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Olfaction and brain size in the bowhead (Balaena mysticetus)

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Abstract

Although there are several isolated references to the olfactory anatomy of mysticetes, it is usually thought that olfaction is rudimentary in this group. We investigated the olfactory anatomy of bowhead whales and found that these whales have a cribriform plate and small, but histologically complex olfactory bulb. The olfactory bulb makes up approximately 0.13% of brain weight, unlike odontocetes where this structure is absent. We also determined that 51% of olfactory receptor genes were intact, unlike odontocetes, where this number is less than 25%. This suggests that bowheads have a sense of smell, and we speculate that they may use this to find aggregations of krill on which they feed.

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... On the one hand, several authors posit that some cetacean species have lost their nasal (Kishida et al., 2007) and oral chemoreception (Jiang et al., 2013) in the course of evolution, as airborne odorants may be considered irrelevant due to their aquatic lifestyle (Thewissen et al., 2011). Firstly, corresponding anatomical structures are rudimentary or absent, at least in adult animals. ...
... The authors of these behavioral studies noticed that dolphins were able to perceive orally what other mammals perceive by smell wherefore they called this perception "quasiolfaction" (Kuznetzov, 1990) or "water-borne sense of smell" (Nachtigall, 1986). Taken together, this second set of studies suggests that cetaceans might have, to some extent, access to chemosensory information through the olfactory (Thewissen et al., 2011) and/or taste systems (Watkins and Wartzok, 1985;Pihlström, 2008). As anatomical, neuroanatomical, and molecular evidence draw unclear conclusions, behavioral studies are needed. ...
... One can therefore wonder whether olfactory cues may contribute to fast localization. Similarly, it has been suggested that some Mysticeti may detect prey by using odors in air although they are produced underwater (Thewissen et al., 2011). ...
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Chemosensory perception in cetaceans remains an intriguing issue as morphological, neuroanatomical and genetic studies draw unclear conclusions, while behavioral data suggest that dolphins may use it for food selection or socio-sexual interactions. Experimental approaches have been scarce due to the practical difficulties of testing chemoreception in wild dolphins. Go/no-go tasks are one elegant way to investigate discrimination abilities; however, they require to train the animals, thus preventing spontaneous responses and hence the expression of preferences. Here, we aimed at testing potential spontaneous responses to chemical stimuli and developed novel procedures. First, we conducted a study to test whether captive dolphins respond to a biologically relevant smell. Therefore, we placed dead fish within an opaque barrel at the border of the pool and counted the number of respirations at proximity as an indicator of investigation. The same dead fishes were presented several times during experiments lasting three consecutive days. From the second day on (i.e. when the odor composition changed), dolphins breathed more often close to the fish-smelling barrel than close to the visually identical but empty control barrel. Second, we conducted a study to test whether dolphins are able to discriminate food flavors. Captive dolphins are commonly provided with ice cubes as a source of enrichment. We took this opportunity to provide ice cubes with different flavors and to compare the reaction to these different flavors as a measure of discrimination. Hence, we used the latency of return to the ice cube begging spot as a measure of discrimination from the previous ice cube flavor. Thus, our method used a non-invasive and easily replicable technique based on the spontaneous begging responses of dolphins toward more or less attractive items bearing biological relevance. The procedures used enabled us to show that dolphins may discriminate odors and flavors respectively.
... In 2 bottlenose dolphins, the adnexa volume was calculated by subtracting the in situ brain volume from the volume of the cranium in magnetic resonance images. Other values for endocranial adnexa were taken from the literature [Kojima, 1951;Jacobs and Jensen, 1964;Thewissen et al., 2011;Ridgway and Hanson, 2014]. ...
... Montgomery et al. [2013] suggested that the differences in cetacean EQ are driven mainly by differences in body mass, not dramatic change in brain mass. [Turner, 1912]; Ba, B. acutorostrata [Knudsen et al., 2002], mean data from 35 specimens; Oo, O. orca [Ridgway and Hanson, 2014]; Bp, B. physalus, Mn, M. novaeangliae [Jacobs and Jensen, 1964]; Pm, P. macrocephalus [Kojima, 1951]; Bmu, B. musculus [Guldberg, 1885]; Bmy, B.mysticetus [Thewissen et al., 2011]. The small Platanista gangetica brain on the left has a different pattern of gyri and sulci and appears to be less convoluted than the others. ...
... The proportion of brain in the endocranial volume varies between cetaceans. For example, the B. mysticetus brain only occupies between 35 and 41% of the volume of the cranial vault [Thewissen et al., 2011]. In fin and humpback whales the brain is closer to 60% of endocranial volume, and it is about 70% in sperm whales [Jacobs and Jensen, 1964]. ...
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We compared mature dolphins with 4 other groupings of mature cetaceans. With a large data set, we found great brain diversity among 5 different taxonomic groupings. The dolphins in our data set ranged in body mass from about 40 to 6,750 kg and in brain mass from 0.4 to 9.3 kg. Dolphin body length ranged from 1.3 to 7.6 m. In our combined data set from the 4 other groups of cetaceans, body mass ranged from about 20 to 120,000 kg and brain mass from about 0.2 to 9.2 kg, while body length varied from 1.21 to 26.8 m. Not all cetaceans have large brains relative to their body size. A few dolphins near human body size have human-sized brains. On the other hand, the absolute brain mass of some other cetaceans is only one-sixth as large. We found that brain volume relative to body mass decreases from Delphinidae to a group of Phocoenidae and Monodontidae, to a group of other odontocetes, to Balaenopteroidea, and finally to Balaenidae. We also found the same general trend when we compared brain volume relative to body length, except that the Delphinidae and Phocoenidae-Monodontidae groups do not differ significantly. The Balaenidae have the smallest relative brain mass and the lowest cerebral cortex surface area. Brain parts also vary. Relative to body mass and to body length, dolphins also have the largest cerebellums. Cortex surface area is isometric with brain size when we exclude the Balaenidae. Our data show that the brains of Balaenidae are less convoluted than those of the other cetaceans measured. Large vascular networks inside the cranial vault may help to maintain brain temperature, and these nonbrain tissues increase in volume with body mass and with body length ranging from 8 to 65% of the endocranial volume. Because endocranial vascular networks and other adnexa, such as the tentorium cerebelli, vary so much in different species, brain size measures from endocasts of some extinct cetaceans may be overestimates. Our regression of body length on endocranial adnexa might be used for better estimates of brain volume from endocasts or from endocranial volume of living species or extinct cetaceans.
... The volumetric discrepancy between brain and endocranial volume [2,9,37,38] is quantitatively more important than the relatively minor adjustment for brain tissue density. Bowhead whales provide an extreme example as the bowhead brain only occupies approximately 40 percent of the cranial cavity [39] while the remaining 60 percent is filled with adnexa and cerebrospinal fluid. Adnexa in this context refers collectively to the non-brain tissues present within the cranial cavity; specifically, the meninges (which includes the dura mater, arachnoid, and pia mater) (Fig 1B), cranial nerves, dural sinuses, and a collection of arteries and veins which includes the rete mirabile. ...
... The rete is a specific structure consisting of a meshwork of blood vessels, which is present in most terrestrial artiodactyls [40][41][42][43][44] and cetaceans [2,45,46]. Although a rete is present in all cetaceans, it appears to be disproportionately expanded in extant mysticetes [39,45]. Although discrepancies between brain and endocranial volume in cetaceans have been observed, they have been generally disregarded, except within the Basilosauridae, an extinct family of cetaceans which are thought to have possessed a significant endocranial rete mirabile [27,30,[47][48][49][50]. ...
... A beluga head (NSB-DWM 2019LDL10) was provided by Iñupiat subsistence hunters in Point Lay, Alaska, in cooperation with the North Slope Borough, Department of Wildlife Management (NSB-DWM). Additional information on a bowhead whale (NSB-DWM 2008B11) expands on data published in Thewissen et al. [39] and Ridgway et al. [2], specifically providing data on adnexa mass. Pig and goat heads were received in fresh states from domestic animals culled for reasons unrelated to this research. ...
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Most authors have identified two rapid increases in relative brain size (encephalization quotient, EQ) in cetacean evolution: first at the origin of the modern suborders (odontocetes and mysticetes) around the Eocene-Oligocene transition, and a second at the origin of the delphinoid odontocetes during the middle Miocene. We explore how methods used to estimate brain and body mass alter this perceived timing and rate of cetacean EQ evolution. We provide new data on modern mammals (mysticetes, odontocetes, and terrestrial artiodactyls) and show that brain mass and endocranial volume scale allometrically, and that endocranial volume is not a direct proxy for brain mass. We demonstrate that inconsistencies in the methods used to estimate body size across the Eocene-Oligocene boundary have caused a spurious pattern in earlier relative brain size studies. Instead, we employ a single method, using occipital condyle width as a skeletal proxy for body mass using a new dataset of extant cetaceans, to clarify this pattern. We suggest that cetacean relative brain size is most accurately portrayed using EQs based on the scaling coefficients as observed in the closely related terrestrial artiodactyls. Finally, we include additional data for an Eocene whale, raising the sample size of Eocene archaeocetes to seven. Our analysis of fossil cetacean EQ is different from previous works which had shown that a sudden increase in EQ coincided with the origin of odontocetes at the Eocene-Oligocene boundary. Instead, our data show that brain size increased at the origin of basilosaurids, 5 million years before the Eocene-Oligocene transition, and we do not observe a significant increase in relative brain size at the origin of odontocetes.
... In 2 bottlenose dolphins, the adnexa volume was calculated by subtracting the in situ brain volume from the volume of the cranium in magnetic resonance images. Other values for endocranial adnexa were taken from the literature[Kojima, 1951;Jacobs and Jensen, 1964;Thewissen et al., 2011;Ridgway and Hanson, 2014]. We estimated the surface area of the cerebral cortex in formalin-fixed brains using stereological methods [Elias and Schwartz, 1969;Ridgway and Brownson, 1984]. ...
... Montgomery et al.[2013]suggested that the differences in cetacean EQ are driven mainly by differences in body mass, not dramatic change in brain mass.The table is organized by increasing adnexa mass from left to right. Tt, T. truncatus (current study); Ha, H. ampullatus[Turner, 1912]; Ba, B. acutorostrata[Knudsen et al., 2002], mean data from 35 specimens; Oo, O. orca[Ridgway and Hanson, 2014]; Bp, B. physalus, Mn, M. novaeangliae[Jacobs and Jensen, 1964]; Pm, P. macrocephalus[Kojima, 1951]; Bmu, B. musculus[Guldberg, 1885]; Bmy, B.mysticetus[Thewissen et al., 2011].In evolutionary history, the animals with the largest brains relative to body mass, the Delphinidae, have experienced a large decrease in body mass[Montgomery et al., 2013]. Studies such as Marino et al.[2004]and Montgomery et al.[2013]relied heavily on EQ derived from endocranial volume[also see Gingerich, 2015]. ...
... The proportion of brain in the endocranial volume varies between cetaceans. For example, the B. mysticetus brain only occupies between 35 and 41% of the volume of the cranial vault[Thewissen et al., 2011]. In fin and humpback whales the brain is closer to 60% of endocranial volume, and it is about 70% in sperm whales [Jacobs and Jensen, 1964]. ...
... In cetaceans, however, the use of chemical cues such as DMS remains unclear and has seldom been studied. Baleen whales (mysticetes) possess the anatomical structures involved in olfaction, that is, a complete main olfactory system (olfactory epithelium, nerve and bulb, Breathnach, 1960;Oelschläger, 1992;Thewissen, George, Rosa, & Kishida, 2011;Hirose, Kishida, & Nakamura, 2018). However, they lack the dorsal domain of the olfactory bulb, an area known to induce innate avoidance behavior against odors of predators and spoiled foods (Kishida, Thewissen, Hayakawa, Imai, & Agata, 2015). ...
... However, the proportion of OR pseudogenes varies greatly among different species, with some having about 65% of their OR genes still functional (Liu et al., 2019). Several authors have thus suggested they could use chemicals such as DMS as long-distance cues while foraging or navigating in the pelagic environment (Drake et al., 2015;Hagelin, Straley, Nielson, & Szabo, 2012;Thewissen et al., 2011;Torres, 2017). In a recent behavioral response experiment, humpback whales (Megaptera novaeangliae) were exposed to a prey extract (krill hydrolysate) and to DMS hundreds of meters away (Bouchard et al., 2019). ...
... Odontocetes lack the canonical olfactory structures that allow the perception of airborne chemicals in terrestrial mammals such as the olfactory mucosa, nerve and bulb (Breathnach, 1960;Oelschläger & Buhl, 2008). They also lost most of the vertebrate genes involved in olfaction (Kishida et al., 2007;McGowen et al., 2008;Thewissen et al., 2011). These results support the hypothesis that the conventional sense of smell is inexistent or strongly reduced in odontocetes and would explain the absence of significant behavioral response toward DMS at medium range (hundreds of meters) in the present experiment. ...
Article
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For most marine vertebrates, chemical cues provide crucial information during navigation and foraging, but their use by cetaceans is still poorly understood. In contrast to baleen whales, toothed whales (odontocetes) are scarcely equipped for chemoreception: they lack the conventional anatomical structures (i.e., olfactory epithelium, nerves and bulbs) involved in olfaction and have reduced taste buds on the tongue. Several behavioral studies have however shown that captive dolphins can perceive chemical solutions, including odorants, in their oral cavity. To investigate whether odontocetes could use infochemicals in their foraging ecology, we implemented a behavioral response experiment in wild bottlenose dolphins and long‐finned pilot whales. We tested dimethyl sulfide (DMS) as a potentially attractive stimulus since it is a chemical signature of highly productive marine areas, known to attract several marine predators including fishes and seabirds. We assessed cetacean responses to DMS exposure by analyzing their movements and surface behaviors recorded by onboard observers. In both species, results did not reveal any significant attraction or behavioral reaction toward DMS when compared to a control chemical stimulus, apart from a short‐distance response in bottlenose dolphins. These results suggest that while odontocetes may perceive DMS in water, it apparently does not play a significant role in their foraging ecology. Testing potentially more attractive compounds such as prey extracts with the present method and analyzing surface, underwater and acoustic responses would provide further insights on odontocete feeding behavior. It would also provide valuable clues to studies on the anatomical structures involved in their chemosenses.
... In 2 bottlenose dolphins, the adnexa volume was calculated by sub- tracting the in situ brain volume from the volume of the cranium in magnetic resonance images. Other values for endocranial ad- nexa were taken from the literature [Kojima, 1951;Jacobs and Jensen, 1964;Thewissen et al., 2011;Ridgway and Hanson, 2014]. ...
... The table is organized by increasing adnexa mass from left to right. Tt, T. truncatus (current study); Ha, H. ampullatus [Turner, 1912]; Ba, B. acutorostrata [Knudsen et al., 2002], mean data from 35 specimens; Oo, O. orca [Ridgway and Hanson, 2014]; Bp, B. physalus, Mn, M. novaeangliae [Jacobs and Jensen, 1964]; Pm, P. macrocephalus [Kojima, 1951]; Bmu, B. musculus [Guldberg, 1885]; Bmy, B.mysticetus [Thewissen et al., 2011]. In evolutionary history, the animals with the largest brains relative to body mass, the Delphinidae, have expe- rienced a large decrease in body mass [Montgomery et al., 2013]. ...
... The proportion of brain in the endocranial volume varies between ceta- ceans. For example, the B. mysticetus brain only occupies between 35 and 41% of the volume of the cranial vault [Thewissen et al., 2011]. In fin and humpback whales the brain is closer to 60% of endocranial volume, and it is about 70% in sperm whales [Jacobs and Jensen, 1964]. ...
... In contrast, mysticetes possess a relatively larger number of intact OR genes than odontocetes (Kishida et al. 2015a(Kishida et al. , 2015b (Fig. 2), and all mysticete species examined to date (the bowhead whale and the minke whale) possess a highly reduced but fully equipped olfactory nervous systems (Hirose et al. 2018;Thewissen et al. 2011) (Fig. 3). All these pieces of evidence suggest that mysticetes have a sense of smell, and anatomical structures of their MOE suggest that they can smell in the air but not underwater (Kishida et al. 2015a;Thewissen et al. 2011) (Fig. 3). ...
... In contrast, mysticetes possess a relatively larger number of intact OR genes than odontocetes (Kishida et al. 2015a(Kishida et al. , 2015b (Fig. 2), and all mysticete species examined to date (the bowhead whale and the minke whale) possess a highly reduced but fully equipped olfactory nervous systems (Hirose et al. 2018;Thewissen et al. 2011) (Fig. 3). All these pieces of evidence suggest that mysticetes have a sense of smell, and anatomical structures of their MOE suggest that they can smell in the air but not underwater (Kishida et al. 2015a;Thewissen et al. 2011) (Fig. 3). These observations raise two questions. ...
... Scale bar, 1 mm. Pictures modified after Thewissen et al. (2011) and Kishida et al. (2015b) The olfactory marker protein (OMP), a small cytoplasmic protein expressed only in mature olfactory chemosensory neurons, plays an important role in the olfactory signal transduction cascade across vertebrates (Danciger et al. 1989;Margolis 1980;Reisert et al. 2007). OMP-knockout mice show considerably reduced ability to respond to odor stimuli, but the loss of this gene is not lethal (Buiakova et al. 1996;Youngentob and Margolis 1999;Youngentob et al. 2001) and some species of anosmic odontocetes do not have the intact OMP gene (Springer and Gatesy 2017). ...
Article
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Amniotes originated on land, but aquatic/amphibious groups emerged multiple times independently in amniotes. On becoming aquatic, species with different phylogenetic backgrounds and body plans have to adapt themselves to handle similar problems inflicted by their new environment, and this makes aquatic adaptation of amniotes one of the greatest natural experiments. Particularly, evolution of the sense of smell upon aquatic adaptation is of great interest because receptors required for underwater olfaction differ remarkably from those for terrestrial olfaction. Here, I review the olfactory capabilities of aquatic/amphibious amniotes, especially those of cetaceans and sea snakes. Most aquatic/amphibious amniotes show reduced olfactory organs, receptor gene repertoires, and olfactory capabilities. Remarkably, cetaceans and sea snakes show extreme examples: cetaceans have lost the vomeronasal system, and furthermore, toothed whales have lost all of their olfactory nervous systems. Baleen whales can smell in the air, but their olfactory capability is limited. Fully aquatic sea snakes have lost the main olfactory system but they retain the vomeronasal system for sensing underwater. Amphibious species show an intermediate status between terrestrial and aquatic species, implying their importance on understanding the process of aquatic adaptation. The olfactory capabilities of aquatic amniotes are diverse, reflecting their diverse phylogenetic backgrounds and ecology.
... The structure and function of the mysticete brain are less well known, and our limited knowledge is based mostly on a handful of studies in balaenopterids (Butti et al., 2015;Dell et al., 2016;Hof and Van der Gucht, 2007;Kraus and Pilleri, 1969;Pilleri, 1966a,b;Ratner et al., 2010). Several studies focused on the bowhead whale brain (Breathnach, 1955;Duffield et al., 1992;Pilleri, 1964;Raghanti et al., 2018;Thewissen et al., 2011), and those results will be summarized here in the context of cetacean neuroanatomy. ...
... The bowhead EQ for mature length animals is similar to that of the blue whale around 0.2 (see data in Ridgway et al., 2016). Notably, the bowhead whale brain occupies only 35%À41% of the braincase, with the remainder of space being occupied by the dural rete mirabile (Thewissen et al., 2011). The amount of nonbrain tissue in the cranial vault of cetaceans is variable and one must wonder about the function of such extensive vascular networks. ...
... Most cetaceans have dramatically reduced olfaction, with altered olfactory bulb anatomy and a reduced number of olfactory receptor genes in the majority of mysticetes to virtually no olfaction in odontocetes (Dehnhardt, 2002;Kishida et al., 2015;Oelschläger and Oelschläger, 2008;Pihlströ m, 2008). The bowhead whale, in contrast, possesses an olfactory bulb that makes up approximately 0.13% of brain mass, a nonoccluded cribriform plate, and retains a higher number of functioning olfactory receptors (Thewissen et al., 2011;Chapter 18). In short, it appears that the bowhead has a more developed sense of smell relative to humans, who have a higher percentage of olfactory receptor pseudogenes than the bowhead and whose olfactory bulb makes up a smaller proportion of overall brain size (Thewissen et al., 2011). ...
Chapter
Bowhead whales are one of the least encephalized mammals, possessing a small brain relative to their body size (e.g., a 3 kg brain in a 30,000 kg body). Features of the bowhead whale brain include a blunted temporal lobe and a gyrification index that is less than most cetaceans. Rather than having a cerebrum that is wider than long like odontocetes, the bowhead cerebrum is longer than it is wide. The hippocampus is very small and located within the lateral ventricle, which is ventral to the corpus callosum. The cytoarchitecture of the bowhead cerebral cortex is consistent with that of other cetaceans. The cortex is thin overall with a relatively thick, prominent layer I. As with other cetaceans, there is no granular layer IV. Notably, high numbers of von Economo neurons and fork neurons are found in all regions of the cortex. The highest numbers of these special neurons are observed at the apex of gyri.
... Although there is some discrepancy in the historical literature regarding the presence of olfactory bulbs among species, it is highly likely that these structures are present in all mysticetes, but are often lost during dissection [10]. Indeed, recent work on the bowhead whale (Balaena mysticetus) has confirmed the presence of large, well-developed olfactory bulbs in this species [13]. Genetic studies have also revealed that mysticetes have a high proportion of functional genes coding for olfactory receptors (OR), which are transmembrane proteins responsible for odorant binding expressed at the surface of olfactory neurons [13][14][15]. ...
... Indeed, recent work on the bowhead whale (Balaena mysticetus) has confirmed the presence of large, well-developed olfactory bulbs in this species [13]. Genetic studies have also revealed that mysticetes have a high proportion of functional genes coding for olfactory receptors (OR), which are transmembrane proteins responsible for odorant binding expressed at the surface of olfactory neurons [13][14][15]. Mysticetes are thus thought to have a functional sense of smell, but this hypothesis has yet to be tested experimentally. A preliminary study [16] conducted on humpback whales (Megaptera novaeangliae), a species that feeds on krill as well as several schooling fish species depending on prey availability [17,18], showed that feeding humpback whales oriented into the wind significantly more often than in other directions. ...
... While it has been speculated that baleen whales use DMS as an indicator of prey aggregation [13,16], we did not observe any differences in the whales' exploration of the stimulus area, or their surface behaviour, between the DMS and control trials. One possible cause could be the concentration of DMS used in this experiment, which was much higher than what is found in the marine environment, making the stimulus too strong to be recognized as a natural foraging cue by the whales. ...
Article
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Baleen whales face the challenge of finding patchily distributed food in the open ocean. Their relatively well-developed olfactory structures suggest that they could identify the specific odours given off by planktonic prey such as krill aggregations. Like other marine predators, they may also detect dimethyl sulfide (DMS), a chemical released in areas of high marine productivity. However, dedicated behavioural studies still have to be conducted in baleen whales in order to confirm the involvement of chemoreception in their feeding ecology. We implemented 56 behavioural response experiments in humpback whales using two food-related chemical stimuli, krill extract and DMS, as well as their respective controls (orange clay and vegetable oil) in their breeding (Madagascar) and feeding grounds (Iceland and Antarctic Peninsula). The whales approached the stimulus area and stayed longer in the trial zone during krill extract trials compared to control trials, suggesting that they were attracted to the chemical source and spent time exploring its surroundings, probably in search of prey. This response was observed in Iceland, and to a lesser extend in Madagascar, but not in Antarctica. Surface behaviours indicative of sensory exploration, such as diving under the stimulus area and stopping navigation, were also observed more often during krill extract trials than during control trials. Exposure to DMS did not elicit such exploration behaviours in any of the study areas. However, acoustic analyses suggest that DMS and krill extract both modified the whales’ acoustic activity in Madagascar. Altogether, these results provide the first behavioural evidence that baleen whales actually perceive prey-derived chemical cues over distances of several hundred metres. Chemoreception, especially olfaction, could thus be used for locating prey aggregations and for navigation at sea, as it has been shown in other marine predators including seabirds.
... Anosmia, the lack of a sense of smell, in toothed whales is supported by several morphological, neuroanatomical, and biomolecular investigations. In baleen whales, the peripheral olfactory apparatuses are reduced but still existent during the entire lifetime ( Godfrey, Geisler, & Fitzgerald, 2013 ;Thewissen, George, Rosa, & Kishida, 2011 ). By contrast, in recent toothed whales, the peripheral olfactory structures (bulbs, tracts, and nerves) have been lost or extremely reduced during evolutionary remodeling and shifts of the nasal apparatus ( Breathnach, 1960 ;Kellogg, 1928 ;Kruger, 1959 ;Morgane & Jacobs, 1972 ). ...
... The " echolocation-priority " hypothesis ( Hoch, 2000 ) proposes that the importance of olfaction had decreased with the development of the sonar system, which led to degeneration and to total loss of the sense of smell in cetaceans that use echolocation. The " filter-feeder " hypothesis ( Cave, 1988 ;Godfrey et al., 2013 ;Thewissen et al., 2011 ) suggests that in mysticetes, which do not rely on echolocation, the olfactory sense has been maintained due to the importance of locating planktonic prey by its characteristic odor. ...
... Mysticetes appear to have maintained a functional olfactory system, indicating that they can smell in air (Berta et al. 2014, and literature cited therein). In particular, there is mounting evidence that baleen whales use olfaction of air molecules to detect prey patches by sensing the odor dimethyl sulfide (DMS; Thewissen et al. 2011, Kishida andThewissen 2012), which is a volatile compound released by certain species of phytoplankton when they are consumed by zooplankton (Dacey and Wakeham 1986), a common prey item of baleen whales. DMS is detectable within a few meters of the ocean surface, overlapping with the breath intake zone of baleen whale blowholes. ...
... DMS is detectable within a few meters of the ocean surface, overlapping with the breath intake zone of baleen whale blowholes. Genetic studies also support the hypothesis that baleen whales sense DMS through their olfactory system in order to locate their prey (Kishida et al. 2007, Thewissen et al. 2011, Kishida and Thewissen 2012) and a preliminary study indicates that foraging baleen whales orient upwind toward odor plumes. 2 Figure 2. Scale-of-senses schematic of the hypothetical interchange of sensory modalities used by baleen whales to locate prey at variable scales. The line for audition of signals from prey is faded to denote a lack of evidence for this sensory system in baleen whales. ...
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Research on cetacean foraging ecology is central to our understanding of their spatial and behavioral ecology. Yet, functional mechanisms by which cetaceans detect prey across different scales remain unclear. Here, I postulate that cetaceans utilize a scale-dependent, multimodal sensory system to assess and increase prey encounters. I review the literature on cetacean sensory systems related to foraging ecology, and hypothesize the effective scales of each sensory modality to inform foraging opportunities. Next, I build two “scale-of-senses” schematics for the general groups of dolphins and baleen whales. These schematics illustrate the hypothetical interchange of sensory modalities used to locate and discriminate prey at spatial scales ranging from 0 m to 1,000 km: (1) vision, (2) audition (sound production and sound reception), (3) chemoreception, (4) magnetoreception, and somatosensory perception of (5) prey, or (6) oceanographic stimuli. The schematics illustrate how a cetacean may integrate sensory modalities to form an adaptive foraging landscape as a function of distance to prey. The scale-of-senses schematic is flexible, allowing for case-specific application and enhancement with improved cetacean sensory data. The framework serves to improve our understanding of functional cetacean foraging ecology, and to develop new hypotheses, methods, and results regarding how cetaceans forage at multiple scales.
... Gatesy et al. [2013] suggested that a Hippopotamidae-Cetacea clade separated from a ruminant clade approximately 60 million years ago and that the ancestors of hippopotami and cetaceans divided 55 million years ago. Most artiodactyls within the Cetartiodactyla possess a vomeronasal system and a developed main olfactory system, whereas the vomeronasal system is lost and the main olfactory system is degraded in cetaceans [Meisami and Bhatnagar, 1998;Kishida et al., 2007Kishida et al., , 2015aKishida et al., , 2015bMcGowen et al., 2008;Thewissen et al., 2011]. Baleen whales lack the dorsal domain of the olfactory bulb [Kishida et al., 2015b], and the olfactory bulb is absent in toothed whales [Oelschläger et al., 2010]. ...
... Recent genetic [McGowen et al., 2008;Kishida et al., 2007Kishida et al., , 2015a and morphological [Thewissen et al., 2011;Kishida et al., 2015b] studies have found a depressed olfactory system in aquatic mammals, indicating a reduced need for this system in water, like traditional theories [Allison, 1952;Meisami and Bhatnagar, 1998]. ...
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The olfactory system of mammals comprises a main olfactory system that detects hundreds of odorants and a vomeronasal system that detects specific chemicals such as pheromones. The main (MOB) and accessory (AOB) olfactory bulbs are the respective primary centers of the main olfactory and vomeronasal systems. Most mammals including artiodactyls possess a large MOB and a comparatively small AOB, whereas most cetaceans lack olfactory bulbs. The common hippopotamus (Hippopotamus amphibius) is semiaquatic and belongs to the order Cetartiodactyla, family Hippopotamidae, which seems to be the closest extant family to cetaceans. The present study evaluates the significance of the olfactory system in the hippopotamus by histologically analyzing the MOB and AOB of a male common hippopotamus. The MOB comprised six layers (olfactory nerve, glomerular, external plexiform, mitral cell, internal plexiform, and granule cell), and the AOB comprised vomeronasal nerve, glomerular, plexiform, and granule cell layers. The MOB contained mitral cells and tufted cells, and the AOB possessed mitral/tufted cells. These histological features of the MOB and the AOB were similar to those in most artiodactyls. All glomeruli in the AOB were positive for anti-Gαi2, but weakly positive for anti-Gαo, suggesting that the hippopotamus vomeronasal system expresses vomeronasal type 1 receptors with a high affinity for volatile compounds. These findings suggest that the olfactory system of the hippopotamus is as well developed as that of other artiodactyl species and that the hippopotamus might depend on its olfactory system for terrestrial social communication.
... Cetaceans are divided into the suborders Odontoceti (toothed whales) and Mysticeti (filter-feeding baleen whales). Cetaceans have dramatically reduced olfaction, with altered olfactory bulb anatomy and decreased olfactory receptor genes in mysticetes (from ~1,000 olfactory receptors in artiodactyls to only 60 olfactory receptors in the minke whale) to virtually no olfactory sensory capabilities detected for odontocetes (Kishida, Thewissen, Usip, et al. (2015), Niimura, Nei (2007), Oelschläger, Ridgway, Knauth (2010), Thewissen, George, Rosa, Kishida (2011)). Cetaceans possess a particularly thin cortex (Morgane, Jacobs, Mcfarland (1980)) and are the most gyrencephalic of all mammals ( Figure 8), with gyrencephalic indices greater than 5, which is greater than what would be expected for their brain sizes (Manger, Prowse, Haagensen, Hemingway (2012), Ridgway, Brownson (1984)), but expected based on their expansive surface area and cortical depth (Mota and Herculano-Houzel, 2015). ...
... However, a ubiquitous and dense distribution of VENs across all cortical regions characterizes the bowhead whale. Bowhead whales are the least encephalized of all cetacean species and may be in a more basal phylogenetic position among mysticetes(Marx (2011), Price, Bininda-Emonds, Gittleman (2005, Thewissen, George, Rosa,Kishida (2011)). ...
Chapter
Comparative neuroanatomical studies have contributed substantial information about the brains of large mammals and expanded our understanding of cortical organization among species. In this chapter, we review some features of the largest extant mammals and include, where evidence is available, details about the organization and characteristics of the cerebral cortex, neuron morphology, subcortical structures, and cerebellum. We conclude with a brief discussion of putative cognitive and behavioral specializations associated with these species.
... Cetaceans in general have experienced a reduction of olfactory receptor genes through pseudogenization, but mysticetes have retained some functionality of olfactory ability (Kishida et al. 2007;Thewissen et al. 2011;Berta et al. 2015b). Anatomical evidence indicates that fossil and modern mysticetes retain distinct olfactory bulbs and a cribriform plate (Cave 1988;Pihlström 2008), and bowhead whales in particular have a welldeveloped sense of smell relative to other cetaceans (Thewissen et al. 2011;Kishida and Thewissen 2012). ...
... Cetaceans in general have experienced a reduction of olfactory receptor genes through pseudogenization, but mysticetes have retained some functionality of olfactory ability (Kishida et al. 2007;Thewissen et al. 2011;Berta et al. 2015b). Anatomical evidence indicates that fossil and modern mysticetes retain distinct olfactory bulbs and a cribriform plate (Cave 1988;Pihlström 2008), and bowhead whales in particular have a welldeveloped sense of smell relative to other cetaceans (Thewissen et al. 2011;Kishida and Thewissen 2012). Baleen whales have been observed to orient themselves downwind of odor plumes produced by plankton, perhaps also using vibrissae around the blowhole to determine the direction of the wind (Drake et al. 2015). ...
Article
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The origin of baleen and filter feeding in mysticete cetaceans occurred sometime between approximately 34 and 24 million years ago and represents a major macroevolutionary shift in cetacean morphology (teeth to baleen) and ecology (raptorial to filter feeding). We explore this dramatic change in feeding strategy by employing a diversity of tools and approaches: morphology, molecules, development, and stable isotopes from the geological record. Adaptations for raptorial feeding in extinct toothed mysticetes provide the phylogenetic context for evaluating morphological apomorphies preserved in the skeletons of stem and crown edentulous mysticetes. In this light, the presence of novel vascular structures on the palates of certain Oligocene toothed mysticetes is interpreted as the earliest evidence of baleen and points to an intermediate condition between an ancestral condition with teeth only and a derived condition with baleen only. Supporting this step-wise evolutionary hypothesis, evidence from stable isotopes show how changes in dental chemistry in early toothed mysticetes tracked the changes in diet and environment. Recent discoveries also demonstrate how this transition was made possible by radical changes in cranial ontogeny. In addition, genetic mutations and the possession of dental pseudogenes in extant baleen whales support a toothed ancestry for mysticetes. Molecular and morphological data also document the dramatic developmental shifts that take place in extant fetal baleen whales, in skull development, resorption of a fetal dentition and growth of baleen. The mechanisms involved in this complex evolutionary transition that entails multiple, integrated aspects of anatomy and ecology are only beginning to be understood, and future work will further clarify the processes underlying this macroevolutionary pattern.
... The degree of encephalization in cetaceans has been attributed to the unique communication and navigation systems cetaceans have evolved relative to their terrestrial counterparts, particularly as olfactory signals are either diminished or not used at all (Niimura and Nei, 2007;Oelschläger et al., 2010;Thewissen et al., 2011;Kishida et al., 2015). All cetaceans communicate through vocalizations. ...
... However, very little is known about the brain of the bowhead whale (Balaena mysticetus; Duffield et al., 1992). The bowhead whale is in a basal phylogenetic position among mysticetes (Price et al., 2005;Marx, 2011) and is one of the least encephalized cetacean (Marino, 1998;Marino et al., 2004;Hof et al., 2005;Thewissen et al., 2011). Here, we provide a preliminary assessment of the structure and cytoarchitecture of the bowhead whale cerebral cortex relative to other cetacean species. ...
Article
Few studies exist of the bowhead whale brain and virtually nothing is known about its cortical cytoarchitecture or how it compares to other cetaceans. Bowhead whales are one of the least encephalized cetaceans and occupy a basal phylogenetic position amongst mysticetes. Therefore, the bowhead whale is an important specimen for understanding the evolutionary specializations of cetacean brains. Here, we present an overview of the structure and cytoarchitecture of the bowhead whale cerebral cortex gleaned from Nissl‐stained sections and magnetic resonance imaging (MRI) in comparison with other mysticetes and odontocetes. In general, the cytoarchitecture of cetacean cortex is consistent in displaying a thin cortex, a thick, prominent layer I, and absence of a granular layer IV. Cell density, composition, and width of layers III, V, and VI vary among cortical regions, but cetacean cortex is cell‐sparse relative to that of terrestrial mammals. Notably, all regions of the bowhead cortex possess high numbers of von Economo neurons and fork neurons, with the highest numbers observed at the apex of gyri. The bowhead whale is also distinctive in having a significantly reduced hippocampus that occupies a space below the corpus callosum within the lateral ventricle. Consistent with other balaenids, bowhead whales possess what appears to be a blunted temporal lobe, which is in contrast to the expansive temporal lobes that characterize most odontocetes. The present report demonstrates that many morphological and cytoarchitectural characteristics are conserved among cetaceans, while other features, such as a reduced temporal lobe, may characterize balaenids amongst mysticetes. This article is protected by copyright. All rights reserved.
... The cribriform plate and the ethmoturbinates are responsible for olfaction, a key sensory modality for most mammals. There is no doubt that the cribriform plate and the ethmoturbinates are present in baleen whales, as has already been mentioned by several authors (e.g., Flower, 1866;Edinger, 1955;Breathnach, 1960;Godfrey et al., 2013;Buono et al., 2015), indicating the persistence of the olfactory sense in modern mysticetes, although the presence or absence and the size of the olfactory bulb may be variable between, and even within, species (Langworthy, 1935;Ries and Langworthy, 1937;Breathnach, 1955;Jansen and Jansen, 1969;Thewissen et al., 2011). Because mysticetes are not known to echolocate , the olfaction may still play an important role for detecting food such as plankton swarms, like procellariiform birds and seals do (Nevitt, 1999;Kowalewsky et al., 2006;Ichishima, 2008;Thewissen et al., 2011). ...
... There is no doubt that the cribriform plate and the ethmoturbinates are present in baleen whales, as has already been mentioned by several authors (e.g., Flower, 1866;Edinger, 1955;Breathnach, 1960;Godfrey et al., 2013;Buono et al., 2015), indicating the persistence of the olfactory sense in modern mysticetes, although the presence or absence and the size of the olfactory bulb may be variable between, and even within, species (Langworthy, 1935;Ries and Langworthy, 1937;Breathnach, 1955;Jansen and Jansen, 1969;Thewissen et al., 2011). Because mysticetes are not known to echolocate , the olfaction may still play an important role for detecting food such as plankton swarms, like procellariiform birds and seals do (Nevitt, 1999;Kowalewsky et al., 2006;Ichishima, 2008;Thewissen et al., 2011). Conversely, the degree of reliance on olfaction in modern odontocetes is unclear. ...
Article
A cribriform plate, a perpendicular plate, and two lateral masses are major components of the ethmoid bone of mammals. Notwithstanding the noticeable bone, virtually sitting in the center of the skull, extensive modifications of the skull of modern cetaceans, especially odontocetes (toothed whales), and the lack of clarity as to what characteristics delimit each element of the ethmoid has made the problem of the nature of the cetacean ethmoid more complicated and elusive than in other, less modified mammals. Furthermore, contention as to whether a perpendicular plate of the ethmoid, or the mesethmoid, exists in all mammals including cetaceans has remained unsettled. In odontocetes, the mesethmoid has been variably identified not only as the osseous nasal septum but also as the mediodorsal region of the posterior wall of the nasal passage below the nasals, as a mass of bone encased by the vomer in front of the osseous nasal cavity at the base of the rostrum, and as a combination of some portions mentioned above. The presence or absence of the mesethmoid in various groups of mammals has attracted the attention of some biologists, and here, I demonstrate that cetaceans have no mesethmoid. The close inspection of the ontogenetic changes of the basicranial elements in cetaceans reveals that a mass of bone ensheathed by the vomer in front, or at the level of the osseous nasal cavity is actually the presphenoid. It is highly likely that in odontocetes the posterior wall of the nasal passages below the nasals consists of the combination of the frontal, the imperforated cribriform plate, the paired ectethmoids, and the vomer, the latter three of which partially concealing the presphenoid dorsally and laterally as the ontogeny proceeds. In contrast, mysticetes clearly display ethmoturbinates and a cribriform plate, which are morphologically similar to those in terrestrial mammals. J. Morphol., 2016.
... Odontoceti were found to possess a well-developed olfactory tubercle (Oelschläger and Oelschläger, 2009). In bowhead whales (Balaena mysticetus), a complex olfactory bulb and olfactory tracts are present and more than half of the OR genes are intact, suggesting a potentially functional sense of smell (Thewissen et al., 2011;Kishida et al., 2015a). However, OR genes are reported to be functionally reduced by pseudogenization in Odontoceti (Kishida et al., 2007). ...
... As phytoplankton attracts zooplankton and zooplankton in turn attracts fish, the ability to detect DMS might allow dolphins to find fish. Indeed, prey detection by using chemical cues has already been suggested for bowhead whales (Thewissen et al., 2011). ...
Article
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A large part of the literature on sensory perception and behavior in dolphins is devoted to its well-developed vocal and echolocation abilities. In this review, we aim to augment current knowledge by examining the literature on dolphins’ entire “Merkwelt” (which refers to everything a subject perceives, creating a crucial part of the subject’s Umwelt). We will show that despite extensive knowledge on audition, aspects such as context relatedness, the social function of vocalizations or socio-sexual recognition, remain poorly understood. Therefore, we propose areas for further lines of investigation. Recent studies have shown that the sensory world of dolphins might well be much more diverse than initially thought. Indeed, although underwater and aerial visual systems differ in dolphins, they have both been shown to be important. Much debated electro- and magnetoreception appear to be functional senses according to recent studies. Finally, another neglected area is chemoreception. We will summarize neuroanatomical and physiological data on olfaction and taste, as well as corresponding behavioral evidence. Taken together, we will identify a number of technical and conceptual reasons for why chemosensory data appear contradictory, which is much debated in the literature. In summary, this article aims to provide both an overview of the current knowledge on dolphin perception, but also offer a basis for further discussion and potential new lines of research.
... Furthermore, there is still room for doubt that cetaceans keep some vestigial abilities on perception from their terrestrial evolutionary past. For example, looking to the other sensory modalities that were thought to be lost, there are evidences for chemoreception, including olfaction and gustation in dolphins (Kremers et al., 2016;Ridgway, 1988), while some authors have claimed that airborne odorants may be considered irrelevant to an aquatic lifestyle (Thewissen et al., 2011), although fish perceive the chemical solutions both by olfaction and taste (Kuznetzov, 1990). When considering hearing, it is worth remembering that the mammalian ear evolved for hearing in air. ...
... Ainsi, il y a encore lieu de douter que les cétacés aient réellement perdu toute capacité de perception auditive aérienne. Par exemple, en se focalisant sur d'autres modalités sensorielles que l'on croyait perdues, il existe aujourd'hui des preuves montrant des capacités de chemoréception, y compris l'olfaction et la gustation chez les dauphins (Kremers et al., 2016, Ridgway, 1988, malgré l'idée que les odeurs transportées par l'air seraient non pertinentes pour un mode de vie aquatique (Thewissen et al., 2011). Lorsque l'on considère l'audition, il convient de rappeler que l'oreille des mammifères a évolué pour entendre les signaux sonores émis dans l'air. ...
Thesis
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Studies on animal bioacoustics, traditionally relying on non-human primate and songbird models, converge towards the idea that social life appears as the main driving force behind the evolution of complex communication. Comparisons with cetaceans is also particularly interesting from an evolutionary point of view. They are indeed mammals forming complex social bonds, with abilities in acoustic plasticity, but that had to adapt to marine life, making habitat another determining selection force. Their natural habitat constrains sound production, usage and perception but, in the same way, constrains ethological observations making studies of captive cetaceans an important source of knowledge on these animals. Beyond the analysis of acoustic structures, the study of the social contexts in which the different vocalizations are used is essential to the understanding of vocal communication. Compared to primates and birds, the social function of dolphins’ acoustic signals remains largely misunderstood. Moreover, the way cetaceans’ vocal apparatus and auditory system adapted morphoanatomically to an underwater life is unique in the animal kingdom. But their ability to perceive sounds produced in the air remains controversial due to the lack of experimental demonstrations. The objectives of this thesis were, on the one hand, to explore the spontaneous contextual usage of acoustic signals in a captive group of bottlenose dolphins and, on the other hand, to test experimentally underwater and aerial abilities in auditory perception. Our first observational study describes the daily life of our dolphins in captivity, and shows that vocal signalling reflects, at a large scale, the temporal distribution of social and non-social activities in a facility under human control. Our second observational study focuses on the immediate context of emission of the three main acoustic categories previously identified in the dolphins’ vocal repertoire, i.e. whistles, burst-pulses and click trains. We found preferential associations between each vocal category and specific types of social interactions and identified context-dependent patterns of sound combinations. Our third study experimentally tested, under standardized conditions, the response of dolphins to human-made individual sound labels broadcast under and above water. We found that dolphins were able to recognize and to react only to their own label, even when broadcast in the air. Apart from confirming aerial hearing, these findings go in line with studies supporting that dolphins possess a concept of identity. Overall, the results obtained during this thesis suggest that some social signals in the dolphin repertoire can be used to communicate specific information about the behavioural contexts of the individuals involved and that individuals are able to generalize their concept of identity for human-generated signals.
... Loggerhead sea turtles orient to airborne odours emanating from islands [105] and green sea turtles are preferentially attracted to the airborne odours of island mud [106]. Diverse vertebrate species (sea turtle, seabirds, harbour seal, bowhead whale) orient to the airborne odour of dimethyl sulfide, a metabolic byproduct of phytoplankton that is associated with fish schools that are otherwise difficult to locate [107][108][109][110][111]. ...
... They also retain MOS structure and olfactory functions. Bowhead whales employ the MOS to detect dimethyl sulfide, the krill metabolite mentioned earlier [111]. The retention of some MOS function might explain the difference in auditory systems between the two suborders. ...
Article
To make maps from airborne odours requires dynamic respiratory patterns. I propose that this constraint explains the modulation of memory by nasal respiration in mammals, including murine rodents (e.g. laboratory mouse, laboratory rat) and humans. My prior theories of limbic system evolution offer a framework to understand why this occurs. The answer begins with the evolution of nasal respiration in Devonian lobe-finned fishes. This evolutionary innovation led to adaptive radiations in chemosensory systems, including the emergence of the vomeronasal system and a specialization of the main olfactory system for spatial orientation. As mammals continued to radiate into environments hostile to spatial olfaction (air, water), there was a loss of hippocampal structure and function in lineages that evolved sensory modalities adapted to these new environments. Hence the independent evolution of echolocation in bats and toothed whales was accompanied by a loss of hippocampal structure (whales) and an absence of hippocampal theta oscillations during navigation (bats). In conclusion, models of hippocampal function that are divorced from considerations of ecology and evolution fall short of explaining hippocampal diversity across mammals and even hippocampal function in humans. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.
... Most toothed whales lack the ability to smell, and most of their olfactory receptor (OR) and marker protein genes are dysfunctional (McGowen et al., 2014;Springer and Gatesy, 2017). Bowheads, and possibly other mysticetes, partially rely on airborne scent to locate aggregations of copepods and euphausiids that have distinctive odors (Thewissen et al., 2011). Anatomical structures supporting olfaction are still present in bowheads (olfactory epithelium, olfactory bulb of the brain), and bowheads have some functional ORs (Thewissen et al., 2011). ...
... Bowheads, and possibly other mysticetes, partially rely on airborne scent to locate aggregations of copepods and euphausiids that have distinctive odors (Thewissen et al., 2011). Anatomical structures supporting olfaction are still present in bowheads (olfactory epithelium, olfactory bulb of the brain), and bowheads have some functional ORs (Thewissen et al., 2011). Bowheads lack a dorsal region (domain) of the olfactory bulb that supports avoidance behaviors in response to odors of predators (Kishida et al., 2015). ...
Chapter
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Bowhead whales are some of the largest animals that occupy the Arctic Circle. Despite the challenges of living and giving birth in icy waters, having huge blubber stores, eating a fat-rich diet, and undergoing arduous migrations, bowheads achieved the longest known life span of mammals of 268 years. Their longevity is extended by fixed mutations that prevent DNA damage and cancer and through evolutionary modifications to their metabolism that compensate for an oxygen-poor environment. Recently, the bowhead genome and transcriptome libraries were made publicly available for study. Analyses suggest that their life span has been extended by evolutionary changes that result in the upregulation of DNA repair pathways. Molecular biologists are now undertaking laboratory experiments with whale samples that are informed by the bowhead genome and transcriptome to tackle questions that were inaccessible using classical model organisms such as rodents or fish. Biomedical researchers are also applying insights gained from research on bowheads into investigations of potential therapies for aging, senescence, and cancer. Moreover, researchers are using these results to inform our understanding of the evolutionary history of these traits. This chapter reviews the molecular basis for bowhead whale longevity and survival in their unique habitat and offers insights for further exploration into the molecular mechanisms that shape the extraordinary lives of these animals.
... Baleen whales are arguably the most efficient foragers among vertebrates by exploiting abundant small prey along with developing extreme body size (Goldbogen et al., 2019). How large mysticetes locate these high-density patches is not fully understood, but oceanographic cues, maternally driven site fidelity to traditional feeding areas are important, and olfaction may play a role as well (Chapters 4, 24, 28, this volume; Moore and Reeves, 1993;Baumgartner and Mate, 2003;Thewissen et al., 2011). While the mechanics of prey ingestion varies amongst mysticetes, balaenids (bowhead and right whales) strain prey-laden water with their baleen as they swim (see Chapter 14). ...
Chapter
Based on several lines of evidence, bowhead whales appear to have metabolic rates that are lower than other similar-sized baleen whales. Low metabolic rates offer some disadvantages, such as slow growth rates, delayed maturation, and long intercalf intervals; however, they also offer some advantages. When food is limited, as in winter, or years with low prey densities, it may be possible for a bowhead to persist for long periods at a relatively low metabolic cost. Selection may have modified the bowhead to store large amounts of lipid in the form of thick blubber, to survive the high variability in the arctic and seasons when “food is virtually lacking” (Chapter 7). That is, a large bowhead whale (with its thick blubber) can likely survive a year or years on its lipid reserves. In nature, however, given the stresses associated with migration, reproduction, and predation, it is unclear how long a bowhead could actually persist on limited nutrition. Kraus and Rolland nicely summarized a strategy for the closely related North Atlantic right whale which applies to bowheads as well, “survive the lean years, and reproduce in the good ones.”
... Much of the broad research on the evolution of the brain in cetaceans has centered on endocast volumes and brain volumes adjusted for body size, as a measure of relative cognitive ability, through evolutionary time (e.g., Marino et al., 2004;Montgomery et al., 2013). These methods have been criticized because of the large or at least highly variable amount of extra-brain material (adnexa) within the braincase of cetaceans (Ridgway, Carlin, Van Alstyne, Hanson, & Tarpley, 2016;Thewissen et al., 2011a). It has also been noted that blubber contributes to body mass and size, but has no association with brain functionality, thus artificially decreasing the EQ (Thewissen, 2018). ...
Article
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Studies surrounding the evolution of sensory system anatomy in cetaceans over the last ~100 years have shed light on aspects of the early evolution of hearing sensitivities, the small relative size of the organ of balance (semicircular canals and vestibule), brain (endocast) shape and relative volume changes, and ontogenetic development of sensory‐related structures. Here, I review advances in our knowledge of sensory system anatomy as informed by the use of nondestructive imaging techniques, with a focus on applied methods in computed tomography (CT and μCT), and identify the key questions that remain to be addressed. Of these, the most important are: Is lower frequency hearing sensitivity the ancestral condition for whales? Did echolocation evolve more than once in odontocetes; and if so, when and why? How has the structure of the cetacean brain changed, through the evolution of whales, and does this correspond to changes in hearing sensitivities? Finally, what are the general pathways of ontogenetic development of sensory systems in odontocetes and mysticetes? Answering these questions will allow us to understand important macroevolutionary patterns in a fully aquatic mammalian group and provides baseline data on species for which we have limited biological information because of logistical limitations.
... The only significant mammal group for which chemical communication has not been demonstrated are whales and dolphins (cetaceans). However, it is possible and may be discovered in future, as baleen (mysticete) whales have a good olfactory system, which they may also use to detect upwind concentrations of plankton by smell (as albatross do, Chapter 10) (Thewissen et al. 2011). Some baleen whales have a Harderian gland, which in some rodents produces pheromones, though it may have other functions (Funasaka et al. 2010 Hölldobler and Carlin (1987) introduced the idea of anonymous signals (pheromones) contrasted with variable signature mixtures (though their terminology was different) (see also Hölldobler & Wilson 2009, p. 270). ...
... Olfactory epithelium has also been found in bowhead whales, and this species appears to react to airborne smells. It is thought that any sense of olfaction may be useful in locating the presence of planktonic prey by airborne smell (Thewissen et al. 2011). ...
... This study aims to link gene expression and phenotype within the ribs of bowheads throughout ontogeny to help elucidate the evolutionary origins of these traits in Eocene whales (archaeocetes) and their evolutionarily close relatives. Bowhead whales are an ideal study taxon because molecular biology techniques traditionally applied to terrestrial mammals have been successfully used on this species (Ball et al., 2017(Ball et al., , 2015Kishida & Thewissen, 2012;Schweikert, Fasick, & Grace, 2016;Thewissen, George, Rosa, & Kishida, 2011;Thewissen et al., 2017;Tian et al., 2017;Zhu, Ge, Wen, Xia, & Yang, 2018). Moreover, the field of skeletal biology has a solid understanding of age-related changes in bone phenotype and bone cell activity in at least rodents and humans (Almeida & O'Brien, 2013; Burr & Allen, 2019). ...
Chapter
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The bowhead whale is of the largest and longest lived animals on earth (Fig. 20.1). Despite the challenges of living and giving birth in arctic waters, having vastblubber stores, eating a fat-rich diet, and migrations, bowheads are estimated to reach ages of up to 268 years (George et al., 1999; Mayne et al., 2019; Seim et al., 2014; Tacutu et al., 2012). Recently, the bowhead genome and transcriptome libraries (Keane et al., 2015; Seim et al., 2014) were made publicly available for study. Bowheads have probably benefited from both the expansion and decay in different parts of their genome in evolving a long and caompartively healthy life. Here we discuss the expansions (duplication) and losses (inactivation) in genes associated with the derived anatomy of physiology of cetaceans, and when evidence supports it, bowheads. Duplication of genes allows for new copies to be free from selection for their original function and instead evolve novel functions. Gene loss/inactivation can be the result of an evolutionary relaxation in selection for a function that became obsolete but can also be a mechanism for adaptation as gene inactivations in whales may improve replication accuracy (Huelsmann et al., 2019). Molecular biologists are now undertaking laboratory experiments with whale samples that are informed by the bowhead genome and transcriptome to tackle questions that were inaccessible using classical model organisms such as rodents or fish. Biomedical researchers are applying insights gained from research on bowheads into investigations of potential therapies for aging, senescence, and cancer. Moreover, evolutionary biologists are using these results to inform our understanding of how different key traits evolved sequentially in deep time. This chapter reviews the molecular basis for bowhead whale longevity and survival in their unique environment and offers insights for further exploration into the molecular mechanisms that shape the extraordinary lives of these animals.
... Globally, DMS and DMSP have been implicated as infochemicals across a wide range of marine biota, from zooplankton (1) to baleen whales (49). The explanation we provide for plastic ingestion patterns seen in procellariiform seabirds should be explored in other groups, including sea turtles (50), penguins (51), various species of marine fishes (52,53), and even marine mammals (54), all of which have been shown to either detect or use these compounds in foraging contexts. ...
Article
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Plastic debris is ingested by hundreds of species of organisms, from zooplankton to baleen whales, but how such a diversity of consumers can mistake plastic for their natural prey is largely unknown. The sensory mechanisms underlying plastic detection and consumption have rarely been examined within the context of sensory signals driving marine food web dynamics. We demonstrate experimentally that marine-seasoned microplastics produce a dimethyl sulfide (DMS) signature that is also a keystone odorant for natural trophic interactions. We further demonstrate a positive relationship between DMS responsiveness and plastic ingestion frequency using procellariiform seabirds as a model taxonomic group. Together, these results suggest that plastic debris emits the scent of a marine infochemical, creating an olfactory trap for susceptible marine wildlife.
... Foraging in mysticetes is likely a combination of multiple sensory processes and the dominant modality utilized is thought to be highly dependent on scale (Baumgartner et al., 2007;Kenney et al., 2001;Torres, 2017), available sensory cues in the environment, and the sensory ecology of the particular species. Anatomical and behavioral evidence has demonstrated potential for the use of olfaction to detect wind-borne dimethyl sulfide, a compound generated by plankton, in order to detect prey patches or oceanographic features near which prey could be found (Bouchard et al., 2019;Thewissen et al., 2011). Though evidence is limited, it has also been speculated that animals could use passive acoustic cues to pick up information from background ocean soundscapes or nearby conspecifics (Torres, 2017). ...
Article
North Atlantic right whales (NARWs; Eubalaena glacialis) possess an arrangement of fine hairs on the rostrum and chin that may be used for hydrodynamic sensing during feeding. These hairs occur across mysticete species and are known to possess adequate innervation in the subdermal follicle to support their consideration as sensory hairs (vibrissae). However, the small size of the hair structure with respect to the enormous scale of the animal's body has caused doubts regarding their utility and prompted speculation that the hairs may be vestigial or minimally functional. Here we show that NARW hairs occur in abundance on the leading surface of the head in a unique and characteristic arrangement. We consider the sensory hairs in context of the fluid environment in which this species forages and argue that the size of the hair is scaled to the size of the animal's small planktonic prey, thus suggesting that the hairs play an important role in the sensory ecology of these animals.
... For example, all modern whales have lost the vomeronasal organs during their transition from land to water (Pihlström, 2008;Kishida et al., 2015). Some modern whales still possess highly degenerated main olfactory systems, but they can smell only in air, not underwater (Thewissen et al., 2011). Loss of the vomeronasal organ is also documented in sirenians (Pihlström, 2008). ...
Article
Fully aquatic adaptation generally leads amniotes to change sensory modalities drastically. Terrestrial snakes rely heavily on chemical cues to locate and recognize prey, but little is known about how sea snakes find prey fishes underwater. Sea snakes of the genus Hydrophis are fish-eating marine elapids which adapted from land to water approximately 5-10 million years ago. Here, using two species of captive Hydrophis snakes, we show that they can recognize and discriminate their preferred fish species solely by using olfactory cues. However, they locate places where their preferred fishes may hide without relying on chemical cues. These findings indicate that Hydrophis snakes find prey in water as follows: they use visual cues to locate a place where their prey fishes are likely to hide, and then use chemical cues to find and attack prey. As is the case for other aquatic amniotes, snakes also modified their sensory modalities upon becoming aquatic.
... This study aims to link gene expression and phenotype within the ribs of bowheads throughout ontogeny to help elucidate the evolutionary origins of these traits in Eocene whales (archaeocetes) and their evolutionarily close relatives. Bowhead whales are an ideal study taxon because molecular biology techniques traditionally applied to terrestrial mammals have been successfully used on this species (Ball et al., 2017(Ball et al., , 2015Kishida & Thewissen, 2012;Schweikert, Fasick, & Grace, 2016;Thewissen, George, Rosa, & Kishida, 2011;Thewissen et al., 2017;Tian et al., 2017;Zhu, Ge, Wen, Xia, & Yang, 2018). Moreover, the field of skeletal biology has a solid understanding of age-related changes in bone phenotype and bone cell activity in at least rodents and humans (Almeida & O'Brien, 2013; Burr & Allen, 2019). ...
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Bowhead whales are among the longest‐lived mammals with an extreme lifespan of about 211 years. During the first 25 years of their lives, rib bones increase in mineral density and the medulla transitions from compact to trabecular bone. Molecular drivers associated with these phenotypic changes in bone remain unknown. This study assessed expression levels of osteogenic genes from samples of rib bones of bowheads. Samples were harvested from prenatal to 86‐year‐old whales, representing the first third of the bowhead lifespan. Fetal to 2‐year‐old bowheads showed expression levels consistent with the rapid deposition of the bone extracellular matrix. Sexually mature animals showed expression levels associated with low rates of osteogenesis and increased osteoclastogenesis. After the first 25 years of life, declines in osteogenesis corresponded with increased expression of EZH2 , an epigenetic regulator of osteogenesis. These findings suggest EZH2 may be at least one epigenetic modifier that contributes to the age‐related changes in the rib bone phenotype along with the transition from compact to trabecular bone. Ancient cetaceans and their fossil relatives also display these phenotypes, suggesting EZH2 may have shaped the skeleton of whales in evolutionary history. Research Highlights • How the rib bones of whales respond to aging remains poorly understood. We show that, under the control of the epigenetic regulator EZH2 , ribs of aging bowhead whales experience a decline in extracellular matrix production, and increased erosion.
... 须鲸虽然保留部分与嗅觉有关的结构, 但也出现了不 同程度的退化 [54] . 近年来的研究从分子层面上探讨了 鲸类嗅觉退化的遗传学基础. ...
... Baleen whales have retained the olfactory function, whereas it has been lost in toothed whales (Berta et al., 2014;Thewissen et al., 2011). Mysticetes may therefore be able to detect chemicals that indicate prey productivity or salinity levels and orientate themselves based on olfactory gradients (Hagelin et al., 2012;Nevitt, 2000Nevitt, , 2008Nevitt and Bonadonna, 2005). ...
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Understanding the biogeography of a species begins by mapping its presence over time and space. The use of home ranges, breeding and feeding areas, migration paths and movement patterns between the two are also inherent to their ecology. However, this is an overly simplified view of life histories. It ignores nuanced and complex exchanges and responses to the environment and between conspecifics. Having previously advocated for a more species-centric approach in a discussion of ‘whale geography’, I look to better understand the driving factors of migrations, and the information streams guiding the movement, which is key to the biogeography of large whale species. First, I consider the processes underlying the navigation capacities of species to complete migration, and how, and over what scales, sensory information contributes to cognitive maps. I specifically draw on examples of large-scale, en masse migrators to then apply this to whales. I focus on the acoustic sense as the principal way whales gain and exchange information, drawing on a case study of grey whale ( Eschrichtius robustus) calling behaviour to illustrate my arguments. Their consistent employment of far-propagating calls appears to be tied to travel behaviours and probably aids navigation and social cohesion. The range over which calls are being propagated to conspecifics, or perhaps being echoed back to the individual, underlies the distance over which the cognitive maps are being both formed and employed. I believe understanding these processes edges us closer to understanding species biogeography.
... In theory, this could lead to a false signature of increased relative CB and CX size in cetaceans. The olfactory neuropils are still present in mysticetes (Thewissen, George, Rosa, & Kishida, 2011) but the available data are limited, prohibiting their exclusion in these species. However, in mysticetes the olfactory bulbs are proportionally quite small (~0.13% brain volume; Thewissen et al., 2011) so we consider their influence to have a negligible effect on our analyses. ...
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Cetaceans possess brains that rank among the largest to have ever evolved, either in terms of absolute mass or relative to body size. Cetaceans have evolved these huge brains under relatively unique environmental conditions, making them a fascinating case study to investigate the constraints and selection pressures that shape how brains evolve. Indeed, cetaceans have some unusual neuroanatomical features, including a thin but highly folded cerebrum with low cortical neuron density, as well as many structural adaptations associated with acoustic communication. Previous reports also suggest that at least some cetaceans have an expanded cerebellum, a brain structure with wide‐ranging functions in adaptive filtering of sensory information, the control of motor actions, and cognition. Here, we report that, relative to the size of the rest of the brain, both the cerebrum and cerebellum are dramatically enlarged in cetaceans and show evidence of co‐evolution, a pattern of brain evolution that is convergent with primates. However, we also highlight several branches where cortico‐cerebellar co‐evolution may be partially decoupled, suggesting these structures can respond to independent selection pressures. Across cetaceans, we find no evidence of a simple linear relationship between either cerebrum and cerebellum size and the complexity of social ecology or acoustic communication, but do find evidence that their expansion may be associated with dietary breadth. In addition, our results suggest that major increases in both cerebrum and cerebellum size occurred early in cetacean evolution, prior to the origin of the major extant clades, and predate the evolution of echolocation.
... Prey search is surely a multimodal process, perhaps involving a combination of olfactory senses (which are poorly developed in cetaceans, although perhaps not in balaenids [41]), sensory taste buds in the oral cavity (also limited in cetaceans, see [42]) and mechanoreception, where foraging whales may monitor impacts of plankton with bristles on their rostrum or on the tongue itself [4]. Our study supports the notion that whales can use their eyes in prey search, even in turbid and relatively dark environments. ...
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North Atlantic right whales ( Eubalaena glacialis ) feed during the spring and early summer in marine waters off the northeast coast of North America. Their food primarily consists of planktonic copepods, Calanus finmarchicus , which they consume in large numbers by ram filter feeding. The coastal waters where these whales forage are turbid, but they successfully locate copepod swarms during the day at depths exceeding 100 m, where light is very dim and copepod patches may be difficult to see. Using models of E. glacialis visual sensitivity together with measurements of light in waters near Cape Cod where they feed and of light attenuation by living copepods in seawater, we evaluated the potential for visual foraging by these whales. Our results suggest that vision may be useful for finding copepod patches, particularly if E. glacialis searches overhead for silhouetted masses or layers of copepods. This should permit the whales to locate C. finmarchicus visually throughout most daylight hours at depths throughout their foraging range. Looking laterally, the whales might also be able to see copepod patches at short range near the surface. This article is part of the themed issue ‘Vision in dim light’.
Chapter
Mammals possess relatively larger brains compared to body size, and there are many studies focusing on the evolutionary changes of the relative brain size in mammals. A recent study showed that increased resolution in olfaction drove the enlargement of mammalian brains. However, the olfactory bulbs are degenerated among highly encephalized mammals, primates and whales. Several species of whales possess functional olfactory bulbs, but their olfactory bulbs lack a specific area known to induce innate avoidance behavior against odors of predators and spoiled foods. In this chapter, evolutionary changes of the encephalization quotient among mammals and the degeneration processes of olfactory bulbs among whales are discussed from paleontological, anatomical, and genomic points of view.
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Animals perceive surrounding environments using sensory modalities, and it is therefore hypothesized that transition to a new environment causes modification of the sensory systems. In this chapter, olfactory systems of three fully aquatic amniotes-odontocetes, mysticetes and hydrophiin sea snakes-are reviewed and compared in order to understand the aquatic adaptation and the evolution of olfactory sensory systems in amniotes. Reduction of the olfactory organs and the olfactory receptor genes has been confirmed in all three groups. However, the remaining olfactory capacities of the groups are completely different from each other: odontocetes have no sense of olfaction, whereas mysticetes still use the main olfactory system for smelling in air, and sea snakes use the accessory olfactory system for smelling underwater. These findings suggest that fully aquatic adaptation generally causes reduction of the olfactory systems which had been evolved to be optimized for life on land, but the olfactory capacities of different aquatic amniotes are not the same, and that both phylogenetic constraints and ecological demands affect the formation of olfactory capacities upon becoming aquatic.
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The megafauna (Greek μεγα: great; Latin fauna: animal life) of Antarctica is defined by absence. Two classes of vertebrates, reptiles and amphibians, are missing from the continent and its surrounding waters, and Antarctica has lacked true land vertebrates since dinosaurs last roamed the continent in the late Cretaceous. The ocean is the foundation of all vertebrate life in Antarctica, and none of its native birds and mammals can survive permanently in the continent's frigid, white interior. Antarctic vertebrates are all classified as marine and ultimately derive their food from the sea. Unlike in much of the Arctic, the harsher climate of Antarctica does not allow for significant plant growth, and no vertebrate herbivores exist. Antarctica's long isolation from other landmasses has resulted in the absence of surface predators such as the polar fox Alopex lagopus or polar bear Ursus maritimus, an important distinction between Antarctic and Arctic habitats. Antarctica and the Southern Ocean present some of the most challenging environmental conditions on Earth, including extreme cold, wind, dryness, radical seasonal changes in photoperiod, and extensive ice cover. But Antarctica also offers tremendous opportunity because it is a continent free of terrestrial mammalian predators, and the Southern Ocean surrounding the Antarctic continent includes some of the most productive marine habitats in the world. © Springer International Publishing Switzerland 2015. All rights are reserved.
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CetaceanCetacea/cetaceans minds have been the topic of intense scientific interest for decades, and our continued study of them takes us on a complicated journey that requires us to regard cetacean brainsBrain and behavior as simultaneously very different and very familiar to us. Cetacean brains have undergone one of the most dramatic transformations during their evolutionEvolution from terrestrial animals to the highly acoustic and socially sophisticated animals we know today. Their brains are a challenging combination of highly conserved mammalian characteristics along with a unique neocortical organization that suggests that it processes information through alternative neural strategies to those of the primate brain. Their sensorium and perceptual capacities, especially in the realm of communicationCommunication, are unusual even for a fully aquatic mammal. Their cognitive and social capacities make it clear that there are striking convergences in psychology between cetaceansCetacea/cetaceans and many terrestrial carnivores as well as primates such as we are, including the reliance on strong social bondsSocial bonds and, in many cases, culturalCultural traditions.
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Various toothed whales (Odontoceti) are unique among mammals in lacking olfactory bulbs as adults and are thought to be anosmic (lacking the olfactory sense). At the molecular level, toothed whales have high percentages of pseudogenic olfactory receptor genes, but species that have been investigated to date retain an intact copy of the olfactory marker protein gene (OMP), which is highly expressed in olfactory receptor neurons and may regulate the temporal resolution of olfactory responses. One hypothesis for the retention of intact OMP in diverse odontocete lineages is that this gene is pleiotropic with additional functions that are unrelated to olfaction. Recent expression studies provide some support for this hypothesis. Here, we report OMP sequences for representatives of all extant cetacean families and provide the first molecular evidence for inactivation of this gene in vertebrates. Specifically, OMP exhibits independent inactivating mutations in six different odontocete lineages: four river dolphin genera (Platanista, Lipotes, Pontoporia, Inia), sperm whale (Physeter), and harbor porpoise (Phocoena). These results suggest that the only essential role of OMP that is maintained by natural selection is in olfaction, although a non-olfactory role for OMP cannot be ruled out for lineages that retain an intact copy of this gene. Available genome sequences from cetaceans and close outgroups provide evidence of inactivating mutations in two additional genes (CNGA2, CNGA4), which imply further pseudogenization events in the olfactory cascade of odontocetes. Selection analyses demonstrate that evolutionary constraints on all three genes (OMP, CNGA2, CNGA4) have been greatly reduced in Odontoceti, but retain a signature of purifying selection on the stem Cetacea branch and in Mysticeti (baleen whales). This pattern is compatible with the 'echolocation-priority' hypothesis for the evolution of OMP, which posits that negative selection was maintained in the common ancestor of Cetacea and was not relaxed significantly until the evolution of echolocation in Odontoceti.
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The fossil record of early cetaceans provides a remarkably complete picture of how the terrestrial ancestors of modern whales turned into the highly specialized marine mammals. The origin of cetaceans was originally thought to be defined by their adoption of an aquatic lifestyle, and the morphological and physiological changes that such a step necessitates. This chapter provides an overview of the changes that affected the major sense organs during the terrestrial-aquatic transition of cetaceans. The baleen apparatus is organized into a series of thin, continuously growing keratinous plates, which are lined up into a rack and suspended from the margin of the upper jaw. Cetacean echolocation capabilities are difficult to test in the wild and have only been experimentally demonstrated in about a dozen species. As in all sciences, paleontologists strive to maximize sample sizes in order to characterize morphological, geographical, and temporal variation within both species and higher taxonomic categories.
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All mammals, and indeed all tetrapods have a skeleton that is divided into two main components: the axial skeleton, comprising the skull, vertebral column, and rib cage; and the appendicular skeleton, which includes the shoulder girdle, the pelvis, and both the fore- and hind limbs. Modern whales and dolphins stand apart from both other mammals and most of their archaeocete ancestors in having a greatly altered facial region with posteriorly displaced nostrils, markedly different ear bones, a shortened neck, a largely immobilized forelimb, and virtually no trace of the pelvis and hind limb. In cetaceans, the protective membranes or meninges surrounding the brain are well developed and often partially ossify during ontogeny. Information on cetacean sensory organs can be gleaned from osteological correlates relating to the eye, nose, and ear, and thus the senses of sight, smell, hearing, and balance.
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Large marine regions, including the exceptionally productive Southern Ocean, are iron-limited. As a result, there has been substantial interest in iron-fertilizing high nutrient low chlorophyll (HNLC) areas in an effort to sequester atmospheric carbon dioxide. More recently, research has shifted to quantifying the beneficial effects of iron recycling by marine biota. Marine top predators such as whales and seabirds have been examined specifically in this regard as they have high biomass, form dense aggregations, and excrete bioavailable iron in concentrations seven orders of magnitude higher than ambient seawater. Despite it being well established that marine fauna link the iron and carbon cycles, the connection of this process to the sulfur cycle has rarely been considered. The chemoattraction of specific marine fauna to algal-derived dimethyl sulfide (DMS) is key in triggering dense, multi-species foraging aggregations that induce iron recycling, augmenting carbon assimilation. The goal of this paper is twofold; first, to highlight DMS chemoattraction as a behavior that catalyzes carbon sequestration via natural iron fertilization, and second, to identify knowledge gaps that recent biogeochemical advances can address. Fostering this interdisciplinary research will enhance our understanding of global climate regulation, ecosystem services provided by marine top predators, and the biogeochemical cycles of carbon, iron, and sulfur in HNLC waters.
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How baleen whales locate prey and how environmental change may influence whale foraging success are not well understood. Baleen whale foraging habitat has largely been described at a population level, yet population responses to change are the result of individual strategies across multiple scales. This study aimed to determine how the foraging behaviour of individual whales varied relative to environmental conditions along their movement path. Biotelemetry devices provided information on humpback whale (Megaptera novaeangliae) movement at two spatial scales in East Antarctica, and a mixed modelling approach was used at a medium scale (tens of kilometres) to determine which environmental factors correlated with a change in foraging behaviour. Water temperature was linked to a change in foraging behaviour at both spatial scales. At the medium scale, warmer water was associated with the resident state, commonly assumed to represent periods of foraging behaviour. However, fine-scale analyses suggested that cooler water was associated with a higher feeding rate. Variation in whale foraging behaviour with changes in water temperature adds support to the hypothesis that whales may be able to track environmental conditions to find prey. Future research should investigate this pattern further, given the predicted rise in water temperatures under climate-change scenarios.
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Mysticete whales filter small prey from seawater using baleen, a unique keratinous oral tissue that grows from the palate, from which it hangs in hundreds of serial plates. Laboratory experiments testing effects of oils on material strength and flexibility, particle capture and tissue architecture of baleen from four mysticete species (bowhead, Balaena mysticetus; North Atlantic right, Eubalaena glacialis; fin, Balaenoptera physalus; humpback, Megaptera novaeangliae) indicate that baleen is hydrophilic and oleophobic, shedding rather than adsorbing oil. Oils of different weights and viscosities were tested, including six petroleum-based oils and two fish or plankton oils of common whale prey. No notable differences were found by oil type or whale species. Baleen did not adsorb oil; oil was readily rinsed from baleen by flowing water, especially from moving fringes. Microscopic examination shows minimal wrinkling or peeling of baleen's cortical keratin layers, probably due to oil repelling infiltrated water. Combined results cast doubt on fears of baleen fouling by oil; filter porosity is not appreciably affected, but oil ingestion risks remain. Particle capture studies suggest potentially greater danger to mysticetes from plastic pollution than oil.
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Marine amniotes, a polyphyletic group, provide an excellent opportunity for studying convergent evolution. Their sense of smell tends to degenerate, but this process has not been explored by comparing fully aquatic species with their amphibious relatives in an evolutionary context. Here, we sequenced the genomes of fully aquatic and amphibious sea snakes and identified repertoires of chemosensory receptor genes involved in olfaction. Snakes possess large numbers of the olfactory receptor (OR) genes and the type-2 vomeronasal receptor (V2R) genes, and expression profiling in the olfactory tissues suggests that snakes use the ORs in the main olfactory system (MOS) and the V2Rs in the vomeronasal system (VNS). The number of OR genes has decreased in sea snakes, and fully aquatic species lost MOS which is responsible for detecting airborne odours. By contrast, sea snakes including fully aquatic species retain a number of V2R genes and a well-developed VNS for smelling underwater. This study suggests that the sense of smell also degenerated in sea snakes, particularly in fully aquatic species, but their residual olfactory capability is distinct from that of other fully aquatic amniotes. Amphibious species show an intermediate status between terrestrial and fully aquatic snakes, implying their importance in understanding the process of aquatic adaptation.
Chapter
Sensory receptors are specialized cells for transducing information from an animal’s environment into nerve impulses that are transmitted to the central nervous system for processing and integration to detect external variables and initiate responses that enhance survival. Each type of receptor has its own sensory modality such as photoreception (vision), mechanoreception (hearing, pressure, vibration, orientation, and acceleration), chemoreception (taste and smell), thermoreception (temperature), electroreception (electric field), and magnetoreception (magnetic field), although not all receptor types are present in every species, and some are more highly developed (i.e., provide greater acuity) than others. Although marine mammals evolved from terrestrial ancestors, the propagation and reception of light and sound in air and water are so different that these sensory systems have been modified for either a fully aquatic (Cetacea and Sirenia) or amphibious (pinnipeds and sea otters) lifestyle. Specialized tactile hairs (vibrissae) in some marine mammals, tactile sensitivity in the forepaws of sea otters, and electroreception in at least one species of Cetacea provide additional sensory information under disphotic (twilight) or aphotic (no solar light) conditions, which characterize most of the marine environment and some freshwater habitats. In contrast, chemosensory (olfaction and gustation) ability shows a convergent, evolutionary reduction associated with the transition from a terrestrial to aquatic life. Finally, emerging evidence indicates a magnetic sensory ability in Cetacea and pinnipeds for orientation and navigation during individual dives and long-distance migrations.
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The cetacean visual system is a product of selection pressures favoring underwater vision, yet relatively little is known about it across taxa. Previous studies report several mutations in the opsin genetic sequence in cetaceans, suggesting the evolutionary complete or partial loss of retinal cone photoreceptor function in mysticete and odontocete lineages, respectively. Despite this, limited anatomical evidence suggests cone structures are partially maintained but with absent outer and inner segments in the bowhead retina. The functional consequence and anatomical distributions associated with these unique cone morphologies remain unclear. The current study further investigates the morphology and distribution of cone photoreceptors in the bowhead whale and beluga retina and evaluates the potential functional capacity of these cells’ alternative to photoreception. Refined histological and advanced microscopic techniques revealed two additional cone morphologies in the bowhead and beluga retina that have not been previously described. Two proteins involved in magnetosensation were present in these cone structures suggesting the possibility for an alternative functional role in responding to changes in geomagnetic fields. These findings highlight a revised understanding of the unique evolution of cone and gross retinal anatomy in cetaceans, and provide prefatory evidence of potential functional re‐assignment of these cells. This article is protected by copyright. All rights reserved.
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In a species of baleen whale, we identify olfactory epithelium that suggests a functional sense of smell and document the ontogeny of the surrounding olfactory anatomy. Whales must surface to breathe, thereby providing an opportunity to detect airborne odorants. Although many toothed whales (odontocetes) lack olfactory anatomy, baleen whales (mysticetes) have retained theirs. Here, we investigate fetal and postnatal specimens of bowhead whales (Balaena mysticetus). Computed tomography (CT) reveals the presence of nasal passages and nasal chambers with simple ethmoturbinates through ontogeny. Additionally, we describe the dorsal nasal meatuses and olfactory bulb chambers. The cribriform plate has foramina that communicate with the nasal chambers. We show this anatomy within the context of the whole prenatal and postnatal skull. We document the tunnel for the ethmoidal nerve (ethmoid foramen) and the rostrolateral recess of the nasal chamber, which appears postnatally. Bilateral symmetry was apparent in the postnatal nasal chambers. No such symmetry was found prenatally, possibly due to tissue deformation. No nasal air sacs were found in fetal development. Olfactory epithelium, identified histologically, covers at least part of the ethmoturbinates. We identify olfactory epithelium using six explicit criteria of mammalian olfactory epithelium. Immunohistochemistry revealed the presence of olfactory marker protein (OMP), which is only found in mature olfactory sensory neurons. Although it seems that these neurons are scarce in bowhead whales compared to typical terrestrial mammals, our results suggest that bowhead whales have a functional sense of smell, which they may use to find prey.
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For many marine tetrapods, vision is important for finding food and navigating underwater, and eye size has increased to improve the capture of light in dim ocean depths. Odontocete whales, in contrast, rely instead on echolocation for navigation and prey capture. We tested whether the evolution of echolocation has influenced the orbit size, a proxy for eye size, and examined how orbit size evolved over time. We also assessed variation in orbit size amongst whales and tested how body size, diving ability, sound production, foraging habitat, and prey capture strategy influenced the orbit size using phylogenetic independent contrasts and phylogenetic ANOVAs. Using measurements of orbit length and bizygomatic width, we calculated proportional orbit size for 70 extant and 29 extinct whale taxa, with an emphasis on Odontoceti. We then performed ancestral character state reconstruction on a time‐calibrated composite phylogeny. Our analysis revealed that there was no shift in proportional orbit size from archaeocetes through stem odontocetes, indicating that the evolution of echolocation did not influence the orbit size. Proportional orbit size increased in Ziphiidae, Phocoenidae, and Cephalorhynchus. Proportional orbit size decreased in Balaenidae, Physeteridae, Platanistidae, and Lipotidae. Body size, diving ability, foraging environment, and prey capture strategy had a significant influence on orbit size, but only without phylogenetic correction. An increase in orbit size is associated with deep diving behavior in beaked whales, while progenesis and retention of juvenile features into adulthood explain the pattern observed in Phocoenidae and Cephalorhynchus. Decrease in proportional orbit size is associated with adaptation toward murky freshwater environments in odontocetes and skim feeding in balaenids. Our study reveals that the evolution of echolocation had little effect on orbit size, which is variable in whales, and that adaptation for different feeding modes and habitat explains some of this variance. Ancestral character state reconstruction of orbit size shows that orbit size was not influenced by the evolution of echolocation in odontocetes. However some lineages show increases in orbit size consistent with deep‐diving behavior and paedomorphosis, while other lineages show decreases in orbit size, consistent with adaptation to freshwater habitats.
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The stem odontocete Agorophius pygmaeus (Ashley Formation, lower Oligocene, South Carolina; 29.0–26.57 Ma) has been a critical point of comparison for studies of early neocete evolution owing to its early discovery as well as its transitional anatomy relative to archaeocete whales and modern odontocetes. Some time during the late nineteenth century the holotype skull went missing and has never been relocated; supplementary reference specimens have since been recently referred to the species from the Ashley Formation and the overlying Chandler Bridge Formation (upper Oligocene; 24.7–23.5). New crania referable to Agorophius sp. are identifiable to the genus based on several features of the intertemporal region. Furthermore, all published specimens from the Chandler Bridge Formation consistently share larger absolute size and a proportionally shorter exposure of the parietal in the skull roof than specimens from the Ashley Formation (including the holotype). Furthermore, these specimens include well-preserved ethmoid labyrinths and cribriform plates, indicating that Agorophius primitively retained a strong olfactory sense. These new crania suggest that at least two species of Agorophius are present in the Oligocene of South Carolina, revealing a somewhat more complicated taxonomic perspective.
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The annual migration of bowhead whales (Balaena mysticetus) past Barrow, Alaska, has provided subsistence hunting to Iñupiat for centuries. Bowheads recurrently feed on aggregations of zooplankton prey near Barrow in autumn. The mechanisms that form these aggregations, and the associations between whales and oceanography, were investigated using field sampling, retrospective analysis, and traditional knowledge interviews. Oceanographic and aerial surveys were conducted near Barrow during August and September in 2005 and 2006. Multiple water masses were observed, and close coupling between water mass type and biological characteristics was noted. Short-term variability in hydrography was associated with changes in wind speed and direction that profoundly affected plankton taxonomic composition. Aggregations of ca. 50-100 bowhead whales were observed in early September of both years at locations consistent with traditional knowledge. Retrospective analyses of records for 1984-2004 also showed that annual aggregations of whales near Barrow were associated with wind speed and direction. Euphausiids and copepods appear to be upwelled onto the Beaufort Sea shelf during E or SE winds. A favorable feeding environment is produced when these plankton are retained and concentrated on the shelf by the prevailing westward Beaufort Sea shelf currents that converge with the Alaska Coastal Current flowing to the northeast along the eastern edge of Barrow Canyon.
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Over the past 55-60 million years cetacean (dolphin, whale, and porpoise) brains have become hyperexpanded so that modern cetacean encephalization levels are second only to modern humans. At the same time, brain expansion proceeded along very different lines than in other large-brained mammals so that substantial differences between modern cetacean brains and other mammalian brains exist at every level of brain organization. Perhaps the most profound difference between cetacean and other mammalian brains is in the architecture of the neocortex. Cetaceans possess a unique underlying neocortical organizational scheme that is particularly intriguing in light of the fact that cetaceans exhibit cognitive and behavioral complexity at least on a par with our closest phylogenetic relatives, the great apes. The neurobiological complexity underlying these cognitive capacities may involve the extreme multiplication of vertical structural units in the cetacean neocortex.
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Antarctic procellariiform seabirds are known for their well-developed sense of smell, yet few behavioral experiments have addressed how these birds use olfactory cues to forage at sea. I describe results from controlled, shipboard experiments performed in Antarctic waters near Elephant Island. Birds were presented with plain or krill-scented (Euphausia superba) vegetable oil slicks, and their behavioral responses were compared. Krill-scented vegetable oil slicks were highly attractive to some but not all procellariiform species foraging in this area (p < 0.001, G-test). Cape petrels Daption capense and southern giant petrels Macronectes giganteus appeared at krill-scented slicks within 1 min, whereas black-browed albatrosses Diomedea melanophris appeared within 3 min. Cape petrels D, capense showed the strongest attraction: these birds were observed as much as 5 times as frequently at krill-scented slicks as compared to unscented control slicks (p < 0.001, G-test), while storm-petrels (Oceanites oceanicus and Fregetta tropica) and Antarctic Fulmars Fulmarus glacialoides responded in equal numbers to krill-scented and unscented slicks. When considered with respect to previously published findings, these results suggest a greater complexity in the significance of odors to the foraging ecology of different tube-nosed species than has commonly been assumed.
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We compiled age estimates and baleen plate delta C-13 data from 86 bowhead whales (Balaena mysticetus L., 1758). We used previous whale age estimates based on aspartic acid racemization (AAR) and corpora counts to extend the use of VC data for age determination from cycle counting to a modified exponential model using annual baleen growth increments. Our approach used the growth increment data from individual whales in a nonlinear mixed effects model to assess both population-level and whale-specific growth parameters. Although age estimates from baleen-based models become less precise as the whales age, and baleen growth and length near steady state, the growth increment model shows promise in estimating ages of bowhead whales 10-13.5 m long with baleen lengths <250 cm, where other techniques are less precise or the data are scarce. Ages estimated using the growth increment data from such whales ranged from 6.4 to 19.8 years.
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MANY Procellariiform seabirds make their living flying over vast expanses of seemingly featureless ocean waters in search of food. The secret of their success is a mystery, but an ability to hunt by smell has long been suspected1–7. Here we present experimental evidence that Procellariiform seabirds can use a naturally occurring scented compound, dimethyl sulphide, as an orientation cue. Dimethyl sulphide has been studied intensely for its role in regulating global climate8–11 and is produced by phytoplankton in response to zooplankton grazing12. Zooplankton, including Antarctic krill (Euphamia super ha)13, are in turn eaten by seabirds and other animals14. Results from controlled behavioural experiments performed at sea show that many Procellariiforms can detect dimethyl sulphide, and that some species (for example, storm petrels) are highly attracted to it. To our knowledge, this constitutes the first evidence that dimethyl sulphide is part of the natural olfactory landscape overlying the southern oceans.
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Much of the potential of sensory information for understanding primate feeding has been ignored because the subject is usually approached from a nutritional perspective rather than a sensory one. However, nutrients are abstract constructs of modern science, so how can we expect primates to know what they are? To argue that a foraging primate is avoiding fiber or searching for a particular nutrient class such as protein, we have to establish a sensory link to these abstract food components. This review synthesizes widely scattered information on the sensory ecology of primates and asks how the senses might convey information on food location, abundance, and quality. Primates receive a barrage of sensory inputs, which help them make efficient feeding decisions about food distributed in time and space. We do not treat these senses in a traditional manner, but divide them into those that receive input from outside the animal (external senses) and from inside the digestive system (internal senses). We treat less completely some areas that have been reviewed in past issues of Evolutionary Anthropology, such as color vision,1 taste,2 and food physics.3.
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The large brain of modern cetaceans has engendered much hypothesizing about both the intelligence of cetaceans (dolphins, whales, and porpoises) and the factors related to the evolution of such large brains. Despite much interest in cetacean brain evolution, until recently there have been few estimates of brain mass and/or brain–body weight ratios in fossil cetaceans. In the present study, computed tomography (CT) was used to visualize and estimate endocranial volume, as well as to calculate level of encephalization, for two fully aquatic mid-late Eocene archaeocete species, Dorudon atrox and Zygorhiza kochii. The specific objective was to address more accurately and more conclusively the question of whether relative brain size in fully aquatic archaeocetes was greater than that of their hypothesized sister taxon Mesonychia. The findings suggest that there was no increase in encephalization between Mesonychia and these archaeocete species. Peer Reviewed http://deepblue.lib.umich.edu/bitstream/2027.42/44975/1/10914_2004_Article_223701.pdf
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Chemosensory receptors are essential for the survival of organisms that range from bacteria to mammals. Recent studies have shown that the numbers of functional chemosensory receptor genes and pseudogenes vary enormously among the genomes of different animal species. Although much of the variation can be explained by the adaptation of organisms to different environments, it has become clear that a substantial portion is generated by genomic drift, a random process of gene duplication and deletion. Genomic drift also generates a substantial amount of copy-number variation in chemosensory receptor genes within species. It seems that mutation by gene duplication and inactivation has important roles in both the adaptive and non-adaptive evolution of chemosensation.
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Olfactory receptor (OR) genes constitute the molecular basis for the sense of smell and are encoded by the largest gene family in mammalian genomes. Previous studies suggested that the proportion of pseudogenes in the OR gene family is significantly larger in humans than in other apes and significantly larger in apes than in the mouse. To investigate the process of degeneration of the olfactory repertoire in primates, we estimated the proportion of OR pseudogenes in 19 primate species by surveying randomly chosen subsets of 100 OR genes from each species. We find that apes, Old World monkeys and one New World monkey, the howler monkey, have a significantly higher proportion of OR pseudogenes than do other New World monkeys or the lemur (a prosimian). Strikingly, the howler monkey is also the only New World monkey to possess full trichromatic vision, along with Old World monkeys and apes. Our findings suggest that the deterioration of the olfactory repertoire occurred concomitant with the acquisition of full trichromatic color vision in primates.
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Olfaction, which is an important physiological function for the survival of mammals, is controlled by a large multigene family of olfactory receptor (OR) genes. Fishes also have this gene family, but the number of genes is known to be substantially smaller than in mammals. To understand the evolutionary dynamics of OR genes, we conducted a phylogenetic analysis of all functional genes identified from the genome sequences of zebrafish, pufferfish, frogs, chickens, humans, and mice. The results suggested that the most recent common ancestor between fishes and tetrapods had at least nine ancestral OR genes, and all OR genes identified were classified into nine groups, each of which originated from one ancestral gene. Eight of the nine group genes are still observed in current fish species, whereas only two group genes were found from mammalian genomes, showing that the OR gene family in fishes is much more diverse than in mammals. In mammals, however, one group of genes, gamma, expanded enormously, containing approximately 90% of the entire gene family. Interestingly, the gene groups observed in mammals or birds are nearly absent in fishes. The OR gene repertoire in frogs is as diverse as that in fishes, but the expansion of group gamma genes also occurred, indicating that the frog OR gene family has both mammal- and fish-like characters. All of these observations can be explained by the environmental change that organisms have experienced from the time of the common ancestor of all vertebrates to the present.
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An olfactory receptor (OR) multigene family is responsible for the well-developed sense of smell possessed by terrestrial tetrapods. Mammalian OR genes had diverged greatly in the terrestrial environment after the fish-tetrapod split, indicating their importance to land habitation. In this study, we analysed OR genes of marine tetrapods (minke whale Balaenoptera acutorostrata, dwarf sperm whale Kogia sima, Dall's porpoise Phocoenoides dalli, Steller's sea lion Eumetopias jubatus and loggerhead sea turtle Caretta caretta) and revealed that the pseudogene proportions of OR gene repertoires in whales were significantly higher than those in their terrestrial relative cattle and also in sea lion and sea turtle. On the other hand, the pseudogene proportion of OR sequences in sea lion was not significantly higher compared with that in their terrestrial relative (dog). It indicates that secondary perfectly adapted marine vertebrates (cetaceans) have lost large amount of their OR genes, whereas secondary-semi-adapted marine vertebrates (sea lions and sea turtles) still have maintained their OR genes, reflecting the importance of terrestrial environment for these animals.
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Chapter
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Chapter
Organisms living today are grouped together taxonomically because they are similar to each other and different from others. How similar organisms are within a group and how different the group is from other groups depends on the broader context of similarities and differences uniting and distinguishing groups. The rank to which a group is assigned depends in part on similarities and differences, but also on what we know about evolutionary history. Extant whales (order Cetacea) have long been known to be mammals because they share with other mammals such basic distinguishing characteristics as endothermy, lactation, large brains, and a high level of activity. Living cetaceans share, in addition, a suite of special characteristics related to life in water that distinguish them from land mammals: These include large body size, a reduced and simplified dentition, an audition-dominated sensory and communication system, a hydrodynamically streamlined body form with a muscular propulsive tail, and of course many ancillary anatomical, behavioral, and physiological differences.
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Smells are surer than sounds and sights to make your heart-strings crack.—Rudyard KiplingSo begins this thorough compendium of current knowledge of human chemosensation.While clearly the best work available on the topic, it suffers the inevitable shortcomings of such collections: with each chapter by a different author, there is a certain disjointedness and overlapping. The editors have overcome this to a degree by organizing the book into seven parts: "Neural Basis," "Psychophysical Integration," "Chemosensory Regulation of Behavior," "Clinical Problems," "Transport Disorders," "Sensorineural Disorders," and "Systemic Conditions."With the notable absence of Robert Henkin, the authors include the gurus of chemosensation. Overall, the work represents the best scientific writing in the field.Not that the volume is without problems. The chapter on depression and the chemical senses is years out of date, referring to Diagnostic and Statistical Manual of Mental Disorders-III criteria (1980) rather than the DSM-III-R (1987).
Book
Approaching intelligence as a biological phenomenon, the author has developed some unique and perhaps controversial, theories about the nature of intelligence, based on the evolution of the 400 million year record of the brain cavities of vertebrate fossils. The book presents the full scope of the organic evolution of the vertebrate brain, beginning with the earliest endocasts from late Silurian and early Devonian times, up to the evolution of the hominids and, most recently, modern man about 250,000 yr ago. The author examines such things as the trend towards an increase in relative brain size and its relevancy to intelligence as an evolving behavioral capacity; the evolution of cognitive capacities for representing reality, which is treated as a necessary consequence of neural organization; and the selection pressures associated with the major evolutionary transitions (from water to land, to the air, to nocturnal and fossorial niches, and finally to the elaborate social worlds,) delineating their significance to the brain's development.
Chapter
This chapter discusses the physiology and behavioral responses of aquatic birds to chemical stimulants. It presents comparisons of aquatic versus terrestrial chemical sensations in aquatic birds. It focuses on avian olfaction, homing and foraging by olfactory cues, avian chemesthesis, and avian gustation. It also examines evolutionary changes in avian chemical senses using fossil records of basal ornithurines and extinct Pelecaniformes, and comparative analysis of extant species of Anseriformes, Pelecaniformes, Procellariformes, Gaviiformes, Sphenisciformes, Charadriiformes, and Podicipediformes.
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The manner of operation of the mysticete olfactory apparatus is described and its source of activation is indicated.
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The underwater existence of marine mammals has encouraged a variety of special biophysical adaptations to their environment. Their sensory and communication systems reflect the transmission properties of sea water. For example, vision is keen in spectra that penetrate water best, vocalization is broadband and used at the frequencies that appear to fit their activities best—the differences in sensory use match the intriguing variety of behavior observed for each species. To date most of the observations of animal interactions with their marine environment have dealt with sound. There has been some work on vision and studies are underway to determine animal sensitivities to hydrodynamic pressure, chemical traces and magnetic fields. The species that have been recorded to date are listed and vocalizations are generally compared. Methods for observation of sensory mechanisms are noted along with a discussion of other aspects of marine mammal biophysics including vibrissal sensation and the biophysics of movement in a fluid environment.
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Serial sections of 13 embryos and fetuses of the harbor porpoise from 10 mm crown-rump length up to 167 mm total length were studied. Unlike the adult animals, ontogenetic stages of 18–27 mm crown-rump length still show a typical mammalian olfactory bulb. The olfactory bulb primordium is penetrated by olfactory nerve fibers, the latter passing through the cribriform plate. However, the olfactory bulb anlage is gradually reduced in later stages, its placodal component being largely uncoupled from the telencephalon. As a ganglionlike structure, the remains of the placodal component stay in contact with the nasal septum and mucosa via thin bundles of nerve fibers. The ganglion and plexus can be traced within the meninges until the adult stage of the porpoise. There is strong evidence that they represent the material of the terminalis system, which cannot be distinguished from the olfactory system in earlier stages. A vomeronasal organ could not be detected in the embryonal and fetal material investigated.
Article
There have been very few studies of brain size and encephalization in cetaceans and essentially none that have made direct quantitative comparisons of cetaceans and another mammalian group using large normative samples. In the present study two different measures of encephalization were calculated and used to rank and compare 21 odontocete species and 60 anthropoid primate species. Comparisons were made both within and between the two groups. Results show that the encephalization level of Homo sapiens is still extraordinary relative to that of nonhuman species. Nevertheless, a subset of delphinid odontocetes are significantly more highly encephalized than the most highly encephalized anthropoid primates and narrow the gap in encephalization between humans and nonhumans substantially. These findings may have implications for comparative models of the relative importance of brain size versus brain organization for the evolution of intelligence.
Article
The sense of smell relies on the diversity of olfactory receptor (OR) repertoires in vertebrates. It has been hypothesized that different types of ORs are required in terrestrial and marine environments. Here we show that viviparous sea snakes, which do not rely on a terrestrial environment, have significantly lost ORs compared with their terrestrial relatives, supporting the hypothesis. On the other hand, oviparous sea snakes, which rely on a terrestrial environment for laying eggs, still maintain their ORs, reflecting the importance of the terrestrial environment for them. Furthermore, we found one Colubroidea snake (including sea snakes and their terrestrial relatives)-specific OR subfamily which had diverged widely during snake evolution after the blind snake-Colubroidea snake split. Interestingly, no pseudogenes are included in this subfamily in sea snakes, and this subfamily seems to have been expanding rapidly even in an underwater environment. These findings suggest that the Colubroidea-specific ORs detect nonvolatile odorants.