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The Marine Mammal Ear: Specializations for Aquatic Audition and Echolocation

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The Marine Mammal Ear: Specializations for Aquatic Audition and Echolocation 35 The Marine Mammal Ear: Specializations for Aquatic Audition and Echolocation Darlene R. Ketten 1. Introduction analysis is given of generalized cetacean ear anat­ omy emphasizing how unique structures in ceta­ "Marine mammal" is a broad categorization for ceans relate to the ability of a mammalian ear to over 150 species that have one feature in common: hear in water. Specific anatomical differences the ability to function effectively in an aquatic among modern odontocete and mysticete ears environment. They have no single common aqua­ are discussed in relation to their role in species­ tic ancestor and are distributed among four orders specific frequency ranges, which, in turn, are cor­ (see Appendix 1). Each group arose during the related with differences in habitat and feeding Eocene in either the temperate northern Pacific behavior. Lastly, a comparison is made of modern Ocean or in the Tethys Sea, a paleolithic body of and ancestral cetacean cranial features to allow water from which the Mediterranean and middle speculations on the auditory capacity and behavior eastern limnetic basins were formed. Otariids (sea of extinct species. Since Cetacea evolved from lions), odobenids (walrus), and marine fissipeds terrestrial species and many specimens represent (sea otters) developed primarily in the Pacific, intermediate stages in the transition to water, this while the earliest cetacean (whale), sirenian (man­ comparison also provides an opportunity to trace atee and dugong), and phocid (true seal) fossils the progressive refinement of a mammalian audi­ come from regions bordering Tethys Sea remnants tory system from terrestrial through amphibious (Kellogg 1936; Domning 1982; Barnes, Domning, to fully aquatic. and Ray 1985). The level of adaptation to the marine environment varies in marine mammals; 1.1 Adaptive Radiation of Cetacea many are amphibious and only the Cetacea and Sirenia are fully aquatic, unable to move, repro­ Protocetid fossils center on the northern Tethys duce, or feed on land. Structural changes in the Sea. It is likely that cetacean radiations are linked ears of marine mammals parallel their degree of to the tectonic uplift and closure of the Tethys, aquatic adaptation, ranging from minor in amphib­ which generated a warm, productive, shallow sea ious littoral species, such as otters and sea lions, to with abundant food supplies (McKenzie 1970; extreme in the pelagic great whales. Davis 1972; Lipps and Mitchell 1976). Theexploi­ This chapter focuses on the cetacean ear as the tation ofthe Tethys shallows 50 to 60 million years most fully adapted auditory system of marine ago by an amphibious, mesonychid condylarth, a mammals. It first describes peripheral auditory cat-like, hooved carnivore, led to the development anatomy in the two extant suborders of Cetacea, ofthe Archaeoceti from which the two extant lines the Odontoceti (toothed whales, porpoises, and of cetaceans are derived (Fig. 35.1) (Kellogg 1936; dolphins) and Mysticeti (baleen or whalebone Barnes and Mitchell 1978; Fordyce 1980; Ginger­ whales), and then compares these structures with ich et al. 1983). One line, the Odontoceti, has what is known offossil cetacean ears. A functional species in virtually every aquatic habitat, from In: !he Evolutionary Biology o/Hearing. Douglas B. Webster, Richard R. Fay and Arthur N. Popper (eds.), Spnnger-Verlag, 1992, pp 717-750. 718 Darlene R. Ketten PALEOCENE EOCENE OLIGOCENE MIOCENE PLlO'1 PLEISTOCENE· RECENT I I I I~CENEN l<l l;l ~ I ~ ,,"'--:::KO'::'G~IID~A~EI--+-V MESONYCHIDAE _." PHYSETERIDAE \ ~, ~ \\ '...------+---..,......---------:===::<'1 , .<. "' ~, ~<J' ' .... -:;-::":":':=*:;;:=1- , ,_ ~ .".-=-,..J.. \\ AETIOCETIDAE . .. ... , (' ~', t<' ~ ' ......... FIGURE 35.1. Cetacean phylogeny. A theoretical be established reliably. This is the case for the fresh­ phylogenetic tree traces the development of ances­ water, riverine dolphins which appear abruptly as tral and modem families of Cetacea. Extinctions are four distinct lines in the late Miocene and may have indicated by a cross-bar. Dashed lines indicate esti­ evolved in parallel. (Revised version by Barnes and mated links for that family with antecedents. Question Folkens after Barnes, Domning, and Ray 1985; copy­ marks indicate that links with earlier families cannot right Pieter A. Folkens.) estuarine river dolphins to deep-diving, bathy­ water, a dark, dense medium compared to terres­ pelagic whales. There are over 65 recognized trial environments. The physical demands ofwater extant odontocete species, ofdiverse sizes (l to 30 are apparent in virtually every aspect ofodontocete meters) and shapes, and all are efficient, raptorial and mysticete anatomy. Olfaction and vision in carnivores (Leatherwood, Caldwell, and Winn some species are poor compared even to other 1976; Leatherwood et al, 1982; Watkins and Wart­ marine mammals (Dawson 1980; Kastelein, Zwey­ zok 1985). The second line, the Mysticeti, has 11 pfenning, and Spekreijse 1990; Kuznetzov 1990; species, which are typically large, pelagic plankti­ Watkins and Wartzok 1985). It is not surprising, vores (Ridgway 1972; Gaskin 1976). therefore, that sound is believed to be the fun­ Like any mammal, cetaceans are faced with a damental sensory and communication channel in need for locating food sources, navigating, and Cetacea. All odontocetes tested to date echolocate; froding mates. As Archaeocetes entered the ocean, i.e., they "image" their environment by analyzing more ofthese functions had to be accomplished in echoes from a self-generated ultrasonic signal ofup 35. The Marine Mammal Ear 719 to 200 kHz (Kellogg 1959; Norris et al. 1961; 1980; Ridgwayetal. 1981; Thomas, Chun, and Au Pilleri 1983; Kamminga, Engelsma, and Terry 1988; Popov and Supin 1990a, 1990b). Interspe­ 1989). Mysticetes are not believed to echolocate, cies comparisons of audiograms are equivocal but they may use infrasonic frequencies! (Weston since techniques vary widely and reports for even and Black 1965; Watkins et al. 1987; Edds 1988; the same species vary by as much as two octaves Clark 1990; Dahlheim and Ljungblad 1990). Ceta­ (see Popper 1980). Critical ratio and critical band ceans, as a group, therefore evolved abilities to measurements indicate odontocetes are generally exploit both ends ofthe acoustic spectrum and use better than most mammals at detecting signals in the broadest range of acoustic channels of any noise. 2 Critical ratio functions for dolphins paral­ mammalian order. lel those ofhumans but the absolute dolphin ratios are narrower and the critical bands are not a con­ stant factor of the ratio over a wide range of fre­ 2. Sound Production quencies (Johnson 1968; Thomas, Pawloski, and Characteristics and Audition Au 1990). Humans have 24 critical bands which are estimated to be Y3 ofan octave or 2.5 times the 2.1 Audiometric Data critical ratio in the frequency range of speech (Pickles 1982). In Tursiops truncatus (bottlenosed In order to accurately interpret auditory structures dolphin), there are 40 critical bands (Johnson of any species, it is necessary to have some mea­ 1968) which vary between 10 times the critical sure of its sensitivity. For practical and historical ratio at 30 kHz and 8 times the critical ratio at 120 reasons, underwater measures ofauditory sensitiv­ kHz (Moore and Au 1983). ity are available for very few marine mammals Au (1990) found that echolocation performance (Watkins and Wartzok 1985; Thomas, Pawloski, as a function of noise in Tursiops is 6 to 8 dB lower and Au 1990; Awbrey 1990). Consequently, most than that expected from an ideal receiver. Target speculations about cetacean hearing are based on detection thresholds as small as 5 cm at 5 meters inferences from recordings ofemitted sounds or on have been reported, implying a minimal angular psychophysical data from experiments on very few resolution of -0.5°, but the most common range is odontocete species. The available odontocete data 1° to 4° for both horizontal and vertical resolution are extensively reviewed in McCormick etal. (Bullock and Gurevich 1979; Au 1990). Minimal (1980), Popper (1980), Watkins and Watzok intensity discrimination is 1 dB (equal to human) (1985), and Awbrey (1990) and are only briefly and temporal discrimination is approximately 8%of summarized here. At present, there are no direct signal duration (superior to human). Frequency dis­ audiometric data for mysticetes. crimination in Tursiops (0.3 to 1.5% relative dis­ In odontocetes, electrophysiological and behav­ crimination limens) and Phocoena (0.1 to 0.2%) is ioral audiograms indicate best. sensitivity (the superior to human and rivals that of microchiropte­ frequency of a pure tone that can be detected at a ran bats (Grinnell 1963; Simmons 1973; Suk­ lower intensity than all others) varies by spe­ horuchenko 1973; Thompson and Herman 1975; cies from 12 kHz in Orcinus orca (killer whale) Long 1980; Pollak 1980). These data, despite limi­ (Schevill and Watkins, 1966; Hall and Johnson tations in number or consistency of experiments, 1971) to over 100kHz in Phocoena phocoena suggest odontocetes have no single auditory capac­ (harbour porpoise) (Voronov and Stosman 1970; ity better than that of some other animal, but their M~hl and Andersen 1973). The majority ofspecies measured are delphinids with best sensitivities in the 40 to 80 kHz range (Johnson 1967; Bullock et 2The critical band is a measure offrequency discrimina­ al. 1968; Bullock and Ridgway 1972; Ridgway tion based on the ability to detect a signal embedded in
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