An examination of cetacean brain structure with a novel hypothesis correlating thermogenesis to the evolution of a big brain

This review examines aspects of cetacean brain structure related to behaviour and evolution. Major considerations include cetacean brain-body allometry, structure of the cerebral cortex, the hippocampal formation, specialisations of the cetacean brain related to vocalisations and sleep phenomenology, paleoneurology, and brain-body allometry during cetacean evolution. These data are assimilated to demonstrate that there is no neural basis for the often-asserted high intellectual abilities of cetaceans. Despite this, the cetaceans do have volumetrically large brains. A novel hypothesis regarding the evolution of large brain size in cetaceans is put forward. It is shown that a combination of an unusually high number of glial cells and unihemispheric sleep phenomenology make the cetacean brain an efficient thermogenetic organ, which is needed to counteract heat loss to the water. It is demonstrated that water temperature is the major selection pressure driving an altered scaling of brain and body size and an increased actual brain size in cetaceans. A point in the evolutionary history of cetaceans is identified as the moment in which water temperature became a significant selection pressure in cetacean brain evolution. This occurred at the Archaeoceti - modern cetacean faunal transition. The size, structure and scaling of the cetacean brain continues to be shaped by water temperature in extant cetaceans. The alterations in cetacean brain structure, function and scaling, combined with the imperative of producing offspring that can withstand the rate of heat loss experienced in water, within the genetic confines of eutherian mammal reproductive constraints, provides an explanation for the evolution of the large size of the cetacean brain. These observations provide an alternative to the widely held belief of a correlation between brain size and intelligence in cetaceans.     

鲸类远距离活体采样技术发展概述及其在中国鲸类研究中的应用前景

鲸类位于海洋生态系统食物链的顶端,在国际海洋环境保护研究中备受关注。鲸类的生活环境使得科研人员难以接近它们,为了在保证动物生命安全的前提下进行采样研究,科研人员发明了鲸类远距离活体采样技术。鲸类远距离活体采样工具出现于1973年,由捕鲸鱼叉改制而来,其后40余年,鲸类活体采样工具先后经历了捕鲸鱼叉、十字弓、复合弓、气枪、手持杆等多种不同动力的采样系统交替出现的发展历程。活体采样技术对动物的影响是科研人员关注的核心问题,为此,科研人员开展了大量研究对活体采样技术的风险性进行评价,并最终认可了这一技术的无损伤性。现今,鲸类远距离活体采样技术已成为国际鲸类研究的重要手段。我国是鲸类资源相对丰富的国家,但该技术在我国鲸类研究中的应用仍处于起步阶段,仅在香港海域的中华白海豚（Sousa chinensis）研究中进行过尝试,鲸 类远距离活体采样技术在我国有着广泛的应用前景和发展空间。本文详细介绍了鲸类远距离活体采样技术的发展历程和科研应用,并从遗传学、毒理学、细胞生物学和内分泌学方面对该技术在我国鲸类研究中的应用前景做了展望。     

鲸类分子系统学研究进展

综述了近年来分子生物学标记技术在鲸类系统学研究中的进展。分子生物学证据支持鲸目与有蹄类之间有较近的亲缘关系,并支持鲸类的单系起源,但鲸类不同类群(须鲸类、抹香鲸类及不包括抹香鲸类的齿鲸类)之间的系统发生关系仍存在争议。抹香鲸类到底与须鲸类还是与其它齿鲸类有更近的亲缘关系,不同的分子生物学家所得到的结果并不一致。此外,分子生物学技术还被用于解决须鲸亚目和齿鲸亚目内科间以及科内种间的系统发生关系,特别是齿鲸亚目的海豚科、鼠豚科和淡水豚类。通过分子标记技术来研究鲸类种下的遗传结构是鲸类分子系统学研究中的一个新热点,使用的标记主要是mtDNA控制区、核DNA微卫星和主要组织相容性复合体(major histo-compatibilitv complex,MHC)等。     

Morbillivirus infection in live stranded, injured, trapped, and captive cetaceans in southeastern Queensland and northern New South Wales, Australia

We report serologic evidence of cetacean morbillivirus (CMV) infection in five of eight cetacean species found live stranded, injured, or trapped along the coast of southeastern Queensland and northern New South Wales, Australia between December 2005 and January 2011. Antibody to CMV was detected in 13 of 27 (48%) wild cetaceans sampled. Antibody prevalence was significantly higher in clinically diseased (69%) compared to nondiseased (18%) animals (P=0.018). There was high antibody prevalence (83%, n=6) in melon-headed whales (Peponocephala electra). Two of 13 (15%) captive cetaceans sampled between November 2005 and January 2011 had CMV antibodies and, as infection was unlikely to have occurred while in captivity, CMV infection appears to have been present in Australian wild cetaceans since at least 1985. These results indicate that morbillivirus infection is occurring without widespread cetacean mortality in this region. However, as the deaths of two immature Australian offshore bottlenose dolphins (Tursiops truncatus) were attributed to CMV infection, morbillivirus infection should be included in the differential diagnosis of disease in cetaceans in Australia. Captive cetacean populations may be prone to significant mortality as a result of CMV introduction, so strict quarantine procedures should be enforced when injured or stranded cetaceans are hospitalized and rehabilitated at Australian zoos and marine parks.     

Characteristic metabolism of free amino acids in cetacean plasma: cluster analysis and comparison with mice

From an evolutionary perspective, the ancestors of cetaceans first lived in terrestrial environments prior to adapting to aquatic environments. Whereas anatomical and morphological adaptations to aquatic environments have been well studied, few studies have focused on physiological changes. We focused on plasma amino acid concentrations (aminograms) since they show distinct patterns under various physiological conditions. Plasma and urine aminograms were obtained from bottlenose dolphins, pacific white-sided dolphins, Risso's dolphins, false-killer whales and C57BL/6J and ICR mice. Hierarchical cluster analyses were employed to uncover a multitude of amino acid relationships among different species, which can help us understand the complex interrelations comprising metabolic adaptations. The cetacean aminograms formed a cluster that was markedly distinguishable from the mouse cluster, indicating that cetaceans and terrestrial mammals have quite different metabolic machinery for amino acids. Levels of carnosine and 3-methylhistidine, both of which are antioxidants, were substantially higher in cetaceans. Urea was markedly elevated in cetaceans, whereas the level of urea cycle-related amino acids was lower. Because diving mammals must cope with high rates of reactive oxygen species generation due to alterations in apnea/reoxygenation and ischemia-reperfusion processes, high concentrations of antioxidative amino acids are advantageous. Moreover, shifting the set point of urea cycle may be an adaptation used for body water conservation in the hyperosmotic sea water environment, because urea functions as a major blood osmolyte. Furthermore, since dolphins are kept in many aquariums for observation, the evaluation of these aminograms may provide useful diagnostic indices for the assessment of cetacean health in artificial environments in the future.     

委内瑞拉东南加勒比海岸七种海洋鲸类的潜在地理分布

本研究阐述了委内瑞拉沿海最常见的海洋鲸类的潜在地理分布情况。通过GIS分析,鲸类分布与地形和深度是相反的,以此可以获得鲸类潜在的分布图。已报告确认了16个物种(有402个目击报告),其中小布氏鲸(Balaenoptera edeni)、座头鲸(Megaptera novaeangliae)、海豚(Delphinus spp.)、圭亚那侏型豚(Sotalia guianensis)、花斑原海豚(Stenella frontalis)、长吻原海豚(Stenella longirostris)和宽吻海海豚(Tursiops truncatus)是最常见的。小布氏鲸和宽吻海海豚有可能分布于整个海岸,包括江河区域。座头鲸则可能季节性地集中分布在大陆架上的海岛沿岸和浅水区域。海豚(Delphinus spp.)有可能分布于高边坡区或沿海上升流区。花斑原海豚可能分布在东北区的西部,中部沿海以及与委内瑞拉海岸平行的岛屿周围。长吻原海豚则分布于浅海和远海区域。在一些高产的生态系统内新的物种可能正在形成,而这些潜在可能的分布图可以作为在高产生态系统内确立关键栖息地的标准,由此我们可以在委内瑞拉水域为鲸类建立新的保护区。     

A review of the human activities impacting cetaceans in the eastern tropical Atlantic

• 1. The eastern tropical Atlantic (ETA), extending from Mauritania south to Angola, is inhabited by at least 34 cetacean species. Knowledge of cetaceans and the human activities affecting them in the ETA is scant.
• 2. Available literature was reviewed over three eras of ETA cetacean research: the whaling era (1700s–1950s); the stranding and specimen era (1950s–70s); and the modern field research era (1980s–present). Eight human activities were documented to impact ETA cetacean species: directed takes (whaling and small cetaceans); by‐catch or entanglement in fishing gear; the ETA tuna purse seine fishery; overfishing; habitat loss and degradation; vessel strikes; marine ecotourism; and live captures for display. Climate change may represent a future threat.
• 3. Directed takes of small cetaceans were documented in 12 ETA countries, and incidental by‐catch (especially in gillnets) in at least nine countries. Additionally, unknown levels of cetacean mortality occur in ETA tuna purse seine fisheries. The use of cetaceans as ‘bushmeat’ was documented in 15 countries and involved at least 23 species. Little information could be found on cetacean mortality in Liberia, Benin, Cameroon, Equatorial Guinea, São Tomé and Príncipe or the Democratic Republic of the Congo.
• 4. Human activities were most frequently and widely reported to impact on common bottlenose dolphins Tursiops truncatus and Atlantic humpback dolphins Sousa teuszii, which are particularly vulnerable to anthropogenic interactions due to their nearshore occurrence.
• 5. The lack of information on the scale of impacts and on cetacean abundance and population structure in the ETA currently hinders assessments of the sustainability of mortality levels.

     

MODIFYING GILLNETS TO REDUCE ENTANGLEMENT OF CETACEANS

To reduce the number of cetaceans caught incidentally in gillnets, two forms of acoustic modifications have previously been proposed. These modifications seek to make gillnets more obvious to cetaceans so they can avoid them, and include making gillnets more reflective to cetacean sonar and placing active sound emitters in the nets. I discuss the relationship between sonar and net entanglement, and address the assumptions and logic of net modification strategies. I argue that neither strategy is likely to be effective, and that reductions in the number of cetaceans killed in gillnets are best achieved through the closure of specific areas to gillnetting.     

Comparative analysis of the prion protein (PrP) gene in cetacean species

The partial PrP gene sequence and the deduced protein of eight cetacean species, seven of which have never been reported so far, have been determined in order to extend knowledge of sequence variability of the PrP genes in different species and to aid in speculation on cetacean susceptibility to prions. Both the nucleotide and the deduced amino acid sequences have been analysed in comparison with some of the known mammalian PrPs. Cetacean PrPs present typical features of eutherian PrPs. The PrP gene from the species of the family Delphinidae gave identical nucleic acid sequences, while differences in the PrP gene were found in Balaenopteridae and Ziphidae. The phylogenetic tree resulting from analysis of the cetacean PrP gene sequences, together with reported sequences of some ungulates, carnivores and primates, showed that the PrP gene phylogenesis mirrors the species phylogenesis. The PrP gene of cetaceans is very close to species where natural forms of TSEs are known. From an analysis of the sequences and the phylogenesis of the PrP gene, susceptibility to or occurrence of prion diseases in cetaceans can not be excluded.     

Towards a new paradigm of non-captive research on cetacean cognition

Contemporary knowledge of impressive neurophysiology and behavior in cetaceans, combined with increasing opportunities for studying free-ranging cetaceans who initiate sociable interaction with humans, are converging to highlight serious ethical considerations and emerging opportunities for a new era of progressive and less-invasive cetacean research. Most research on cetacean cognition has taken place in controlled captive settings, e.g., research labs, marine parks. While these environments afford a certain amount of experimental rigor and logistical control they are fraught with limitations in external validity, impose tremendous stress on the part of the captive animals, and place burdens on populations from which they are often captured. Alternatively, over the past three decades, some researchers have sought to focus their attention on the presence of free-ranging cetacean individuals and groups who have initiated, or chosen to participate in, sociable interactions with humans in the wild. This new approach, defined as Interspecies Collaborative Research between cetacean and human, involves developing novel ways to address research questions under natural conditions and respecting the individual cetacean's autonomy. It also offers a range of potential direct benefits to the cetaceans studied, as well as allowing for unprecedented cognitive and psychological research on sociable mysticetes. Yet stringent precautions are warranted so as to not increase their vulnerability to human activities or pathogens. When conducted in its best and most responsible form, collaborative research with free-ranging cetaceans can deliver methodological innovation and invaluable new insights while not necessitating the ethical and scientific compromises that characterize research in captivity. Further, it is representative of a new epoch in science in which research is designed so that the participating cetaceans are the direct recipients of the benefits.     

Trajectories and Constraints in Brain Evolution in Primates and Cetaceans

A negative allometric relationship between body mass (BM) and brain size (BS) can be observed for many vertebrate groups. In the past decades, researchers have proposed several hypotheses to explain this finding, but none is definitive and some are possibly not mutually exclusive. Certain species diverge markedly (positively or negatively) from the mean of the ratio BM/BS expected for a particular taxonomic group. It is possible to define encephalization quotient (EQ) as the ratio between the actual BS and the expected brain size. Several cetacean species show higher EQs compared to all primates, except modern humans. The process that led to big brains in primates and cetaceans produced different trajectories, as shown by the organizational differences observed in every encephalic district (e.g., the cortex). However, these two groups both convergently developed complex cognitive abilities. The comparative study on the trajectories through which the encephalization process has independently evolved in primates and cetaceans allows a critical appraisal of the causes, the time and the mode of quantitative and qualitative development of the brain in our species and in the hominid evolutionary lineage.     

BUFFERING CAPACITY OF THE LOCOMOTOR MUSCLE IN CETACEANS: CORRELATES WITH POSTPARTUM DEVELOPMENT, DIVE DURATION, AND SWIM PERFORMANCE

Skeletal muscles of marine mammals must support the metabolic demands of exercise during periods of reduced blood flow associated with the dive response. Enhanced muscle buffering could support anaerobic metabolic processes during apnea, yet this has not been fully investigated in cetaceans. To assess the importance of this adaptation in the diving and swimming performance of cetaceans, muscle buffering capacity due to non-bicarbonate buffers was measured in the longissimus dorsi of ten species of odontocete and one mysticete. Immature specimens from a subset of these species were studied to assess developmental trends. Fetal and neonatal cetaceans have low buffering capacities (range: 34.8–53.9 slykes) that are within the range measured for terrestrial mammals. A lengthy developmental period, independent of muscle myoglobin postnatal development, is required before adult levels are attained. Adult cetacean buffering capacities (range: 63.7–94.5 slykes) are among the highest values recorded for mammals. Cetacean species that demonstrate extremely long dive durations or high burst speed swimming tend to have greater buffering capacities. However, the wide range of body size across cetaceans may complicate these trends. Enhanced muscle buffering capacity may enable small-bodied species to extend breath-hold beyond short aerobic dive limits for foraging or predator evasion when necessary.     

Attitudes of Scottish City Inhabitants to Cetacean Conservation

In 2003, a survey was conducted in two major Scottish cities in order to investigate current perceptions of the public towards cetaceans and their conservation. Public concern about cetacean conservation was high. Overall the issues considered to be the greatest threats to cetacean populations were related to pollution: oil spills, and chemical and sewage pollution (serious threat: 68, 65, and 63%, respectively). Concern was also high regarding the depletion of cetacean prey from over-fishing, entanglement in fishing gear, marine litter and global warming, (serious threat: 54, 51, 44, and 43%, respectively). Conservation issues that are of specific concern to Scottish waters were also noted: military activities, fish farming and oil exploration. Least concern was expressed about whale-watching (not a threat: 48%). Women and older respondents expressed significantly higher levels of concern about cetacean conservation. Generally, the opinions of the public were similar to those of a test group of marine conservation professionals and advocates, although the public tended to show slightly greater levels of concern for most issues. However, the public expressed significantly higher levels of concern over oil spills, sewage pollution and chemical pollution than did marine conservation professionals/advocates. Most participants (60%) were unsure as to whether there was currently sufficient legal protection for cetaceans in Scotland, but eight out of ten respondents thought that there should be legislation specifically for cetacean conservation. Moreover, 40% stated that the proposal of a law specifically for the protection of cetaceans would make them view a political party or politician more favourably. Eighty percent of those interviewed were in favour of seeing more marine environmental education, including information on cetaceans and their environment, in the Scottish school curriculum.     

MORPHOLOGY OF THE EYE AND SURROUNDING STRUCTURES OF THE BOWHEAD WHALE, BALAENA MYSTICETUS

Observations were made on eyes from 46 bowhead whales, Balaena mysticetus , taken in the subsistence harvest near Barrow, Point Hope, Savoonga, and Kaktovik, Alaska. Data reported here include palpebral, eyeball, corneal, scleral, pupillary, and lens dimensions. These quantitative data have allowed us to compare structures relative to one another and sometimes to compare them with similar structures in other species. We found, for example, that the cornea is almost three times as thick at its periphery as at its center; that when the ratio of scleral thickness and eyeball size are compared, the ratio, in the bowhead whale, is twice that of any other cetacean for which data were available; and that the corneal and pupillary width to height ratios indicate a less elongated cornea and pupil than has been reported in other cetaceans. We also found a strong correlation between body length and eyeball size indicating that within the species, unlike what is seen between species, larger animals have larger eyes. Novel observations include the presence of three periorbital fatty layers, 112 ciliary processes, the presence of scleral canals, the absence of an obvious fovea or macular region in the retina, a holangiotic pattern of fundic vessels, the presence of zonular fibers and a lens sheath, and the absence of an obvious pupillary operculum. Anatomical features like the wide angle of divergence and the palpebral dimensions suggest the absence of binocular vision while features like the size of the palpebral sac, abundant conjuctival fat, and the prominence of the retractor bulbi muscle suggest mechanisms for the protrusion and retraction of the eyeball.     

鲸类二次水生生境适应Epac1和Epac2基因的分子进化

心率即心脏跳动的速度,不仅反映了心脏的功能,还与寿命的长短及能量代谢有关。与大多数陆生哺乳动物相比,鲸类心率显著降低。降低的心率有助于鲸类寿命的延长及能量的高效利用,便于其适应极端的海洋环境,而这一适应的分子机制尚不清楚。鉴于此,本研究采用基于最大似然法的枝模型、枝位点模型结合蛋白质功能差异分析等方法,对控制心率的环状腺苷酸结合蛋白（Epac1 和Epac2）基因进行适应性探究。分析结果表明,Epac1在长寿鲸类即须鲸类和抹香鲸（Physeter macrocephalus）组合进化支中检测到加速进化过程,且枝位点模型在须鲸类祖先支中检测到的强烈的正选择位点均位于功能重要的催化区;另外,该蛋白质在鲸类中还发生了显著的功能修饰（θ=0.5296 ± 0.1300;P<0.001）。对Epac2进行相同的分析发现,该基因在寿命长达200年之久的弓头鲸（Balaena mysticetus）中检测到的正选择位点同样位于功能重要的催化区。上述结果提示Epac1和Epac2在鲸类中均产生了适应性进化,这一方面可能有助于鲸类心率降低,另一方面也可能与其较长的寿命及高效的能量利用有关。     

Results of a short study of interactions of cetaceans and longline fisheries in Atlantic waters: environmental correlates of catches and depredation events

In the Atlantic, economic losses have been reported from shark, swordfish and tuna longline fisheries due to depredation by cetaceans. We examined interactions of odontocete cetaceans with commercial longliners operating in waters off Brazil and the Azores archipelago during 2006–2007, analysing relationships between catches, depredation on hooked fish, cetacean sightings, acoustic records of cetacean presence and environmental variables. Data were provided by skippers of six vessels and by on-board observers for two vessels. The percentage of longline sets depredated by cetaceans was low (ranging from 1% to 9% of total sets per ship) but the proportion of fish damaged was high (up to 100%) when depredation occurred. Catches were related to the phase of the moon, cloud cover, sea surface temperature and water depth whereas cetacean sightings were primarily related to catches. In particular there was a positive association between Delphinus delphis sightings and catches of swordfish, and between Stenella frontalis sightings and mako catches. Acoustic detection was low when depredation by false killer whales occurred although high rates of clicks were detected when delphinids were sighted and false killer whales were by-caught. This may indicate that false killer whales are not echolocating when feeding on fish hooked on a longline. Guest editor: V. D. Valavanis Essential Fish Habitat Mapping in the Mediterranean     

Diversity versus disparity and the radiation of modern cetaceans

Modern whales are frequently described as an adaptive radiation spurred by either the evolution of various key innovations (such as baleen or echolocation) or ecological opportunity following the demise of archaic whales. Recent analyses of diversification rate shifts on molecular phylogenies raise doubts about this interpretation since they find no evidence of increased speciation rates during the early evolution of modern taxa. However, one of the central predictions of ecological adaptive radiation is rapid phenotypic diversification, and the tempo of phenotypic evolution has yet to be quantified in cetaceans. Using a time-calibrated molecular phylogeny of extant cetaceans and a morphological dataset on size, we find evidence that cetacean lineages partitioned size niches early in the evolutionary history of neocetes and that changes in cetacean size are consistent with shifts in dietary strategy. We conclude that the signature of adaptive radiations may be retained within morphological traits even after equilibrium diversity has been reached and high extinction or fluctuations in net diversification have erased any signature of an early burst of diversification in the structure of the phylogeny.     

Sequence variation in the Tbx4 gene in marine mammals

The amino-acid sequences of the T-domain region of the Tbx4 gene, which is required for hindlimb development, are 100% identical in humans and mice. Cetaceans have lost most of their hindlimb structure, although hindlimb buds are present in very early cetacean embryos. To examine whether the Tbx4 gene has the same function in cetaceans as in other mammals, we analyzed Tbx4 sequences from cetaceans, dugong, artiodactyls and marine carnivores. A total of 39 primers were designed using human and dog Tbx4 nucleotide sequences. Exons 3, 4, 5, 6, 7, and 8 of the Tbx4 genes from cetaceans, artiodactyls, and marine carnivores were sequenced. Non-synonymous substitution sites were detected in the T-domain regions from some cetacean species, but were not detected in those from artiodactyls, the dugong, or the carnivores. The C-terminal regions contained a number of non-synonymous substitutions. Although some indels were present, they were in groups of three nucleotides and therefore did not cause frame shifts. The dN/dS values for the T-domain and C-terminal regions of the cetacean and artiodactylous Tbx4 genes were much lower than 1, indicating that the Tbx4 gene maintains it function in cetaceans, although full expression leading to hindlimb development is suppressed.     

Cytochrome b nucleotide sequences and the identification of five primary lineages of extant cetaceans

Relationships among and within baleen and toothed whales were examined using the complete sequence of the mitochondrial cytochrome b gene. Based on parsimony analyses of conservative nucleotide substitutions, five primary evolutionary lineages of extant cetaceans were identified, one represented by baleen whales (Mysticeti) and four represented by odontocetes (toothed whales). Based on the most comprehensive representation of taxa, both cetaceans and artiodactyls, the most parsimonious relationship among the five lineages is (Mysticeti, Odontoceti (Platanistoidea (Physeteroidea (Ziphioidea (Delphinida))))). This relationship, however, is labile and sensitive to ingroup representation and the choice of outgroup. The short nodes among the five cetacean lineages suggest that the divergence among these lineages occurred over a narrow time period, a finding consistent with the limited fossil evidence that indicates a major cetacean radiation 30-34 Mya. The level of divergence among the five cetacean lineages, and that seen between cetaceans and artiodactyls, suggests that cetaceans and artiodactyls had a common ancestor approximately 60 Mya.