It’s the prey that matters
Although many people think of dinosaurs as being the largest creatures to have lived on Earth, the true largest known animal is still here today—the blue whale. How whales were able to become so large has long been of interest. Goldbogen et al. used field-collected data on feeding and diving events across different types of whales to calculate rates of energy gain (see the Perspective by Williams). They found that increased body size facilitates increased prey capture. Furthermore, body-size increase in the marine environment appears to be limited only by prey availability.
The largest animals are marine filter feeders, but the underlying mechanism of their large size remains unexplained. We measured feeding performance and prey quality to demonstrate how whale gigantism is driven by the interplay of prey abundance and harvesting mechanisms that increase prey capture rates and energy intake. The foraging efficiency of toothed whales that feed on single prey is constrained by the abundance of large prey, whereas filter-feeding baleen whales seasonally exploit vast swarms of small prey at high efficiencies. Given temporally and spatially aggregated prey, filter feeding provides an evolutionary pathway to extremes in body size that are not available to lineages that must feed on one prey at a time. Maximum size in filter feeders is likely constrained by prey availability across space and time.
Large body size can improve metabolic and locomotor efficiency. In the oceans, extremely large body size evolved multiple times, especially among edentulous filter feeders that exploit dense patches of small-bodied prey (1, 2). All of these filter feeders had smaller, toothed ancestors that targeted much larger, single prey (3, 4). The ocean has hosted the rise and fall of giant tetrapods since the Triassic, but the largest known animals persist in today’s oceans, comprising multiple cetacean lineages (5–8). The evolution of specialized foraging mechanisms that distinguish the two major whale clades—biosonar-guided foraging on individual prey in toothed whales (Odontoceti) and engulfment filter feeding on prey aggregations in baleen whales (Mysticeti)—likely led to the diversification of crown cetaceans during the Oligocene (~33 to 23 million years ago). The origin of these foraging mechanisms preceded the recent evolution of the largest body sizes (9, 10), and the diversification of these mechanisms across this body size spectrum was likely enhanced by scale-dependent predator-prey processes (11). It is hypothesized that toothed whales evolved larger body sizes to enhance diving capacity and exploit deep-sea prey using more powerful biosonar (12), whereas baleen whales evolved larger sizes for more efficient exploitation of abundant, but patchily distributed, small-bodied prey (13). Cetacean foraging performance is constrained by diving physiology because cetaceans must balance two spatially decoupled resources: oxygen at the sea surface and higher-quality food at depth (14). In both lineages, large body size confers an ecological benefit that arises from the scaling of fundamental physiological processes; in some species, anatomical, molecular, and biochemical adaptations further enhance diving capacity (13). As animal size increases, mass-specific oxygen storage is constant yet mass-specific oxygen usage decreases (13). Therefore, larger air-breathers should have greater diving capacity and thus be capable of feeding for longer periods at a given depth, leading to higher feeding rates overall. In theory, this leads to relatively greater dive-specific energy intake with increasing body size; and, with unlimited prey at the scale of foraging grounds and seasons, larger divers will also exhibit greater energetic efficiencies (i.e., energy intake relative to energy use) while foraging. We hypothesized that the energetic efficiency of foraging will increase with body size because larger animals will have greater diving capacities and more opportunities to feed more frequently per dive. Filter-feeding baleen whales will exhibit relatively higher efficiencies compared with single-prey–feeding toothed whales, because they can exploit greater biomass at lower trophic levels. This study uses whale-borne tag data to provide a comparative test of these fundamental predictions.
Our direct measures of foraging performance using multisensor tags (Fig. 1) show that the largest odontocetes, such as sperm whales (Physeter macrocephalus) and beaked whales (Ziphiidae), exhibited high feeding rates during long, deep dives (Fig. 2). By investing time and energy in prolonged dives, these whales accessed deeper habitats that contained less mobile and potentially more abundant prey (15), such as weakly muscularized, ammoniacal squid. Conversely, rorqual whales performed fewer feeding events per dive despite their large body size, because they invested large amounts of energy to engulf larger volumes of prey-laden water (16). The energetic efficiency (EE, defined as the energy from captured prey divided by the expended energy, including diving costs and postdive recovery) is determined largely by the number of feeding events per dive (Fig. 2) and the amount of energy obtained during each feeding event (Fig. 3). This amount of energy obtained per feeding event was calculated from prey type and size distributions historically found in the stomachs of odontocetes (except for killer whales, for which we used identified prey remains from visually confirmed prey capture events), as well as the acoustically measured biomass, density, and distribution of krill at rorqual foraging hotspots (17). Our results show that although larger odontocetes appear to feed on larger prey relative to the prey of smaller, toothed whales, these prey were not disproportionally larger (Fig. 3 and table S11), and toothed whales did feed more frequently on this smaller prey type. Thus, the energy obtained from prey in a dive did not outweigh the increased costs associated with larger body size and deeper dives (fig. S2), thereby causing a decrease in EE with increasing body size in odontocetes (Fig. 4). In contrast, the measured distribution and density of krill biomass suggests that larger rorquals are not prey-limited at the scale of individual dives. Because larger rorquals have relatively larger engulfment capacities (16), rorquals exhibited much more rapid increases in energy captured from prey with increasing body size (Fig. 3). If they can detect and exploit the densest parts of an individual krill patch, as evidenced by their ability to maneuver more and increase feeding rates per dive when krill density is higher (14), then EE should increase with body size (Fig. 4). These results were robust to assumptions about trait similarity from shared ancestry as well as the scaling of metabolic rate (MR), which we simulated over a wide range as (MR ∝ Mc0.45:0.75, where Mc is cetacean body mass).
Beaked whales (Ziphiidae) and some sperm whales (P. macrocephalus) exhibit high feeding rates during long, deep dives, whereas rorquals and delphinids feed less frequently during shorter, shallower dives. Balaenids were excluded from this analysis because they are continuous-ram filter feeders and do not exhibit discrete feeding events like rorquals and odontocetes.