JOURNAL OF PALEONTOLOGY, v. 57, NO. 2, P. 197-207, 3 FIGS.

, MARCH 1983

THE CORRELATION BETWEEN HIGH LIMB-BONE DENSITY

AND AQUATIC HABITS IN RECENT MAMMALS

WILLIAM P. WALL
Department of Biology, Georgia College, Milledgeville 31061

ABSTRACT-Measurements of volume and weightfor limb bones froma seriesof Recentmammals

resultedin the recognitionof two groupscorrespondingto differenthabitats,aquaticand terrestrial.
Most aquatic mammals studied exhibited significantlyhigher limb-bone density than did the
terrestrialmammals. It is proposedthat the higherbone density of aquatic mammals is an ad-
aptation to reduce problems of buoyancy. Cetaceansand some "pinnipeds"have secondarily
reducedbone density with the acquisitionof lung collapse duringdeep dives. The greaterbone
densityof aquaticmammalsis at least partiallyachievedthroughincreaseddepositionof compact
bone alongthe shaftsof limb bones. As a resultit is possibleto differentiatevisuallyaquaticfrom
terrestriallimb elements by sectioningthe bone and examiningthe percentageof compact bone
present.Fossil bones can be interpretedin the same manner,thus providinga quantifiabletest for
the determinationof life habits in extinct mammals.

INTRODUCTION
ity of most mammals is less than 1.0. If an
commonly have difficulty
PALEONTOLOGISTS animal has a lower specific gravity than water
interpreting the mode of life of fossil organ- it would be difficult to remain submerged for
isms, especially whether an animal was an extended period. Because of this it is ad-
aquatic or terrestrial. The controversy over vantageous for an aquatic organism to have
whether sauropods were amphibious or ter- a high specific gravity. Aquatic birds proba-
restrial is a classic example (see Coombs, bly display the greatest variety of methods
1975). Many authors dealing with the subject used to overcome buoyancy. Boobies and
of aquatic adaptations in fossil groups failed tropicbirds use momentum from an aerial
to make detailed comparisons with known dive to keep them submerged for short pe-
aquatic organisms (for example, Scott, 1937; riods. Anhingas and cormorants have re-
Troxell, 1921). I shall attempt to present here duced oil glands (in the absence of the water-
a quantifiable approach to the study of pre- proofing oil the water-laden feathers flatten
sumed aquatic fossil mammals through com- to the skin surface thereby increasing the an-
parison with Recent semi-aquatic and aquat- imals' specific gravity; Owre, 1967). Numer-
ic mammals. ous aquatic birds utilize gastroliths to in-
The method of locomotion employed by crease their density as well as for grinding up
aquatic tetrapods is one line of evidence used food; the more exclusively aquatic birds, such
to determine the life habits of a fossil organ- as penguins, reduce buoyancy by increasing
ism. Animals that are highly adapted for life the weight of the skeleton (Olson and Hasa-
in the water have grossly modified limbs and gawa, 1979, have demonstrated an increase
vertebral columns (as in marine turtles, pen- in bone density in a fossil group of pelecan-
guins, and cetaceans). Therefore extinct ple- iform birds also).
siosaurs, mosasaurs, and ichthyosaurs that The only method for overcoming buoy-
exhibit similar modifications also likely lived ancy found in birds and available to aquatic
in the water. Grossly observable adaptations mammals is increased bone density. Al-
of the limbs of amphibious animals, like the though the high density of sirenian bones is
hippopotamus, are more difficult to recognize believed to be a means of reducing buoyancy
(but detailed comparisons may provide some (Domning, 1978) the subject has not been
useful information; see Wall, 1981). widely studied in the Mammalia because the
Because water makes up most of the soft most highly aquatic mammals, the Cetacea,
tissue in an animal the density of soft tissue have relatively light bones (the reason for this
is close to one. Because of large air spaces in apparent anomaly is discussed below).
the body cavity and viscera the specific grav- The major purpose of this paper is to show
Copyright ? 1983, The Society of Economic 197 0022-3360/83/0057-0197$03.00
and
Paleontologists and
Mineralogists
The Paleontological Society
198 WILLIAM P. WALL
the results of a study comparing relative limb-
bone density of Recent aquatic and terrestrial
mammals. In addition suggestions will be
presented to explain any observed differences
in bone density between aquatic and terres-
trial mammals and how to quantitatively rec-
ognize these differences.
MATERIALS AND METHODS
Bone density of a large number of Recent
mammals was determined to demonstrate
whether a clear separation of living mammals
into two groups, aquatic and terrestrial, could
be made based on specific gravity of the skel-
eton. Limb elements from 49 genera of mam-
mals (Table 1) were used. I restricted my study
to limb elements because the distinction be-
tween compact and cancellous bone is more
apparent in limb bones than in other ele-
ments. Measuring both right and left limbs
from the same individual served to test the
reliability of the experimental method. A third
advantage of limb elements is that they are
more frequently available as identifiable fos-
sils.
Bone density was determined from thor-
oughly soaked, relatively unweathered, de-
greased, museum specimens. Wet volume was
recorded by measuring the amount of water
displaced when the soaked bone was sub-
merged. Wet weights were recorded and the
ratio of weight to volume provided a close
estimate of the overall density of the bone
(for details on procedure followed see Beh-
rensmeyer, 1975).
Repeated trials on several of the bones
showed that experimental error fell within an
acceptable range of 3-7%. I was concerned,
however, primarily with the internal consis-
tency of the experimental method to validate
relative comparisons among taxa. Therefore,
density figures presented in this paper should
be regarded as relative instead of absolute
densities. An independent investigation may
arrive at slightly different densities for the
limb elements measured here but the di-
chotomy between aquatic and terrestrial
forms should still be apparent.
T-tests were performed using mean density
and variance to determine if the differences
between aquatic and terrestrial mammals was
significant.
After determining the densities of all the
specimens, I sectioned some of the bones lon-
gitudinally with a bandsaw. Cross-sectional
measurements of compact bone and total
bone diameter were taken at three different
places along the shaft (proximal end, middle,
and distal end) with dial calipers. Measure-
ments from the three regions were averaged
to produce an overall index of the relative
amount of compact bone in each limb ele-
ment sectioned.
Comments on general life habits and taxo-
nomic names of the animals used in this study
were taken from Walker et al. (1975) unless
stated otherwise.
Specimens used in this study consisted of
both wild mammals and mammals raised in
zoological parks. The two groups can be dis-
tinguished by a small w or z after the speci-
men numbers in Table 1. The specimens are
housed in the American Museum of Natural
History, New York (AMNH); Georgia Col-
lege, Milledgeville (GC); National Museum
of Natural History, Washington, DC
(NMNH); and University of Massachusetts,
Amherst (UMA).
RESULTS
Almost all of the specimens examined
showed a good correlation between aquatic
habits and higher limb-bone density (Table
1). Different limb bones showed varying
amounts of separation between mean density
for aquatics as opposed to terrestrials. For
the humerus, aquatic mammals averaged a
density of 1.48 whereas terrestrial mammals
had a density of 1.2. Only three aquatic mam-
mals examined were clearly within the range
of terrestrial mammal bone density; these
were the elephant seal (Mirounga angusti-
rostris),hooded seal (Cystophora cristata), and
walrus (Odobenus rosmarus). Combined ra-
dius and ulna proved to be denser than the
humerus in both aquatics and terrestrials but
the aquatics overall were much denser (1.62
compared to 1.27). Bone densities for the el-
ephant seal, hooded seal, and walrus again
were in the terrestrial range, but in addition
the Weddell seal (Leptonychotes weddell) also
fell within the range of bone density for ter-
restrial mammals.
Results for the hindlimb were basically the
same as for the forelimb. The femur in aquat-
ic mammals had an average density of 1.46
and for terrestrial mammals it was only 1.2.
Again the elephant seal had a low density but
 LIMB-BONE DENSITY AND AQUA TIC HABITS 199

TABLE 1-Mean limb-bone volume and density (in parentheses)for aquaticand terrestrialmammalsstudied (w =
wild and z = zoo animals); volume in cm3, density in g/cm3.

Taxon N Humerus Radius-ulna Femur Tibia-fibula

TERRESTRIAL GROUP
Rhinocerosunicornis 2 3,645 (1.31) 2,383 (1.27) 3,895 (1.3) 1,960 (1.25)
(Indianrhinoceros)
NMNH 336953z
Ceratotheriumsimum 3 3,430 (1.29) 2,340 (1.3) 3,175 (1.3) 1,515 (1.37)
(Whiterhinoceros)
AMNH 238245z
NMNH 164592w
Dicerosbicornis 2 3,320 (1.33) 2,200 (1.41) 3,110 (1.31) 1,510 (1.41)
(Blackrhinoceros)
NMNH 162931w
Didermocerossumatrensis 2 1,190 (1.24) 773(1.26) 1,544 (1.25) 738 (1.3)
(Sumatran rhinoceros)
NMNH 49561z
Bison americanus 3 1,120 (1.19) 640(1.19) 1,150 (1.14) 750 (1.27)
(Bison)
AMNH 19175z
NMNH 49760z
Tapirusterrestris 4 420 (1.25) 262 (1.37) 568 (1.25) 288 (1.35)
(Braziliantapir)
AMNH 100252z
NMNH 261025z
UMA 24z
Equus burchelli 2 384 (1.18) 303 (1.26) 605 (1.18) 379(1.19)
(Grant'szebra)
NMNH 162959w
Sus scrofa 2 173 (1.02) 126 (1.04) 171 (1.03) 125 (0.98)
(Europeanwild hog)
NMNH 15184w
Lama guanacoe 2 333(1.19) 268 (1.37) 378 (1.16) 314(1.31)
(Guanaco)
NMNH 92137w
Phacochoerusaethiopicus 2 201 (1.19) 147 (1.15) 175(1.13) 153 (1.06)
(Warthog)
NMNH 36864w
Tayassupecari 2 72 (1.22) 42 (1.32) 61 (1.21) 55 (1.31)
(White-lippedpeccary)
NMNH 257318w
Ursus arctos 2 580 (1.29) 452 (1.38) 588 (1.32) 480 (1.21)
(Alaskanbrown bear)
NMNH 123386w
Rangifer tarandus 1 222(1.21) 167 (1.35) 265 (1.28) 355 (0.96)
(Caribou)
AMNH 24206z
Felis leo 2 525 (1.29) 380 (1.38) 473 (1.27) 377 (1.37)
(Lion)
NMNH 172677w
Taurotragus oryx 1 1,260 (1.22) 873 (1.3) 1,345 (1.18) 945 (1.29)
(Eland)
AMNH 80189z
Okapiajohnstoni 1 630 (1.26) 610 (1.28) 770(1.1) 510 (1.36)
(Okapi)
AMNH 149148z
Tragelaphusstrepsiceros 1 350(1.21) 245 (1.27) 455 (1.09) 392(1.19)
(Greaterkudu)
AMNH 79328z
Cervuseldi 1 177 (1.12) 128 (1.33) 228 (1.24) 185 (1.23)
(Eld deer)
AMNH 35704z
Hippotragusequinus 1 333 (1.27) 270 (1.26) 425 (1.27) 370(1.23)
(Roan antelope)
AMNH 80134z
200 WILLIAM P. WALL

TABLE1-Continued

Taxon N Humerus Radius-ulna Femur Tibia-fibula

Alces alces 1 355 (0.96) 290(1.12) 385(1.18) 380 (0.98)

(Moose)
AMNH 16868z
Didelphis virginiana 2 6 (1.14) 5 (1.21) 6(1.24) 6(1.1)
(Opposum)
UMA 1319w
Gazella dorcas 1 16(1.19) 15(1.21) 29 (1.06) 25(1.26)
(Gazelle)
AMNH 17416z
Aplodontia rufa 2 2 (0.97) 1(1.16) 2 (1.08) 2(1.12)
(Mountain beaver)
UMA 1319w
Macaca mulata 2 15(1.32) 14(1.31) 24 (1.26) 20(1.14)
(Rhesus macaque)
UMA 2304z
Connochaetes gnu 1 219(1.14) 169 (1.21) 266(1.19) 183 (1.24)
(White-lipped gnu)
AMNH 14138z
Procyon lotor 15 10(1.16) 7 (1.29) 15(1.13) 12(1.14)
(Raccoon)
UMA 1709w, 1777w,
2649w, 3361w, 3481w,
3482w, 3483w, 3484w
Agouti paca 2 17(1.24) 13(1.23)
(Paca)
UMA 2323w
AQUATIC GROUP
Hippopotamus amphibius 9 1,984 (1.53) 1,222 (1.63) 2,453(1.51) 1,217 (1.63)
(Hippopotamus)
AMNH 15898z
NMNH 162976w, 162977w,
162980w, 254987z
Choeropsis liberiensis 3 368(1.51) 218(1.74) 429 (1.53) 246 (1.62)
(Pygmy hippopotamus)
AMNH 148452z
NMNH 314046z
Hydrochoerus hydrochoerus 2 60(1.49) 37 (1.58) 82(1.51) 58 (1.48)
(Capybara)
NMNH 241103w
Enhydra lutris 5 34(1.65) 17 (1.82) 51(1.46) 35 (1.6)
(Sea otter)
NMNH 21336w, 49492w,
263315w
Arctocephalus australis 2 180 (1.34) 140 (1.67) 34(1.47) 85(1.55)
(South American fur seal)
NMNH 23331w
Callorhinus ursinus 2 287 (1.58) 260 (1.69) 65 (1.7) 123 (1.63)
(Northern fur seal)
NMNH 258588w
Pusa hispida 2 37 (1.62) 24(1.71) 28 (1.55) 46(1.81)
(Ring seal)
NMNH 504208w
Leptonychotes weddelli 2 205 (1.31) 158 (1.3) 120 (1.34) 257 (1.4)
(Weddell's seal)
NMNH 504875w
Mirounga angustirostris 2 1,050(1.15) 740 (1.25) 452 (1.08) 470 (1.23)
(Elephant seal)
NMNH 260867w
Odobenus rosmarus 2 1,865 (1.26) 1,050 (1.31) 735 (1.35) 910(1.35)
(Walrus)
NMNH 500254w
 LIMB-BONE DENSITY AND AQUATIC HABITS 201

TABLE I-Continued

Taxon N Humerus Radius-ulna Femur Tibia-fibula

Trichechus manatus 3 235 (2.0) 94 (2.35)
(Manatee)
AMNH 14161z
NMNH 527909w
Lutra canadensis 1 6 (1.54) 4 (1.71) 7 (1.32) 7 (1.41)
(Otter)
UMA 2290w
Zalophus californianus 1 377 (1.5) 245 (2.01) 94 (1.59) 89 (2.04)
(California sea lion)
AMNH 80269z
Ondatra zibethicus 2 1(1.68) 2 (1.37)
(Muskrat)
UMA 2238w
Castor canadensis 11 9 (1.72) 8 (1.73) 26(1.61) 22 (1.57)
(Beaver)
UMA 1274w, 1775w,
2062w, 2063w, 2065w,
2237w
Thalarctos maritimus 1 630 (1.39) 360 (1.65) 640 (1.33) 360 (1.65)
(Polar bear)
NMNH 275124w
Otaria flavescens 1 620 (1.39) 590 (1.49) 160 (1.42) 360 (1.65)
(South American sea lion)
AMNH 73120w
Eumetopias jubatus 2 900 (1.35) 820 (1.46) 285 (1.39) 420 (1.54)
(Steller sea lion)
AMNH 77883w
Hydrurga leptonix 1 334 (1.44) 240(1.48) 155 (1.55) 298 (1.45)
(Leopard seal)
AMNH 36200w
Cystophora cristata 1 212(1.27) 134 (1.27) 97 (1.46) 78 (1.45)
(Hooded seal)
AMNH 184659w
Monachus monachus 2 215(1.39) 160(1.45) 124(1.42) 298 (1.45)
(Monk seal)
AMNH 73607w
Erignathus barbatus 2 112(1.35) 65 (1.64) 83 (1.67) 170 (1.43)
(Bearded seal)
AMNH 75248w

the walrus and hooded seal were somewhat
higher, above the terrestrial mammal range
and denser than the polar bear (Thalarctos
maritimus). The combined tibia-fibula was
relatively denser than the femur in aquatic
mammals but only slightly higher than the
femur in terrestrial mammals. Again the tib-
ia-fibula shows a distinct difference in density
between aquatics (1.55) and terrestrials (1.22).
The walrus, elephant seal and to a lesser ex-
tent the Weddell seal were within the range
of terrestrial mammal bone density. Al-
though some of the difference in density be-
tween the front and hindlimbs can be attrib-
uted to the absence of a hindlimb in sirenians,
most of the difference probably results from
restrictions on position of the centers of
buoyancy and gravity.
T-values (t) and the degrees of freedom (df)
obtained for the various limb elements were:
humerus, t = 31, df= 45; radius-ulna, t=
29.9, df= 45; femur, t = 38.2, df= 46; and
tibia-fibula, t = 36.5, df = 45. In spite of some
overlap between the two groups, high t-val-
ues were obtained, indicating that the bone
density of aquatic mammals is significantly
higher than the bone density of terrestrial
mammals (P < 0.001).
Mean variance for terrestrial mammal bone
density was low (0.009) whereas aquatic
mammal bone density showed a high mean
variance (0.036). I believe that low variance
 202 WILLIAM P. WALL

HUMERUS RADIUS-ULNA
* CASTOR CASTOR
* PROCYON A PROCYON
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I 1 ! I I !5 I
1.0 I1. 1.2 1.3 1.4 1.5 1.6 1.7 1.8 10 1 12 13 14 1-5 16 17 8
18 19 22.0
BONE DENSITY (gm/cc) BONE DENSITY (gm/cc)

FEMUR
* CASTOR TIBIA- FIBULA
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* PROCYON * CASTOR
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BONE DENSITY (gm/cc) BONE DENSITY (gm/cc)

FIGUREI1-Graphs of limb-bone densities comparingdifferentgrowthstagesof a terrestrial(Procyon)

and aquatic (Castor)mammal (the 2 smallest Procyonare juveniles, and the smallest Castor is a
juvenile).

in terrestrial mammal bone density indicates ic adaptation, no overall size correlation could
a relatively narrow optimum range of bone be determined for aquatic mammals. The
density that is a compromise between strength lower bone density of the pygmy hippopot-
and weight. Aquatic mammals exhibit a much amus (Choeropsis liberiensis) compared with
broader range in bone density simply because the larger Hippopotamus amphibius is prob-
there are different degrees to which an animal ably related in part to its small size; however,
can be adapted aquatically. For example, po- accounts of the behavior of these two animals
lar bears, which spend much of their time on indicate that H. amphibius spends consid-
land or ice and rarely swim completely sub- erably more time in water than C. liberiensis.
merged, have only slightly more dense bones A comparison of different age groups of
than other bears, whereas the permanently raccoons (Procyon lotor) and beavers (Castor
aquatic manatee (Trichechus manatus) has canadensis) (Figure 1) showed that while bone
bone densities commonly over 2.0. density increased with age in both terrestrial
Bone density in terrestrial mammals and aquatic mammals (relative age was in-
showed a slight increase with an increase in dicated by difference in size and degree of
body size. The smallest mammal included in closure ofepiphyses) overall bone density was
the study was the mountain beaver (Aplo- much higher in the aquatic beavers. Increase
dontia rufa); this animal had a femur with a in bone density with age was expected be-
density of 1.08 whereas the largest terrestrial cause laminar compact bone is deposited lat-
mammal studied, the Indian rhinoceros er in growth (Kluge, 1977).
(Rhinoceros unicornis), had a femur density Variation in bone density within an indi-
of 1.3. Because of the differing levels of aquat- vidual was usually less than between indi-
 LIMB-BONE DENSITY AND AQUATIC HABITS
viduals, particularly if they belonged to dif-
ferent age groups. When adult size was
reached, rate of increase in bone density rap-
idly declined. Since adult Castor and Procyon
exhibit relatively little variation in bone den-
sity it is likely that taxa represented by data
from only a single adult individual in Table
1 are typical of other members of the same
species. Castor and Procyon show differences
in rate of bone density increase. The proximal
element in the forelimb and hindlimb in Cas-
tor showed a much greater increase in density
from juvenile (UMA 2063) to adult than was
seen in Procyon.
DISCUSSION
Reduced bone density in highly aquatic
mammals. -As noted above, many ceta-
ceans have relatively light bones (an uniden-
tified cetacean forelimb, GC 574, had the fol-
lowing bone densities and volumes: humerus,
density 1.16, volume 1,830 cc; radius, den-
sity 1.26, volume 810 cc; ulna, density 1.25,
volume 508 cc). My results also show that
some phocids, particularly the elephant seal
(Mirounga) with an average limb-bone den-
sity of only 1.18, have relatively light bones.
This is not true of all phocids, however. The
ringed seal (Pusa hispida), bearded seal (Erig-
nathus barbatus), and leopard seal (Hydrurga
leptonyx) had an average density for all limb
elements of 1.67, 1.48, and 1.52 respectively,
placing them high in the range of aquatic
mammals. The five otariids included in my
study, South American fur seal (Arctoce-
phalus australis), northern fur seal (Callor-
hinus ursinus), Steller sea lion (Eumetopias
jubatus), South American sea lion (Otaria
flavescens), and California sea lion (Zalophus
californianus) all had high limb-bone densi-
ties. Average bone density for each otariid
was 1.51, 1.65, 1.43, 1.48, and 1.78 respec-
tively. The walrus, family Odobenidae, how-
ever, had a relatively low bone density for
the size of the animal (a limb-bone average
density of only 1.32).
High limb-bone density in all of the otar-
iids studied, some phocids, and aquatic mus-
telids (the sea otter, Enhydra lutris, had an
average limb-bone density of 1.63) indicates
to me that lower bone density in Mirounga,
Leptonychotes, and Odobenus is a second-
arily derived condition. The light bones of
some cetaceans may exhibit a similar sec-
203
ondarily derived state. Extinct archaeocete
whales had relatively more dense bones than
odontocetes or mysticetes (Kellogg, 1936).
I believe secondary reduction in bone den-
sity in some of the most highly aquatic mam-
mals is related to diving habits. Cetaceans
and "pinnipeds" are the only mammals which
commonly take deep dives. To avoid nitro-
gen narcosis and decompression sickness
elaborate physiological mechanisms evolved
(see Alexander, 1975). One of these adapta-
tions is that the lungs are only partially full
(seals and whales both expel air before a dive;
Hildebrand, 1974; Alexander, 1975) when the
animal submerges. At great depths the lungs
can collapse completely with no ill effects.
When lungs of whales are compressed the
animal is heavier than the surrounding water,
but when the lungs are expanded fully whales
float. Apparently whales, and probably to a
lesser extent some "pinnipeds," use air space
in the lungs as a "gas bladder" similar to use
of true gas bladders by teleosts. A regulatory
system employing reduction in lung capacity
to overcome buoyancy is superior to the stat-
ic mechanism of increased bone density found
in other aquatic mammals which are not deep
divers. As a result it is easy to understand
why cetaceans and some "pinnipeds" have
secondarily reduced bone density.
Internal architecture of mammalian limb
bones.-Greater bone density may be
achieved by increasing the percentage of hy-
droxyapatite (the mineral portion of bone).
Hydroxyapatite crystals have a density of
about 3.1 to 3.2 (Berry and Mason, 1959).
Because the density of this mineral is far
higher than the overall bone density encoun-
tered in mammals, an increased deposition
ofhydroxyapatite might account for the higher
bone densities in aquatic mammals. How-
ever, overall strength of a bone is derived
from a bipartite system composed of hy-
droxyapatite and collagen (see Kluge, 1977).
Hydroxyapatite is suited to resisting com-
pressive force but is relatively weak under
tension; collagen exhibits the opposite traits.
Because bones are subject to compressive and
tensile forces both components should be
maintained at a relatively stable percentage
depending on function.
An alternative method of increasing bone
density is simply to deposit more bone (or
resorb less of what is deposited), thereby re-
204 WILLIAM P. WALL

TABLE 2-Percentage of compact bone in the limb ele- that hypofunctioning of the thyroid gland
ments.
probably was responsible for increased bone
Taxon Humerus Radius Femur Tibia deposition. I already suggested why many ce-
TERRESTRIAL GROUP
taceans do not have dense bones; the fact that
Ceratotherium 33.8% 26.2% 25.2% 26.6% sirenians have extremely dense bones is as-
Bison 17.9 17.1 19.4 18.7 sociated with their different life habits from
Tapirus 22.3 19.4 19.5 23.8 those of cetaceans. Sirenians are not deep
Rangifer 16.2 22.6 18.3 21.1
Taurotragus 27.7 20.5 21.9 21.8 divers, therefore these animals are not sub-
Okapia 26.2 20.7 23.2 23.7 jected to nitrogen narcosis or decompression
Tragelaphus 25.9 21.7 25.1 sickness. It seems likely that the ability to
Cervus 21.2 23.2 19.7 24.1
Hippotragus 28.1 26.5 25.1 24.9 remain submerged for feeding is the major
Alces 19.7 12.6 14.6 14.5 selective force acting on sirenians. Increased
Gazella 20.3 17.8 24.2
Connochaetes 21.5 22.1 24.1 22.1 bone deposition is a relatively simple, effi-
Procyon 18.7 20.7 cient way of accomplishing this end. How-
AQUATIC GROUP ever, the extremely dense bones of most si-
Hippopotamus 35.0 32.5 44.0 38.9 renians probably only allow the animal to
Choeropsis 31.6 34.4 32.9 31.1 achieve neutral buoyancy or slightly greater
Odobenus 25.32 32.8 40.1 23.1
Trichechus 54.2 54.2 density than water. Trichechus may be able
Zalophus 29.0 31.0 48.1 36.3 to regulate its water depth by muscular con-
Castor 52.5 43.3 traction of its lungs (Domning, 1978) but its
ability is not comparable to the lung adap-
tations seen in cetaceans. That sirenian bones
are denser than those of other aquatic mam-
ducing the marrow cavity. This approach has mals utilizing high bone density to overcome
the advantage of maintaining the structural buoyancy can be attributed to their more ful-
integrity of the bone. ly aquatic existence.
To determine whether increased bone den- Comparison of bones in Figure 2 shows
sity in aquatic mammals is the result of this that the amphibious mammal has relatively
second method, I sectioned a sample of bones more compact bone than do the terrestrial
from aquatic and terrestrial mammals. Re- mammals. Additional weight is also provid-
sults indicate that an increase in bone de- ed by tight packing of cancellous bone in the
position accounts for the higher density in marrow cavity. Many of the lightly built ter-
aquatic mammals (Table 2). Although the restrial mammals have very little cancellous
sample size is small the difference between bone (even the moderately heavy Bison has
aquatic and terrestrial mammal bones is sig- a relatively bone-free marrow cavity; see Fig-
nificant (t-values and degrees of freedom for ure 2). Aquatic mammals, however, for ex-
the different limb elements were: humerus, ample Hippopotamus, have filled the marrow
t = 3.1, df = 17; radius, t = 2.66, df = 13; fe- cavity with cancellous bone. The white rhi-
mur, t = 8.59, df= 16; and tibia, t = 3.1, noceros (Ceratotherium simum) also fills the
df= 14). marrow cavity with cancellous bone (prob-
Trichechus manatus exhibits the extreme ably in response to the animal's great weight,
to which increased bone deposition can be up to 3.5 metric tons). Comparing the de-
carried. The medullary cavity of manatee velopment of cancellous bone in Ceratoth-
bones is almost entirely filled with dense, erium and Hippopotamus (Figure 3), how-
compact bone. The solid nature of manatee ever, clearly shows differences between the
bones has been known for a long time, but two. Cancellous bone in the rhino is finely
the reason for it has been controversial. Faw- textured and can easily be differentiated from
cett (1942) noted that dense bones would be peripheral compact bone. In the hippopota-
useful in overcoming buoyancy, but because mus, cancellous bone is much more solidly
he believed that other aquatic mammals did constructed and along the periphery merges
not have dense bones he discounted in- with the thick, surrounding layer of compact
creased weight as an aquatic adaptation. bone.
Fawcett compared sirenian bones to patho- Relative percentages of compact bone for
logic conditions in humans and concluded the limb elements sectioned are given in Ta-
 LIMB-BONE DENSITY AND AQUA TIC HABITS 205

FIGURE2- Sectioned femora of, from left to right, Bison, Ceratotherium, and Hippopotamus to illustrate
differences in amount of compact bone deposited in each.

FIGURE3-Detailed illustration of sectioned femoral heads of Ceratotherium (left) and Hippopotamus

(right) to show differences in cancellous bone construction between a large terrestrial and a large
semi-aquatic mammal.
206 WILLIAM P. WALL
ble 2. It is important to note that these per-
centages only approximate the true total since
they represent values taken at only 3 planes
along the bone. Because of the proximity of
muscle attachment sites (such as a third tro-
chanter or deltoid crest) or other structural
reasons some bones show local thickening of
compact bone. As a result, percentage of
compact bone may appear artifically high in
Table 2. A good example of this complicating
factor is the humerus of Ceratotherium. Just
above the olecranon fossa there is a short,
distinct swelling of compact bone (at the dis-
tal plane where one of the measurements was
taken). Substituting a measurement from a
spot where compact bone thickness is more
typical, the Ceratotherium humerus contains
only 20.1% compact bone (in view of the
local swelling the overall percentage would
be somewhat higher). Limb bones of aquatic
mammals tend to be of much more uniform
compact bone thickness (since the overall
thickness of compact bone probably already
exceeds most local stresses). Compact bone
percentage for aquatic mammals is therefore
more accurate and the actual dichotomy be-
tween aquatic and terrestrial mammals is
probably greater than indicated in Table 2.
Importance of bone density studies to pa-
leontology.--Absence of a definite correla-
tion between size and density in aquatic
mammal bones is a factor that was not con-
sidered previously in the field of taphonomy.
One factor regulating bone transport in an
aquatic system is the settling velocity of the
bone (which is partly dependent on the bone's
density). Korth (1979) presented an equation
that predicted the settling velocity of a par-
ticular bone if the area of the foramen mag-
num of the skull were known. Korth obtained
a good correlation between his formula and
actual settling velocities for seven placental
mammals ranging in size from a shrew to a
horse. Korth did not include aquatic mam-
mals in his study. I believe that Korth's meth-
od is accurate for predicting the settling ve-
locity of a terrestrial mammal bone, but
because of the increased bone density of many
aquatic mammals Korth's formula would
probably underestimate the settling velocity
of aquatic mammal bones.
The discussion above shows that Recent
aquatic and terrestrial mammals can be dis-
tinguished on the basis of sectioned material.
High bone densities in fossil mammals have
previously been looked at only in terms of
rib pachyostosis. Most semi-aquatic mam-
mals, however (such as Hippopotamus), do
not have pachyostotic ribs. Though density
studies involving weight and volume are not
possible, I believe it is possible to differen-
tiate fossil aquatic from fossil terrestrial
mammal limb bones. Complete, well-pre-
served material will provide the most useful
information. The bone should be longitudi-
nally sectioned, and measurements of com-
pact bone and entire bone diameter taken at
several places. If compact bone exceeds 30%
of average bone diameter the fossil mammal
probably was at least semi-aquatic (especially
if all the limb elements exceed 30%). Relative
distribution of compact bone should also be
observed to determine whether the percent-
age obtained is consistent with the distribu-
tion of compact bone throughout the limb
element. Presence or absence of cancellous
bone in the marrow cavity should also be
considered (particularly if it is possible to de-
termine the character of cancellous bone as
in the discussion of Ceratotherium and Hip-
popotamus above).
In conjunction with other skeletal charac-
ters traditionally taken to imply aquatic hab-
its (such as elevated position of orbit), sec-
tioned limb bones should provide added
insight to the problem of determining aquatic
habits in fossil mammals.
CONCLUSION
Increased bone density is highly correlated
with aquatic habits in mammals. Somewhere
along the various evolutionary lines leading
toward aquatic existence bone density be-
came more important than it is in terrestrial
mammals. I believe that the transitional stage
during which selection for increased bone
density occurred was when total body sub-
mergence became a habitual part of the an-
imals' life style. Many terrestrial mammals
spend at least some time in water (good ex-
amples being the moose, Alces, and African
elephant, Loxodonta), but they do not have
unusually dense bones because they generally
remain partially above the surface where
buoyancy is not a problem. Truly aquatic
mammals spend much of their time with most
of their body below the water surface, and
therefore high bone density plays an impor-
 LIMB-BONE DENSITY AND AQUATIC HABITS
tant role in achieving neutral buoyancy for
the entire body or becoming slightly denser
than water.
Higher density of limb bones of aquatic
mammals is primarily the result of greater
deposition of compact bone along the shafts.
Since there are visual differences between the
internal architecture of aquatic and terrestrial
mammal limb bones fossil mammal bones
can be sectioned and placed in either an
aquatic or terrestrial group.
ACKNOWLEDGMENTS
I thank M. C. Coombs, M. Voorhies, D.
Domning, T. A. Griffiths, C. R. Schloyer, and
B. J. Verts for their advice and criticism of
the manuscript. In addition I thank C. J.
Gamble, A. E. Pratt, and D. G. Smith for
their aid during development of this project.
Finally I thank K. F. Koopman (AMNH), C.
O. Handley (NMNH), and D. Klingener
(UMA) for allowing me access to specimens
for this study. This research was partially
supported by NSF Doctoral Dissertation
Grant DEB-7914783.
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REVISEDMANUSCRIPTRECEIVEDJUNE 3, 1982