The Impact of Whaling on the Ocean Carbon Cycle: Why Bigger Was Better

Abstract

Background

Humans have reduced the abundance of many large marine vertebrates, including whales, large fish, and sharks, to only a small percentage of their pre-exploitation levels. Industrial fishing and whaling also tended to preferentially harvest the largest species and largest individuals within a population. We consider the consequences of removing these animals on the ocean's ability to store carbon.

Methodology/Principal Findings

Because body size is critical to our arguments, our analysis focuses on populations of baleen whales. Using reconstructions of pre-whaling and modern abundances, we consider the impact of whaling on the amount of carbon stored in living whales and on the amount of carbon exported to the deep sea by sinking whale carcasses. Populations of large baleen whales now store 9.1×106 tons less carbon than before whaling. Some of the lost storage has been offset by increases in smaller competitors; however, due to the relative metabolic efficiency of larger organisms, a shift toward smaller animals could decrease the total community biomass by 30% or more. Because of their large size and few predators, whales and other large marine vertebrates can efficiently export carbon from the surface waters to the deep sea. We estimate that rebuilding whale populations would remove 1.6×105 tons of carbon each year through sinking whale carcasses.

Conclusions/Significance

Even though fish and whales are only a small portion of the ocean's overall biomass, fishing and whaling have altered the ocean's ability to store and sequester carbon. Although these changes are small relative to the total ocean carbon sink, rebuilding populations of fish and whales would be comparable to other carbon management schemes, including ocean iron fertilization.

About the Authors:

Andrew J. Pershing

* E-mail: [email protected]

Affiliations School of Marine Sciences, University of Maine, Orono, Maine, United States of America, Gulf of Maine Research Institute, Portland, Maine, United States of America

Line B. Christensen

Affiliation: Fisheries Centre, University of British Columbia, Vancouver, British Columbia, Canada

Nicholas R. Record

Affiliations School of Marine Sciences, University of Maine, Orono, Maine, United States of America, Gulf of Maine Research Institute, Portland, Maine, United States of America

Graham D. Sherwood

Affiliation: Gulf of Maine Research Institute, Portland, Maine, United States of America

Peter B. Stetson

Affiliations School of Marine Sciences, University of Maine, Orono, Maine, United States of America, Gulf of Maine Research Institute, Portland, Maine, United States of America

Introduction

Ecosystems play a central role in regulating the concentration of atmospheric carbon dioxide. Whether an ecosystem acts as a source or sink for atmospheric carbon dioxide depends on the relative rates of photosynthesis and respiration. Research on the organic carbon cycle in the ocean has focused on the processes that limit primary productivity and the removal of carbon from the euphotic zone through the biological pump [1]. Primary production in the ocean is limited by the availability of macronutrients (principally, nitrogen) and micronutrients, notably iron [2]. On annual or longer scales, the availability of these nutrients is controlled by physical processes such as vertical mixing, upwelling, or atmospheric deposition. Carbon is removed from the euphotic zone by the sinking of organic matter. Dead phytoplankton cells are the dominant component of the flux, but zooplankton feces and vertical migrations can contribute significantly [1]. On land, humans directly influence the carbon stored in terrestrial ecosystems through logging and the burning of forests and grasslands. In the open ocean, the carbon cycle is assumed to be free of direct human influences [3].

Humans have had a substantial impact on the abundance, biomass, and size structure of populations of fish and whales [4], [5], [6]. Yet, due to their low abundance relative to plankton, marine vertebrates are not included in most models of marine biogeochemistry [7], [8], [9]. Although only a small part of the ocean's total carbon budget, marine vertebrates contribute to the movement and storage of inorganic [10] and, as we will show, organic carbon. These species may also influence the availability of micronutrients such as iron [11]. The nature of the exploitation, which focused on the largest individuals and species, further magnified the impact of fishing and whaling on the carbon cycle due to the inherent metabolic efficiency of large animals. As considerations of body size are central to our calculations, our analysis will focus on baleen whales, although our arguments also apply to fish and sharks.

Results

Compared to phytoplankton that have life spans measured in days, whales and large fish live for many decades. The carbon accumulated in the body of a long-lived vertebrate will remain out of the atmosphere for the animal's life. In terms of their size and potential to store carbon for years or decades, marine vertebrates are the only organisms in the ocean comparable to large trees. Industrial whaling has largely ceased, however, the biomass of whales is less than 25% of pre-whaling levels [6], [12] (Table 1). The impact of whaling was even more catastrophic for specific populations. For example, blue whales in the Southern Ocean have been reduced by more than 99% [6]. Assuming a population recovery rate of 3% yr−1 and the pre- and post-whaling biomasses in Table 1, we estimate that whaling removed 1.7×107 tons of carbon from marine ecosystems (Figure 1). The total carbon removed depends on the value of r used. Stock assessments for many populations of large whales suggest that most populations are recovering at rates around 6%, but values over 10% have been reported [13]. Using a higher r increases the total carbon removed.

[Figure omitted. See PDF.]

Figure 1. Biomass of eight species of large whales.

Each line represents a different biomass accumulation rate (r) as indicated in the key. Each r implies a distinct level of whaling in order to reach the specified 2001 biomass levels. The total biomass of whales that must be removed for each r is also indicated in the key.

https://doi.org/10.1371/journal.pone.0012444.g001

[Figure omitted. See PDF.]

Table 1. Pre-whaling and modern (2001) abundance and biomass of 8 species or species groups of baleen whales (blue = Balaenoptera musculus, fin = B. physalus, humpback = Megaptera novaeangliae, sei/Bryde's = B. borealis and B. brydei, minke = B. acutorostrata and B. bonaerensis, gray = Eschrichtius robustus, right = Eubalaena spp., bowhead = Balaena mysticetus) from [12].

https://doi.org/10.1371/journal.pone.0012444.t001

The accounting above only considers the impact of whaling on the carbon stored in whale populations. The responses of marine ecosystems to fishing and whaling are complex and highly variable. Strong top-down effects have been reported in some ecosystems [14], [15], [16], although alternative explanations may apply even in some of the most cited examples [17], [18]. Even in the Southern Ocean, the response of the ecosystem following intense whaling is not clear and was complicated by physical changes [19], [20], [21]. On large spatial and long time scales, the most likely response to the reduction of one species is an increase in its competitors. For ecosystems heavily impacted by whaling, this means an increase in smaller species as has been observed in the Pacific [22] and in the Ross Sea [19].

Unlike the carbon stored in trees, carbon stored in animal tissue must be constantly maintained by feeding. The rate, R, at which carbon is respired by an animal depends on its mass, m, raised to a power α:where γ(T) is a temperature dependent coefficient. Values of α near 3/4 have been found for a wide range of organisms [23], [24]. This relationship means that larger animals require less food per unit mass and thus, they are more efficient at storing carbon than smaller animals [25]. The amount of krill that supported the 3.3×105 blue whales lost from the Southern Ocean could support 2.2×106 minke whales (7 tons each) or 5.2×108 penguins (5 kg each) (Figure 2a). However, the biomass in these populations would be only 50% or 8%, respectively, of the biomass of the missing blue whales.

[Figure omitted. See PDF.]

Figure 2. Consequences of reducing the abundance of large species on abundance and biomass.

a) Abundance (light blue, scale on left) and biomass (dark blue, scale on right) of blue whales lost from the Southern Ocean. Based on metabolic scaling, the same amount of food could support larger populations of minke whales or penguins, but the biomass of these populations would be less than the original blue whale population. b) Abundance spectra for southern hemisphere mysticetes before whaling (dark circles) and in 2001 (light squares). The regression line for the pre-whaling spectrum (dashed line) has a slope and 95% confidence bound of −0.36±1.01, while the 2001 spectrum (black line) has a slope of 2.05±1.30 and the regression is significant (p<0.05, r2 = 0.83, n = 6). c) Impact of steepening the abundance spectra on the total biomass contained in four different communities. In all cases, the food requirements of the community were kept constant as the slope varied. The communities differ in the range of masses contained in the community: 2 (circles), 3 (squares), 4 (triangles), and 5 (diamonds) orders of magnitude.

https://doi.org/10.1371/journal.pone.0012444.g002

The calculations represented in Figure 2a envision the complete replacement of one population by another. A more likely scenario is that the food that went to the removed individuals is spread over a range of species or size classes. Marine communities tend to be strongly size structured, and over a large range of masses, the abundance, N, tends to follow a power law:where N0 is a scaling constant [26], [27]. For a community feeding on the same food source, the slope of the spectrum, β, should be near 3/4 [22]. The total carbon consumed by the community per unit time (Rtot) is then the product of the abundance spectrum and R(m) from above:using α = 3/4. Communities that are strongly fished tend to have steeper abundance spectra (larger β), and the size distribution of baleen whales in the Southern Ocean supports this view. Prior to whaling, β was not significantly different from zero, while in 2001, β was nearly 2 (Figure 2b). The latter value is comparable to other heavily-exploited ecosystems such as the North Sea [28]. Assuming total consumption by the community remains the same, steepening the size spectrum will lead to an increase in the number of organisms in the community but a decrease in biomass. For the community of baleen whales with masses spanning two orders of magnitude, increasing β from 3/4 to 2 (a 166% increase) results in a 30% decrease in biomass (Figure 2c). In the Southern Ocean, the species that consume Antarctic krill range from penguins to blue whales. For a community with a 5 order of magnitude range, steepening the spectrum reduces the total biomass by more than 70%. In other words, the same amount of primary productivity can support a higher biomass of large individuals due to the increase in metabolic efficiency with increasing size.

The direct removal of carbon by whaling and fishing, coupled with the steepening of the size spectra mean that marine ecosystems now store less carbon than they once did. In addition, the reduction of the populations of large vertebrates also altered how carbon is transferred from one ecosystem to another in the ocean [29]. From a carbon-cycle perspective, the most interesting movements of carbon are those from the euphotic zone to the deep ocean which can sequester carbon for hundreds to thousands of years [1]. Whale falls are the most well-studied example of this large vertebrate flux and are common enough that communities of organisms have adapted to exploit this resource [30], [31]. Using estimates of current population sizes, we calculate that the total carbon flux from 8 baleen whale taxa is currently 2.8×104 tons C yr−1 (Table 1). Using estimates of pre-whaling abundance, the total flux would be nearly an order of magnitude greater, or 1.9×105 tons C yr−1, a value consistent with earlier estimates [32]. Genetic work suggests that pre-whaling populations may have been a factor of 10 larger than indicated by catch records [6]. These estimates provide an upper-bound on the pre-whaling flux of 1.9×106 tons C yr−1, or 0.1% of the ocean's net carbon sink [33]. Although less established than whale falls, non-predation deaths of tuna, billfish, sharks, and other large pelagic fish should also contribute to a flux of organic carbon out of the euphotic zone. As with biomass, an increase in smaller competitors could compensate for some of the lost carbon flux; however, since smaller animals have higher predation rates, much of the potential flux will be lost to consumption.

By combining the estimates of carbon export with those for whale biomass, we estimated the total carbon footprint of whaling. For this calculation, we transferred the carbon removed by whaling into a pool that we call the atmosphere (Figure 3a). We recognize that how and when the carbon in a killed whale reaches the atmosphere will depend on the manner in which it was processed and the products that were produced from its carcass. We also used the flux estimates described above to compute the carbon exported by the whale population in each year. The exported carbon was removed from the atmospheric pool. We also computed an undisturbed atmospheric pool by removing the carbon exported by the 1900 population for each year. The total carbon footprint of whaling is then the difference between the atmospheric pool with and without whaling (Figure 3b). Assuming a recovery rate (r) of 3% gives an estimate of 2.35×107 tons C added to the atmospheric pool by whaling.

[Figure omitted. See PDF.]

Figure 3. Carbon footprint of 20th Century whaling.

A. Total carbon in the atmospheric carbon pool. Each line corresponds to a different biomass accumulation rate (r) as in Figure 1. Whales killed by whaling where added to the atmospheric pool. A proportion of the population in each year was assumed to die and sink. This export flux was removed from the atmospheric pool. B. Difference in atmospheric carbon with and without whaling.

https://doi.org/10.1371/journal.pone.0012444.g003

Discussion

The carbon stored in populations of marine vertebrates is only a small part of the total carbon in marine ecosystems; however, the impact of rebuilding stocks of fish and whales would be comparable to existing carbon sequestration projects. For example, rebuilding the southern hemisphere blue whale population would sequester 3.6×106 tons C in living biomass. Assuming 82 tons C ha−1 of forest [34], the new blue whales would be equivalent to preserving 43,000 hectares of temperate forest, an area comparable in size to the City of Los Angeles. Rebuilding all of the whale populations in Table 1 would store 8.7×106 tons C, equivalent to 110,000 hectares of forest or an area the size of the Rocky Mountain National Park. As a population nears its carrying capacity, the rate at which it is accumulating carbon slows, but even at carrying capacity, marine vertebrate populations can still export carbon through sinking carcasses. If restored to pre-industrial levels, southern hemisphere blue whales would remove 70,000 tons C yr−1 through sinking of dead whales. Restoring all whale populations would export an additional 160,000 tons C yr−1. This flux would be equivalent to preserving 843 hectares of forest each year.

Ocean iron fertilization is the most widely discussed idea for sequestering carbon in the ocean, and our calculations suggest that rebuilding whale and fish populations would compare favorably with these schemes. Iron fertilization schemes revolve around the observation that primary productivity in large areas of the ocean is limited by the availability of iron [2]. If iron is added to these regions, then phytoplankton should bloom and carbon should be exported through the biological pump. In theory, it should be possible to add a few hundred tons of iron sulfate to the Southern Ocean and sequester millions of tons of carbon [35]. While several experiments have demonstrated the iron limitation hypothesis, these experiments have had mixed success at stimulating export. The most successful experiment, in terms of the measured carbon export, exported a maximum of 900 tons C [36]. At these rates, it would take 200 such blooms each year to match the export potential of fully restored whale populations. Given that larger experiments have produced little or no export [37] and that iron fertilization could have unintended consequences such as increases in toxic species [38], [39], conserving populations of large marine vertebrates may represent a more ecologically sound alternative.

The main disadvantage to using populations of large vertebrates as a carbon management tool is that, while humans may be responsible for their low population levels, there are often limited options for accelerating the rebuilding of these populations. For commercial fish species, reducing fishing mortality is a necessary step; however, as evidenced by the slow recovery of Newfoundland cod, reducing fishing does not guarantee a recovery [40]. Hunting of baleen whales has largely ceased. The greatest threats to current whale populations are likely mortality due to ship strikes [41] and potentially reduced food supplies due to climate variability or competition with humans [42]. A better accounting for the potential of these species to sequester and export carbon could allow organizations to claim carbon credits for actions that support the rebuilding of these populations.

Our calculations add to a growing body of literature on the importance of large organisms to the ocean's biogeochemical cycles. In addition to storing and exporting organic carbon, fish can export inorganic carbon through the excretion of calcium carbonate [10], while whales and krill in the Southern Ocean may help retain iron in the surface waters [11]. Our analysis also suggests that marine ecosystems with larger individuals or larger species could support a higher biomass due to the increase in metabolic efficiency with body size. Due to the strong relationship between fecundity and body size in fish [43], [44], a community with a fully populated size spectrum would have a higher reproductive output and would likely be more resilient than a population with a truncated size spectrum. These calculations suggest that conserving larger species and largest individuals within species should be a top conservation priority.

Materials and Methods

Part 1. Whale populations before and after whaling

Our study builds from Christensen's comprehensive assessment of world-wide whale populations [12]. She estimated both the pre-whaling abundance and the modern (2001) values. As discussed above, estimates of pre-whaling abundance based on catch records could underestimate the true pre-whaling abundances due to underreporting. Independently assessing the accuracy of the pre-whaling abundance estimates is exceedingly difficult. Population genetic techniques are one approach, and these analyses consistently yield pre-whaling levels much higher, up to a factor of 10, than stock assessment-based methods [6]. Although considerable uncertainly exists surrounding the pre-whaling estimates we use, these values represent conservative estimates of the population sizes.

Right (Eubalaena glacialis, E. japonica, and E. australis) and bowhead (Balaena mysticetus) whales were included in the population and biomass calculations. However, these species were treated separately in calculations of vertical flux and whaling as discussed below. Christensen did not estimate the abundance of southern hemisphere right whales. For this population, we used estimates from [45].

We excluded sperm whales (Physester macrocephalus) from our calculations. This species tends to feed at great depth. The prey available at these depths likely derives a portion of its nutrition from the organic matter sinking from the photic zone. Thus, by feeding on these animals and returning to the surface to respire, sperm whales could potentially counteract the export of carbon which we aim to calculate. Determining whether sperm whales represent a net upward or downward flux of carbon is an interesting calculation, but one that is beyond the scope of this study.

To estimate the flux of carbon from whale populations, we must first estimate the number of whales that die each year. For simplicity, we will consider a generic whale population with general mysticete characteristics. Our model is a simple age structured model, and we assume that the population is at steady state with a total population of K. We divide the population into age classes of size one year. We assume that whales do not live longer than n years. Studies of populations of large baleen whales suggest that females become sexually mature between 5–10 years [13], [46], [47], [48]. All baleen whales have a well-defined annual reproductive cycle, with pregnancy lasting the majority of a year followed by several months of nursing. This sets the absolute maximum calf production rate at 0.5 births female−1 yr−1. The actual production rate will be lower, as females do not always become pregnant immediately following a birth.

Whales have few predators and their natural mortality rates are very low [49], [50]. Demographic studies of modern whale populations generally assume a constant mortality rate for all age classes and then add an additional mortality term for calves [13], [49], [51] We will use this simple formulation and solve for s (non-calf) and s1 (calf) survival rates that balance the prescribed fecundity schedule:(1)where r is the fecundity (births per individual), a is the age at which females become mature, and n is the maximum age. We can remove the recursion:(2)producing an explicit function for all ages except N1.

For a population to be at steady state, the age-dependent fecundity must be balanced by mortality:(3)Introducing the expression for Nj into equation (2):We can remove s1N1 from both sides:and then split the summation on the right:We can incorporate sn−2 into the first summation on the right by adjusting the limit of the sum:To make things simpler, we adjust the limits of the summations so that both on the right involve powers of j:It is then easy to see that most of the terms cancel, leaving only 1/s1 on the right hand side. This simplifies toWe then apply the identity:to the remaining summation:(4)

Equation 2 has five parameters: r, s1, s, m, and n that define the population dynamics of our simple model. If the identity in (4) holds, then the population will be in steady-state, the presumed condition before whaling. Specific values of these parameters are not known, but the ranges are generally well established (Table 2). We employed a Monte-Carlo procedure to find a range of plausible parameter combinations. We created 10,000 populations (combinations of the five parameters) by picking a value for each parameter from a normal distribution. The means of the distributions were assumed to be the midpoint of the range in Table 2, and the standard deviation was assumed to be half of the range. For each population, we applied equation (4) to find a new value for each parameter while leaving the other four parameters fixed that produced a steady-state population. Thus, we created 50,000 steady-state populations. These were ranked based on the likelihood of selecting each combination from the normal distributions. We then used the 1,000 most-likely populations to estimate the mean parameter values for each species (Table 3).

[Figure omitted. See PDF.]

Table 2. Parameters ranges input into the demographic model.

https://doi.org/10.1371/journal.pone.0012444.t002

[Figure omitted. See PDF.]

Table 3. Demographic parameters for steady state populations.

https://doi.org/10.1371/journal.pone.0012444.t003

The population parameters define a steady-state age structure. In order to estimate the population biomass and carbon flux, we need to know the mass of a whale of a certain age. Lockyer [52] fit von Bertalanffy weight-at-age relationships for blue, fin, and sei whales. Using these results and additional growth and longevity information [53], [54], [55], we established models for each species and applied the models to the age distributions to compute an average mass for each species (Table 4). Longevity information was especially hard to come by. In our model, whales that survive past the maximum age are removed; thus, we seek the maximum age possible for each species. When possible, we used the maximum reported age as the lower bound for our calculations and then specified a proportionally higher upper bound.

[Figure omitted. See PDF.]

Table 4. Parameters for von Bertalanffy mass-at-age model and carbon export potential.

https://doi.org/10.1371/journal.pone.0012444.t004

Using the mortality terms (s and s1), we can estimate the number of whales lost from each age class. We can then apply the weight-at-age functions to convert the number of whales dying into tons of dead whales. Using the proportions of bone, lipid, and protein in Jelmert & Oppen-Berntsen [32], we can convert the total biomass into tons of carbon. By normalizing to a population of size 1, we have the gross flux in terms of carbon lost from each population per year per whale in the population. We computed the flux for females and males using the 1,000 most likely parameter configurations for each of the 8 populations. We then computed the mean flux for each population, as well as the 95% confidence limits (Table 4).

Smith and Baco [30] estimate that up to 90% of whale mortalities become whale falls. We used their most conservative estimate and assumed that 50% of mortalities (or equivalently 50% of each carcass produced) reach the seafloor. The balaenid species (right whales–Eubaleana spp. and bowhead whales–Balaena mysticetus) present a special problem for sinking fluxes. These whales were dubbed “right” by whalers due to their high quantities of blubber and their tendency to float when killed. We expect that most natural whale deaths would be caused by disease or starvation. These whales would tend to be in poor condition and more likely to sink. We thus assumed that 10% of mortalities resulted in export. While we believe the proportions used for all whales are conservative, these numbers have not been measured. Combining the population estimates with the fluxes, we can produce the expected pre- and post- whaling carbon fluxes (Table 4).

Part 2: Biomass removed by whaling

For this section, we compute the total impact of whaling during the 20th C in terms of carbon storage and carbon flux. For this calculation, we excluded right and bowhead whales as these species were fully exploited prior to the 20th C [12]. We began by assuming that the pre-whaling abundances (and the implied biomasses) for the non-balaenid species computed by Christensen represented conditions in 1900. We assumed that whale populations accumulate biomass at a steady rate r. In reality, the biomass accumulation rate should be slower when whale biomass is high, reflecting density dependence. However, the impact of this change is small. We further assumed a constant exploitation rate for the period 1900–1970. To compute the exploitation rate, we worked backward from the 2001 biomass to estimate the biomass in 1970 using r. Then, we computed the exploitation rate required to reach the 1970 biomass from the 1900 value. We performed these calculations for four values of r: 1, 3, 5, and 10% yr−1 (Figures 1 and 3). We presented the 3% calculations in the main text to add an extra measure of caution to the calculations.

Part 3: Body size and carbon storage

We start by assuming an underlying power law relationship between abundance and size (mass):The energy (R) required by all individuals of size m in the community is then the product of N(m) and the metabolic rate:using the standard 3/4 scaling for metabolism and where γ(T) is a temperature dependent coefficient on metabolic rate. The total of carbon consumed by a community is then proportional to the integral of R(m) between the smallest (m0) and largest (m*) sizes:Assuming β≠0.25:(5)Assuming the total carbon consumed does not change, then changing the spectral slope by a factor q leads to a change in N0:(6)Setting (5) equal to (6) and Nnew = rN0, we can solve for the proportional change r:(7)The total biomass in the new community is now:(8)The new biomass is a factor f times the original biomass:(9)

Part 4: Size spectrum in southern ocean mysticetes

Christensen's original analysis of pre and post whaling populations distinguished between whale populations in the North Atlantic, North Pacific, and southern hemisphere. We used logarithmic regression to fit the slope (β) and intercept (N0) of the abundance spectrum:for the three regions, before and after whaling. Significant relationships were only found for the southern hemisphere (Figure 2b). Before whaling, the slope of the abundance spectrum (β) was not significantly different from 0, while in 2001, the slope was 2 (p<0.05, r2 = 0.83, n = 6).

Acknowledgments

Helpful comments on these ideas were provided by Charles Greene and by the staff at the Gulf of Maine Research Institute.

Author Contributions

Conceived and designed the experiments: AP. Performed the experiments: AP LBC NRR. Analyzed the data: AP LBC NRR GDS PBS. Contributed reagents/materials/analysis tools: AP. Wrote the paper: AP LBC NRR GDS PBS.

Citation: Pershing AJ, Christensen LB, Record NR, Sherwood GD, Stetson PB (2010) The Impact of Whaling on the Ocean Carbon Cycle: Why Bigger Was Better. PLoS ONE5(8): e12444. https://doi.org/10.1371/journal.pone.0012444

References

1. Ducklow HW, Steinberg DK, Buesseler KO (2001) Upper ocean carbon export and the biological pump. Oceanography 14: 50–58.HW DucklowDK SteinbergKO Buesseler2001Upper ocean carbon export and the biological pump.Oceanography145058

2. Martin JH, Fitzwater SE (1988) Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic. Nature 331: 341–343.JH MartinSE Fitzwater1988Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic.Nature331341343

3. IPCC (2007) Climate Change 2007 - The Physical Science Basis. Contribution of Working Group 1 to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change;. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, et al., editors. Cambridge, U. K.: Cambridge University Press. 996 p.IPCC2007Climate Change 2007 - The Physical Science Basis. Contribution of Working Group 1 to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change;S. SolomonD. QinM. ManningZ. ChenM. MarquisCambridge, U. K.Cambridge University Press996

4. Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423: 280–283.RA MyersB. Worm2003Rapid worldwide depletion of predatory fish communities.Nature423280283

5. Baum JK, Myers RA, Kehler DG, Worm B, Harley SJ, et al. (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299: 389–392.JK BaumRA MyersDG KehlerB. WormSJ Harley2003Collapse and conservation of shark populations in the Northwest Atlantic.Science299389392

6. Roman J, Palumbi SR (2003) Whales before whaling in the North Atlantic. Science 301: 508–510.J. RomanSR Palumbi2003Whales before whaling in the North Atlantic.Science301508510

7. Moore JK, Doney SC, Lindsay K (2004) Upper ocean ecosystem dynamics and iron cycling in a global three-dimensional model. Global Biogeochemical Cycles 18: JK MooreSC DoneyK. Lindsay2004Upper ocean ecosystem dynamics and iron cycling in a global three-dimensional model.Global Biogeochemical Cycles18

8. Doney SC, Lima I, Lindsay K, Moore JK, Dutkiewicz S, et al. (2001) Marine biogeochemical modeling: recent advances and future challenges. Oceanography 14: 93–107.SC DoneyI. LimaK. LindsayJK MooreS. Dutkiewicz2001Marine biogeochemical modeling: recent advances and future challenges.Oceanography1493107

9. Hofmann E, Druon JN, Fennel K, Friedrichs M, Haidvogel D, et al. (2008) Eastern US continental shelf carbon budget: integrating models, data assimilation, and analysis. Oceanography 21: 86–104.E. HofmannJN DruonK. FennelM. FriedrichsD. Haidvogel2008Eastern US continental shelf carbon budget: integrating models, data assimilation, and analysis.Oceanography2186104

10. Wilson RW, Millero FJ, Taylor JR, Walsh PJ, Christensen V, et al. (2009) Contribution of fish to the marine inorganic carbon cycle. Science 323: 359–362.RW WilsonFJ MilleroJR TaylorPJ WalshV. Christensen2009Contribution of fish to the marine inorganic carbon cycle.Science323359362

11. Nicol S, Bowie A, Jarman S, Lannuzel D, Meiners KM, et al. (2010) Southern Ocean iron fertilization by baleen whales and Antarctic krill. Fish and Fisheries 11: 203–209.S. NicolA. BowieS. JarmanD. LannuzelKM Meiners2010Southern Ocean iron fertilization by baleen whales and Antarctic krill.Fish and Fisheries11203209

12. Christensen LB (2006) Marine mammal populations: reconstructing historical abundances at the global scale. Vancouver, BC Canada: Fisheries Centre, University of British Columbia. LB Christensen2006Marine mammal populations: reconstructing historical abundances at the global scaleVancouver, BC CanadaFisheries Centre, University of British Columbia

13. Branch TA, Matsuoka K, Miyashita T (2004) Evidence for increases in Antarctic blue whales based on Bayesian modelling. Marine Mammal Science 20: 726–754.TA BranchK. MatsuokaT. Miyashita2004Evidence for increases in Antarctic blue whales based on Bayesian modelling.Marine Mammal Science20726754

14. Frank KT, Petrie B, Choi JS, Leggett WC (2005) Trophic cascades in a formerly cod-dominated ecosystem. Science 308: 1621–1623.KT FrankB. PetrieJS ChoiWC Leggett2005Trophic cascades in a formerly cod-dominated ecosystem.Science30816211623

15. Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315: 1846–1850.RA MyersJK BaumTD ShepherdSP PowersCH Peterson2007Cascading effects of the loss of apex predatory sharks from a coastal ocean.Science31518461850

16. Springer AM, Estes JA, van Vliet GB, Williams TM, Doak DF, et al. (2003) Sequential megafaunal collapse in the North Pacific Ocean: An ongoing legacy of industrial whaling? Proceedings of the National Academy of Sciences 100: 12223–12228.AM SpringerJA EstesGB van VlietTM WilliamsDF Doak2003Sequential megafaunal collapse in the North Pacific Ocean: An ongoing legacy of industrial whaling?Proceedings of the National Academy of Sciences1001222312228

17. Greene CH, Pershing AJ (2007) Climate-driven changes in Arctic Ocean outflow force ecosystem regime shift in NW Atlantic. Science 315: 1084–1085.CH GreeneAJ Pershing2007Climate-driven changes in Arctic Ocean outflow force ecosystem regime shift in NW Atlantic.Science31510841085

18. Whitehead H, Reeves R (2005) Killer whales and whaling: the scavenging hypothesis. Biology Letters 1: 415–418.H. WhiteheadR. Reeves2005Killer whales and whaling: the scavenging hypothesis.Biology Letters1415418

19. Ainley D, Ballard G, Ackley S, Blight LK, Eastman JT, et al. (2007) Paradigm lost, or is top-down forcing no longer significant in the Antarctic marine ecosystem? Antarctic Science 19: 283–290.D. AinleyG. BallardS. AckleyLK BlightJT Eastman2007Paradigm lost, or is top-down forcing no longer significant in the Antarctic marine ecosystem?Antarctic Science19283290

20. Nicol S, Croxall J, Trathan P, Gales N, Murphy E (2007) Paradigm misplaced? Antarctic marine ecosystems are affected by climate change as well as biological processes and harvesting. Antarctic Science 19: 291–295.S. NicolJ. CroxallP. TrathanN. GalesE. Murphy2007Paradigm misplaced? Antarctic marine ecosystems are affected by climate change as well as biological processes and harvesting.Antarctic Science19291295

21. Nicol S, Worby A, Leaper R (2008) Changes in the Antarctic sea ice ecosystem: potential effects on krill and baleen whales. Marine And Freshwater Research 59: 361–382.S. NicolA. WorbyR. Leaper2008Changes in the Antarctic sea ice ecosystem: potential effects on krill and baleen whales.Marine And Freshwater Research59361382

22. Essington TE (2006) Pelagic ecosystem response to a century of commercial fishing and whaling. In: Estes JA, Demaster DP, Doak DF, Williams TM, Brownell RL Jr, editors. Whales, Whaling, and Ocean Ecosystems. Berkely, CA: University of California Press. pp. 38–49.TE Essington2006Pelagic ecosystem response to a century of commercial fishing and whaling.JA EstesDP DemasterDF DoakTM WilliamsRL Brownell JrWhales, Whaling, and Ocean EcosystemsBerkely, CAUniversity of California Press3849

23. Kleiber M (1932) Body size and metabolism. Hilgardia 6: 315–332.M. Kleiber1932Body size and metabolism.Hilgardia6315332

24. Brown JH, Gillooly JF (2003) Ecological food webs: High-quality data facilitate theoretical unification. Proceedings of the National Academy of Sciences 100: 1467–1468.JH BrownJF Gillooly2003Ecological food webs: High-quality data facilitate theoretical unification.Proceedings of the National Academy of Sciences10014671468

25. Lambertsen RH (1992) Crassicaudosis: a parasitic disease threatening the health and population recovery of large baleen whales. In Health and management of free-ranging mammals – Part One (M. Artois, ed.). Revue scientifique et technique (International Office of Epizootics) 11: 1131–1141.RH Lambertsen1992Crassicaudosis: a parasitic disease threatening the health and population recovery of large baleen whales. In Health and management of free-ranging mammals – Part One (M. Artois, ed.).Revue scientifique et technique (International Office of Epizootics)1111311141

26. Sheldon RW, Prakash A, Sutcliffe WH Jr (1972) The size distribution of particles in the ocean. Limnology & Oceanography 17: 327–340.RW SheldonA. PrakashWH Sutcliffe Jr1972The size distribution of particles in the ocean.Limnology & Oceanography17327340

27. Kerr SR, Dickie LM (2001) The Biomass Spectrum: a Predator-Prey Theory of Aquatic Production. New York: Columbia University Press. SR KerrLM Dickie2001The Biomass Spectrum: a Predator-Prey Theory of Aquatic ProductionNew YorkColumbia University Press

28. Jennings S, Blanchard JL (2004) Fish abundance with no fishing: predictions based on macroecological theory. Journal Of Animal Ecology 73: 632–642.S. JenningsJL Blanchard2004Fish abundance with no fishing: predictions based on macroecological theory.Journal Of Animal Ecology73632642

29. Tynan CT (2004) Cetacean populations on the SE Bering Sea shelf during the late 1990s: implications for decadal changes in ecosystem structure and carbon flow. Marine Ecology Progress Series 272: 281–300.CT Tynan2004Cetacean populations on the SE Bering Sea shelf during the late 1990s: implications for decadal changes in ecosystem structure and carbon flow.Marine Ecology Progress Series272281300

30. Smith CR, Baco AR (2003) Ecology of whale falls at the deep-sea floor. Oceanography and Marine Biology: an Annual Review 41: 311–354.CR SmithAR Baco2003Ecology of whale falls at the deep-sea floor.Oceanography and Marine Biology: an Annual Review41311354

31. Butman CA, Carlton JT, Palumbi SR (1995) Whaling effects on deep-sea biodiversity. Conservation Biology 9: 462–464.CA ButmanJT CarltonSR Palumbi1995Whaling effects on deep-sea biodiversity.Conservation Biology9462464

32. Jelmert A, Oppen-Berntsen DO (1996) Whaling and deep-sea biodiversity. Conservation Biology 10: 653–654.A. JelmertDO Oppen-Berntsen1996Whaling and deep-sea biodiversity.Conservation Biology10653654

33. Sarmiento JL, Gruber N (2002) Sinks for anthropogenic carbon. Physics Today August 2002: 30–36.JL SarmientoN. Gruber2002Sinks for anthropogenic carbon.Physics Today August20023036

34. FAO (2006) Global Forest Resources Assessment 2005. Rome: Food and Agriculture Organization of the United Nations. FAO2006Global Forest Resources Assessment 2005RomeFood and Agriculture Organization of the United Nations

35. Smetacek V, Naqvi SWA (2008) The next generation of iron fertilization experiments in the Southern Ocean. Philosophical Transactions of the Royal Society a-Mathematical Physical and Engineering Sciences 366: 3947–3967.V. SmetacekSWA Naqvi2008The next generation of iron fertilization experiments in the Southern Ocean.Philosophical Transactions of the Royal Society a-Mathematical Physical and Engineering Sciences36639473967

36. Buesseler KO, Andrews JE, Pike SM, Charette MA (2004) The effects of iron fertilization on carbon sequestration in the Southern Ocean. Science 304: 414–417.KO BuesselerJE AndrewsSM PikeMA Charette2004The effects of iron fertilization on carbon sequestration in the Southern Ocean.Science304414417

37. Mazzocchi MG, González HE, Vandromme P, Borrione Is, d'Alcalà MR, et al. (2009) A non-diatom plankton bloom controlled by copepod grazing and amphipod predation: Preliminary results from the LOHAFEX iron-fertilisation experiment. GLOBEC International Newsletter 15: 3–6.MG MazzocchiHE GonzálezP. VandrommeIs BorrioneMR d'Alcalà2009A non-diatom plankton bloom controlled by copepod grazing and amphipod predation: Preliminary results from the LOHAFEX iron-fertilisation experiment.GLOBEC International Newsletter1536

38. Trick CG, Bill BD, Cochlan WP, Wells ML, Trainer VL, et al. (2010) Iron enrichment stimulates toxic diatom production in high-nitrate, low-chlorophyll areas. Proceedings of the National Academy of Sciences of the United States of America 107: 5887–5892.CG TrickBD BillWP CochlanML WellsVL Trainer2010Iron enrichment stimulates toxic diatom production in high-nitrate, low-chlorophyll areas.Proceedings of the National Academy of Sciences of the United States of America10758875892

39. Buesseler KO, Doney SC, Karl DM, Boyd PW, Caldeira K, et al. (2008) Environment - Ocean iron fertilization - Moving forward in a sea of uncertainty. Science 319: 162–162.KO BuesselerSC DoneyDM KarlPW BoydK. Caldeira2008Environment - Ocean iron fertilization - Moving forward in a sea of uncertainty.Science319162162

40. Sherwood GD, Rideout RM, Fudge SB, Rose GA (2007) Influence of diet on growth, condition and reproductive capacity in Newfoundland and Labrador cod (Gadus morhua): insights from stable carbon isotope (d13C). Deep-Sea Research Part II 54: 2794–2809.GD SherwoodRM RideoutSB FudgeGA Rose2007Influence of diet on growth, condition and reproductive capacity in Newfoundland and Labrador cod (Gadus morhua): insights from stable carbon isotope (d13C).Deep-Sea Research Part II5427942809

41. Laist DW, Knowlton AR, Mead JG, Collet AS, Podesta M (2001) Collisions between ships and whales. Marine Mammal Science 17: 35–75.DW LaistAR KnowltonJG MeadAS ColletM. Podesta2001Collisions between ships and whales.Marine Mammal Science173575

42. Greene CH, Pershing AJ, Kenney RD, Jossi JW (2003) Impact of climate variability on the recovery of endangered North Atlantic right whales. Oceanography 16: 96–101.CH GreeneAJ PershingRD KenneyJW Jossi2003Impact of climate variability on the recovery of endangered North Atlantic right whales.Oceanography1696101

43. Hutchings JA (2005) Life history consequences of over-exploitation to population recovery in Northwest Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 62: 824–832.JA Hutchings2005Life history consequences of over-exploitation to population recovery in Northwest Atlantic cod (Gadus morhua).Canadian Journal of Fisheries and Aquatic Sciences62824832

44. Walsh MR, Munch SB, Chiba S, Conover DO (2006) Maladaptive changes in multiple traits caused by fishing: impediments to population recovery. Ecology Letters 9: 142–148.MR WalshSB MunchS. ChibaDO Conover2006Maladaptive changes in multiple traits caused by fishing: impediments to population recovery.Ecology Letters9142148

45. IWC (2001) Report of the workshop on the comprehensive assessment of right whales: a worldwide comparison. In: Best PB, Bannister JL, Brownell RL Jr, Donovan GP, editors. Right Whales: Worldwide Status. Cambridge, UK: International Whaling Commission. pp. 1–60.IWC2001Report of the workshop on the comprehensive assessment of right whales: a worldwide comparison.PB BestJL BannisterRL Brownell JrGP DonovanRight Whales: Worldwide StatusCambridge, UKInternational Whaling Commission160

46. Barlow J, Clapham PJ (1997) A new birth-interval approach to estimating demographic parameters of humpback whales. Ecology 78: 535–546.J. BarlowPJ Clapham1997A new birth-interval approach to estimating demographic parameters of humpback whales.Ecology78535546

47. Gabriele CM, Straley JM, Neilson JL (2007) Age at first calving of female humpback whales in southeastern Alaska. Marine Mammal Science 23: 226–239.CM GabrieleJM StraleyJL Neilson2007Age at first calving of female humpback whales in southeastern Alaska.Marine Mammal Science23226239

48. Kraus S, Hamilton P, Kenney R, Knowlton A, Slay C (2001) Reproductive parameters of the North Atlantic right whale. J Cetacean Res Manage 2: 231–236.S. KrausP. HamiltonR. KenneyA. KnowltonC. Slay2001Reproductive parameters of the North Atlantic right whale.J Cetacean Res Manage2231236

49. Mizroch SA, Herman LM, Straley JM, Glockner-Ferrari DA, Jurasz C, et al. (2004) Estimating the adult survival rate of central North Pacific humpback whales (Megaptera novaeangliae). Journal of Mammalogy 85: 963–972.SA MizrochLM HermanJM StraleyDA Glockner-FerrariC. Jurasz2004Estimating the adult survival rate of central North Pacific humpback whales (Megaptera novaeangliae).Journal of Mammalogy85963972

50. Mizroch SA, Rice DW (2006) Have North Pacific killer whales switched prey species in response to depletion of the great whale populations? Marine Ecology-Progress Series 310: 235–246.SA MizrochDW Rice2006Have North Pacific killer whales switched prey species in response to depletion of the great whale populations?Marine Ecology-Progress Series310235246

51. Gabriele CM, Straley JM, Mizroch SA, Baker CS, Craig AS, et al. (2001) Estimating the mortality rate of humpback whale calves in the central North Pacific Ocean. Canadian Journal of Zoology-Revue Canadienne De Zoologie 79: 589–600.CM GabrieleJM StraleySA MizrochCS BakerAS Craig2001Estimating the mortality rate of humpback whale calves in the central North Pacific Ocean.Canadian Journal of Zoology-Revue Canadienne De Zoologie79589600

52. Lockyer C (1976) Body weights of some species of large whales. Journal du Conseil 36: 259–273.C. Lockyer1976Body weights of some species of large whales.Journal du Conseil36259273

53. George JC, Bada J, Zeh J, Scott L, Brown SE, et al. (1999) Age and growth estimates of bowhead whales (Balaena mysticetus) via aspartic acid racemization. Canadian Journal of Zoology-Revue Canadienne De Zoologie 77: 571–580.JC GeorgeJ. BadaJ. ZehL. ScottSE Brown1999Age and growth estimates of bowhead whales (Balaena mysticetus) via aspartic acid racemization.Canadian Journal of Zoology-Revue Canadienne De Zoologie77571580

54. Stevick PT (1999) Age-length relationships in humpback whales: a comparison of strandings in the western North Atlantic with commercial catches. Marine Mammal Science 15: 725–737.PT Stevick1999Age-length relationships in humpback whales: a comparison of strandings in the western North Atlantic with commercial catches.Marine Mammal Science15725737

55. Reeves RR, Stewart BS, Clapham PJ, Powell JA (2002) National Audubon Society Guide to Marine Mammals of the World. New York, NY: Alfred A. Knopf, Inc. 527 p.RR ReevesBS StewartPJ ClaphamJA Powell2002National Audubon Society Guide to Marine Mammals of the WorldNew York, NYAlfred A. Knopf, Inc527