Baleen whale prey consumption based on high-resolution foraging measurements.

Baleen whales influence their ecosystems through immense prey consumption and nutrient recycling1-3. It is difficult to accurately gauge the magnitude of their current or historic ecosystem role without measuring feeding rates and prey consumed. To date, prey consumption of the largest species has been estimated using metabolic models3-9 based on extrapolations that lack empirical validation. Here, we used tags deployed on seven baleen whale (Mysticeti) species (n = 321 tag deployments) in conjunction with acoustic measurements of prey density to calculate prey consumption at daily to annual scales from the Atlantic, Pacific, and Southern Oceans. Our results suggest that previous studies3-9 have underestimated baleen whale prey consumption by threefold or more in some ecosystems. In the Southern Ocean alone, we calculate that pre-whaling populations of mysticetes annually consumed 430 million tonnes of Antarctic krill (Euphausia superba), twice the current estimated total biomass of E. superba10, and more than twice the global catch of marine fisheries today11. Larger whale populations may have supported higher productivity in large marine regions through enhanced nutrient recycling: our findings suggest mysticetes recycled 1.2 × 104 tonnes iron yr-1 in the Southern Ocean before whaling compared to 1.2 × 103 tonnes iron yr-1 recycled by whales today. The recovery of baleen whales and their nutrient recycling services2,3,7 could augment productivity and restore ecosystem function lost during 20th century whaling12,13.

Feeding morphology and body size shape resource partitioning in an eared seal community.

Body size and feeding morphology influence how animals partition themselves within communities. We tested the relationships among sex, body size, skull morphology and foraging in sympatric otariids (eared seals) from the eastern North Pacific Ocean, the most diverse otariid community in the world. We recorded skull measurements and stable carbon (δ13C) and nitrogen (δ15N) isotope values (proxies for foraging) from museum specimens in four sympatric species: California sea lions (Zalophus californianus), Steller sea lions (Eumetopias jubatus), northern fur seals (Callorhinus ursinus) and Guadalupe fur seals (Arctocephalus townsendi). Species and sexes had statistical differences in size, skull morphology and foraging significantly affecting the δ13C values. Sea lions had higher δ13C values than fur seals, and males of all species had higher values than females. The δ15N values were correlated with species and feeding morphology; individuals with stronger bite forces had higher δ15N values. We also found a significant community-wide correlation between skull length (indicator of body length), and foraging, with larger individuals having nearshore habitat preferences, and consuming higher trophic level prey than smaller individuals. Still, there was no consistent association between these traits at the intraspecific level, indicating that other factors might account for foraging variability.

Discovery of a sensory organ that coordinates lunge feeding in rorqual whales.

Top ocean predators have evolved multiple solutions to the challenges of feeding in the water. At the largest scale, rorqual whales (Balaenopteridae) engulf and filter prey-laden water by lunge feeding, a strategy that is unique among vertebrates. Lunge feeding is facilitated by several morphological specializations, including bilaterally separate jaws that loosely articulate with the skull, hyper-expandable throat pleats, or ventral groove blubber, and a rigid y-shaped fibrocartilage structure branching from the chin into the ventral groove blubber. The linkages and functional coordination among these features, however, remain poorly understood. Here we report the discovery of a sensory organ embedded within the fibrous symphysis between the unfused jaws that is present in several rorqual species, at both fetal and adult stages. Vascular and nervous tissue derived from the ancestral, anterior-most tooth socket insert into this organ, which contains connective tissue and papillae suspended in a gel-like matrix. These papillae show the hallmarks of a mechanoreceptor, containing nerves and encapsulated nerve termini. Histological, anatomical and kinematic evidence indicate that this sensory organ responds to both the dynamic rotation of the jaws during mouth opening and closure, and ventral groove blubber expansion through direct mechanical linkage with the y-shaped fibrocartilage structure. Along with vibrissae on the chin, providing tactile prey sensation, this organ provides the necessary input to the brain for coordinating the initiation, modulation and end stages of engulfment, a paradigm that is consistent with unsteady hydrodynamic models and tag data from lunge-feeding rorquals. Despite the antiquity of unfused jaws in baleen whales since the late Oligocene (∼23-28 million years ago), this organ represents an evolutionary novelty for rorquals, based on its absence in all other lineages of extant baleen whales. This innovation has a fundamental role in one of the most extreme feeding methods in aquatic vertebrates, which facilitated the evolution of the largest vertebrates ever.

Independent evolution of baleen whale gigantism linked to Plio-Pleistocene ocean dynamics.

Vertebrates have evolved to gigantic sizes repeatedly over the past 250 Myr, reaching their extreme in today's baleen whales (Mysticeti). Hypotheses for the evolution of exceptionally large size in mysticetes range from niche partitioning to predator avoidance, but there has been no quantitative examination of body size evolutionary dynamics in this clade and it remains unclear when, why or how gigantism evolved. By fitting phylogenetic macroevolutionary models to a dataset consisting of living and extinct species, we show that mysticetes underwent a clade-wide shift in their mode of body size evolution during the Plio-Pleistocene. This transition, from Brownian motion-like dynamics to a trended random walk towards larger size, is temporally linked to the onset of seasonally intensified upwelling along coastal ecosystems. High prey densities resulting from wind-driven upwelling, rather than abundant resources alone, are the primary determinant of efficient foraging in extant mysticetes and Late Pliocene changes in ocean dynamics may have provided an ecological pathway to gigantism in multiple independent lineages.

Extensively remodeled, fractured cetacean tympanic bullae show that whales can survive traumatic injury to the ears.

Underwater human activities and anthropogenic noise in our oceans may be a major source of habitat degradation for marine life. This issue was highlighted by the opening of the United States Eastern Seaboard for seismic oil and gas exploration in 2014, which generated massive media coverage and widespread concern that seismic surveys could kill or deafen whales. We discovered 11 new specimens of fractured and healed cetacean ear bones, out of a survey of 2127 specimens housed in museum collections. This rare condition has been previously reported only in two specimens of blue whales (Balaenoptera musculus) from the early 1900s, summarized by Fraser & Purves (1953). All of our new specimens are represented by species for which this condition had never been reported previously, including both baleen and toothed whales. The baleen whale specimens (Balaenoptera physalus, Balaenoptera borealis, Balaenoptera acutorostrata) were collected during Canadian commercial whaling operations in the Atlantic Ocean in the 1970s; the specimens include ear bones with well-healed fractures, demonstrating that baleen whales are capable of overcoming traumatic injury to the ears. The toothed whale specimens (Delphinus sp., Berardius bairdii) were found dead on beaches in 1972 and 2001, respectively, with less remodeled fractures. Thus, ear injuries may be more lethal to the echolocating toothed whales, which rely on hearing for navigation and foraging. We explore several hypotheses regarding how these injuries could have occurred, and conclude that the most parsimonious explanations appear to be both direct and indirect effects of lytic processes from disease or calcium depletion, or damage from external pressure waves. Although further research is required to confirm whether the fractures resulted from natural or human-induced events, this study underscores the importance of museum collections and the work of stranding networks in understanding the potential effects of modern human activities on marine mammal health.

The rise of ocean giants: maximum body size in Cenozoic marine mammals as an indicator for productivity in the Pacific and Atlantic Oceans.

Large consumers have ecological influence disproportionate to their abundance, although this influence in food webs depends directly on productivity. Evolutionary patterns at geologic timescales inform expectations about the relationship between consumers and productivity, but it is very difficult to track productivity through time with direct, quantitative measures. Based on previous work that used the maximum body size of Cenozoic marine invertebrate assemblages as a proxy for benthic productivity, we investigated how the maximum body size of Cenozoic marine mammals, in two feeding guilds, evolved over comparable temporal and geographical scales. First, maximal size in marine herbivores remains mostly stable and occupied by two different groups (desmostylians and sirenians) over separate timeframes in the North Pacific Ocean, while sirenians exclusively dominated this ecological mode in the North Atlantic. Second, mysticete whales, which are the largest Cenozoic consumers in the filter-feeding guild, remained in the same size range until a Mio-Pliocene onset of cetacean gigantism. Both vertebrate guilds achieved very large size only recently, suggesting that different trophic mechanisms promoting gigantism in the oceans have operated in the Cenozoic than in previous eras.

Repeated mass strandings of Miocene marine mammals from Atacama Region of Chile point to sudden death at sea.

Marine mammal mass strandings have occurred for millions of years, but their origins defy singular explanations. Beyond human causes, mass strandings have been attributed to herding behaviour, large-scale oceanographic fronts and harmful algal blooms (HABs). Because algal toxins cause organ failure in marine mammals, HABs are the most common mass stranding agent with broad geographical and widespread taxonomic impact. Toxin-mediated mortalities in marine food webs have the potential to occur over geological timescales, but direct evidence for their antiquity has been lacking. Here, we describe an unusually dense accumulation of fossil marine vertebrates from Cerro Ballena, a Late Miocene locality in Atacama Region of Chile, preserving over 40 skeletons of rorqual whales, sperm whales, seals, aquatic sloths, walrus-whales and predatory bony fish. Marine mammal skeletons are distributed in four discrete horizons at the site, representing a recurring accumulation mechanism. Taphonomic analysis points to strong spatial focusing with a rapid death mechanism at sea, before being buried on a barrier-protected supratidal flat. In modern settings, HABs are the only known natural cause for such repeated, multispecies accumulations. This proposed agent suggests that upwelling zones elsewhere in the world should preserve fossil marine vertebrate accumulations in similar modes and densities.

Downsizing a heavyweight: factors and methods that revise weight estimates of the giant fossil whale Perucetus colossus.

Extremes in organismal size have broad interest in ecology and evolution because organismal size dictates many traits of an organism's biology. There is particular fascination with identifying upper size extremes in the largest vertebrates, given the challenges and difficulties of measuring extant and extinct candidates for the largest animal of all time, such as whales, terrestrial non-avian dinosaurs, and extinct marine reptiles. The discovery of Perucetus colossus, a giant basilosaurid whale from the Eocene of Peru, challenged many assumptions about organismal extremes based on reconstructions of its body weight that exceeded reported values for blue whales (Balaenoptera musculus). Here we present an examination of a series of factors and methodological approaches to assess reconstructing body weight in Perucetus, including: data sources from large extant cetaceans; fitting published body mass estimates to body outlines; testing the assumption of isometry between skeletal and body masses, even with extrapolation; examining the role of pachyostosis in body mass reconstructions; addressing method-dependent error rates; and comparing Perucetus with known physiological and ecological limits for living whales, and Eocene oceanic productivity. We conclude that Perucetus did not exceed the body mass of today's blue whales. Depending on assumptions and methods, we estimate that Perucetus weighed 60-70 tons assuming a length 17 m. We calculated larger estimates potentially as much as 98-114 tons at 20 m in length, which is far less than the direct records of blue whale weights, or the 270 ton estimates that we calculated for body weights of the largest blue whales measured by length.

Novel muscle and connective tissue design enables high extensibility and controls engulfment volume in lunge-feeding rorqual whales.

Muscle serves a wide variety of mechanical functions during animal feeding and locomotion, but the performance of this tissue is limited by how far it can be extended. In rorqual whales, feeding and locomotion are integrated in a dynamic process called lunge feeding, where an enormous volume of prey-laden water is engulfed into a capacious ventral oropharyngeal cavity that is bounded superficially by skeletal muscle and ventral groove blubber (VGB). The great expansion of the cavity wall presents a mechanical challenge for the physiological limits of skeletal muscle, yet its role is considered fundamental in controlling the flux of water into the mouth. Our analyses of the functional properties and mechanical behaviour of VGB muscles revealed a crimped microstructure in an unstrained, non-feeding state that is arranged in parallel with dense and straight elastin fibres. This allows the muscles to accommodate large tissue deformations of the VGB yet still operate within the known strain limits of vertebrate skeletal muscle. VGB transverse strains in routine-feeding rorquals were substantially less than those observed in dead ones, where decomposition gas stretched the VGB to its elastic limit, evidence supporting the idea that eccentric muscle contraction modulates the rate of expansion and ultimate size of the ventral cavity during engulfment.

New evidence for the antiquity of Desmostylus (Desmostylia) from the Skooner Gulch Formation of California.

Desmostylus is an extinct marine mammal genus that belongs to Desmostylia, a clade of extinct herbivorous mammals. While desmostylian remains are widely reported from Paleogene and Neogene marine strata of the North Pacific Rim, occurrences of the genus Desmostylus are almost entirely limited to middle Miocene strata, with only a few early Miocene records from Japan. Here we report a Desmostylus tooth from the earliest Miocene (Aquitanian) Skooner Gulch Formation in northern California, USA. This specimen exhibits cuspules around the crown, a primitive trait of the subfamily Desmostylidae, as seen in more basal branching desmostylid taxa such as Cornwallius and Ounalashkastylus, but with a high tooth crown and thickened enamel. The specimen is also diagnostically different from all other desmostylid genera, such as Cornwallius, and Ounalashklastylus. The Aquitanian age of the Skooner Gulch Formation implies that the distinctive tooth morphology of Desmostylus has persisted, largely unchanged, for more than 15 million years and that desmostylids possibly originated in western North America.

Unexpected decadal density-dependent shifts in California sea lion size, morphology, and foraging niche.

Many marine mammal populations are recovering after long eras of exploitation.1,2 To what degree density-dependent body size declines in recovering species reflect a general response to increased resource competition is unknown. We examined skull size (as a proxy for body size), skull morphology, and foraging dynamics of the top marine predator, the California sea lion (Zalophus californianus), which have been steadily increasing over the last few decades and have approached or reached their carrying capacity in southern California.3 We show that, contrary to predictions, male California sea lions increased rather than decreased their average body size over a 46-year (1962-2008) recovery period. Larger males had proportionally longer oral cavities and more powerful bite strength, and their foraging niche expanded. Females between 1983 and 2007 maintained stable skull dimensions, but their isotopic niche was broader than contemporary males. Increased male body size is compatible with an intensification of density-dependent sexual selection for larger and more competitive individuals concurrent with an expanding foraging niche. High foraging variability among females would explain their body size stability during decades of population recovery. We demonstrate that body size reduction is not the universal response to population recovery in marine mammals and show that selective ecological dynamics could contribute to protecting populations against the increased density-dependent intraspecific competition. However, prey shifts associated with climate change will likely prevent California sea lions (and other marine mammals) from attaining these ecological dynamics, augmenting their vulnerability to resource competition and diminishing their capacity to overcome it.

Regaining creativity in science: insights from conversation.

The 'early modern' (Renaissance) workshop was predicated on the idea that informal, open-ended cooperation enables participants to experience difference and develop new insights, which can lead to new ways of thinking and doing. This paper presents the insights that emerged from a conversation event that brought wide-ranging voices together from different domains in science, and across the arts and industry, to consider science leadership as we look to the future in a time of interlocking crises. The core theme identified was a need to regain creativity in science; in the methods of scientific endeavours, in the way science is produced and communicated, and in how science is experienced in society. Three key challenges for re-establishing a culture of creativity in science emerged: (i) how scientists communicate what science is and what it is for, (ii) what scientists value, and (iii) how scientists create and co-create science with and for society. Furthermore, the value of open-ended and ongoing conversation between different perspectives as a means of achieving this culture was identified and demonstrated.

Expanding ocean protection and peace: a window for science diplomacy in the Gulf.

The ecological state of the Persian or Arabian Gulf (hereafter 'Gulf') is in sharp decline. Calls for comprehensive ecosystem-based management approaches and transboundary conservation have gone largely unanswered, despite mounting marine threats made worse by climate change. The region's long-standing political tensions add additional complexity, especially now as some Gulf countries will soon adopt ambitious goals to protect their marine environments as part of new global environmental commitments. The recent interest in global commitments comes at a time when diplomatic relations among all Gulf countries are improving. There is a window of opportunity for Gulf countries to meet global marine biodiversity conservation commitments, but only if scientists engage in peer-to-peer diplomacy to build trust, share knowledge and strategize marine conservation options across boundaries. The Gulf region needs more ocean diplomacy and coordination; just as critically, it needs actors at its science-policy interface to find better ways of adapting cooperative models to fit its unique marine environment, political context and culture. We propose a practical agenda for scientist-led diplomacy in the short term and lines of research from which to draw (e.g. co-production, knowledge exchange) to better design future science diplomacy practices and processes suited to the Gulf's setting.

Lateral palatal foramina do not indicate baleen in fossil whales.

Today's mysticetes filter-feed using baleen, a novel integumentary structure with no apparent homolog in any living mammal. The origins of filter-feeding and baleen can be informed by the fossil record, including rare instances of soft tissue preservation of baleen and also by potential osteological correlates of baleen. Lateral palatal foramina on the roof of the mouth have been proposed as potential osteological correlates of baleen and their presence in some tooth-bearing stem mysticetes has led to the hypothesis that these early mysticetes possessed both teeth and incipient baleen. Here, we test this hypothesis by examining lateral palatal foramina in both filter-feeding and non-filter-feeding cetaceans, including crown and stem odontocetes and in stem cetaceans (or archaeocetes). We also confirm the presence of lateral palatal foramina in 61 species of terrestrial artiodactyls. CT scanning demonstrates consistent internal morphology across all observed taxa, suggesting that the lateral palatal foramina observed in extant mysticetes are homologous to those of terrestrial artiodactyls. The presence of lateral palatal foramina in terrestrial artiodactyls and non-filter-feeding whales (odontocetes and archaeocetes) suggests that these structures are not unique predictors for the presence of baleen in fossil whales; instead, these structures are more probably associated with gingiva or other oral tissue.

Oh, the shark has such teeth: Did megatooth sharks play a larger role in prehistoric food webs?

Extinct megatooth sharks were globally distributed and contributed to ocean food chains that were potentially one to two steps longer than any food chain today.

New data from the first discovered paleoparadoxiid (Desmostylia) specimen shed light into the morphological variation of the genus Neoparadoxia.

Desmostylia is an extinct clade of marine mammals with two major sub-clades, Desmostylidae and Paleoparadoxiidae, known from Oligocene to Miocene strata of the North Pacific coastline. Within Paleoparadoxiidae, three genera have been identified: Archaeoparadoxia, Paleoparadoxia, and Neoparadoxia. The latter taxon is the geochronologically youngest palaeoparadoxiid and Neoparadoxia is characterized by a comparatively larger body size, although it is known only from a few specimens within a short temporal and geographic range. Here we report the discovery of an isolated tooth, which we identify as Neoparadoxia cf. N. cecilialina, constituting only the second individual specimen of Neoparadoxia with preserved dentition yet reported. This specimen was collected near Corona, California, USA, and we attribute it to the "Topanga" Formation, extending the geographic range of this taxon in Southern California. While the exact geographic locality was not recorded when it was collected in 1913, we establish two potential localities based on associated hand-written museum label and new stratigraphic information. Although initially identified as Desmostylus hesperus, this specimen of Neoparadoxia was collected 10 years before the first named paleoparadoxiid from Japan. We expect that description of more complete desmostylian material from elsewhere in Southern California will clarify the taxonomic richness and paleoecological role of this clade in Cenozoic marine mammal assemblages.

New Holocene grey whale (Eschrichtius robustus) material from North Carolina: the most complete North Atlantic grey whale skeleton to date.

Skeletal remains and historical accounts indicate that grey whales (Eschrichtius robustus) existed in the North Atlantic Ocean from the Pleistocene into the seventeenth century. Fossil and sub-fossil occurrences in this basin are rare, distributed from the east coast of the United States to Iceland and Europe. Here, we report an incomplete skeleton of a Holocene grey whale from Pender County, North Carolina, USA. This specimen represents a physically immature individual and is the most complete North Atlantic grey whale specimen reported to date. It comprises 42 cranial and postcranial elements, including the cranium, parts of the rostrum, both mandibles, both scapulae, humeri, radii and ulnae, most of the vertebral column anterior to the lumbar region and numerous ribs. Its provenance near the inlet of a large estuary is consistent with previous findings from the southeastern USA and parallels the species' habitat use in Baja California breeding and calving grounds in the North Pacific Ocean. Radiocarbon dating indicates an age of 827 ± 172 years before present. Cut marks on multiple skeletal elements indicate that the animal was butchered, suggesting some level of human exploitation of the species in the southeastern USA in the twelfth century, approximately 500 years prior to its extirpation in the North Atlantic.

Fossil Sirenia from the Pleistocene of Qatar: new questions about the antiquity of sea cows in the Gulf Region.

One of the largest and least documented populations of dugongs (Dugong dugon) resides in the coastal waters of the United Arab Emirates, and waters surrounding Saudi Arabia, Bahrain, and Qatar. The archaeological record of dugongs in the Gulf Region is abundant, but little is known about their fossil record in the region. Here we report an isolated sirenian rib fragment from the Futaisi Member of the Fuwayrit Formation near the town of Al Ruwais, in northern Qatar. The Fuwayrit Formation is a marine Pleistocene deposit exposed onshore in Qatar and the United Arab Emirates. Based on the correlative dating of the basal Futaisi Member with other onshore platforms, the rib fragment is approximately 125 ka. We propose that this isolated rib (likely the first rib from the right side) belongs to Dugongidae, with strong similarities to extant Dugong. We cannot, however, eliminate the possibility that it belongs to an extinct taxon, especially given its similarities with other fossil dugongid material from both Qatar and elsewhere in the world. Aside from reflecting the presence of Gulf seagrass communities in the Pleistocene, this occurrence also suggests that different (and potentially multiple) lineages of sirenians inhabited the Gulf Region in the geologic past.

Grouping behavior in a Triassic marine apex predator.

Marine tetrapods occupy important roles in modern marine ecosystems and often gather in large aggregations driven by patchy prey distribution,1,2 social or reproductive behaviors,3,4 or oceanographic factors.5 Here, we show that similar grouping behaviors evolved in an early marine tetrapod lineage, documented by dozens of specimens of the giant ichthyosaur Shonisaurus in the Luning Formation in West Union Canyon, Nevada, USA.6,7 A concentration of at least seven skeletons closely preserved on a single bedding plane received the bulk of previous attention. However, many more specimens are preserved across ∼106 square meters and ∼200 stratigraphic meters of outcrop representing an estimated >105-6 years. Unlike other marine-tetrapod-rich deposits, this assemblage is essentially monotaxic; other vertebrate fossils are exceptionally scarce. Large individuals are disproportionately abundant, with the exception of multiple neonatal or embryonic specimens, indicating an unusual demographic composition apparently lacking intermediate-sized juveniles or subadults. Combined with geological evidence, our data suggest that dense aggregations of Shonisaurus inhabited this moderately deep, low-diversity, tropical marine environment for millennia during the latest Carnian Stage of the Late Triassic Period (237-227 Ma). Thus, philopatric grouping behavior in marine tetrapods, potentially linked to reproductive activity, has an antiquity of at least 230 million years.