Ziphiidae (beaked whales) are a successful family of medium- to large-sized toothed whales. Their extant members perform regular deep dives beyond the photic zone to forage for cephalopods and fish. Conversely, extinct long-snouted stem ziphiids are interpreted as epipelagic predators. However, some aspects of this hypothesis remain unclear due to the lack of clear morphological proxies for recognizing regular deep divers.
We compared the forelimb, neck, and pterygoid sinus system of the fossil
ziphiid
Reconstruction of the neck musculature suggests that
Ziphiidae (beaked whales) are a successful family of medium- to large-sized odontocetes (toothed cetaceans) currently represented by at least 22 extant species in 5 genera (Dalebout et al., 2014). The best-known modern ziphiids perform regular dives to reach foraging grounds up to 3000 m, beyond the photic zone, where they capture cephalopods, crustaceans, and bathypelagic fish via suction (Clarke, 1996; Heyning and Mead, 1996; Hooker and Baird, 1999; Johnson et al., 2004; MacLeod et al., 2003; Minamikawa et al., 2007; Schorr et al., 2014; Tyack et al., 2006).
Accordingly, Ziphiidae share a unique set of morphological, physiological,
and behavioural adaptations allowing them to optimize the travel time to
reach their foraging grounds. First, extant ziphiids travel from the surface
in a vertical position with a slow fluke rate at which the animal is gliding
between each fluking period (Tyack et al., 2006). Furthermore, their
shortened and fused neck stabilizes their head to maintain a streamlined
body during the descent phase (Buchholtz, 2001; Lambert et al., 2013).
Likewise, their reduced flipper tucks in an indentation along the body wall
to decrease drag forces (Mead et al., 1982). Rommel et al. (2006)
have noticed that
Unlike extant beaked whales, some of the long-snouted stem ziphiids
(
Nonetheless, some aspects of this hypothesis remain unclear. Concerning the
humerus morphology of
Furthermore, stem ziphiids share with their modern representatives the presence of an enlarged HF and the reduction of the bony lamina laterally limiting the HF (Bianucci et al., 1994, 2010; Lambert et al., 2013). This feature suggests that stem ziphiids were able to hear at great depth, just like modern ziphiids (Lambert et al., 2013). However, proportions of the HF were never quantified in Ziphiidae and compared to other odontocetes.
We have provided here a detailed description of some postcranial remains of
the stem ziphiid
The fossil specimens MUSM 2542 and 2548 were excavated and subsequently transported to the Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima (MUSM). They were prepared and consolidated by means of mechanical tools and standard fossil vertebrate preparation techniques by W. Aguirre under the scientific supervision of R. Varas-Malca in the Departamento de Paleontología de Vertebrados at MUSM.
IRSNB – Institut Royal des Sciences Naturelles de Belgique, Brussels,
Belgium MNHN – Muséum National d'Histoire Naturelle, Paris, France MUSM – Museo de Historia Natural de la Universidad Nacional Mayor de San
Marcos, Lima, Peru MSNUP – Museo di Storia Naturale dell'Università di Pisa, Italy NMNZ – National Museum of New Zealand Te Papa Tongarewa, Wellington, New
Zealand NRM – Naturhistoriska Riksmuseet, Stockholm, Sweden SNM – Statens Naturhistoriske Museum, Copenhagen, Denmark USNM – National Museum of Natural History, Smithsonian Institution,
Washington, DC, USA
Set of linear measurements taken on the forelimb and skull of odontocetes.
The terminology used by Marx et al. (2016) and Fitzgerald (2016) was followed
to describe the postcranial remains of
A set of 11 linear measurements for the forelimb and 4 linear measurements
for the HF of odontocetes were selected with regard to the preserved parts
of
Two separate methods were applied to correct for intraspecific variation related to ontogenetic development. In the case of forelimb measurements, the method of the log-shape ratios was used (Mosimann, 1970). A variable “size” was computed as the geometric mean of all measurements of a particular structure for each individual. Each measurement for each specimen was then divided by the variable size. Finally, log transformation was performed on each divided measurement. The log-shape ratio procedure removes the effect of size, a variable that is interesting in the case of the HF. To keep the effect of size, raw measurements of the HF were analysed after applying a natural logarithmic transformation (Marcus, 1990). For each dataset, the median of the corrected values was computed for each sampled species and was used for the next analyses.
Set of linear measurements taken for the study exemplified in
Phylogenetic comparative methods were required to evaluate the degree of association between deep-diving abilities and proportions of the forelimb and HF due to the disparity of odontocete species compared. Indeed, measurements from closely related species are statistically non-independent, thus precluding the use of statistical methods before correction (Felsenstein, 1985).
The topology of the subtree and divergence time used in this analysis were
taken from the cetacean tree by McGowen et al. (2009), including all extant
species sampled in this study. Up to now, no phylogenetic analysis includes
the fossil species
A phylogenetic principal component analysis (pPCA; Revell, 2009) was performed to visualize the results for the measurements of the forelimb and the HF of odontocetes with regard to their specialization for deep diving. The pPCA is an exploratory tool similar to the principal component analysis (PCA). The latter is used to reduce the dimensions of a multivariate set of observations, allowing for a discussion of the pattern of variation in the dataset. The original data are translated in a new coordinate system centred toward the mean of the different traits of the dataset and where the rotated axes correspond to the major axes of variation. The PCA conserves the variance and thus the distances between observations. Unlike a conventional PCA, the pPCA takes into account the topology of the tree by centring the dataset toward the estimated phenotype of the root node of the tree instead of the mean and by inversely weighting the covariance matrix by the phylogeny. Consequently, the major axes do not maximize variation, but represent the non-phylogenetic residual variation (Revell, 2009).
A Q-mode for phylogenetic regression method (D-PGLS) was used to control for the phylogenetic independence of the measurement residuals (Adams, 2014). A Brownian motion model of evolution was assumed. The D-PGLS is an extension of the phylogenetic generalized least squares (PGLS). The PGLS is a statistical method aiming at estimating the parameters of a linear regression between two variables while removing the effect of kinships (Martins and Hansen, 1997). The covariance due to the phylogeny is incorporated into the residual error, thus making them statistically independent. The main problem with the PGLS is that it can only accommodate one dependent variable, while our dataset contained multiple measurements. The D-PGLS is a distance-based method using a matrix of pairwise distances among specimens instead of the variance–covariance matrices used in the traditional PGLS (Adams, 2014). This method bears the advantage of accommodating multiple dependent variables, no matter the number of trait dimensions.
Multilinear linear models without phylogenetic correction were also performed using a multivariate analysis of variance (MANOVA) to see if the results differed from the D-PGLS.
While the measurements were the dependent variables, deep-diving specialization was chosen as the categorical explanatory variable. An arbitrary criterion was chosen to assess deep-diving species based on records of the deepest foraging dives for each species. Species were considered specialized deep divers when their deepest foraging dives recorded were 700 m or beyond. Deepest foraging dive depths for each species were collected from the literature (see Dataset 3, Ramassamy et al., 2018). Deepest foraging dives rather than mean foraging dives were selected for two reasons. First, quantitative data were not accessible for all species. Second, deepest foraging dives were assumed to better reflect maximal diving performances for each species, which would be limited by morphological or physiological factors, such as the HF size.
No depth records were found for
The extinct
All statistical analyses were performed with the software R 3.2.2 (R Development Core Team, 2015) with the packages car (Fox and Weisberg, 2011), geomorph (Adams and Otarola-Castillo, 2013), phytools (Revell, 2012), and caper (Orme, 2013). The script is available in Dataset 1 (Ramassamy et al., 2018).
Order Suborder Family Genus
Specimen MUSM 2548: three cervical vertebrae including the axis, three thoracic and two thoracic–post-thoracic vertebrae all lacking the neural spine (Figs. 2–3), fused manubrium and left part of the second sternebra (Fig. 4), 11 complete to subcomplete ribs (Fig. 5); skull and mandibles are still in the field. Specimen MUSM 2542: partial right scapula lacking the acromion, the anterior part of the scapular blade, and the broken coracoid process (Fig. 6); partial left and right humeri (Fig. 7), complete left radius (Fig. 8); skull, mandibles, and other vertebrae of this individual are still in the field.
The specimens were discovered in the 200 m thick section of sediments from the Pisco Formation exposed at Cerro Colorado. They were identified under the fieldwork numbers O37 and O39 in the map provided by Bianucci et al. (2016b).
Two depositional sequences of the Pisco Formation, P1 and P2, are
represented at Cerro Colorado and separated by an angular unconformity (Di
Celma et al., 2016, 2017). The specimens MUSM 2542 and MUSM
2548 originate from the P1 sequence (the “lower allomember” of Di Celma et
al., 2016), consisting of nearshore conglomerates and fine-grained
sandstones, bioturbated sandy siltstones, and mudstones (Di Celma et al.,
2016). The lower allomember is rich in marine fossil vertebrates, such as
cartilaginous and bony fish, marine turtles, crocodiles, sea turtles, sea
birds, and seals (Bianucci et al., 2016b; Landini et al., 2017a, b; Parham and Pyenson, 2010; Stucchi et al., 2016). Cetaceans are
represented by diverse taxa: Physeteroidea (
Both specimens were identified based on complete skulls and mandibles that
were left on the field. They are attributed to the family Ziphiidae based on
the enlargement of the hamular fossa of the pterygoid. In MUSM 2548, this is
further confirmed by the presence of an enlarged apical alveolus on the
mandible. The two skulls have an extremely elongated rostrum, representing
approximately 75 % of the total condylobasal length. Furthermore, MUSM
2548 displays the medial fusion of the premaxillae dorsal to the mesorostral
groove along the rostrum. These two characteristics are typical of the genus
Cervical vertebrae of the specimen MUSM 2548,
Thoracic and post-thoracic vertebrae of the specimen MUSM 2548,
Sternum of the specimen MUSM 2548,
Ribs of the specimen MUSM 2548,
Right scapula of the specimen MUSM 2542,
Humeri and left radius of MUSM 2542,
The species
Both specimens are interpreted as adults based on the fully fused epiphyses
of the vertebrae of MUSM 2548, the humeral head fused to the humeral shaft,
and the epiphyseal ankylosis of each epiphysis of the radius in MUSM 2542.
In the small odontocete
One cervical vertebra is referred to as C5 or C6 based on the presence of a
vertebrarterial canal extended along the whole dorsoventral height of the
centrum, the presence of a lower transverse process measuring 29 mm
transversely, and the anterior and posterior articular facets dorsoventrally
smaller than transversely wide. These features were observed in C5 and C6 of
several extant ziphiid species (
All thoracic and post-thoracic vertebrae possess a centrum transversely wider than dorsoventrally high (Table 2) and oval in shape. An exception to this pattern is the anterior epiphysis of vertebra A, which is dorsoventrally higher than transversely wide and more rectangular (Fig. 3a). Vertebrae A, B, and G are identified as thoracics because of the presence of a fovea for the rib tuberculum on the upper transverse process and a fovea for the rib capitulum along their centrum (Fig. 3a–b and 3d). In posterior view of vertebrae A, B, and G, the fovea for the rib capitulum is located along the dorsolateral surface of the centrum. The extent of this fovea suggests these to be posterior to the thoracic vertebra 1. Indeed, in all extant Ziphiidae examined, the fovea extends along the whole lateral surface of the centrum.
The shaft of the right humerus is broken at mid-length, slightly displacing dorsally the distal articulation with the radius and the ulna (Fig. 7a–d). The humeral head is hemispherical and separated from the great tuberosity by a neck visible in ulnar and radial view (Fig. 7c–d). In lateral view, the head of the humerus represents one-third of the total length of the humerus (Fig. 7b). In medial view, the surface of the great tuberosity is flattened, approximately reaching the same proximal level as the head of the humerus. In lateral view, a deltoid ridge is developed along the anterior margin of the humerus at approximately mid-length of the humerus.
In distal view, the articular facets for the radius and the ulna are separated by the distal crest. In lateral view, each articular facet occupies approximately half of the distal surface of the humerus.
The axis of
Heavily abraded posteroventrally, the partial atlas of the middle Miocene
Berardiinae
A ventral tubercle is rarely present on the atlas of extant ziphiids, except
in
Measurements of the vertebrae from specimen MUSM 2548,
Summary of the main features relative to neck musculature in extant and fossil Ziphiidae. All specimens were directly consulted.
Similar insertion areas are observed in
In
Conversely, many extant Ziphiidae display extensive fusion of the neck
vertebrae; none of the species with data available bear a free axis at the
adult stage (Lambert et al., 2015). For example, in
Comparison of muscular insertions along the atlas and axis in
Comparative reconstructions of the cervical complex in several
cetaceans with neck muscle origins discussed in this paper. The
reconstructions concerned
Even though the neural spine of the axis is not preserved in
Even though the bad preservation of the region around the supraspinatus
fossa and the acromion in
The relationship between HF proportions and deep-diving abilities was revealed
as significant with and without phylogenetic correction (with phylogenetic
correction:
Comparison of the muscle origins and insertions of the scapula
and humerus in lateral view in
Phylomorphospace of the principal components 1 and 2 for the
hamular fossa of the pterygoid sinus
Phylomorphospace of the principal components 1 and 2 for the
forelimb
The relationship between forelimb measurements after log-shape ratio
transformation and deep-diving abilities was revealed as not significant with and
without phylogenetic correction (with phylogenetic correction:
Our reconstruction of neck muscles in the stem ziphiids
In addition, the proportionally longer cervical vertebrae of long-snouted stem ziphiids compared to crown beaked whales allowed for wider lateral and dorsoventral movements.
We also interpret the low degree of fusion of the cervical vertebrae in
The more extensive fusion of the cervical vertebrae in the extant ziphiids
The cervical vertebra of the specimen MUSM 2548 identified as C5–C6 bears a
small lower process similar in shape and development to C6 of
While the spinous process of the axis was not preserved for
Neck rigidity might be related to deep-diving specialization in Ziphiidae. However, differences in the degree of flexibility observed among extant ziphiids advocate for a more complex functional interpretation. Data on potential differences in swimming and feeding strategies between extant ziphiid species are currently insufficient to explain the contrasted neck morphologies observed.
Our reconstruction of the forelimb muscles of
Results of the D-PGLS indicate that the morphology of the forelimb is not associated with deep-diving abilities, suggesting that forelimb proportions cannot be used to assess deep-diving specialization in odontocetes.
Functional aspects of the flipper of ziphiids remain poorly known, but we
suspect the flipper shape of
Our measurements of the HF were sufficient to discriminate ziphiids from
other odontocetes. Furthermore, the variation in HF measurements is
correlated with deep-diving specialization, thus suggesting that enlargement
of the HF is a good proxy to assess deep-diving abilities. The increase in
size of the HF in deep divers happens in two different ways: either by the
anteroposterior and dorsoventral enlargement of the HF as in ziphiids,
Although it remains unclear if
First,
A second plausible explanation for the enlarged HF of
A last explanation for the enlargement of the HF in
A combination of these features is also possible. Currently, we are unable to favour one hypothesis or the other.
Ziphiid postcranial elements are rare in the fossil record (Bianucci et al.,
2016a; de Muizon, 1984; Ramassamy, 2016). As a result, the description of
cervical vertebrae and forelimb elements of the stem ziphiid
Our reconstruction of the neck muscles of
The proportions of the forelimb bones of
Finally, our measurements of the hamular fossa of the pterygoid sinus are
sufficient to evaluate deep-diving abilities in odontocetes with and without
phylogenetic correction. The enlargement of the hamular fossa is also
present in
Dataset 1: R script used for the analysis.
Dataset 2: complete set of linear measurements used in the present study.
Dataset 3: list of supplementary references for the maximum depth records.
All data information can be found at
All authors took part in the fieldwork and collected field data. OL, GB, MU, and BR identified and interpreted the ziphiid remains. Measurements were taken by AC, GB, OL, and BR. Photos were taken by BR, AC, and GB. BR wrote the paper and performed the analyses. All authors commented on the paper at all stages.
The authors declare that they have no conflict of interest.
This article is part of the special issue “Secondary adaptation of tetrapods to life in water – Proceedings of the 8th International Meeting, Berlin 2017”. It is a result of the 8th International Meeting on the Secondary Adaptation of Tetrapods to Life in Water, Berlin, Germany, 3–8 April 2017.
We thank the following colleagues for kindly allowing us to access some of the comparative material we used in this study: Morten T. Olsen and Daniel K. Johansson for access to the SNM collection, S. Bruaux for the IRSNB collection, Christian de Muizon and Christine Lefèvre for the MNHN collections, Chiara Sorbini for the MSNUP collections, and Charles Potter for the USNM collections. We are indebted to Klaas Post for his help in the field to collect and identify the specimens.
We thank Walter Aguirre, who collected the specimens, and Walter Aguirre, Rodolfo Salas-Gismondi, and Rafael Varas-Malca, who prepared the specimens and provided assistance during our stay at the MUSM.
BR also wishes to thank his supervisors Mette E. Steeman and Thomas Pape for the
advice they provided on the paper, which is part of his PhD thesis. He
also thanks Andrew Steward from the Te Papa Tongarewa Museum of New Zealand for
the photographs of
We thank the reviewers, Annalisa Berta and Mark D. Uhen, and the Chief Editor Florian Witzmann, who provided relevant comments and improved the quality of the paper.
The research was partially supported by a grant from the Dansk Slots- og Kulturstyrelsen (FORM.2016-0021) to B. Ramassamy, a grant from the Italian Ministero dell'Istruzione dell'Università e della Ricerca (PRIN project 2012YJSBMK), and by a National Geographic Society Committee for Research Exploration grant (9410-13), both to G. Bianucci. Edited by: Florian Witzmann Reviewed by: Annalisa Berta and Mark D. Uhen