Evidence from sperm whale clans of symbolic marking in non-human cultures.

Culture, a pillar of the remarkable ecological success of humans, is increasingly recognized as a powerful force structuring nonhuman animal populations. A key gap between these two types of culture is quantitative evidence of symbolic markers-seemingly arbitrary traits that function as reliable indicators of cultural group membership to conspecifics. Using acoustic data collected from 23 Pacific Ocean locations, we provide quantitative evidence that certain sperm whale acoustic signals exhibit spatial patterns consistent with a symbolic marker function. Culture segments sperm whale populations into behaviorally distinct clans, which are defined based on dialects of stereotyped click patterns (codas). We classified 23,429 codas into types using contaminated mixture models and hierarchically clustered coda repertoires into seven clans based on similarities in coda usage; then we evaluated whether coda usage varied with geographic distance within clans or with spatial overlap between clans. Similarities in within-clan usage of both "identity codas" (coda types diagnostic of clan identity) and "nonidentity codas" (coda types used by multiple clans) decrease as space between repertoire recording locations increases. However, between-clan similarity in identity, but not nonidentity, coda usage decreases as clan spatial overlap increases. This matches expectations if sympatry is related to a measurable pressure to diversify to make cultural divisions sharper, thereby providing evidence that identity codas function as symbolic markers of clan identity. Our study provides quantitative evidence of arbitrary traits, resembling human ethnic markers, conveying cultural identity outside of humans, and highlights remarkable similarities in the distributions of human ethnolinguistic groups and sperm whale clans.

The Evolution of Unusually Small Amelogenin Genes in Cetaceans; Pseudogenization, X-Y Gene Conversion, and Feeding Strategy.

Among extant cetaceans, mysticetes are filter feeders that do not possess teeth and use their baleen for feeding, while most odontocetes are considered suction feeders, which capture prey by suction without biting or chewing with teeth. In the present study, we address the functionality of amelogenin (AMEL) genes in cetaceans. AMEL encodes a protein that is specifically involved in dental enamel formation and is located on the sex chromosomes in eutherians. The X-copy AMELX is functional in enamel-bearing eutherians, whereas the Y-copy AMELY appears to have undergone decay and was completely lost in some species. Consistent with these premises, we detected various deleterious mutations and/or non-canonical splice junctions in AMELX of mysticetes and four suction feeding odontocetes, Delphinapterus leucas, Monodon monoceros, Kogia breviceps, and Physeter macrocephalus, and in AMELY of mysticetes and odontocetes. Regardless of the functionality, both AMELX and AMELY are equally and unusually small in cetaceans, and even their functional AMELX genes presumably encode a degenerate core region, which is thought to be essential for enamel matrix assembly and enamel crystal growth. Furthermore, our results suggest that the most recent common ancestors of extant cetaceans had functional AMELX and AMELY, both of which are similar to AMELX of Platanista minor. Similar small AMELX and AMELY in archaic cetaceans can be explained by gene conversion between AMELX and AMELY. We speculate that common ancestors of modern cetaceans employed a degenerate AMELX, transferred from a decaying AMELY by gene conversion, at an early stage of their transition to suction feeders.

Toxic Identification and Evaluation of Androgen Receptor Antagonistic Activities in Acid-Treated Liver Extracts of High-Trophic Level Wild Animals from Japan.

Sulfuric acid-treated liver extracts of representative high-trophic level Japanese animals were analyzed by toxic identification and evaluation (TIE) with chemically activated luciferase expression (CALUX) and chemical analysis to elucidate androgen receptor (AR) antagonistic activities and potential contributions of organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs). The activities were detected in striped dolphins (n = 5), Stejneger's beaked whales (n = 6), golden eagle (n = 1), and Steller's sea eagle (n = 1) with CALUX-flutamide equivalents (FluEQs) as follow: 38 (20-52), 47 (21-96), 5.0, and 80 µg FluEQ/g-lipid, respectively. The AR antagonism was detected in limited number of specimens at lower levels for finless porpoise, raccoon dog, and common cormorant. Theoretical activities (Theo-FluEQs) were calculated using the concentration of OCPs and PCBs and their IC25-based relative potency (REP) values. These total contribution to CALUX-FluEQ was 126%, 84%, 53%, 55%, and 44% for striped dolphin, Steller's sea eagle, Stejneger's beaked whale, finless porpoise, and golden eagle, respectively, and the main contributor was p,p'-DDE. However, most of the activities for raccoon dog (7.6%) and common cormorant (17%) could not be explained by OCPs and PCBs. This suggests other unknown compounds could function as AR antagonists in these terrestrial species.

A first record of digenean parasites of the dwarf sperm whale Kogia sima with morphological and molecular information.

Two species of digenean trematodes of the family Brachycladiidae were obtained from two male dwarf sperm whales Kogia sima that stranded along the island of Kyushu, southern Japan in 2017. From the liver of the first animal, a single, large gravid specimen of a digenean species was collected. The morphological features were consistent with those of the genus Brachycladium. The worm had a large body and was characterized by anterior caeca without lateral diverticula, the shape of testes, ovary, and eggs. Molecular analyses using gene sequences of the 28S rRNA and the mitochondrial NADH dehydrogenase subunit 3 also supported the inclusion of this specimen into the genus Brachycladium. The identity of this worm is undetermined due to the lack of information on the genus and is reported as Brachycladium sp. From the cranial sinuses of the second animal, 33 specimens of digeneans were collected that were morphologically identified as Nasitrema gondo. This report documents a new host record for N. gondo, and the sequence information is provided for this digenean for the first time. This is the second record of digenean parasites for the family Kogiidae, and the first record with morphological and molecular information. The possibility of digenean infection in the liver and cranial sinus should be kept in mind during the necropsy of stranded kogiids.

Notes on stomach contents of pygmy and dwarf sperm whales (Kogia spp.) from around Japan.

The diets of pygmy (Kogia breviceps) and dwarf (K. sima) sperm whales in Japanese waters are poorly known. We report new information on the diets of these two species from these waters based on identifiable hard-part remains recovered from the stomach contents of 29 whales (11 pygmy and 18 dwarf sperm whales) that stranded between 1991 and 2021; those of a further two dwarf sperm whales were empty. The cephalopod (and secondarily fish and crustacean) component of the diets of these 29 whales, based on analysis of identifiable stomach-content remains, is described. The main prey includes cephalopods, represented by 1556 identifiable lower beaks (and 1483 upper beaks), crustaceans (represented by heavily digested, unidentifiable remains), and fishes (as represented by 92 otoliths). Identified prey comprises 30 species from 16 cephalopod families and 5 families from 5 fish orders. Oceanic cephalopods are the main prey of both whale species, particularly Enoploteuthis (Paraenoploteuthis) chunii and Chiroteuthis (Chirothauma) picteti. Prey diversity index values (Shannon-Weaver's diversity index H') are 2.41 for the pygmy sperm whale and 2.66 for the dwarf sperm whale. Although the main cephalopod component in the diets of these two whale species is similar, Pianka's index (0.40), a measure of niche overlap, is not that high, and may be influenced by differences in prey dominance in different feeding areas.

Scaling of swim speed in breath-hold divers.

1. Breath-hold divers are widely assumed to descend and ascend at the speed that minimizes energy expenditure per distance travelled (the cost of transport (COT)) to maximize foraging duration at depth. However, measuring COT with captive animals is difficult, and empirical support for this hypothesis is sparse. 2. We examined the scaling relationship of swim speed in free-ranging diving birds, mammals and turtles (37 species; mass range, 0·5-90,000 kg) with phylogenetically informed statistical methods and derived the theoretical prediction for the allometric exponent under the COT hypothesis by constructing a biomechanical model. 3. Swim speed significantly increased with mass, despite considerable variations around the scaling line. The allometric exponent (0·09) was statistically consistent with the theoretical prediction (0·05) of the COT hypothesis. 4. Our finding suggests a previously unrecognized advantage of size in divers: larger animals swim faster and thus could travel longer distance, search larger volume of water for prey and exploit a greater range of depths during a given dive duration. 5. Furthermore, as predicted from the model, endotherms (birds and mammals) swam faster than ectotherms (turtles) for their size, suggesting that metabolic power production limits swim speed. Among endotherms, birds swam faster than mammals, which cannot be explained by the model. Reynolds numbers of small birds (<2 kg) were close to the lower limit of turbulent flow (∼ 3 × 10(5) ), and they swam fast possibly to avoid the increased drag associated with flow transition.

Population-level laterality in foraging finless porpoises.

Laterality has been reported in many vertebrates, and asymmetrical cerebral hemisphere function has been hypothesized to cause a left-bias in social behavior and a right-bias in feeding behavior. In this paper, we provide the first report of behavioral laterality in free-ranging finless porpoises, which seems to support the aforementioned hypothesis. We observed the turning behavior of finless porpoises in Omura Bay, Japan, using land-based and unmanned aerial system observations. We found a strong tendency in finless porpoises to turn counterclockwise with their right side down when pursuing and catching fish at the surface of the water. Our results suggest that this population of finless porpoises shows consistent right-biased laterality. Right-biased laterality has been observed in various foraging cetaceans and is usually explained by the dominance of the right eye-left cerebral hemisphere in prey recognition; however, right-biased laterality in foraging cetaceans may have multiple causes.

Disseminated Toxoplasmosis in a Narrow-Ridged Finless Porpoise (Neophocaena asiaeorientalis) with Transplacental Embryonal Transmission.

We describe a case of systemic toxoplasmosis in a female adult narrow-ridged finless porpoise (Neophocaena asiaeorientalis) found in May 2018 inside a gillnet set in the Ariake Sound, southern Japan. The main lesions observed were lymphoplasmacytic and focally necrotizing encephalitis, necrotizing to granulomatous adrenalitis, myocarditis, and inflammation in the intestinal wall, associated with protozoal tissue cysts and tachyzoites. Additionally, the individual had a 5.6 mm (crown-rump length) early-stage embryo in the left uterine horn, which had multifocal necrotizing lesions with intralesional tissue cysts and tachyzoites in the parenchyma. Immunohistochemistry and PCR and sequencing of the internal transcribed spacer 1 region confirmed a Toxoplasma gondii infection. Further genotyping revealed an atypical type II genotype with a type I pattern for the Apico locus. Narrow-ridged finless porpoises are an endangered coastal species already facing various anthropogenic threats. Toxoplasmosis, especially with its ability to transmit to an early-stage embryo, should be considered an emerging threat to this vulnerable species.

Similar circling movements observed across marine megafauna taxa.

Advances in biologging technology have enabled 3D dead-reckoning reconstruction of marine animal movements at spatiotemporal scales of meters and seconds. Examining high-resolution 3D movements of sharks (Galeocerdo cuvier, N = 4; Rhincodon typus, N = 1), sea turtles (Chelonia mydas, N = 3), penguins (Aptenodytes patagonicus, N = 6), and marine mammals (Arctocephalus gazella, N = 4; Ziphius cavirostris, N = 1), we report the discovery of circling events where animals consecutively circled more than twice at relatively constant angular speeds. Similar circling behaviors were observed across a wide variety of marine megafauna, suggesting these behaviors might serve several similar purposes across taxa including foraging, social interactions, and navigation.

Long-term associations among male sperm whales (Physeter macrocephalus).

Little is known about the social structure of male sperm whales (Physeter macrocephalus) after they leave their natal units. While previous studies found no evidence for preferred associations among males, the observation of mass-strandings consisting exclusively of males, suggest that they have strong social bonds. To investigate the social associations among male sperm whales, we used half weight index of association, permutation tests and standardized lagged association rate models on a large photo-identification database collected between 2006 and 2017 in Nemuro Strait, Japan. Our results suggest that while male sperm whales are not as social as females, they do form long term associations, have preferred companionship, and forage in social proximity to each other. The best-fitting model to the standardized lagged association rate showed that associations among males last for at least 2.7 years and as most males leave the area after 2 years, associations may last for longer. Twenty dyads were observed associating over more than 2 years, for a maximum 5 years. One dyad was observed associating on 19 different days and clustered on 7 different days. Male associations may function to enhance foraging or to fend off predators. Such relationships seem to be adapted to a pelagic habitat with uncertain resource availability and predation pressure.

Functions of post-conflict bystander affiliations toward aggressors and victims in bottlenose dolphins.

Post-conflict affiliations initiated by bystanders (bystander affiliation) toward aggressors or victims have been suggested to represent the function of conflict management in some social living species. However, the function of bystander affiliations toward aggressors and victims has not been examined in marine mammals. In the present study, we investigated the function of bystander affiliations to aggressors and victims in bottlenose dolphins: self-protection, the substitute of reconciliation, social facilitation and tension relief of opponents. These bystander affiliations did not reduce post-conflict attacks by former opponents against group members. Bystander affiliation to aggressors tended to be performed by a bystander who had an affiliative relationship with the aggressor but not with the victim. Bystander affiliation to victims also tended to be initiated by a bystander who had an affiliative relationship with the victim but not the aggressor and was close to former opponents at the end of aggressions. Affiliation among group members who stayed near former opponents during aggressions did not increase after aggressions compared to that under control conditions. Renewed aggressions between former opponents decreased after bystander affiliations in our previous study. Bystanders who showed social closeness to former opponents may initiate bystander affiliation toward their affiliative former opponents because they may feel emotion, such as anxiety and excitement, of former opponents. Bystander affiliation toward aggressors and victims may function as tension relief between former opponents. Bystanders of bottlenose dolphins, who may have a relaxed dominant style, might initiate post-conflict affiliation to affiliative individuals unaffected by the dominance relationships among them, unlike despotic species.

Serologic survey of Brucella infection in cetaceans inhabiting along the coast of Japan.

A serologic investigation of Brucella infection was performed in 7 species of cetaceans inhabiting along the coast of Japan. A total of 32 serum samples were examined by enzyme-linked immunosorbent assay (ELISA) using Brucella abortus and B. canis antigens. One serum sample from five melon-headed whales (Peponocephala electra) was positive for B. abortus. No serum sample showed positive for B. canis. The ELISA-positive melon-headed whale serum demonstrated a strong band appearance only against B. abortus antigens in Western blot analysis. Many detected bands were discrete, while some of them had a smeared appearance. The present results indicate that Brucella infection occurred in melon-headed whale population and the bacterial antigenicity is more similar to that of B. abortus than B. canis.

Organohalogen contaminants in striped dolphins (Stenella coeruleoalba) from Japan: present contamination status, body distribution and temporal trends (1978-2003).

Organohalogen contaminants including PCBs, DDTs, CHLs, HCHs, HCB, PBDEs and HBCDs were determined in striped dolphins (Stenella coeruleoalba) found stranded at Gogo-shima (n=6, 2003) and collected from Taiji (n=15, 1978-1992) in Japan. All target compounds were significantly detected in all the specimens, indicating ubiquitous contamination of oceanic cetaceans in northwest Pacific Ocean. Examination of body distribution of organohalogens in the six specimens from Gogo-shima showed no significant difference in concentrations among the analyzed tissues, except for brain, which had lower levels possibly due to the existence of blood-brain barrier. For evaluating temporal trends, archived blubber samples of adult male stripped dolphins collected in 1978, 1979, 1986 and 1992 were analyzed. Concentrations of PCBs, DDTs and HCHs did not change significantly during 1978-2003. In contrast, remarkable increasing trends of PBDEs and HBCDs were observed, suggesting growing consumption in Japan and surrounding countries in recent years.

Revision of the taxonomic status of Synthesium elongatum (Ozaki, 1935) (Brachycladiidae), an intestinal digenean of narrow-ridged finless porpoise (Neophocaena asiaeorientalis).

Synthesium elongatum (Brachycladiidae) is an intestinal digenean described from the finless porpoise (Neophocaena asiaeorientalis) in Japan. Few records of this species exist and there is a remarkable morphological similarity between S. elongatum and S. tursionis, such that a synonymy between the species has been suggested previously. However, no morphological and/or molecular analysis has been carried out to clarify the taxonomic status of S. elongatum. In this study, we collected specimens of Synthesium sp. from N. asiaeorientalis in western Japan. The specimens possess lobed testes within the third quarter of the body, a round ovary, and vitellaria extending to level of uterine field, which are diagnostic characters for both S. elongatum and S. tursionis. They were morphologically identified to S. elongatum or S. tursionis due to the fact that the available morphometric data for both species overlap remarkably. A molecular analysis of the mitochondrial ND3 gene showed that the pairwise nucleotide distances between these specimens and S. tursionis were small, and phylogenetic analysis showed that these specimens and S. tursionis are in the same clade. Therefore, it was indicated that S. elongatum and S. tursionis are the same species and, consequently, S. elongatum is a synonym of S. tursionis.

Detection of serum antibodies to Brucella in Russian aquatic mammals.

A serologic survey of Brucella infection was performed in Caspian seals (Pusa caspica, n=71), Baikal seals (P. sibirica, n=7), ringed seals (P. hispida hispida, n=6), and beluga whales (Delphinapterus leucas, n=4) inhabiting Russian waters, by enzyme-linked immunosorbent assay (ELISA) using Brucella abortus and B. canis as antigens. The sera of 4 Caspian seals (4%) tested positive for B. abortus. The same sera samples demonstrated weaker yet detectable affinity for B. canis antigens. Several discrete bands against B. abortus and B. canis antigens were detected on Western blot analysis of the ELISA-positive seal sera; the bands against B. canis were weaker than those against B. abortus. The sera of 3 beluga whales (75%) were positive for B. abortus antigens but showed no binding to B. canis antigens in the ELISA. The positive whale sera showed a strong band appearance only against B. abortus antigens in the Western blot analysis. Many detected bands were discrete, while some of them had a smeared appearance. The present results indicate that Brucella infection occurred in Caspian seals and beluga whales inhabiting Russian waters, and that the Brucella strains infecting the seals and the whales were antigenetically distinct.

Stroke frequency, but not swimming speed, is related to body size in free-ranging seabirds, pinnipeds and cetaceans.

It is obvious, at least qualitatively, that small animals move their locomotory apparatus faster than large animals: small insects move their wings invisibly fast, while large birds flap their wings slowly. However, quantitative observations have been difficult to obtain from free-ranging swimming animals. We surveyed the swimming behaviour of animals ranging from 0.5 kg seabirds to 30 000 kg sperm whales using animal-borne accelerometers. Dominant stroke cycle frequencies of swimming specialist seabirds and marine mammals were proportional to mass(-0.29) (R(2)= 0.99, n = 17 groups), while propulsive swimming speeds of 1-2 m s(-1) were independent of body size. This scaling relationship, obtained from breath-hold divers expected to swim optimally to conserve oxygen, does not agree with recent theoretical predictions for optimal swimming. Seabirds that use their wings for both swimming and flying stroked at a lower frequency than other swimming specialists of the same size, suggesting a morphological trade-off with wing size and stroke frequency representing a compromise. In contrast, foot-propelled diving birds such as shags had similar stroke frequencies as other swimming specialists. These results suggest that muscle characteristics may constrain swimming during cruising travel, with convergence among diving specialists in the proportions and contraction rates of propulsive muscles.

Molecular characterization of cytochrome P450 1A1, 1A2, and 1B1, and effects of polychlorinated dibenzo-p-dioxin, dibenzofuran, and biphenyl congeners on their hepatic expression in Baikal seal (Pusa sibirica).

This study attempts to relate the 2,3,7,8-tetrachlorodibenzo-p-dioxin toxic equivalent (TEQ) level with certain responses including the catalytic activities and expression of hepatic cytochrome P450 (CYP) 1A and CYP1B in wild population of Baikal seal (Pusa sibirica). We isolated full-length CYP1A1, 1A2, and 1B1 cDNAs, which encode proteins of 516, 512, and 543 amino acids, respectively. Immunochemical analysis demonstrated that a cross-reactive protein with polyclonal antibody against rat CYP1A1 or CYP1B1 was detected in the seal liver. Total TEQ levels showed significant positive correlations with expression levels of CYP1A1, 1A2, and 1B1 mRNAs, and further with both CYP1A- and CYP1B-like proteins, indicating chronic induction of these CYP isozymes by TEQs. The 50% effective concentration for CYP1A-like protein induction was estimated to be 65 pg TEQ/g wet weight. To evaluate the potential of congener-specific metabolism, profiles of negative correlations between the concentrations of eachcongener normalized to a relatively recalcitrant congener, PCB169, and CYP1A-like protein levels were also estimated. Significant negative correlations of 2,3,7,8-tetrachlorodibenzofuran and PCB77 to CYP1A-like protein expression may possibly be due to the preferential metabolism of these congeners. Anti-rat CYP1A1 and CYP1B1 antisera equivalently inhibited ethoxyresorufin O-deethylase (EROD) activity in the seal microsomes, suggesting that both CYPs are involved in EROD activity. Hepatic EROD revealed an increasing trend at lower TEQs, but a declining trend at higher levels, implying a catalytic inhibition of CYP1A and CYP1B. Furthermore, ratios of CYP1B1/CYP1A1 mRNA expression levels increased with TEQs, indicating the enhanced risk of carcinogenicity by preferential induction of CYP1B1 by TEQs in the liver.

Population- and growth-related differences in helminthic fauna of finless porpoises (Neophocaena asiaeorientalis) in five Japanese populations.

A survey of helminths and ectoparasites, including epizoits, was conducted in narrow-ridged finless porpoises (Neophocaena asiaeorientalis) from Japanese five populations using dead stranded or incidentally caught animals. In total, 13 helminth species were found (6 nematodes, 4 trematodes, 2 cestodes and 1 acanthocephalan) in 137 porpoises. A new location record of Stenurus nanjingensis and a new host record of Tetrabothrius sp. were obtained. Eight species of helminth were considered common in the Japanese populations of the finless porpoise: Pharurus sunameri, Pharurus asiaeorientalis, Nasitrema spathulatum, Nasitrema sunameri, Halocercus pingi, Halocercus sunameri, Campula oblonga and Synthesium elongatum. No anisakid nematodes were found. N. spathulatum was found only in the western waters of the Seto Inland Sea. Low prevalence of C. oblonga in the Omura Bay was demonstrated. H. pingi was mostly found in very young porpoises before starting to eat prey, indicating prenatal or transmammary infection. However, a congeneric species, H. sunameri, mainly infected weaned porpoises, indicating that these two species possess different transmission pathways. This study provides information on the geographical distribution and prevalence of helminth parasites in finless porpoises off the Japanese coast.

Polybrominated diphenyl ethers (PBDEs) and their hydroxylated and methoxylated analogues in the blood of harbor, Dall's and finless porpoises from the Japanese coastal waters.

This study investigated the accumulation of polybrominated diphenyl ethers (PBDEs) and their hydroxylated and methoxylated analogues (OH-PBDEs and MeO-PBDEs) in the blood of harbor porpoises, Dall's porpoises, and finless porpoises stranded or bycaught in Japanese coastal waters and in the North Pacific Ocean. Moreover, we suggested the origins of these contaminants and the factors affecting their pattern of accumulation. Levels of PBDEs in Dall's porpoises were one order of magnitude greater than those in the other species. OH-PBDE and MeO-PBDE levels were comparable to those of PBDEs. However, no correlation was found between the levels of OH-PBDEs and PBDEs, whereas a strong correlation was found between that of OH-PBDEs and MeO-PBDEs (p < 0.001). 6OH-BDE47, reported compound biosynthesized by marine low-trophic level organisms, was the dominant congener. These results suggest that PBDEs found in these porpoise species derive from flame retardants, but OH-PBDEs and MeO-PBDEs are mainly of natural origins.