Sensory Evolution on the Threshold

Sensory Evolution on the Threshold: Adaptations in Secondarily Aquatic Vertebrates

J. G. M. Thewissen
Sirpa Nummela
Copyright Date: 2008
Edition: 1
Pages: 358
https://www.jstor.org/stable/10.1525/j.ctt1pppx4
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  • Book Info
    Sensory Evolution on the Threshold
    Book Description:

    From crocodiles and penguins to seals and whales, this comprehensive and authoritative synthesis explores the function and evolution of sensory systems in animals whose ancestors lived on land. Together, the contributors explore the dramatic transformation of smell, taste, sight, hearing, balance, mechanoreception, magnetoreception, and electroreception that occurred as lineages of amphibians, reptiles, birds, and mammals returned to aquatic environments. Each chapter integrates data from fields including sensory physiology, anatomy, paleontology, and neurobiology. A one-stop source for information on the sense organs of secondarily aquatic tetrapods,Sensory Evolution on the Thresholdsheds new light on both the evolution of aquatic vertebrates and the sensory biology of their astonishing transition.

    eISBN: 978-0-520-93412-2
    Subjects: Zoology

Table of Contents

  1. Front Matter
    (pp. i-iv)
  2. Table of Contents
    (pp. v-vi)
  3. CONTRIBUTORS
    (pp. vii-viii)
  4. 1 Introduction: ON BECOMING AQUATIC
    (pp. 1-26)
    J. G. M. Thewissen and Sirpa Nummela

    Vertebrate life became terrestrial about 370 million years ago when a lobe-finned fish evolved into the giant-salamander-like shape of a labyrinthodont amphibian. The transition is well documented in the fossil record, and important discoveries continue to fill out its details. Over the eons subsequent to the water-to-land transition, vertebrates became more and more independent from water. The new land vertebrates are called tetrapods, a group that includes modern amphibians, reptiles, birds, and mammals. The term refers to their extremities: the replacement of four paired fins by four paired legs. Amphibians still return to the water to avoid dehydration of their...

  5. Chemical Senses
    • 2 The Physics and Biology of Olfaction and Taste
      (pp. 29-34)
      Simo Hemilä and Tom Reuter

      Traditionally, the chemical senses include olfaction and gustation: olfaction (smell) reports on gaseous substances carried by air over long distances, and gustation (taste) provides information about food material already in the mouth. However, in recent times behavioral, physiological, histological, and molecular studies have increased our understanding of vertebrate chemoreception, and four chemical senses are recognized by some authors, reflecting the diversity in function and physiology (Dulac and Axel, 1995; Eisthen, 1997; Zufall and Munger, 2001; Mombaerts, 2004; Breer et al., 2005). For the purpose of this volume, three chemical senses are important: olfaction, vomeronasal sense, and gustation (Fig. 7.1 in...

    • 3 The Chemical Stimulus and Its Detection
      (pp. 35-42)
      Heather L. Eisthen and Kurt Schwenk

      One of the most difficult aspects of studying the chemical senses is that researchers do not know which properties of the stimulus are relevant for detection and perception. In this article, we explain what we do and do not know about the features of chemical stimuli, the ways in which these features are detected and coded by chemosensory organs and the central nervous system of tetrapod vertebrates, and the characteristics of a stimulus that might make it likely to stimulate a particular chemosensory organ.

      Before sensory stimuli can affect an animal’s physiology or behavior (i.e., be “perceived”), they have to...

    • 4 Comparative Anatomy and Physiology of Chemical Senses in Amphibians
      (pp. 43-64)
      John O. Reiss and Heather L. Eisthen

      In this chapter, we first introduce the chemosensory systems of tetrapods, then focus on their structure and function in amphibians. Tetrapods possess three major chemosensory systems, the olfactory, vomeronasal, and gustatory (taste) systems. These are defined anatomically. The olfactory epithelium is found in the nasal cavity, and the axons of the olfactory receptor (OR) neurons project to the olfactory bulb at the rostral pole of the telencephalon. Most tetrapods also possess a vomeronasal system, an accessory olfactory system, the sensory epithelium of which is usually located in an organ that is distinct from the main nasal cavity. The axons of...

    • 5 Comparative Anatomy and Physiology of Chemical Senses in Nonavian Aquatic Reptiles
      (pp. 65-82)
      Kurt Schwenk

      The nonavian reptiles are an exceptionally diverse group of tetrapods that have radiated into a variety of habitats, including marine and freshwater environments. While most aquatic reptiles retain strong ties to the land, some species are among the most fully aquatic of any tetrapod, including, for example, the marine turtles (Cheloniidae) and pelagic sea snakes (Elapidae). Indeed, some species of seasnake have forsaken their connection to the land entirely, not even returning to give birth. They thus achieve a level of adaptive commitment to the water comparable to those most aquatic of tetrapods, the Cetacea. Nonetheless, only about 8% (approximately...

    • 6 Comparative Anatomy and Physiology of Chemical Senses in Aquatic Birds
      (pp. 83-94)
      Tobin L. Hieronymus

      Birds are incredibly speciose in the extant time plane, comprising nearly two-thirds of all living sauropsid species. Although not as morphologically diverse as their combined reptilian relatives, they are ecologically diverse, occupying habitats ranging from polar oceans to equatorial deserts. Within this ecological diversity, a number of avian taxa swim or forage facultatively in shallow-water settings and are thus aquatic in some sense. However, one of the most concerted bodies of data on avian chemical sensation pertains to the procellariiform seabirds (petrels, albatross, and shearwaters; see Fig. 1.6 and Table 1.3 in this volume for a brief discussion of bird...

    • 7 Comparative Anatomy and Physiology of Chemical Senses in Aquatic Mammals
      (pp. 95-110)
      Henry Pihlström

      Among Recent mammals, about 200 species can reasonably be considered aquatic or semiaquatic, that is, they regularly forage and/or seek refuge in water and have some specific morphological or physiological adaptations for aquatic living. From a sensory biology point of view, life in water places certain restrictions on mammals. Vision, hearing, and the tactile senses all function somewhat differently in water than they do in air, and the same is true for the three main chemical senses: olfaction, vomeronasal sense, and taste.

      The olfactory receptor gene family is the largest identified gene family in mammals(Sullivan, 2002). This indicates the importance...

  6. Vision
    • 8 The Physics of Light in Air and Water
      (pp. 113-120)
      Ronald H. H. Kröger

      Light is electromagnetic radiation in a frequency range from about 3 X 1011Hz to about 3.4 X 1016Hz, including the infrared and ultraviolet regions (Hecht, 2002). The electromagnetic waves that make up light are not continuous, since light comes in tiny wave packages—quanta of light called photons. Light is thus not a continuous stream of waves that are high or low in amplitude (intensity). Instead, light is a rain of photons that may be a downpour (bright light) or a trickle (dim light). This characteristic of light is especially important under low-light conditions, when vision is dependent...

    • 9 Comparative Anatomy and Physiology of Vision in Aquatic Tetrapods
      (pp. 121-148)
      Ronald H. H. Kröger and Gadi Katzir

      Vertebrate eyes are of the simple or camera type, unlike the complex or faceted eyes of most arthropods (Land and Nilsson, 2002). In camera eyes, the optical system creates an inverted image of the environment. That image is encoded and preprocessed by the retina before visual information is transmitted to the brain in highly condensed form. Here we present the optical elements of a typical tetrapod eye and discuss the functional differences of vision in air and water, with examples from secondarily aquatic reptiles and birds. For further reading the reader is referred to standard textbooks (e.g., Davson, 1990; Kaufman...

    • 10 Structure and Function of the Retina in Aquatic Tetrapods
      (pp. 149-172)
      Tom Reuter and Leo Peichl

      Kröger and Katzir (chapter 9 in this volume) have described the optical apparatus of the eye and its adaptations to function in water. Unlike these peripheral structures, no structural changes in the anatomy or histology of the retina are necessary for underwater vision at shallow depths, where the illumination usually is relatively bright and spectrally broad. Thus the retinae of ducks, and freshwater and sea turtles are comparable to those of terrestrial birds and tortoises (Granda and Dvorak, 1977; Zueva, 1982; Jane and Bowmaker, 1988; Bowmaker et al., 1997; Bartol and Musick, 2001; Loew and Govardovskii, 2001). The vertebrate retina...

  7. Hearing
    • 11 The Physics of Sound in Air and Water
      (pp. 175-182)
      Sirpa Nummela and J. G. M. Thewissen

      A vibrating sound source sets molecules in the transmitting medium, air or water, into motion, and these movements of the molecules lead to deviations from the static pressure. The deviations then propagate as longitudinal waves in the medium and are called sound waves. Sound waves received by the ear cause specialized neurons to fire, and these neurons may respond to one of two properties of sound. First, actual displacement of the molecules that transmit the sounds are detected by the ears of some vertebrates, and these ears are called displacement ears. In nearly all tetrapods, however, the ears are sensitive...

    • 12 Comparative Anatomy and Function of Hearing in Aquatic Amphibians, Reptiles, and Birds
      (pp. 183-210)
      Thomas Hetherington

      This chapter describes patterns of evolutionary change in the auditory systems of amphibian, reptilian, and avian lineages that have returned to an aquatic lifestyle. It starts with a description of the basic features of the ancestral terrestrial auditory system, discusses the functional implications of placing such a system underwater, and moves on to descriptions of the auditory systems of different amphibious and aquatic tetrapod lineages. There are large gaps in our functional understanding of how the auditory systems of many aquatic tetrapods actually work underwater, but nonetheless some general patterns can still be discerned.

      Outer ear structures function to collect...

    • 13 Hearing in Aquatic Mammals
      (pp. 211-224)
      Sirpa Nummela

      The mammalian auditory system is a complex biological structure of well-understood function and with parts that easily fossilize, thus providing exciting opportunities to study evolution. Mammals have inherited their hearing mechanism from mammal-like reptiles, synapsids. The organization of the ear is explained by Hetherington (chapter 12 in this volume) and Nummela and Thewissen (Fig. 11.1 in this volume). Primitively, mammals have an outer ear pinna, three small bones in their middle ear, and, in therian mammals, an elongated and coiled cochlea. The evolution of the auditory system in synapsids is well documented by fossils, as well as by embryology: bones...

  8. Balance
    • 14 The Physics and Physiology of Balance
      (pp. 227-232)
      Justin S. Sipla and Fred Spoor

      The sensory organ of balance, or vestibular system, is located in the inner ear of all vertebrates and provides an organism with accurate information on its body movements. This information is transmitted to the brain for participation in muscular reflex arcs that function to stabilize the trunk, head, and visual field during postural and locomotor activities. The focus in this brief review is on part of the organ of balance, the semicircular canal system, because it is the comparative, functional, and evolutionary morphology of this part that is increasingly well understood.

      The vestibular system was one of the first sensory...

    • 15 Comparative and Functional Anatomy of Balance in Aquatic Reptiles and Birds
      (pp. 233-256)
      Justin A. Georgi and Justin S. Sipla

      The inner ear of vertebrates, which houses all of the vestibular endorgans responsible for the sensation of balance and orientation, is a structure of complex morphology and functional dynamics. The complexity of this system allows for variations in its morphology to affect changes in its functional response, and, in this way, the vestibular system may be fine-tuned to specific sensory demands imposed by an organism’s behavior, including the specifics of locomotor function.

      Accurate perception of balance and orientation is a key factor for successful locomotion. Prior research into the relationship between vestibular morphology and locomotion has uncovered a correlation between...

    • 16 Comparative and Functional Anatomy of Balance in Aquatic Mammals
      (pp. 257-284)
      Fred Spoor and J. G. M. Thewissen

      The first comprehensive comparative study to associate morphological diversity of the mammalian inner ear with particular locomotor behaviors is the seminal two-volume monograph published by Albert Gray in 1907 and 1908. That the otolith and semicircular canal systems of the inner ear are not part of the organ of hearing, but form a separate organ of balance, had been discovered not long before (Breuer, 1874; Brown, 1874; Mach, 1875). Subsequent studies focused on the functional relationship between the semicircular canals and locomotion. These studies used empirical evidence by comparing animals with diverse behaviors, as well as biophysical models of the...

  9. Mechanoreception
    • 17 The Physics and Physiology of Mechanoreception
      (pp. 287-294)
      Guido Dehnhardt and Björn Mauck

      Mechanoreception can be considered as a fundamental sensory modality developed in all animal phyla. In tetrapods it comprises the auditory system (Hetherington, chapter 12 in this volume; Nummela, chapter 13 in this volume), the lateral line system of amphibians (not covered in this section, but see Bleckmann, 1994; Coombs et al., 1989), and somatosensory systems. Generally, the somatosensory system of secondarily aquatic tetrapods can be divided into the spinal system innervating the body surface, deep tissues, and extremities, and the trigeminal system innervating facial areas such as the muzzle of mammals or the beak of birds. In the next chapter,...

    • 18 Mechanoreception in Secondarily Aquatic Vertebrates
      (pp. 295-314)
      Guido Dehnhardt and Björn Mauck

      Although for a long time mechanoreception has been considered as a passive and thus merely receptive sense (Krueger, 1982), this chapter provides evidence that especially secondarily aquatic tetrapods may actively use this sensory modality for the exploration of their environment. Reptiles, birds, and mammals are sensitive to tactile stimulation almost over the entire body surface; however, each class has developed special tactile sense organs the animals can use for actively seeking mechanosensory information. As secondarily aquatic tetrapods often live in environments where visibility is poor, mechanosensory information that might suplement or even subsititute for vision could be of special importance....

  10. Magnetoreception and Electroreception
    • 19 Magnetoreception
      (pp. 317-324)
      Michael H. Hofmann and Lon A. Wilkens

      Unlike the other senses, magnetoreception has been investigated in very few animal species. Although this sense is found from mud bacteria to mammals (e.g., Kirschvink et al., 2001) and even in plants (Galland and Pazur, 2005), it is not clear whether this sensory system is widely used or whether it is present only in some specialized groups. The limited information on the magnetic sense is largely due to the fact that magnetic fields penetrate the body and receptors can be located practically anywhere inside the body. Furthermore, the animal’s response to magnetic fields is usually not immediately apparent and affects...

    • 20 Electroreception
      (pp. 325-332)
      Lon A. Wilkens and Michael H. Hofmann

      The electrosense is a remarkable but fundamental sensory modality that appeared early in vertebrate evolution as a mechanism with both near-field and far-field applications in the conductive aquatic environment. In fish, where the electrosense is widely represented, prey and predators are detected at close range in response to the direct current (DC) and low-frequency alternating current electric fields they generate, in contrast to the longdistance navigational cues detected as a consequence of the Earth’s magnetic field and electrochemical potentials. These same signals are available to aquatic tetrapods, although electrosensory taxa are limited to the more aquatic urodele amphibians, caecilians, the...

    • 21 Toward an Integrative Approach
      (pp. 333-340)
      J. G. M. Thewissen and Sirpa Nummela

      The senses are an array of intricate organs that are functionally reasonably well understood and of great importance to the animal. During the transition from land to water, the stimuli for most sense organs changed greatly, and the organs had to adapt to the watery environment. Morphological evolution is best studied when selection pressures are high and taxa undergo major changes, and the transition from land to water therefore offers a unique opportunity to evolutionary biologists.

      A variety of unrelated terrestrial tetrapods have entered the water independently (see chapter 1), and changes in their sense organs can thus be compared...

  11. INDEX
    (pp. 341-351)