DIETARY STUDIES OF MARINE MAMMALS USING STABLE CARBON AND NITROGEN ISOTOPIC RATIOS OF TEETH

MARINE MAMMAL SCIENCE, 15(2):314-334 (April 1999) 0 1999 by the Society for Marine Mammalogy

DIETARY STUDIES OF MARINE MAMMALS USING STABLE CARBON AND NITROGEN

ISOTOPIC RATIOS OF TEETH JANE L. WALKER

STEPHEN A. MACKO Department of Environmental Sciences,

University of Virginia, Charlottesville, Virginia 22903, U.S.A.

ABSTRACT

This study used naturally occurring carbon and nitrogen stable isotopes of teeth to study the diets of marine mammals. The isotopic ratios of non- chemically preserved teeth from eight species of marine mammals, representing 87 individuals that spanned the trophic continuum, were found to reflect nutritional sources. The V3C signals distinguished animals that lived in waters dominated by different primary producers (e.g., seagrass, kelp, and phytoplankton), and ti1” values indicated the diet and trophic level of the species. This research suggests that isotopic signatures of teeth can be used in dietary studies to show differences and similarities among age classes, genders, geographic locations, and time periods.

Key words: carbon isotopes, nitrogen isotopes, teeth, marine mammals, diet.

The difficulty in determining feeding habits of marine mammals is appre- ciable. The ability of the animals to submerge for long periods of time and their capability of feeding underwater hinder field research studies. Even when direct observations are possible, only a part of the total diet is learned. Like- wise, stomach content analysis can provide valuable data about foods consumed but does not reflect the entire diet of the animal.

Stable-isotopic analyses offer advantages over traditional methods of study- ing the diets of marine mammals. Stable isotopes record the nutrients that are assimilated and not simply those ingested. Only small sample amounts (5-10 mg) are needed, and samples can be obtained from museum specimens or fossilized material. Additionally, both short-term and long-term diets can be studied from stable-isotopic analyses.

Metabolic discrimination between the heavy and light isotopes in a pre- dictable manner forms the basis for using the isotopic technique in dietary studies. In laboratory investigations isotopic compositions of organisms that were fed controlled diets were found to reflect the isotopic signatures of the

3 14

WALKER AND MACKO: ISOTOPIC DIETARY STUDIES 315

nutritional sources (DeNiro and Epstein 1978, 1981; Macko et al. 1982, 1987; Ames e t af. 1996; Hobson e t al. 1996). DeNiro and Epstein (1978, 1981) observed that animals were more enriched by about l%o for 13C and approximately 3%0 for 15N when compared to the isotopic compositions of the diet.'

Isotopic enrichment of an animal in relation to its food has been reported from field studies as well, and individual tissues of larger animals have been shown to also reflect the diet (McConnaughey and McRoy 1979, Schoeninger and DeNiro 1984, Hobson and Welch 1992, Ostrom e t al. 1993a, Hobson and Stirling 1997). Schoeninger and DeNiro (1984) found bone collagen of marine and terrestrial feeders to be about 3%0 enriched in ISN for each increase in trophic level, but the S13C values did not correspond to the trophic level. Factors other than trophic level shifts seemed to more strongly influence the S13C compositions (Schoeninger and DeNiro 1984).

Because tissues have different biochemical compositions and are synthesized and catabolized at various rates, the isotopic ratios of individual body com- ponents may differ (DeNiro and Epstein 1978, 1981; Tieszen e t al. 1983; Abend and Smith 1995; Ames e t al. 1996; Hobson et al. 1996; Hobson and Stirling 1997). For instance, skin has a faster turnover rate than teeth. Thus, skin represents only nutrients that have been assimilated relatively recently in comparison to those of teeth (Abend and Smith 1995). Stable isotopes, therefore, can be used to study short-term diets or long-term diets.

Isotopic compositions derived from organic and inorganic fractions of teeth have been used to examine modern diets, as well as to reconstruct historic diets and climatic conditions (DeNiro and Weiner 1988; Ostrom et af. 1989, l993b; Bada et af. 1990; van der Merwe e t al. 1990; Thackeray e t al. 1990; Abend and Smith 1995; Koch et al. 1995; Thewissen e t al. 1996; Hobson and Sease 1998). Ostrom et al. (1989, 19936) examined high-molecular-weight organic material within fossilized reptilian teeth from the Judith River For- mation to suggest a trophic structure during the Late Cretaceous Period. Iso- topic compositions from modern teeth have also provided valuable feeding information about moose, elephants, pilot whales, and Steller sea lions (Bada e t al. 1990, van der Merwe e t al. 1990, Abend and Smith 1995, Koch et al. 1995, Hobson and Sease 1998).

In this study the organic portions of teeth from marine mammals were isotopically determined. Teeth are excellent tissues for isotopic research because they preserve organic matter well, contain a sufficient amount of organic material for analyses, and can reveal short-term and long-term dietary information about an individual. Because marine mammals have numerous teeth, museums are often willing to donate a tooth for the destructive sampling required for isotopic analysis. In addition, museums frequently have modern and historic specimens from which to obtain teeth for comparison studies. These properties make teeth ideal for use in stable-isotopic dietary research of marine mammals.

The dental isotopic signatures from various marine mammal species were compared to the known information about the foods significant to the diet of

Isotopic compositions are expressed as: t iNE = {(Rrample/Rrtandard) - 11 X 1,000.

316 MARINE MAMMAL SCIENCE. VOL. 15. NO. 2, 1999

the respective species. This study also verifies the use of a single tooth to represent the dental isotopic composition of an animal and suggests that isotopic subsamples within a tooth can be used to address short-term dietary quest ions.

METHODS

Teeth from eight species that span the trophic continuum were isotopically analyzed and compared: walrus (Odobenas rosmarm), harp seal (Phoca groenlan- dicas), sea otter (Enhydra Iatris), West Indian manatee (Trichechas manatas), pygmy sperm whale (Kogia breviceps), killer whale (Orcinzss orca), bottlenose dolphin (Tarsiops trancatas), and common dolphin (Delphinas delphis). All of the tooth samples were obtained from private and government collections. Tooth samples from the walrus and harp seal were taken from animals that were killed in seasonal hunts. The other specimens were taken from stranded animals or from incidental catches by fisheries. For instance, the manatees were stranded in the Indian and Banana River systems in Brevard County, Florida, and the common dolphins were accidently killed in squid and mackerel fisheries. Three of the bottlenose dolphin specimens used in this study (571385, 571426, and 571439) were killed in offshore fisheries. The other bottlenose dolphin specimens were stranded animals determined to be from an offshore population based on morphometry, food habits, and internal par- asites as described by Mead and Potter (1995).

Available information about the specimens was recorded (Table 1). The year in which the animal was collected, the estimated degree of latitude and degree of longitude of the capture or stranding location, and the gender of the specimen were usually known. The age class of each specimen was approximated based on information about the natural history of the species along with the recorded weight and length of the specimen or in conjunction with a determined age. A specimen was considered to be young if of nursing age, a subadult if no longer nursing but not sexually mature, and an adult if sexually mature.

Before testing for interspecific isotopic differences, isotopic heterogeneity within and between teeth of individual specimens was examined. A longitu- dinal section of a tooth from an adult sperm whale (Physeter macrocephalas) was subsampled to examine within-tooth heterogeneity. Twelve samples were taken from the center of the tooth from the apex to the pulp region so that the diet of a progressively older animal was represented. Each subsample contained several growth layer groups. The first four subsamples were from dentinal layers deposited when the animal was young, although probably not when the major portion of the nutrients came from nursing. Subsamples 11 and 12 represented the diet of the animal during the years just prior to its death.

Samples representing the long-term diets of a walrus and a bottlenose dolphin were also analyzed and examined to study the isotopic heterogeneity within dental tissue. A sample containing all growth layers was collected from the cleaned, upper right postcanine of a walrus using a carbide bur and a drill.


One side of a bisected, cleaned tooth from a bottlenose dolphin was crushed. Fifteen random samples were analyzed from the powder of the respective walrus and bottlenose dolphin specimens.

The isotopic heterogeneity among teeth of individuals was determined to address if a sample from one tooth could sufficiently represent the dental isotopic signature of the animal. The isotopic differences among teeth of the same individual were estimated for three species from different taxonomic orders. Eight teeth were taken from a young male walrus to represent the Carnivora; twelve teeth of a male bottlenose dolphin represented the toothed Cetacea, and the S13C and 6l5N signatures were determined for a back molar and a front molar of three two-year-old manatees (order Sirenia).

In order to lessen the likelihood of using material that had been isotopically altered or contaminated with organic preservatives, non-chemically preserved specimens were analyzed. All samples were stored at room temperature and cleaned of outer material with a carbide bur attached to a drill. The dried portions of pulp remaining within the teeth were removed prior to analyses so that only the isotopic values of the calcified constituents were compared. The samples were soaked in chilled 30% hydrochloric acid (HC1) to remove carbonates, rinsed with deionized water, and dried. With the exception of the subsampled sperm whale tooth, samples were either crushed to a fine powder or drilled across all of the dentinal layers of the tooth. The results from tooth sections prepared using both crushing and drilling techniques yielded similar isotopic signatures and suggest that the sample preparation method did not alter the isotopic signature (Walker 1995).

Each sample was converted to gases for isotopic analysis using a Dumas combustion technique (Macko et af. 1987). Briefly, samples were combusted in an evacuated quartz tube in the presence of copper and copper oxide at 850°C for one hour. The resulting carbon dioxide and nitrogen gases were cryogenically separated from one another and the other combustion products (e.g., H,O and SO,). The 6l5N and S'3C compositions were assessed on a dual- inlet, triple collector VG PRISM stable-isotope-ratio mass spectrometer by comparing the sample gases with laboratory tank standards that were cali- brated against the international standards of Peedee Belemnite (PDB) for carbon and atmospheric N2 for nitrogen. Based on replicate analyses of homo- geneous materials and standards, the typical reproducibility for one standard deviation for S'3C and 615N analyses is approximately +O.l%o.

The Statistical Package for the Social Sciences (SPSS) was utilized in the analysis of the data. A Lilliefors test assessed normality, and a Box's M test determined equality of the variance-covariance matrices. Multivariate analysis of variance (MANOVA) tested for significant interspecific differences for the two variables S13C and V5N. The statistically analyzed data were reported in terms of Fm+ (the transformed value of the test statistic for an approximate F distribution with rn degrees of freedom for the hypothesis and n degrees of freedom for the error) and P, which indicates the observed significance level.

TubZ

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tion,

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and

age

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Spec

ies

Wal

rus

Wal

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rus

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rus

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rus

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rus

Mea

n SD

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arp

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H

arp

seal

H

arp

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H

arp

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arp

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arp

seal

H

arp

seal

H

arp

seal

H

arp

seal

H

arp

seal

H

arp

seal

M

ean

SD

Cod

e C

arbo

n N

itrog

en

Yea

r La

t. Lo

ng.

Sex

A62

5 A

630

A64

3 A

650

A654

A

673

A67

8 A

686

A69

4 A

697

M92

2324

M

9308

79

M93

0881

M

9308

89

M93

0894

M

9309

30

M93

0934

M

9309

40

M93

0942

M

9309

48

M93

095

1

-13.

8 14

.4

-13.

8 14

.5

-13.

3 15

.4

-13.

4 14

.5

-13.

4 15

.1

-12.

9 14

.5

- 12

.7

13.9

-1

3.7

15.0

-1

3.5

14.6

- 12

.7

14.6

-1

3.3

14.6

0.

4 0.

4 -1

5.0

15.2

-1

5.2

16.2

-1

5.5

15.9

-1

5.8

15.9

-

14.8

14

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-15.

1 15

.8

-15.

0 16

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- 14

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16.5

-1

5.2

15.7

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5.3

14.4

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5.0

15.6

-1

5.1

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0.

3 0.

7

1956

19

56

1956

19

56

1956

19

56

1956

19

56

1956

19

56

1992

19

92

1992

19

92

1992

19

92

1992

19

92

1992

19

92

1992

64

64

64

64

64

64

64

64

64

64

54

54

54

54

54

54

54

54

54

54

170

170

170

170

170

170

170

170

170

170 57

57

57

57

57

57

57

57

57

57

m

m

m

m

m

m

m

m

m

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Tabl

e I.

C

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Spec

ies

~~

~ ~

~

Cod

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r La

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ng.

Sex

Age

cla

ss

Sea

otte

r 27

88

-11.

7 13

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1973

Se

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ter

2793

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1.2

14.9

19

74

Sea

otte

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01

-11.

4 13

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Sea

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05

- 10

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19

76

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r .

2902

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19

76

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04

-10.

3 14

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1976

Se

a ot

ter

291 1

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15.0

19

76

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14

-11.

6 14

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1976

Se

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2919

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76

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0.

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anat

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1990

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11

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1990

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15

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1990

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Man

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CF

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1990

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43

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90

Man

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CF

9044

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1990

M

anat

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46

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90

Man

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CF

9049

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1990

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ean

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0.

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30

2040

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99

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erm

wha

le

5043

14

-11.

4 12

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1975

Py

gmy

sper

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50

4319

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19

75

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y sp

erm

wha

le

5043

38

-12.

5 12

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1976

Py

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sper

m w

hale

50

4484

-1

1.2

12.2

19

75

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y sp

erm

wha

le

5047

34

-12.

1 11

.9

1977

Py

gmy

sper

m w

hale

50

4737

-1

2.1

13.7

1.

978

36

121

37

122

37

122

37

122

37

122

37

122

37

122

37

122

28

81

28

81

28

81

28

81

28

81

28

81

28

81

28

81

28

81

28

81

39

75

37

77

37

76

39

74

32

81

29

94

37

76

~ m

adul

t m

ad

ult

m

adul

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su

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m

m

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m

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m

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ad

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ult

m

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ad

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m

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ad

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Tabl

e 1.

C

ontin

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Spec

ies

Cod

e C

arbo

n N

itrog

en

Yea

r La

t. Lo

ng.

Sex

Age

cla

ss

Pygm

y sp

erm

wha

le

Pygm

y sp

erm

wha

le

Pygm

y sp

erm

wha

le

Pygm

y sp

erm

wha

le

Pygm

y sp

erm

wha

le

Mea

n SD

K

iller

wha

le

Kill

er w

hale

K

iller

wha

le

Kill

er w

hale

K

iller

wha

le

Kill

er w

hale

K

iller

wha

le

Kill

er w

hale

K

iller

wha

le

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er w

hale

K

iller

wha

le

Mea

n SD

B

ottle

nose

dol

phin

B

ottle

nose

dol

phin

B

ottle

nose

dol

phin

B

ottle

nose

dol

phin

B

ottle

nose

dol

phin

B

ottle

nose

dol

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B

ottle

nose

dol

phin

B

ottle

nose

dol

phin

B

ottle

nose

dol

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ean

SD

5047

47

5048

66

5049

02

5501

03

5501

14

US

60-1

U

S 61

-1K

19

63-8

32

1964

-986

19

65-4

19

67-1

57

1967

-1 75

32

04

3265

32

66

3774

5047

66

5048

79

5049

06

5503

75

5504

46

5713

85

5714

26

5714

39

5714

96

- 12

.0

- 1

2.8

-11.

8 -1

1.5

-12.

4 -1

2.0 0.5

-11.

9 -1

3.3

- 1

2.1

- 1

3.9

- 1

3.3

-13.

1 - 1

3.5

- 1

2.8

-11.

9 - 1

2.2

- 1

3.7

- 1

2.9

0.7

- 1

4.4

-13.

7 -1

3.1

-13.

5 -1

3.7

- 1

4.2

- 14

.0

- 14

.2

- 14

.2

-13.

9 0.4

12.0

13

.3

11.7

12

.4

12.0

12

.4

0.9

17.7

18

.1

19.9

16

.3

16.5

18

.6

18.0

16

.6

17.6

17

.5

17.3

17

.6

1 .o

14.4

14

.8

13.6

15

.6

15.5

15

.5

13.7

14

.4

15.6

14

.8

0.8

1978

19

78

1979

19

81

1981

1960

19

61

1963

19

64

1965

19

67

1967

19

66

1967

19

67

1968

1971

19

79

1979

19

84

1984

19

89

1990

19

90

1992

35

37

35

36

39

57

37

38

34

34

38

38

35

48

48

55

36

36

34

41

42

40

41

37

39

76

76

77

75

75

152

123

123

121

121

124

124

121

123

123

166

76

75

79

72

70

67

67

75

74

m f m f m

m

rn

m f m

rn f m f rn f m

m

m

m

m

m

m

m

m

adul

t ad

ult

adul

t ad

ult

adul

t

suba

dult

adul

t su

badu

lt ad

ult

adul

t ad

ult

suba

dult

adul

t ad

ult

adul

t su

badu

lt

adul

t ad

ult

adul

t ad

ult

adul

t Y

oung

ad

ult

You

ng

suba

dult

A

n 4 u

A

0

0

Tabl

e C

ontin

uec

Spec

ies

Cod

e C

arbo

n N

itrog

en

Yea

r La

t. Lo

ng.

Sex

Age

cla

ss

Com

mon

dol

phin

C

omm

on d

olph

in

Com

mon

dol

phin

C

omm

on d

olph

in

Com

mon

dol

phin

C

omm

on d

olph

in

Com

mon

dol

phin

C

omm

on d

olph

in

Com

mon

dol

phin

C

omm

on d

olph

in

Com

mon

dol

phin

C

omm

on d

olph

in

Com

mon

dol

phin

C

omm

on d

olph

in

Com

mon

dol

phin

M

ean

SD

5505

50

5507

50

5507

75

5507

76

5507

78

5507

80

5508

09

5508

13

5508

61

5508

62

5508

66

5509

27

5712

13

5713

34

5713

98

- 14

.6

- 14

.4

- 14

.4

- 14

.4

- 14

.4

-13.

9 - 14

.5

-15.

1 -1

5.1

- 14

.9

- 14

.5

- 14

.7

- 14

.6

-14.

1 - 14

.4

-14.

5 0.3

11.6

11

.4

12.6

13

.7

12.9

13

.5

12.3

12

.7

11.6

12

.5

11.5

13

.5

13.6

11

.6

11.8

12

.4

0.8

1986

19

86

1986

19

86

1986

19

86

1986

19

86

1986

19

86

1986

19

87

1988

19

89

1990

39

39

38

38

39

38

39

39

39

38

39

38

38

39

73

73

73

75

76

74

73

73

73

74

73

75

74

73

m

m

m

m

m

m

m

m

m

m

m

m

m

m

m

adul

t ad

ult

adul

t ad

ult

adul

t ad

ult

adul

t ad

ult

adul

t ad

ult

suba

dult

adul

t su

badu

lt ad

ult

adul

t

322 MARINE MAMMAL SCIENCE, VOL. 15, NO. 2 , 1999

Table 2. P C and 6I5N signatures (%G) for subsamples from sperm whale tooth tepresenting diet of animal as it aged. Sample numbers correspond to progressively older individual.

Subsample Carbon Nitrogen ~

1 2 3 4 5 6 7 8 9

10 11 12

- 12.5 -13.1 -12.7 -12.1 -12.9 -12.9 - 12.8 -13.1 -13.3 -13.6 -13.8 -13.8

17.7 18.1 17.1 17.5 16.1 17.3 16.6 17.3 17.2 17.0 17.0 17.1

RESULTS

Heterogeneity of teeth-The 613C values of the subsampled sperm whale tooth showed a general trend in becoming lower for the dentinal layers that reflected the diet of the animal as it became progressively older (range -13.8%- -12.1%0, Table 2 ) . Within the tooth, the 613C and 6I5N signatures varied by 2 0 . 5 % ~ for one standard deviation. The P 5 N signatures ranged from 16.1%0 to 18.1%0. The lowest SISN values came from subsamples 5 and 7. The most enriched 6l5N compositions were collected from the samples that represented the diet of the animal when young (Subsamples 1 ,2 , and 4; Table 2) . Different portions of a tooth thus provided distinct isotopic signatures that could reflect dissimilar short-term diets.

The isotopic signatures obtained from multiple samples of a tooth of a walrus and bottlenose dolphin varied by less than or equal to +0.4%0 for both 613C and 615N compositions (Table 3). The eight teeth taken from a young male walrus were found to vary by ?0.2%0 for the 6l3C compositions and ?0.3%0 for the 615N signatures. Similarly, the twelve teeth from a male bottlenose dolphin had 6I3C signatures that varied by ?O.~%G and 615N compositions that varied by ?0.4%0. The isotopic signatures of the manatee teeth exhibited more isotopic heterogeneity compared to those of the walrus and bottlenose dolphin. The front molars of the three manatees contrasted by less than 1 . 0 % ~ in both 6l3C and SI5N signatures compared to the back molars. There appeared to be no consistent isotopic trend between the two molars (Table 3).

Isotopic signatures of different species-A comparison of the isotopic signatures of the eight species analyzed (walrus, harp seal, sea otter, West Indian manatee, pygmy sperm whale, killer whale, bottlenose dolphin, and common dolphin) showed distinct separations (F14,158 = 100.45, P < 0.0005, Table 1, 4, Fig. 1). The 613C and 615N compositions of teeth indicated the long-term diets of


Table 3 . Carbon and nitrogen isotopic heterogeneity within single tooth and between different homogenized teeth from single animal. For manatee specimens, front molar was compared to back molar.

Mean (%o) SD (%o)

Heterogeneity n 8'3C 61SN U3C @SN

Within a tooth Walrus 15 -13.4 15.6 0.2 0.3 Bottlenose dolphin 1 5 - 13.5 14.9 0.4 0.4

Walrus 8 -13.4 15.3 0.2 0.3 Bottlenose dolphin 12 -13.3 14.8 0.1 0.4 Manatee

Between teeth

- - A Front 1 -8.5 7.7 Back 1 -9.4 8.0

B Front 1 -11.6 8.7 Back 1 -11.0 8.5

C Front 1 -10.1 9.5 Back 1 -10.6 9.0

- - - - - - - - - -

the animals analyzed, directly reflecting the energy transferred from the foods to the specimens.

The teeth most depleted in '3C came from three species that were collected from the western North Atlantic: harp seals (mean -15.1 t 0.3%0), common dolphins (mean -14.5 2 0.3%0), and bottlenose dolphins (mean -13.9 * 0.4%0, Table 1, 4; Fig. 1). The two species represented by specimens taken from the Pacific Ocean, the walrus and killer whale, had 6% signatures of -13.3 * 0.4%0 and -12.9 5 0.7%0, respectively (Table 1, 4; Fig. 1). The teeth of the pygmy sperm whales, sea otters, and manatees were more enriched in 613C relative to the other species (Table 1, 4; Fig. 1). The sea otters lived in a region where kelp served as the predominant carbon source, and the l3C- enriched nature of kelp was evident in the 613C signatures of the sea otter teeth (mean -11.1 2 0.5%0). The manatee samples had the heaviest 6l3C values (mean -9.9 t 0.8%0). Manatees consume large amounts of sea grasses, which are known to be enriched in 13C (Harrigan et a/. 1989).

Although individuals within a species may exhibit different food preferences, the mean 6l5N compositions for each species (Table 1, 4; Fig. 1) compare well with published isotopic values of food items significant to the diets of the respective species. The manatees, being herbivorous, had the lowest 615N signals (mean 7.8 * 0.8%0). The average 615N values for the tooth samples of the common dolphins and pygmy sperm whales were 1 2 . 4 % ~ ~ The teeth of the sea otters (14.5 5 0.7%0), walruses (14.6 5 0.4%0), and bottlenose dolphins (14.8 t 0.8%0) had similar mean 615N values. The harp seals had teeth that were relatively enriched in 15N (mean 615N = 15.7 5 0.7%0), reflecting a diet of fish. The teeth from killer whales had the most enriched mean 615N values (17.6 ? 1.0%). Because killer whales often feed high on the trophic

Tabl

e 4.

M

ean

a13C

and

6l5

N s

igna

ture

s ?

one

SD

(%o)

and

isot

opic

ran

ges

for

toot

h sa

mpl

es fr

om e

ight

mar

ine

mam

mal

spe

cies

.

Mea

n R

ange

n 6‘

3C (

%o)

6’

” (%

o)

613C

(%

o)

6I5N (%

o)

Wal

rus

10

-13.

3 2 0

.4

14.6

? 0

.4

-13.

8 to

-12

.7

13.9

to 1

5.4

Har

p se

al

11

-15.

1 2 0

.3

15.7

2 0

.7

-15.

8 to

-14

.7

14.4

to 1

6.6

Sea

otte

r 9

-11.

1 t 0

.5

14.5

2 0

.7

-11.

7 to

-10

.3

13.6

to 1

5.7

Man

atee

10

-9

.9 t 0

.8

7.8

? 0

.8

-11.

0 to

-8.

2 6.

4 to

9.0

Py

gmy

sper

m w

hale

12

-1

2.0 t 0

.5

12.4

? 0

.9

-12.

8 to

-11

.2

11.3

to 1

4.3

Kill

er w

hale

11

-1

2.9

2 0

.7

17.6

t 1

.0

-13.

9 to

-11

.9

16.3

to 1

9.9

Bot

tleno

se d

olph

in

9 -1

3.9

5 0

.4

14.8

? 0

.8

-14.

4 to

-13

.1

13.6

to 1

5.6

Com

mon

dol

phin

15

-1

4.5

2 0

.3

12.4

2 0

.8

-15.

1 to

-13

.9

11.4

to 1

3.7


15 - z : z 2 Q '

0

$4 J

l o A% 4A A AA A

Walrus

Harp-

sea Otter

Manat&

WPY Sperm Whale

Killer Whale

Bottlenose Dolphin

Common Ddphin

-20 -15 -10 -5

6°C f%o)

T t Killer m e 1

l o t , , . . , . ::.. .

5 -20 -15 -10 -5

6I3C (k)

Figwe 1. 613C and 615N signatures of teeth (%o) from eight marine mammalian species, representing (a.) each individual animal and (b.) mean values for each species (? one SD.).

continuum, some even eating carnivorous marine mammals, their enriched S15N signatures were not surprising.

DISCUSSION

Heterogeneity of teeth-Dentin comprises the majority of the tooth and makes up most of the sample analyzed. This dental component is deposited in layers until the pulp cavity is filled, which takes many years for most marine mammals. By isotopically sampling different layers, changes in diet that occur as an animal matures can be recorded. By sampling an entire tooth, an average of the isotopic signatures for the represented time can be obtained.

In general, relative enrichment of the isotopic compositions was present in the sperm whale subsamples that represented the growth layer groups of the

326 MARINE MAMMAL SCIENCE, VOL. 1 5 , NO. 2 , 1999

animal when young (Table 2). Immature sperm whales generally nurse from 1.6 to 3.5 yr (Best et al. 1984), although lactose has been found in the stomachs of individuals up to 13 yr old (Rice 1989). Sperm whales are gradually weaned onto solid food, beginning within the first year of life (Rice 1989). Steele and Daniel (1978) found milk from cattle to be isotopically enriched in lSN relative to the diet of the animal. A young animal, which utilizes an enriched diet, preferentially incorporates the heavier isotopes. Thus, the growth layer groups formed when the animal was deriving all or part of its nutrition from milk would be enriched compared to the growth layer groups represented when the individual had been weaned.

Sperm whales primarily prey on a number of different squids (e.g., Dosidicus, Ommastrepher, Morotezlthis, Gonatus, Taningia, Histioteuthis, Mesonychoteuthis). Dermersal fish contribute to the diet as well, often being a more important food source than squid in the high latitudes and tending to be more significant to maies than females (Rice 1989). The gender and capture location of the specimen used in this study were not known.

Schell et al. (1989) utilized V3C signatures along the length of baleen plates to study the nutritional importance of different habitats to migrating bowhead whales (Balaena mysticetus). The research presented here suggests isotopic differences between growth layer groups of teeth may also provide a chronological record of feeding activities. For instance, isotopic differences between growth layer groups may result from annual fluctuations in abundance for prey items. A change in diet, therefore, could be recorded in the isotopic compositions of a single tooth.

The 613C and VrN values for a powdered single tooth and for crushed samples from different teeth of an individual varied less than +0.5%0 for a walrus and a bottlenose dolphin (Table 3). This small difference indicates that a single powder sample can adequately represent the dental isotopic signature of a specimen. The development of teeth occurs at approximately the same time within individual marine mammals of both Carnivora and Cetacea. Wal- ruses possess two sets of teeth during their lives. Like many pinnipeds, walruses have primary teeth that are usually absorbed by birth, and the development of the secondary teeth begins in utero (Fay 1982). Bottlenose dolphins, like other toothed cetaceans, have only one set of teeth during their lives (Martin et al. 1990). Both walruses and bottlenose dolphins have dental layers that are deposited for a number of years before pulp cavity closure. These properties may result in the small dental isotopic variations observed within the multiple samples collected from an individual walrus and a bottlenose dolphin.

Manatees continuously replace their teeth, so that new molars erupt in the back of the jaw and push the other teeth forward (Reynolds and Ode11 1991). As a result of this tooth replacement, dentinogenesis in manatees occurs for a shorter time than it does in most marine mammals. The isotopic signatures of manatee teeth, therefore, reflect the nutrition assimilated within a shorter time period than they do for other marine mammalian species.

The front and back molars of the three young manatees contrasted by less


than ? 1.0%0 in both 6l3C and 615N signatures (Table 3). Because the isotopic compositions of the front molars of the manatees were similar to those of the back molars, the data suggest that a representative sample can document the dental isotopic signatures. Owing to the process of tooth replacement, how- ever, caution should be taken when comparing the dental isotopic signatures of manatees, especially with young animals that might be undergoing a change in diet from milk to vegetation.

Isotopic signatares of d$firent species-The 6% and 615N values reflect the long-term diets of the animals analyzed and indicate the energy transferred along the trophic continuum. Owing to the greater abundance of carbon relative to nitrogen within food sources, more metabolic reactions are required before discernable differences can be observed between the 613C compositions of the diet and those of the consumer. Therefore, the dental 613C values are more similar to those of the primary producers at the base of the food web than are the respective 615N compositions. Because of the distinction in 6°C compositions for various plants, carbon isotopes can illustrate differences in regions dominated by different producers and can be used to trace the flow of nutrients through the ecosystem. The 615N data more clearly denote trophic level shifts between species, as has been shown in previous studies (Schoeninger and DeNiro 1984, Harrigan e t al. 1989, Hobson and Welch 1992, Ostrom et al. 1 9 9 3 ~ ) .

The harp seal teeth were collected from eleven animals killed off Newfound- land and gave the most depleted S13C signatures (mean -15.1 2 0.3%~~) of the species examined (Table 1, 4; Fig. 1). The low S13C signal may be explained by the fact that phytoplankton tends to be more depleted in higher latitudes (Sackett et al. 1965, Rau et al. 1989). The common dolphins and bottlenose dolphins in this study also came from the western North Atlantic but from a location farther south than the harp seals. The mean 613C values were similar for the two species (common dolphin - 14.5 2 0.3%0, bottlenose dolphin - 13.9 ? 0.4%0), with the bottlenose dolphins being slightly higher in l3C content (Table 1, 4; Fig. 1). The observed enrichment of the bottlenose dolphins can be explained by the increase of about 1 . 0 % ~ ~ in 13C for each increase in trophic level and the higher trophic level from which the bottlenose dolphin feeds.

The walrus teeth were collected off Alaska and had an average 613C signature of -13.3% 2 0.4%0 (Table 1, 4; Fig. 1). Walruses are benthic feeders (Fay 1982), and McConnaughey and McRoy (1979) observed enriched 613C values in benthic organisms relative to pelagic organisms. The 13C enrichment of benthic organisms has been attributed to lower water turbulence causing enrichment of benthic primary producers, owing to an increased diffusion resistance of carbon into the benthic plants (France 1995). Other explanations include bacterial utilization and reworking of planktonic carbon in sediments and more complex food webs with more trophic levels (McConnaughey and McRoy 1979, Fry and Sherr 1984).

The killer whale specimens were collected along the eastern North Pacific, from San Miguel Island, California, to Akutan, Alaska. The mean 6I3C com-

328 MARINE MAMMAL SCIENCE, VOL. 15. NO. 2 , 1999

position of the teeth (-12.9 2 0.7%0) was enriched relative to those for walruses, bottlenose dolphins, common dolphins, and harp seals (Table 1 , 4; Fig. 1) . Considering the high trophic level from which killer whales feed, the higher average S13C value was not surprising. The killer whale teeth also reflected a larger difference in carbon sources than most of the other species. Although individual killer whales or pods may have specific food preferences, as a group, they eat a large variety of foods that span the trophic continuum (Hoyt 1981) and therefore have diverse S13C compositions. Our specimens were collected from different geographic locations (Table l ) , offering another explanation for the higher S13C variation. Some of the killer whales in this study could have come from pods that inhabit waters influenced by kelp, which are enriched in l3C relative to most phytoplankton (Sackett et al. 1965, Stephenson et al. 1984, Duggins e t al. 1989). Environmental differences such as light intensity, nutrient concentrations, and species composition affect the S13C values of the primary producers in a region (Wong and Sackett 1978, Gearing et al. 1984, Fogel and Cifuentes 1993), and their isotopic values are reflected throughout the food web of the area.

The S13C values of the pygmy sperm whale teeth (mean -12.0 *0.5%0) were higher than those from the other western North Atlantic species living in plankton-dominated waters (Table 1 , 4; Fig. 1) . They also differed from the -17.2%0 found by Ostrom e t al. (1993a) for S13C ratios of pygmy sperm whale bone from the western North Atlantic in the vicinity of Newfoundland, Canada. Pygmy sperm whales are thought to inhabit waters along the conti- nental shelf and consume primarily cephalopods (Caldwell and Caldwell 1989). Phytoplankton should serve as the primary carbon source, so the reason for the enriched S13C signatures remains unclear.

The sea otters from which the teeth analyzed in this study were derived came from a region containing large kelp beds. The SI3C signature of a single kelp blade (Laminaria longicraris) was shown to range from -20%0 to - 12%0 in a young plant (Stephenson e t al. 1984). Despite this variation, whole kelp plants tend to be clustered in their S13C signatures (-17.6 ? 2.1%0, n = 47, Stephenson e t al. 1984; -17.7 ? 2.3%0, n = 162, Duggins e t al. 1989) and enriched relative to phytoplankton ( - 3 1 % ~ - 2 0 % 0 , Sackett e t al. 1965). The S13C isotopic signatures of the sea otter teeth reflected this enriched carbon source. The sea otter teeth had a mean S13C signature of -11.1 2 0.5%0, whereas most of the other species had mean S13C values of less than -12.5%0 (Table 1 , 4; Fig. 1).

The herbaceous manatees consume large quantities of sea grasses (Reynolds and Ode11 1991). The S13C values of three species of Florida sea grasses are highly variable, ranging from -13.6%0 to -8.4%0 (Harrigan e t al. 1989). A 1%0 trophic enrichment for the S13C signatures of the seagrasses yields a range for 6% compositions of - 12.6%P-7.4%0 for Florida manatees consuming only seagrasses. All of the manatee teeth fell within this expected range for the 6% signatures (Table 1 , 4; Fig. 1).

The S15N signatures for three species of Florida sea grasses fall between 3.4%0 and 3.7%0 (Harrigan et al. 1989). With a 3%0 trophic enrichment over


the 6lSN signatures of sea grasses, Florida manatees feeding solely on sea grasses would have 6lSN values of approximately 6.5%0. The three manatee teeth collected from adults had 615N values (7.0%0, 7.0%0, and 7.5%0) close to 6.5%0, being somewhat enriched in 'SN. Likely the influence of other vegetation in the diet and epiphytic organisms that were inadvertently consumed enriched their 6lSN signature. The subadult manatees had an enriched mean 615N signature of 8.1 5 0.9%0, reflecting the influence of milk in their diet. The I5N enriched values for adults and subadults may also be explained, in part, by nitrogen incorporated from protein produced by symbiotic bacteria in the hindgut. Similar nitrogen enrichment owing to microbial activity within digestive tracts has been suggested in other studies (Sealy et al. 1987).

The diets of common dolphins vary with season and geographic location (Mitchell et al. 1975). Eight of the specimens in this study were caught by a squid fishery, and seven were taken by a mackerel fishery. Stomach content analyses of the specimens revealed that six stomachs contained intact squid. Four additional stomachs had squid beaks, and two others had traces of squid in distal compartments. Six specimens had mackerel in their stomachs, and six stomachs contained small fish or otoliths, which may have been primary or secondary contents. Four small, offshore squid (1. iffecebrosus) from the Grand Banks area in the North Atlantic had an average 6ISN of 9.3 +- O.l%o (Ostrom et al. 1993a). Four Atlantic mackerel (Scomber scombrus) collected from the Newfoundland region had a mean 615N signature of 12.9 2 0.8%0 (Hobson and Montevecchi 1991). The mean 615N value for the teeth of the common dolphins in this study (12.4 ? 0.8%0, Table 1 , 4; Fig. 1 ) reflected an approximate 3.0%0 enrichment compared to the average 615N value of the squid analyzed by Ostrom et al. (1993a) and was slightly depleted relative to the average U5N value of the Atlantic mackerel analyzed by Hobson and Mon- tevecchi (1991). The isotopic results, therefore, suggest that squid are a more important food item to the common dolphin specimens.

Squid are known to be a common component of the diet of pygmy sperm whales. Benthic invertebrates as well as pelagic and demersal fish are thought to supplement the diet (Caldwell and Caldwell 1989). The average 615N signature of the pygmy sperm whale teeth (12.4 +- 0.9%0, Table; 1 , 4; Fig. 1) is 3.1%0 enriched over the average 6I5N value of the squid analyzed by Ostrom et af. (1993a), supporting the idea that pygmy sperm whales commonly prey on squid.

Two of the species represented in this study, the sea otters and walruses, are benthic feeders and had enriched 615N signatures relative to those of many benthic animals. Bivalves collected from Canadian Arctic waters ranged from 7.9%0 to 10.8%0 in 15N, and the mean 615N ratio of sea urchins (Strongyfocen- trotgs sp.) from the same region was 9.9 +_ 0.3%0 (n = 3 , Hobson and Welch 1992). Hermit crabs (Pagurus trigonocheiras) from Alaska had 615N signatures around 12.0%0 (Dunton et af. 1989). Snails (Buccinum sp.) from the Barrow Strait-Lancaster Sound region had 615N values of 12.6 5 0.7%0 (n = 5 , Hob- son and Welch 1992). This same genus of snail (which scavenges on dead and

330 MARINE MAMMAL SCIENCE, VOL. 15, NO. 2 . 1999

decaying flesh) from the Alaskan coast had SISN signatures that ranged from 13.8%0 to 17.1%0 (Dunton et al, 1989).

The mean SISN value of the sea otters collected from Monterey Bay, Cali- fornia (14.5 ? 0.7960, Table 1, 4; Fig. 1) was typical of animals that consume benthic marine organisms (e.g., abalones, snails, sea urchins, clams, and crabs). Walruses prefer clams but also consume polycheates and crustaceans (Fay 1982). The average S15N signature of the teeth of this benthic feeder (14.6 ? 0.4960) was similar to the isotopic composition of the teeth of sea otters (Table 1, 4; Fig. 1).

Mead and Potter (1995) found offshore bottlenose dolphins from the western North Atlantic to consume primarily pelagic squid and fish. Stomach content information from the specimens indicated that the bottlenose dolphins consumed squid and fish. The stomach contents of three of the adults had squid beaks, and three adult stomachs had fish bones and/or otoliths. One specimen (571426) had intact fish, fish bones, otoliths, squid, and numerous squid beaks. The stomach of the subadult (571496) had squid beaks and evidence of fish. The stomachs of the two young specimens (571385, 571439) contained only milk. The mean S15N value for this species (14.8 t 0.8%0) was between those of the squid feeders (pygmy sperm whales) and fish consumers (harp seals) (Table 1, 4; Fig. 1).

The diet of harp seals consists mainly of fish, including Arctic cod (Boreo- gadus saida), capelin (Mallotus villosus), Atlantic herring (Clupeu barengus), and Atlantic cod (Gadus morbuu) (Murie and Lavigne 1991, Sergeant 1991). Cap- elin and Atlantic cod from the east coast of Newfoundland were found to have mean S15N signatures of 13.0%0 (n = 4) and 15.1%0 (n = 2), respectively (Hobson and Montevecchi 1991). Fry (1988) analyzed the SISN signatures of fish from the Georges Bank region and determined that an Atlantic herring had a SISN value of 11.2%0 and an Atlantic cod had a SISN composition of 12.6%0. Amphipods and decapods supplement the diets of harp seals (Sergeant 1991). Hobson and Welch (1992) obtained nitrogen isotopic data for amphipods and decapods from the Barrow Strait-Lancaster Sound region. The 81SN signatures of most of the amphipods were approximately 12%0, and a decapod (Lebbeus poluris) was 14.5 2 0.3%0 (n = 5, Hobson and Welch 1992). The average SISN signature of the harp seal teeth (15.7 -+ 0.7%0, Table 1, 4; Fig. 1) reflected a S15N enrichment in comparison to the isotopic signatures of the represented potential foods.

The teeth from the killer whales were generally enriched in I5N relative to those of the other specimens, indicating a higher trophic position (Table 1 , 4 ; Fig. 1). In all likelihood, the samples came from members of transient pods, as well as killer whales belonging to resident pods. Two of the killer whales were caught in Yukon Harbor, Washington, and are thought to be members of a resident pod, which feeds on migrating fish; these two specimens had SISN signatures (17.5%0, 17.6%0) that were similar, as would be expected for animals living in the same pod and feeding together. Killer whales with more enriched teeth could have come from transient populations, which tend to feed on marine mammals.


In summary, the S13C and S15N signatures of marine mammal teeth reflect the isotopic composition of the diet, recording the assimilated nutrients. The S13C and S15N signatures within a tooth and among teeth of an individual were found to vary less than t l . O % o (usually within +0.4%0). Therefore, one tooth or portion of a tooth that incorporates all of the dentinal layers can be used to reflect the dental isotopic composition of an animal. Long-term diets can be studied using an entire tooth, and short-term diets can be examined using subsets of growth layer groups within a tooth.

The V3C signatures of teeth can be used to study the energy transfer between a consumer and its food, with the W3C compositions of teeth reflecting the S13C values of the primary producers in the regions where the specimens fed. Phytoplankton is the main primary producer in most oceans and serves as the main carbon source for many marine mammals, as reflected by the clustering of the S13C signatures for most of the species. The influence of 13C enriched kelp is observed in the teeth of the sea otters from California, and the Florida manatee teeth reflect the enriched 613C signatures of the sea grasses in their diets.

The P 5 N signatures of teeth reflect diet and trophic level. Herbaceous manatees have the lowest S1>N values. The pygmy sperm whale and common dolphin specimens, which are believed to have consumed significant amounts of squid, have similar V5N values that are considerably more enriched than those of the manatees but lower than the other predators. Sea otters and walruses reflect P 5 N signatures that are consistent for benthic feeders. Bot- tlenose dolphins, consumers of fish and squid, have V 5 N values between those of the squid consumers and the piscivorous harp seals. The killer whales are 15N enriched, showing a high-trophic-level predatory diet.

This research indicates that important natural history information about marine mammals can be derived from the isotopic signatures of their teeth. Within an individual, dietary shifts can be identified if samples from different dentinal layers are collected and isotopically analyzed. Distinct feeding behav- iors for different age classes, genders, and geographic locations within a species can also be studied using this technique. Likewise, dietary shifts over an ex- tended period of time for a given species can be examined. Interspecific dietary differences and similarities can also be addressed.

ACKNOWLEDGMENTS We appreciate the Odum Foundation and the Department of Environmental Sciences

at the University of Virginia for providing funds for this research. The Smithsonian Institution, under the supervision of James Mead and Charles Potter, contributed Sam- ples from pygmy sperm whales, bottlenose dolphins, common dolphins, and a sperm whale. The late Francis “Bud” Fay at the Institute of Marine Science, University of Alaska-Fairbanks gave us dental tissues from walruses. The harp seal teeth were donated by Garry Stenson of the Canadian Department of Fisheries and Oceans. Jim Harvey, with the Moss Landing Marine Laboratories, sent canines from California sea otters. Dale Rice at the National Marine Mammal Laboratory provided teeth from killer whales. We appreciate the efforts of Scott Wright and Ann Spellman of the Florida Marine Research Institute for obtaining molars from manatees.

332 MARINE MAMMAL SCIENCE, VOL. 1 5 , N O . 2 , 1999

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Received: 29 July 1996 Accepted: 12 May 1998

8 1 :223-2 30.

DIETARY STUDIES OF MARINE MAMMALS USING STABLE CARBON AND NITROGEN ISOTOPIC RATIOS OF TEETH

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