of bowhead whales in eastern Canadian Arctic to recover from commercial whaling proposed as result of KW predation
34 Sequential megafaunal collapse: ii) industrial whaling depleted large whales in the north Pacific N Pacific right, bowhead, humpback, blue, gray whales depleted by early 1900s Early post-war industrial whaling focused in far western N Pacific primarily by Japan on fin, sei, sperm whales (A) Progressive spread and intensification of whaling to east by Japan and Soviet Union, as stocks to the east were depleted (B, C) By early 1970s depletion of stocks drives whaling south to exploit Bryde s and female sperm whales(d) minimum of half a million whales removed from N Pacific and southern Bering Sea Combined current biomass of existing whales (1990s early 2000s) ~14% of pre-exploitation levels
35 Sequential megafaunal collapse: iii) in response to depletion of their prey by industrial whaling, killer whales shifted to other species Sequential declines of pinnipeds and sea otters consistent with this hypothesis Initial decline began following collapse of industrial whaling Harbor seals & fur seals first higher energy density and/or less aggressive behavior? Ultimate shift to smaller and less energetically rich prey (sea otters) due to exhaustion of other prey species
36 Killer whales and marine mammal trends in the north Pacific a re-examination of evidence for sequential megafauna collapse and the preyswitching hypothesis we suggest that there are little data to support this hypothesis and much to contradict it. Wade and 23 others 2007
37 Spatial scale and geographic region is important Data presented in Springer et al. are not consistent with a regional approach, e.g., Peak of whale biomass removal differs Known KW predation patterns differ
38 In all three regions, the biomass of large baleen & sperm whales is 5-24 x biomass of pinnipeds Argues against prey switching *from* large whales
39 Trends in biomass do not support the SMC hypothesis, e.g., In WCNA, biomass of humpback and blue whales has increased In Gulf of Alaska, biomass of humpback whales has increased In BSAI, biomass of gray and fin whales has increased
40 Additionally, There was no large population of mammal-eating KWs that preyed primarily upon large whales. Minke whales and small cetaceans have likely always been available Unidirectional prey switching of extended duration is rare and maladaptive The decline of pinnipeds and sea otters was not sequential
41 The sequential megafaunal collapse hypothesis: testing with existing data statistical tests of the timing of the declines do not support the assumption that pinniped declines were sequential DeMaster et al. 2006
42 Assumption 3: Pinniped declines in the 1970s and 1980s in the BSAI were sequential Springer et al Three populations of pinnipeds from same gegraphic region began to decline simultaneously DeMaster et al. 2007
43 This debate continues
44 The Ecosystem Consequences of Consuming, Competing, and Predation: Whales as Drivers of Food Web Restructuring ( Top-Down Forcing ) Despite its popularity among Southern Ocean ecologists 25 years ago, [the] top-down hypothesis (consumer effects on resources) has been largely replaced by an emphasis on bottom-up explanations (Ainley et al. 2009)
45 Trophic cascades in the western Ross Sea ~Nov Adelie penguins (incubating eggs) feed on crystal krill A. silverfish feed on c. krill ~Dec Penguin chicks hatch; adults feed themselves and chicks on krill minke whales arrive and feed on krill ~Jan Krill abundance declines Penguins and minke whales shift to silverfish Older silverfish become cannibalistic Ainley et al and references therein ~Feb Silverfish abundance declines Penguin foraging duration and distance increases Minke whales leave to forage elsewhere Grazing pressure on phytoplakton relaxes
46 So, how do whales impact Southern Ocean ecosystems? They remove a huge amount of krill from the system (and maybe a huge amount of squid, penguins, seals, and whales) They impact other krill predators They may drive evolutionary responses of their prey They have the potential to restructure food webs
47 Let us not forget, the Southern Ocean is a highly perturbed marine ecosystem Whale populations are recovering The planet is warming Fisheries are removing krill and fish (and whales)
48 The Big Unanswered Questions Which is more important: top-down or bottom-up forcing *Both* are important As whales recover, top-down forcing deserves more attention Trophic linkages: which direction and how strong? Squids: what are their trophic links with whales and their importance? What is the distribution and abundance of killer whale ecotypes and to what extent do the specialize in (or switch) prey? What are the indirect effects of food web restructuring? Are whales a year-round component of the ecosystem?
49 Satellite-tracked adult female Type B killer whale 13 Feb, 2010 for 109 days 30 S; 22.4 C North of 60, swim velocity 5-10 km/hr Returned 1 June, 2010 Durban and Pitman 2011
50 Reading Ballance, L.T., R.L. Pitman, R.P. Hewitt, D.B. Siniff, W.Z. Trivelpiece, P.J. Clapham, and R.L. Brownell, Jr The removal of large whales from the Southern Ocean: evidence for long-term ecosystem effects? Pp in: Whales, whaling, and ocean ecosystems. J.A. Estes, D.P. DeMaster, D.F. Doak, T.M. Williams, and R.L. Brownell, Jr. (eds.). University of California Press.
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