The whale pump: marine mammals enhance primary productivity in a coastal basin

It is well known that microbes, zooplankton, and fish are important sources of recycled nitrogen in coastal waters, yet marine mammals have largely been ignored or dismissed in this cycle. Using field measurements and population data, we find that marine mammals can enhance primary productivity in their feeding areas by concentrating nitrogen near the surface through the release of flocculent fecal plumes. Whales and seals may be responsible for replenishing 2.3×10(4) metric tons of N per year in the Gulf of Maine's euphotic zone, more than the input of all rivers combined. This upward "whale pump" played a much larger role before commercial harvest, when marine mammal recycling of nitrogen was likely more than three times atmospheric N input. Even with reduced populations, marine mammals provide an important ecosystem service by sustaining productivity in regions where they occur in high densities.     

Near-real-time acoustic monitoring of beaked whales and other cetaceans using a Seaglider™

In most areas, estimating the presence and distribution of cryptic marine mammal species, such as beaked whales, is extremely difficult using traditional observational techniques such as ship-based visual line transect surveys. Because acoustic methods permit detection of animals underwater, at night, and in poor weather conditions, passive acoustic observation has been used increasingly often over the last decade to study marine mammal distribution, abundance, and movements, as well as for mitigation of potentially harmful anthropogenic effects. However, there is demand for new, cost-effective tools that allow scientists to monitor areas of interest autonomously with high temporal and spatial resolution in near-real time. Here we describe an autonomous underwater vehicle--a glider--equipped with an acoustic sensor and onboard data processing capabilities to passively scan an area for marine mammals in near-real time. The glider was tested extensively off the west coast of the Island of Hawai'i, USA. The instrument covered approximately 390 km during three weeks at sea and collected a total of 194 h of acoustic data. Detections of beaked whales were successfully reported to shore in near-real time. Manual analysis of the recorded data revealed a high number of vocalizations of delphinids and sperm whales. Furthermore, the glider collected vocalizations of unknown origin very similar to those made by known species of beaked whales. The instrument developed here can be used to cost-effectively screen areas of interest for marine mammals for several months at a time. The near-real-time detection and reporting capabilities of the glider can help to protect marine mammals during potentially harmful anthropogenic activities such as seismic exploration for sub-sea fossil fuels or naval sonar exercises. Furthermore, the glider is capable of under-ice operation, allowing investigation of otherwise inaccessible polar environments that are critical habitats for many endangered marine mammal species.     

The first chromosome‐level genome for a marine mammal as a resource to study ecology and evolution

Marine mammals are important models for studying convergent evolution and aquatic adaption, and thus reference genomes of marine mammals can provide evolutionary insights. Here, we present the first chromosome‐level marine mammal genome assembly based on the data generated by the BGISEQ‐500 platform, for a stranded female sperm whale (Physeter macrocephalus). Using this reference genome, we performed chromosome evolution analysis of the sperm whale, including constructing ancestral chromosomes, identifying chromosome rearrangement events and comparing with cattle chromosomes, which provides a resource for exploring marine mammal adaptation and speciation. We detected a high proportion of long interspersed nuclear elements and expanded gene families, and contraction of major histocompatibility complex region genes which were specific to sperm whale. Using comparisons with sheep and cattle, we analysed positively selected genes to identify gene pathways that may be related to adaptation to the marine environment. Further, we identified possible convergent evolution in aquatic mammals by testing for positively selected genes across three orders of marine mammals. In addition, we used publicly available resequencing data to confirm a rapid decline in global population size in the Pliocene to Pleistocene transition. This study sheds light on the chromosome evolution and genetic mechanisms underpinning sperm whale adaptations, providing valuable resources for future comparative genomics.     

Seasonal and diel changes in cetacean vocalizations monitored by passive acoustic methods in Nemuro Strait adjacent to the Shiretoko World Natural Heritage Site

UNESCO World Natural Heritage sites are established to ensure the long-term conservation of natural areas. Nemuro Strait in northern Japan is adjacent to the Shiretoko World Natural Heritage Site, and attracts various trophic levels of marine species, including marine mammals. Although the coexistence of humans and marine mammals is an important issue in this area, the temporal habitat use of cetaceans in this area is unknown. Here, we document seasonal and diel changes in cetacean vocalizations collected using passive acoustic recording devices during November 2012–March 2014. Killer whale calls occurred in spring and summer, and sperm whale clicks were detected in summer. Pacific white-sided dolphin calls were recorded in summer and late fall. No cetaceans were recorded during the sea ice period in February and March. The dolphin calls and unknown click trains were significantly more frequent at night. In contrast, marginal diel changes in killer whale calls were detected. Our results suggest that the majority of cetaceans utilize Nemuro Strait at night during the ice-free period, and we provide new insights into the habitat use and diversity of marine mammals in the Strait.     

THERMOREGULATORY ADAPTATIONS IN MARINE MAMMALS: INTERACTING EFFECTS OF EXERCISE AND BODY MASS. A REVIEW1

A review of thermoregulation in marine mammals led to the following conclusions: very little is known about thermoregulation in large cetaceans. The only measured value for the metabolic rate of a whale, albeit a young one, was substantially higher than the predicted value for a terrestrial mammal of similar size. Very small and newborn marine mammals rely on a high metabolic heat production to sustain their body temperature during exposure to cold or in the water. The considerable insulation of some adult marine mammals may absolve them from the need for a high level of heat production. One marine mammal in tropical or subtropical waters is hypometabolic. There is evidence for a powerful control of thermoregulatory mechanisms by the anterior hypothalamic/preoptic region of the brain in two species. Thermoregulation in marine mammals during exercise remains paradoxical.     

Classification of Brucella spp. isolated from marine mammals by DNA polymorphism at the omp2 locus

A number of recent reports have described the isolation and characterization of Brucella strains from a wide variety of marine mammals such as seals, porpoises, dolphins and a minke whale. These strains were identified as brucellae by conventional typing tests. However, their overall characteristics were not assimilable to those of any of the six currently recognized Brucella species and it was suggested that they comprise a new nomen species to be called Brucella maris. In the present study we analysed DNA polymorphism at the omp2 locus of 33 marine mammal Brucella strains isolated from seals, dolphins, porpoises and an otter. The omp2 locus contains two gene copies (named omp2a and omp2b) coding for porin proteins and has been found particularly useful for molecular typing and identification of Brucella at the species, biovar, or strain level. PCR-restriction fragment length polymorphism (RFLP) and DNA sequencing showed that strains isolated from dolphins and porpoises carry two omp2b gene copies instead of one omp2a and one omp2b gene copy or two similar omp2a gene copies reported in the currently recognized species. This observation was also recently made for a minke whale Brucella isolate. The otter and all seal isolates except one were shown to carry one omp2a and one omp2b gene copy as encountered in isolates from terrestrial mammals. By PCR-RFLP of the omp2b gene, a specific marker was detected grouping the marine mammal Brucella isolates. Although marine mammal Brucella isolates may represent a separate group from terrestrial mammal isolates based on omp2b sequence constructed phylogenetic trees, the divergence found between their omp2b and also between their omp2a nucleotide sequences indicates that they form a more heterogeneous group than isolates from terrestrial mammals. Therefore, grouping the marine mammal Brucella isolates into one species Brucella maris seems inappropriate unless the currently recognized Brucella species are grouped. With respect to the current classification of brucellae according to the preferential host, brucellae isolated from such diverse marine mammal species as seals and dolphins could actually comprise more than one species, and at least two new species, B. pinnipediae and B. cetaceae, could be compatible with the classical criteria of host preferentialism and DNA polymorphism at their omp2 locus.     

Abundance estimation of long-diving animals using line transect methods

Line transect sampling is one of the most widely used methods for estimating the size of wild animal populations. An assumption in standard line transect sampling is that all the animals on the trackline are detected without fail. This assumption tends to be violated for marine mammals with surfacing/diving behaviors. The detection probability on the trackline is estimated using duplicate sightings from double-platform line transect methods. The double-platform methods, however, are insufficient to estimate the abundance of long-diving animals because these animals can be completely missed while the observers pass. We developed a more flexible hazard probability model that incorporates information on surfacing/diving patterns obtained from telemetry data. The model is based on a stochastic point process and is statistically tractable. A simulation study showed that the new model provides near-unbiased abundance estimates, whereas the traditional hazard rate and hazard probability models produce considerably biased estimates. As an illustration, we applied the model to data on the Baird's beaked whale (Berardius bairdii) in the western North Pacific.     

Isotope evidence for the intensive use of marine foods by Late Upper Palaeolithic humans

We report here on direct evidence for the intensive consumption of marine foods by anatomically modern humans at approximately 12,000 years ago. We undertook isotopic analysis of bone collagen from three humans, dating to the late Palaeolithic, from the site of Kendrick's Cave in North Wales, UK. The isotopic measurements of their bone collagen indicated that ca. 30% of their dietary protein was from marine sources, which we interpret as likely being high trophic level marine organisms such as marine mammals. This indicates that towards the end of the Pleistocene modern humans were pursuing a hunting strategy that incorporated both marine and terrestrial mammals. This is the first occurrence of the intensive use of marine resources, specifically marine mammals, that becomes even more pronounced in the subsequent Mesolithic period.     

Technical mitigation to reduce marine mammal bycatch and entanglement in commercial fishing gear: lessons learnt and future directions

Fisheries bycatch is one of the biggest threats to marine mammal populations. A literature review was undertaken to provide a comprehensive assessment and synopsis of gear modifications and technical devices to reduce marine mammal bycatch in commercial trawl, purse seine, longline, gillnet and pot/trap fisheries. Successfully implemented mitigation measures include acoustic deterrent devices (pingers) which reduced the bycatch of some small cetacean species in gillnets, appropriately designed exclusion devices which reduced pinniped bycatch in some trawl fisheries, and various pot/trap guard designs that reduced marine mammal entrapment. However, substantial development and research of mitigation options is required to address the bycatch of a range of species in many fisheries. No reliably effective technical solutions to reduce small cetacean bycatch in trawl nets are available, although loud pingers have shown potential. There are currently no technical options that effectively reduce marine mammal interactions in longline fisheries, although development of catch and hook protection devices is promising. Solutions are also needed for species, particularly pinnipeds and small cetaceans, that are not deterred by pingers and continue to be caught in static gillnets. Large whale entanglements in static gear, particularly buoy lines for pots/traps, needs urgent attention although there is encouraging research on rope-less pot/trap systems and identification of rope colours that are more detectable to whale species. Future mitigation development and deployment requires rigorous scientific testing to determine if significant bycatch reduction has been achieved, as well as consideration of potentially conflicting mitigation outcomes if multiple species are impacted by a fishery.

     

Investigating the Potential Use of Environmental DNA (eDNA) for Genetic Monitoring of Marine Mammals

The exploitation of non-invasive samples has been widely used in genetic monitoring of terrestrial species. In aquatic ecosystems, non-invasive samples such as feces, shed hair or skin, are less accessible. However, the use of environmental DNA (eDNA) has recently been shown to be an effective tool for genetic monitoring of species presence in freshwater ecosystems. Detecting species in the marine environment using eDNA potentially offers a greater challenge due to the greater dilution, amount of mixing and salinity compared with most freshwater ecosystems. To determine the potential use of eDNA for genetic monitoring we used specific primers that amplify short mitochondrial DNA sequences to detect the presence of a marine mammal, the harbor porpoise, Phocoena phocoena, in a controlled environment and in natural marine locations. The reliability of the genetic detections was investigated by comparing with detections of harbor porpoise echolocation clicks by static acoustic monitoring devices. While we were able to consistently genetically detect the target species under controlled conditions, the results from natural locations were less consistent and detection by eDNA was less successful than acoustic detections. However, at one site we detected long-finned pilot whale, Globicephala melas, a species rarely sighted in the Baltic. Therefore, with optimization aimed towards processing larger volumes of seawater this method has the potential to compliment current visual and acoustic methods of species detection of marine mammals.     

An evaluation of active acoustic methods for detection of marine mammals in the Canadian Beaufort Sea

A commercially available fisheries sonar was mounted on an icebreaker and evaluated during an environmental baseline study in the Canadian Beaufort Sea, to determine the applicability of active acoustic monitoring (AAM) for marine mammal detection by comparing marine mammal observer (MMO) visual sightings and active acoustic detections. During 170 h of simultaneous MMO and AAM, 115 bowhead whales (Balaena mysticetus) and four beluga whales (Delphinapterus leucas) were visually sighted by MMOs, while 59 sonar detections of bowhead whales occurred using AAM. The fisheries sonar detected 92% of the cetaceans observed within 2,000 m. Additional observations of ringed seals (Pusa hispida) and bearded seals (Erignathus barbatus) were recorded both by MMOs and AAM. Comparative results indicate that a commercially available active acoustic system can consistently detect marine mammals within varying ranges dictated by water column properties. Shallow environments and strong pycnoclines currently present challenges to AAM.     

Health risks for marine mammal workers

Marine mammals can be infected with zoonotic pathogens and show clinical signs of disease, or be asymptomatic carriers of such disease agents. While isolated cases of human disease from contact with marine mammals have been reported, no evaluation of the risks associated with marine mammal work has been attempted. Therefore, we designed a survey to estimate the risk of work-related injuries and illnesses in marine mammal workers and volunteers. The 17-question survey asked respondents to describe their contact with marine mammals, injuries sustained, and/or illnesses acquired during their period of marine mammal exposure. Most respondents, 88% (423/483), were researchers and rehabilitators. Of all respondents, 50% (243/483) reported suffering an injury caused by a marine mammal, and 23% (110/483) reported having a skin rash or reaction. Marine mammal work-related illnesses commonly reported included: 'seal finger' (Mycoplasma spp. or Erysipelothrix rhusiopathiae), conjunctivitis, viral dermatitis, bacterial dermatitis, and non-specific contact dermatitis. Although specific diagnoses could not be confirmed by a physician through this study, severe illnesses were reported and included tuberculosis, leptospirosis, brucellosis, and serious sequelae to seal finger. Risk factors associated with increased odds of injury and illness included prolonged and frequent exposure to marine mammals; direct contact with live marine mammals; and contact with tissue, blood, and excretions. Diagnosis of zoonotic disease was often aided by veterinarians; therefore, workers at risk should be encouraged to consult with a marine mammal veterinarian as well as a physician, especially if obtaining a definitive diagnosis for an illness becomes problematic.     

Temporal Dynamics of Top Predators Interactions in the Barents Sea

The Barents Sea system is often depicted as a simple food web in terms of number of dominant feeding links. The most conspicuous feeding link is between the Northeast Arctic cod Gadus morhua, the world''s largest cod stock which is presently at a historical high level, and capelin Mallotus villosus. The system also holds diverse seabird and marine mammal communities. Previous diet studies may suggest that these top predators (cod, bird and sea mammals) compete for food particularly with respect to pelagic fish such as capelin and juvenile herring (Clupea harengus), and krill. In this paper we explored the diet of some Barents Sea top predators (cod, Black-legged kittiwake Rissa tridactyla, Common guillemot Uria aalge, and Minke whale Balaenoptera acutorostrata). We developed a GAM modelling approach to analyse the temporal variation diet composition within and between predators, to explore intra- and inter-specific interactions. The GAM models demonstrated that the seabird diet is temperature dependent while the diet of Minke whale and cod is prey dependent; Minke whale and cod diets depend on the abundance of herring and capelin, respectively. There was significant diet overlap between cod and Minke whale, and between kittiwake and guillemot. In general, the diet overlap between predators increased with changes in herring and krill abundances. The diet overlap models developed in this study may help to identify inter-specific interactions and their dynamics that potentially affect the stocks targeted by fisheries.     

200 kHz Commercial Sonar Systems Generate Lower Frequency Side Lobes Audible to Some Marine Mammals

The spectral properties of pulses transmitted by three commercially available 200 kHz echo sounders were measured to assess the possibility that marine mammals might hear sound energy below the center (carrier) frequency that may be generated by transmitting short rectangular pulses. All three sounders were found to generate sound at frequencies below the center frequency and within the hearing range of some marine mammals, e.g. killer whales, false killer whales, beluga whales, Atlantic bottlenose dolphins, harbor porpoises, and others. The frequencies of these sub-harmonic sounds ranged from 90 to 130 kHz. These sounds were likely detectable by the animals over distances up to several hundred meters but were well below potentially harmful levels. The sounds generated by the sounders could potentially affect the behavior of marine mammals within fairly close proximity to the sources and therefore the exclusion of echo sounders from environmental impact analysis based solely on the center frequency output in relation to the range of marine mammal hearing should be reconsidered.     

The Gut Bacterial Community of Mammals from Marine and Terrestrial Habitats

After birth, mammals acquire a community of bacteria in their gastro-intestinal tract, which harvests energy and provides nutrients for the host. Comparative studies of numerous terrestrial mammal hosts have identified host phylogeny, diet and gut morphology as primary drivers of the gut bacterial community composition. To date, marine mammals have been excluded from these comparative studies, yet they represent distinct examples of evolutionary history, diet and lifestyle traits. To provide an updated understanding of the gut bacterial community of mammals, we compared bacterial 16S rRNA gene sequence data generated from faecal material of 151 marine and terrestrial mammal hosts. This included 42 hosts from a marine habitat. When compared to terrestrial mammals, marine mammals clustered separately and displayed a significantly greater average relative abundance of the phylum Fusobacteria. The marine carnivores (Antarctic and Arctic seals) and the marine herbivore (dugong) possessed significantly richer gut bacterial community than terrestrial carnivores and terrestrial herbivores, respectively. This suggests that evolutionary history and dietary items specific to the marine environment may have resulted in a gut bacterial community distinct to that identified in terrestrial mammals. Finally we hypothesize that reduced marine trophic webs, whereby marine carnivores (and herbivores) feed directly on lower trophic levels, may expose this group to high levels of secondary metabolites and influence gut microbial community richness.     

Selected contribution: a three-dimensional model for assessment of in vitro toxicity in balaena mysticetus renal tissue.

This study established two- and three-dimensional renal proximal tubular cell cultures of the endangered species bowhead whale (Balaena mysticetus), developed SV40-transfected cultures, and cloned the 61-amino acid open reading frame for the metallothionein protein, the primary binding site for heavy metal contamination in mammals. Microgravity research, modulations in mechanical culture conditions (modeled microgravity), and shear stress have spawned innovative approaches to understanding the dynamics of cellular interactions, gene expression, and differentiation in several cellular systems. These investigations have led to the creation of ex vivo tissue models capable of serving as physiological research analogs for three-dimensional cellular interactions. These models are enabling studies in immune function, tissue modeling for basic research, and neoplasia. Three-dimensional cellular models emulate aspects of in vivo cellular architecture and physiology and may facilitate environmental toxicological studies aimed at elucidating biological functions and responses at the cellular level. Marine mammals occupy a significant ecological niche (72% of the Earth's surface is water) in terms of the potential for information on bioaccumulation and transport of terrestrial and marine environmental toxins in high-order vertebrates. Few ex vivo models of marine mammal physiology exist in vitro to accomplish the aforementioned studies. Techniques developed in this investigation, based on previous tissue modeling successes, may serve to facilitate similar research in other marine mammals.     

C-values of seven marine mammal species determined by flow cytometry

C-values, which estimate genome size, have puzzled geneticists for years because they bear no relationship to organismal complexity. Though C-values have been estimated for thousands of species, considerably more data are required in order to better understanding genome evolution. This is particularly true for mammals, in which C-values are known for less than 8% of the total number of mammalian species. Among marine mammals, a C-value has been estimated only for the bottlenose dolphin (Tursiops truncatus). Thus examination of additional species of marine mammals is necessary for comparative purposes. It will enable a better understanding of marine mammal genome evolution, and it is also relevant to conservation, because larger genome size has been linked to increased likelihood of extinction in some plant and animal groups. Our study presents C-values of seven marine mammal species, including five cetacean species that are endangered to varying degrees. Similarly to the results for other groups, our results suggest that larger genome size in cetaceans is related to an increased likelihood of extinction.     

Sperm whale depredation of sablefish longline gear in the northeast Pacific Ocean

Interactions between marine mammals and fisheries include competition for prey (catch), marine mammal entanglement in fishing gear, and catch removal off fishing gear (depredation). We estimated the magnitude of sperm whale depredation on a major North Pacific longline fishery (sablefish) using data collected during annual longline surveys. Sperm whale depredation occurs while the longline gear is off‐bottom during retrieval. Sperm whales were observed on 16% of longline survey sampling days, mostly (95% of sightings) over the continental slope. Sightings were most common in the central and eastern Gulf of Alaska (98% of sightings), occasional in the western Gulf of Alaska and Aleutian Islands, and absent in the Bering Sea. Longline survey catches were commonly preyed upon when sperm whales were present (65% of sightings), as evidenced by damaged fish. Neither sperm whale presence (P = 0.71) nor depredation rate (P = 0.78) increased significantly from 1998 to 2004. Longline survey catch rates were about 2% less at locations where depredation was observed, but the effect was not significant (P = 0.34). Estimated sperm whale depredation was <1% of the annual sablefish longline fishery catch off Alaska during 1998 to 2004.     

Distribution of fish in the complex of floodplain-riverbed biotopes of the Irtysh

Distribution, composition, and movements of fish within the floodplain-riverbed complex of the Lower Irtysh are investigated. The principal working tools were hydroacoustic computerized complexes for the detection of fish aggregations and of their movements in the floodplain water course. Twenty-four-hour hydroacoustic observations revealed the predominantly crepuscular-nocturnal type of activity of most fish and the mass downstream migration of juveniles at the onset of the night. Seasonal traits of formation of fish aggregations on key biotopes of the Irtysh are revealed, and their biological harmony is shown. The necessity that fish distribution should be analyzed as a dynamic phenomenon is shown.     

Parasites in stranded cetaceans of Patagonia

There is an increasing interest in parasites of marine mammals of Argentina. Here, we examined several poorly known cetaceans, i.e., 2 spectacled porpoises and 1 Burmeister's porpoise (Phocoenidae), and 1 Gray's beaked whale and 1 Cuvier's beaked whale (Ziphidae); we also updated the parasite information for 1 sperm whale (Physeteridae). These hosts strand only occasionally. We found Anisakis simplex s.l. in 2 spectacled porpoises and the Burmeister's porpoise, and recorded its distribution among the stomach chambers. Anisakis physeteris infected the sperm whale; Corynosoma cetaceum occurred in the duodenal ampulla of the Burmeister's porpoise; Corynosoma australe was found in the posterior-most region of the intestine of 1 spectacled porpoise, while another one had Tetrabothrius sp. in the anal crypts; Corynosoma bullosum and Corynosoma sp. were found in the sperm whale. The only digenean found was Pholeter gastrophilus in the Burmeister's porpoise. Merocercoids of Phyllobothrium delphini were present in the blubber of 1 spectacled porpoise, the sperm whale, and the Gray's beaked whale, while Scolex pleuronectis infected the Gray's beaked whale and 1 spectacled porpoise. No parasites were recovered from the Cuvier's beaked whale. Poor parasite-species assemblages are consistent in marine mammals of Patagonia. Given the conservation status of these hosts, the limited parasitological information gathered is valuable for conservation or management of these hosts in Patagonia.