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At birth, obligatory aquatic mammals must be capable of independent locomotion, surfacing to breathe and maintaining contact with the mother. Precocial development in marine mammals has been described with respect to the importance of respiratory centers in the brain, sensory organs, and the neuromuscular integration of the locomotory system (Buhl and Oelschläger 1988, Oelschläger and Kemp 1998, Rauschmann et al. 2006). Hoyte (1961) found that the cavities of the cochlea, vestibule, and semicircular canals of rabbits were fully grown at birth, whereas the size of the tympanic bulla increased in diameter in the first 22 d of life. However, the systematic representation in previous studies is narrow, and only limited quantitative data on the growth of the middle ear have been reported. Here we present preliminary data on the relative size of the tympanic bulla in comparison to head and body size across a broad spectrum of cetaceans.

We collected two data sets to address this question. Homologous measurements were made on skulls and tympanic bullae from 10 adults and 10 juveniles for Tursiops truncatus (Delphinidae) and Pontoporia blainvillei (Iniidae). In T. truncatus we selected animals that had age estimates based on gingival growth layers, and in P. blainvillei, individuals with known body weights. To reduce the effect of geographic variation, we selected specimens of T. truncatus that were categorized as being from either coastal or intermediate populations ranging from New Jersey to North Carolina. All specimens of P. blainvillei were from the population of the estuary of the Rio de la Plata. In order to consider this question in a broader taxonomic context, we made the same measurements on one adult and one juvenile in 14 species of cetaceans.

Animals were classed as adult or juvenile based on fusion of cranial sutures and the progress of telescoping. We targeted individuals that were listed as juveniles or calves in the museum catalog, which was frequently based on the total length or association with a mother. The specimens (representing six families in Odontoceti and two families in Mysticeti) were from collections at the U.S. National Museum of Natural History (Smithsonian Institution) and the California Academy of Sciences, where we restricted selected specimens to those with complete skulls and known total length measurements. One adult and one juvenile each of the T. truncatus and P. blainvillei specimens were chosen at random to represent each species in the broader taxonomic data set. Statistical analysis was done with SPSS.

Across all samples, we found that the tympanic bulla of juveniles achieved a length and height of nearly adult dimensions, despite their having smaller skulls and bodies. Figures 1 and 2 compare condylobasal length (CBL), tympanic bulla length (TBL) and tympanic bulla height (TBH) of adults and juveniles of Tursiops truncatus and Pontoporia blainvillei, respectively. In both species, TBL and TBH between adults and juveniles were not significantly different, whereas CBL was significantly different (Mann-Whitney U test; see Table 1).

Table 1. Results of Mann-Whitney U tests comparing juveniles and adults of Tursiops truncatus and Pontoporia blainvillei for measurements of the skull and tympanic bulla. Significant differences are denoted by an asterisk (*).
SpeciesMeasurement U n Significance
Tursiops truncatus CBL 020<0.001*
TBL26.50200.076
TBH34.00200.226
Pontoporia blainvillei CBL 019<0.001*
TBL32.50190.307
TBH27.00190.141
image

Figure 1. Means and standard deviations of (a) condylobasal length, (b) tympanic bulla length and (c) tympanic bulla height, for all specimens of Tursiops truncatus. Box represents 25th–75th percentile; inner fences represent 1.5 times value of box. Condylobasal length was significantly different between juveniles and adults whereas measurements of the tympanic bulla were not significantly different between juveniles and adults.

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image

Figure 2. Means and standard deviations of (a) condylobasal length, (b) tympanic bulla length, and (c) tympanic bulla height for all specimens of Pontoporia blainvillei. Condylobasal length was significantly different between juveniles and adults whereas measurements of the tympanic bulla were not significantly different between juveniles and adults.

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In the combined data set, total (body) length (TL) of juvenile specimens ranged from 46% to 81% of adult TL. The CBL ranged from 53% to 93% in juveniles compared to adults, and TBL ranged from 93% to 109% in juveniles compared to adults. Figure 3 presents pairwise comparisons of one juvenile and one adult for each species in this study, indicating that TBL is nearly adult size in juveniles, despite having a shorter CBL.

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Figure 3. Pairwise comparison of tympanic bulla length vs. condylobasal length between one adult and one juvenile of all species in the data set. Legend key: Baac = Balaenoptera acutorostrata; Dele = Delphinapterus leucas; Eugl = Eubalaena glacialis; Glme = Globicephala melas; Grgr = Grampus griseus; Kobr = Kogia breviceps; Meno = Megaptera novaeangliae; Mseu = Mesoplodon europaeus; Oror = Orcinus orca; Phph = Phocoena phocoena; Poda = Phocoenoides dalli; Pnbl = Pontoporia blainvillei; Tutr = Tursiops truncatus; Zica = Ziphius cavirostris.

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Figure 4 is a comparison between the natural log of (a) CBL, (b) TBL, and (c) TBH of adults and juveniles of all species in the data set. The CBL was found to be significantly different between juveniles and adults, whereas no significant difference was found between TBL and TBH for juveniles and adults (Wilcoxon Signed Ranks test; see Table 2).

Table 2. Results of Wilcoxon Signed Ranks Test comparing juveniles and adults in the multi-species data set for measurements of the skull and tympanic bulla. Significant differences are denoted by an asterisk (*).
   n Mean rankSum of ranksSignificance
CBL

Negative ranks

Positive ranks

Ties

Total

0

14

0

14

0

7.50

0

105.00

0.001*
TBL

Negative ranks

Positive ranks

Ties

Total

5

9

0

14

7.70

7.39

38.50

66.50

0.379
TBH

Negative ranks

Positive ranks

Ties

Total

3

10

0

13

8.67

6.50

26.00

65.00

0.173
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Figure 4. Median of the natural log of (a) condylobasal length, (b) tympanic bulla length, and (c) tympanic bulla height, for all species in data set. Tursiops truncatus and Pontoporia blainvillei in these graphs are represented by a single individual chosen at random. Condylobasal length was significantly different between juveniles and adults whereas measurements of the tympanic bulla were not significantly different between juveniles and adults.

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Cetaceans use acoustic signals to orient and communicate. As light penetrates poorly in aquatic environments, a premium is placed on acoustic communication and this increases selective pressure to develop a completely functional organ of hearing at or near the time of birth. Perrin (1975) found that the length of both major components of the tympanoperiotic complex (tympanic bulla and periotic) in juveniles of two delphinid species, Stenella longirostris and S. attenuata, were nearly adult size in spite of smaller skulls and bodies. Our findings agree with those of Perrin (1975) and demonstrate that the phenomenon of precocial development of the tympanic bulla is characteristic across the Cetacea.

Size is an important component of functional morphology, particularly in the geometry of bony auditory components and material composition of associated structures, because these factors determine the vibrational parameters of any structure (Cranford et al. 2008a, b, 2010; Cranford and Krysl 2012). For example, every structure, no matter its complexity, has a family of resonance frequencies at which it will vibrate. These resonance frequencies will be determined by the size, shape, and material properties of the structure.

Selective advantages should accrue to juveniles in aquatic environments that are able to perceive the vocalizations of adults (Evans and Norris 1988, Norris and Evans 1988). Solntseva (2011) noted that unusual adaptations of the middle ears in cetaceans appear at early developmental stages. Similarly, Rauschmann et al. (2006) found the structure of the tympanoperiotic complex in perinatal odontocetes to strongly resemble that of adults, however, they reported only limited quantitative data. In comparison to other mammals, the morphology of the tympanoperiotic complex (TPC) is generally similar among the Cetacea but unique and diagnostic for each species (Kasuya 1973; Oelschläger 1986a, b). The only published data that we found which could plausibly differ from our findings was presented by Bisconti (2001) who reported significant postnatal growth in the posterior process of the periotic in Balaenoptera physalus. However, he did not discuss the functional significance of this growth, and the posterior process is usually considered part of the attachment of the periotic to the skull (Fraser and Purves 1960), and could have different patterns of growth from the tympanic bulla, or even from other parts of the periotic.

The structure of the tympanic bulla across the Cetacea appears to be a lever, with paired fulcra at the “hinge-like” pedicles (Fleischer 1980) and the resistance force contributed by the large mass of the involucrum (Mead and Fordyce 2009). The malleus is fused to the tympanic bulla in cetaceans, allowing motions of the bulla to be transferred to the ossicular chain and into the cochlea. The fact that the overall structure of this lever architecture has remained relatively constant throughout the last 45 million years of cetacean evolution indicates that it was an early and essential adaptation for underwater sound reception and hearing (Kellogg 1936, Lancaster 1990).

Our data demonstrate a pattern of negatively allometric growth of the tympanic bullae compared to the skulls, across a broad range of cetacean taxa. Although this pattern of growth has been reported in the periotic structures of delphinids (Perrin 1975) and a few noncetacean mammals (Hoyte 1961; Ekdale 2010, 2011) we know of no relevant studies to quantify this in the tympanic bullae or homologous structures in other mammals. Other sources of variation including sexual dimorphism, geographic variation, or individual variation could not be distinguished from ontogenetic variation given the sampling method of the broad taxonomic data set. However, the consistency of the trend across taxa and in the species in which multiple individuals were measured strongly supports the conclusion of precocial development. In consideration of the unique function of the tympanic bulla in the obligatory aquatic cetaceans, we interpret this as evidence for precocial development of auditory function in the Cetacea, and that it is a general condition across the cetacean families.

Our results confirm at least two significant implications. One of the major functional features of the tympanic bulla, its size, achieves the adult condition in juvenile animals which underscores the essential nature of fully functional hearing in the survival of cetaceans early in life. Furthermore, future studies of otic function in cetaceans need not be restricted to fully adult specimens, which can be an important consideration in light of the scarcity of quality specimens in some species.

Acknowledgments

  1. Top of page
  2. Acknowledgments
  3. Literature Cited

We gratefully acknowledge the access to the collections of the US National Museum of Natural History and the California Academy of Sciences and appreciate the support and assistance of Charles W. Potter, John Ososky, and Maureen Flannery. We appreciate the assistance of Jamie Kneitel with the statistical analysis. James Powell, Kesina Lee, Debbie Duffield, and Joseph Valleri assisted with the collection of the measurements and we were assisted in preparation of figures by Virginia Wyatt. Support for this work was provided by grants to Ted W. Cranford of San Diego State University (Grant numbers N00244-10-1-0054) by Dr. Frank Stone and CAPT Ernie Young (USN Ret.) at the Chief of Naval Operations, Environmental Readiness Division [CNO45], as well as Dr. Curtis Collins and CDR John Joseph (USN Ret.) from the Naval Postgraduate School. The manuscript was improved by feedback from Eric Ekdale and two anonymous reviewers.

Literature Cited

  1. Top of page
  2. Acknowledgments
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