South African Journal of Marine Science

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Genetic variation in the bottlenose dolphin

Tursiops truncatus along the KwaZulu/Natal coast,
South Africa

J. A. Goodwin , B. D. Durham , V. M. Peddemors & V. G. Cockcroft

To cite this article: J. A. Goodwin , B. D. Durham , V. M. Peddemors & V. G. Cockcroft

(1996) Genetic variation in the bottlenose dolphin Tursiops�truncatus along the KwaZulu/
Natal coast, South Africa, South African Journal of Marine Science, 17:1, 225-232, DOI:
10.2989/025776196784158400

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S. Afr. J. mar. Sci. 17: 225-232
1996 225

GENETIC VARIATION IN THE BOTTLENOSE DOLPHIN

TURSIOPS TRUNCATUS ALONG THE KWAZULUINATAL COAST,
SOUTH AFRICA

J. A. GOODWIN*§, B. D. DURHAMt, v. M. PEDDEMORSt. and V. G. COCKCROFT*§

Genetic variability and differentiation of the bottlenose dolphin Tursiops truncatus population along the
KwaZulu/Natal coast was examined by horizontal starch gel electrophoresis. In all, 19 loci, encoding ]4 al-
lozymes, were resolved for 40 specimens. Three loci (15,8%) were polymorphic. Average heterozygosity for
the population corresponded with values determined for other delphinid populations. However, the heterozy-
gous state of the enzyme G6PD was only found in female bottlenose dolphins, suggesting that this enzyme may
be X-linked in delphinids. Cluster analysis indicated a trend towards a north-south dichotomy in the
KwaZulu/Natal population, a result supported by previously reported pollutant data as well as greater variabi]i-
ty and smaller genetic distances in the southern cluster. However, non-significant FIT values implied a lack of
true genetic structure in the KwaZulu/Natal population. It is proposed that the annual influx of bottlenose dol-
phins from the Eastern Cape coast, in response to the migration of pilchard Sardinops sagax, results in the cap-
ture of dolphins "resident" on the KwaZulu/Natal south coast as well as Eastern Cape "migrants". Genetic vari-
ation between two potentially distinct populations may contribute to the elevated variability in the "resident"
dolphins and the weak structuring of the K waZulu/Natal population. Small sample sizes did not permit the eval-
uation of structure between "preferred areas" within K waZulu/Natal.

The need to identify and characterize discrete
breeding groups within natural populations is impera-
tive for the effective management and conservation of
such populations and becomes even more critical
where numbers are declining. Inshore populations of
the bottlenose dolphin Tursiops truncatus along the
south-east coast of South Africa are heavily impacted
by pollution and effluent runoff from coastal industry
and agriculture (Cockcroft et al. 1989). Coupled with
an increasing rate of entrapment of small cetaceans
in gill nets set to capture large sharks on the
KwaZulu/Natal coast (Cockcroft and Ross 1990),
these factors may be placing portions of the popula-
tion under depletion pressure. This has initiated inten-
sive investigation into the structure and dynamics of
this population and the effects of continued mortality
in the region.
Knowledge of the genetic structure of a population
is required before marine mammals can be effectively
managed and conserved. The assessment of allozyme
variation and the geographical distribution of allele
frequencies can be used to infer bottleneck or disper-
sal events which may have influenced the genetic
structure of a population (Murphy et al. 1991), as well
as providing an indication of the genetic fitness of the
population and its resilience to major environmental
changes. The use of allozyme variability in the deter-
mination of population structure and differentiation in
cetaceans has been well documented. Allozyme data
reflected a significant degree of heterogeneity among
nine schools of long-finned pilot whales Globicephala
melaena off the Faroe Islands (Andersen 1988) and re-
vealed genetic isolation of northern and southern
forms of short-finned pilot whales Globicephala
macrorhynchus off the Pacific coast of Japan (Wada
1988). Population and species differentiation has also
been characterized in the Balaenoptera (Danielsd6ttir
et al. 1991, Wada and Numachi 1991). Data from al-
lozyme electrophoresis has been used in conjunction
with long-term observations to differentiate bottlenose
dolphin populations on the levels of local populations,
subpopulations and groups (Duffield and Wells 1991).
Additionally, the movement of males between maternal
groups has been identified on the basis of genotype
frequency differences.
Several independent field studies have indicated
that bottlenose dolphins occur as resident groups with-
in defined home ranges (Dos Santos and Lacerda
1987, Ballance 1990, Scott et al. 1990). Observational
and genetic data have suggested that inshore bottle-
nose dolphins may form resident matrifocal groups
with which males from adjacent groups interact
(Duffield and Wells 1991). Ross et al. (1987) suggest-
ed that peaks in sighting rates at certain locations
along the K waZulu/N atal coast reflected "preferred
areas" inhabited by resident schools of bottlenose dol-
phins. Later, Cockcroft et al. (1990) delimited six
areas where sighting frequencies were high. These

* Department of Biochemistry and Microbiology, Rhodes University, P.O. Box 94, Grahamstown 6139, South Africa
t Department of Biology, University of Nata], King George V Avenue, Durban 400], South Africa
~ Natal Sharks Board, Private Bag 2, Umhlanga Rocks 4320, South Africa
§ Centre for Dolphin Studies, Port E]izabeth Museum, P.O. Box 13147, Humewood 6013, South Africa
Manuscript received: January 1996
226 South African Journal of Marine Science 17 1996

29°

KWAZULU I NATAL

INDIAN OCEAN

30°

31° 32° E

Fig. 1: The coast of KwaZulu/Natal, showing the location of the subpopulations (Groups 1-6) of the bottlenose
dolphin Tursiops truncatus, according to Cockcroft et al. (1990)
1996 Goodwin et al.: Genetic Variation in Bottlenose Dolphins 227

Table I: Buffer systems and electrophoresis parameters used to resolve presumptive enzyme loci

Enzyme E.C#a Buffer Time (h) Current (rnA)

Fumerase (FUM) 4.2.1.2 TC-Ib 5 35

Glucose-6-phosphate-dehydrogenase (G6PD) 1.1.1.49 phosphateC 7 55
Glucose phosphate isomerase (GPI/ 5.3.1.9 TC-I 5 40
Glutamate pyruvate transaminase (GPT) 2.6.1.2 TC-I1d 2,5 45
Isocitrate dehydrogenase (IDH) 1.1.1.42 phos/cite 7 43
Lactate dehydrogenase (LDH-I, LDH-2, LDH-3) 1.1.1.27 TC-I1 5 50
Mannose phosphate isomerase (MPI) 5.3.1.8 phosphate/TC-II 5 50
Malate dehydrogenase (MOH-I, MDH-2) 1.1.1.37 phos-cit 7 50
Malic enzyme (ME) 1.1.1.40 TC-I1 16 13
6-phosphogluconate dehydrogenase (6PGD) 1.1.1.44 phosphate 5 40
Phosphoglucomutase (PGM-I, PGM-2) 2.7.5.1 phosphate 5 40
Sorbitol deh.rdrogenase (SDH) 1.1.1.14 TC-II 5 50
Superoxide ismutase (SOD) 1.15.1.1 TC-II 5 50
Xanthine dehydrogenase (XDH-I, XDH-2) 1.2.3.2 phos-cit 7 50

n Enzyme Commission numbers (International Union of Biochemistry 1984, as given in Murphy et al. 1991)
b Tris-citrate buffer I (Selander et al. 197 I)
CSelander et al. (1971)
d Tris-citrate buffer II (Selander et al. 197 I)
e Phosphate-citrate buffer (Selander el al. 1971)
f Stained with the method of Harris and Hopkinson (1976)

were approximately 37 km long and were termed
"home ranges". This separation into distinct groups is
supported by differences in pollution residue levels in
bottlenose dolphins from different localities along the
coast (Cockcroft et al. 1989) and by the geographically
isolated behaviour of dolphins removing fish from
fishermens' lines (Garratt 1980, Ross et al. 1987).
Despite these observations, knowledge of the true
social structure and breeding activity of south-east
African coastal bottlenose dolphins is lacking, thereby
precluding an accurate assessment of the effect of cap-
ture mortality on the genetic fitness of the population.
The current study was undertaken to determine the ge-
netic diversity with respect to allozyme variation of
the K waZulu/Natal bottlenose dolphin population and
to investigate the suspected subdivision of the popula-
tion into "resident" groups.
MATERIAL AND METHODS
Samples of organ tissue were collected opportunisti-
cally from 40 T. truncatus captured incidentally in shark
nets along the KwaZulu/Natal coast, South Africa
(Fig. 1), during the period 1988-1990. Carcasses re-
moved from the nets were stored at -20°C pending
necropsy. Samples of kidney, liver, heart, muscle and
skin from inside the blowhole were taken routinely
from thawed carcasses. These were stored in
polypropylene tubes in liquid nitrogen pending
analyses.
Approximately 100 mg of liver tissue was macerat-
ed in 200 I!f cold grinding buffer (10 mM Tris, pH
8,0) and spun at 10 000 g for 10 seconds to remove
tissue debris. Muscle tissue was used to resolve the
loci for malate dehydrogenase (MDH), lactate dehy-
drogenase (LDH) and xanthine dehydrogenase
(XDH). Samples were loaded immediately onto 12%
w/v starch gels (Sigma) by means of sterile wicks
(Whatman No.1) of approximately 3 mm width.
Electrophoresis was conducted at 13-55 rnA for
2,5-16 h (Table I). Several buffer systems were tested
to resolve allozyme loci consistently. Phosphate (pH
6,7), phosphate-citrate (pH 6,7), tris-citrate I (pH 6,3)
and tris-citrate II (pH 8,0) (Selander et al. 1971) gave
the most consistent degree of resolution of alleles
(Table I). The allozyme-specific stains of Murphy et
al. (1991) and Harris and Hopkinson (1976) were used
to reveal alleles (Table I). Stain constituents for man-
nose phosphate isomerase (MPI) were incorporated
into a 2% w/v agar overlay, under which the starch
was incubated. Concentration of the substrate over the
enzyme reduced the incubation time required for this
enzyme, so maintaining sharp resolution of the alleles.
In all, 19 putative loci, encoding 14 enzymes, were
analysed using BIOSYS-l (Release 1.7, Swofford and
Selander 1981). The six "preferred areas" (Cockcroft
et al. 1990, Fig. 1) represented operational taxonomic
units (OTUs) in phenetic analysis. Allele frequency
estimates were used to measure genetic variability
(Nei 1978). A locus was considered polymorphic if
the frequency of the most common allele did not ex-
ceed 95%. The X2 goodness-of-fit test for deviation
from Hardy-Weinberg equilibrium was performed
using the Levene (1949) correction for small sample
228 South African Journal of Marine Science 17
Table II: Genetic diversity of KwaZulu/Natal Tursiops truncatus. The observed and expected heterozygosity,
error (in parenthesis), are shown for each subpopulation (Groups 1-6)
Subpopulation Group Observed (H0)
Zin-Bal I 0,044 (0,031)
Bal-Dur 2 0,068 (0,041)
Ans-Kar 3 0,053 (0,038)
lfa-Uml 4 0,066 (0,037)
Umt-Mar 5 0,100 (0,056)
San-Mza 6 0,105 (0,066)
Mean 0,073 (0,045)
F,S denotes the coefficient of inbreeding (Li and Horvilz ]953)
size. Multilocus deviation from expectations under
random mating within populations was estimated by
F,S = 1- (Ho/HE), where Ho and HE are the observed
and expected values of heterozygosity respectively.
The significance of F,s was tested using X2 = p2 N,
with one degree of freedom, where N is the mean sam-
ple size of the six groups studied (Li and Horvitz
1953). Population structure was analysed using
Wright's (1978) F-statistics. Jack-knifed means and
standard errors of these values were calculated using
the method of Weir and Cockerham (1984). These es-
timation procedures account for the effects of sampling
a limited number of individuals within a limited num-
ber of subpopulations, and a simple weighting proce-
dure allows the combination of data over all alleles
and loci. The estimated genetic variance among popu-
lations was tested using the relationship X2 = 2NT F, with
(s-I) degrees of freedom, where NT is the total num-
ber of samples from s populations (Workman and
Niswander 1970). The Prevosti coefficient (Wright
1978), which uses an arithmetic mean to combine dis-
tances across loci (Swofford and Olsen 1991), was
calculated for all pairwise distances and the data were
used to perform UPGMA cluster analysis.
RESULTS
Of the 19 putative loci scored, three (15,8%, p < 0,05)
were polymorphic. All three (G6PD, 6PGD and MPI)
appeared to be diallelic. The faster-migrating allele was
designated A and the slower allele B in each zymogram.
Genotype frequencies for the enzymes 6PGD and
MPI conformed to Hardy-Weinberg expectations in all
six groups. The heterozygous state of G6PD was
found only in female bottlenose dolphins in this study.
As this is an X-linked locus in humans (Harris and
Hopkinson 1976) and pigs (Mitton et al. 1994), males
were omitted from the analysis of G6PD in this study.
Based on the female sample alone, conformance to
1996
with standard
Expected (HE) Number of samples F,S
0,050 (0,035) 6 0,012
0,056 (0,032) 10 -0,210
0,081 (0,044) 6 0,350
0,063 (0,036) 6 -0,050
0,079 (0,043) 7 -0,270
0,088 (0,048) 5 -0,]90
omo (0,040) 6,7 -0,042
Hardy- Weinberg expectations was observed for all
groups except Group 3 for this locus (X2 = 5,33, df = 1,
p = 0,021).
Observed heterozygosity determined by direct
count ranged from 0,044 in Group 1 to 0,105 in
Group 6 (Table II). Multi-locus estimates of Ho and
HE provided no evidence of deviations from random
mating. Although two of the six populations displayed
fewer heterozygotes than predicted under random
mating (Table 11), none of the fixation indices (Fd
differed significantly from zero. The overall F,s was
also low (-0,042) and not significantly different
from zero (X2 = 0,0 12, df = 1, p > 0,05).
Mean heterozygosity estimates were generally higher
in the southern groups (0,081 ±0,053) than in the north-
ern groups (0,056 ±0,036). Testing of these values re-
vealed that they were marginally non-significant
(t = 4,00, df = 2, p = 0,057). This difference in aver-
age heterozygosity was suspected to have arisen from
a bias in the male/female ratio, resulting from the omis-
sion of males in the analysis of G6PD. However, there
was no significant difference between the number of
males in Groups 1-3 and in Groups 4-6 (t = 1,94,
df=2,p=0,19).
Genetic distances (Wright 1978) ranged from 0,006
(between Groups 5 and 6) to 0,055 (between Groups
1 and 6). An UPGMA phenogram constructed by
cluster analysis of pairwise distances (Fig. 2) subdi-
vides the Natal bottlenose dolphin population into
two major clusters, corresponding to a northern and
southern coastal distribution. Average genetic distances
within the two clusters suggest that groups from the
=
KwaZulufNatal north coast (D 0,033) are more di-
vergent than those from the South Coast (D = 0,015,
t = 2,85, df= 1, P = 0,046). Jack-knifed means of the
FST statistic across all loci were estimated between
these two regional clusters to be (0,094 ± 0,120), at-
tributing 9% of the total genetic variation of the popu-
lation to differences between subpopulations. However,
this heterogeneity was not statistically significant
(X2 = 0,713, df = 1, p > 0,05). Of the three polymor-
1996 Goodwin et al.: Genetic Variation in Bottlenose Dolphins
0,05 0,03 0,02
GENETIC DISTANCE
Fig. 2: North-south subdivision of the KwaZululNatal bottlenose dolphin Tursiops truncatus population, shown by
UPGMA cluster analysis (Wright 1978). Subpopulation limits correspond with localities shown in Figure 1
phic loci, only one (MPI) displayed significant popula-
=
tion structure (X2 5,37, df =
1, P < 0,025). Insufficient
samples prevented a meaningful analysis of the de-
gree of structure among the six designated "preferred
areas" (Cockcroft et al. 1990).
DISCUSSION
This study represents the first genetic study of the
K waZulu/N atal population of bottlenose dolphins.
Previous assessments of the dynamics of this species
along the Natal coast were made from aerial surveys
(Ross et al. 1989, Cockcroft et al. 1991), capture data
from shark nets (Cockcroft 1990, 1992), pollutant analy-
sis (Cockcroft et al. 1989) and from small boat observa-
tions (Peddemors 1995). The degree of representation
by this study may be questioned with regard to the small
sample size (40 individuals). However, the study ac-
counts for 4,4% of the estimated 900 animals in the des-
ignated KwaZulu/Natal population (Ross et al. 1989,
Cockcroft et al. 1991).
Genetic variability in KwaZulu/Natal bottlenose
dolphins appears to be higher than that reported for T.
truncatus off the coast of Japan and the North Pacific
(H = 0,039 ±0,1l3, Shimura and Numachi 1987).
Similarly, lower mean heterozygosities have been ob-
229
Zin - Bal
Ans - Kar ] North Coast
Bal- Our
Ifa - Umt
San - Mza ] South Coast
Umt - Mar
0,00
served for populations of long-finned pilot whales G.
melaena off the Faroe Islands (0,034 ±0,019,
Andersen 1988) and short-finned pilot whales G.
macrorhynchus off the coast of Japan (0,009 ±0,OO7,
Wada 1988). Although the mean heterozygosity of
0,073 ± 0,045 observed for the population under study
is within the range presented for other delphinids
(0,039 ± 0,133 to 0,093 ± 0,182, Shimura and
Numachi 1987) and is similar to an average value of
0,063 ± 0,051 presented for 12 species of toothed
whales by Shimura and Numachi (1987), interpreta-
tion of the level of variability in the present population
must be conducted with caution. As males were ex-
cluded from the analysis of G6PD, the remainder of
only two polymorphic enzymes, for which there was a
complete sample set, may bias the genetic variability
estimates. This problem may be resolved by analysing
several more polymorphic loci (Archie 1985). The ob-
servation that only female bottlenose dolphins were
heterozygous for the enzyme G6PD suggests that this
enzyme is X-linked in cetaceans, as has been observed
for humans (Harris and Hopkinson 1976) and pigs
(Mitton et al. 1994), although this has not been detected
in previous allozyme studies on cetaceans (Andersen
1988, Danielsd6ttir et al. 1991).
The diphyletic topology of the UPGMA pheno-
gram suggests a geographical structuring of the
KwaZulu/Natal bottlenose dolphin population.
230 South African Journal of Marine Science 17
Furthermore, a trend towards a lower average het-
erozygosity and greater average genetic distance with-
in the KwaZulu/Natal north coast group implies a re-
striction in gene flow in this region and greater
divergence between adjacent groups. Independent
field data support this trend; Cockcroft et al. (1989)
reported marked differences in residue levels of PCBs,
t-DDT and dieldrin in the blubber of bottlenose dol-
phins caught off K waZulu/Natal's north and south
coasts. Data from males older than 10 years were re-
analysed, according to the subdivision suggested in
that study. Both PCB (t = 4,53, df = 28, p = 0,0001)
and DDT (t = 2,83, df = 28, p = 0,008) levels were sig-
nificantly higher in males caught north of Ifafa Beach.
However, these trends are not supported by population
heterogeneity estimates. Although the calculated F ST
statistic attributes more than 9% of the total variation
to differences between the northern and southern re-
gions, this difference is not significantly different from
zero, suggesting that interpopulation differences are
insufficient to account for real subdivision.
Despite the failure of allozyme variation to resolve
population structure in bottlenose dolphins, field obser-
vations provide evidence for a mechanism which may
account for the trend towards subdivision. Peddemors
(1995) reported substantial seasonal variation in the
distribution and abundance of bottlenose dolphins off
the KwaZulu/Natal coast. Every year, large schools of
several hundred bottlenose dolphins are reported to
move northwards into that region during winter
(Peddemors 1995). These dolphins appear to be fol-
lowing the annual migration of pilchard Sardinops
sagax (Baird 1971, Heydom et al. 1978). During that
time of year, abundance and catch rates of dolphins in
shark nets increase on the South Coast (Cockcroft et
at. 1990, Peddemors 1995). However, the distribution
into preferred areas, observed prior to the pilchard mi-
gration, is maintained during the influx of dolphins
from the south (Peddemors 1995).
Furthermore, the abundance and distribution of bot-
tlenose dolphins on KwaZulu/Natal's north coast re-
mains similar to that observed during the rest of the
year, with no evidence of a southward movement in
response to the biotic influx. The north-moving
schools appear to migrate as far as Ifafa Beach (Group
4 in this study, Peddemors 1995), despite continued
movement of the pilchard and associated biota past
Durban (Baird 1971). Thereafter, their movements are
unknown. It is possible that they move offshore and
are entrained in the south-flowing Agulhas Current, as
is suspected to occur after the pilchard migration
(Heydorn et al. 1978). Why dolphins leave the migrat-
ing shoals in the vicinity of Ifafa Beach is unknown.
However, the Agulhas Current, which normally lies
close inshore, moves farther offshore between Port
1996
Dumford (North Coast) and Green Point (north of
lfafa) in response to the widening continental shelf
(Heydorn et af. 1978). Over this range, it meanders for
great distances and is characterized by cyclonic eddies
which form inshore of the current boundary (Heydorn
et al.1978). If indeed bottlenose dolphins make use of
the Current's southward movement, it is likely they
would do so while it was close inshore and before it
became associated with other disturbances.
The extent of this migration coincides with the sub-
division tentatively suggested by allozyme data. It is
possible that the KwaZulu/Natal bottlenose dolphins
occupy relatively discrete home ranges, as previously
suggested (Ross et at. 1987, Cockcroft et al. 1990),
and that these are characterized by low-level interac-
tion between groups, maintaining gene flow and pre-
venting structuring of the population. The weak struc-
turing of the KwaZulu/Natal population suggested here
may be a result of the influx of animals from the adja-
cent Eastern Cape population onto the South Coast.
In that case, one of two scenarios may prevail. In the
first case, annual encounters may be characterized by
breeding between animals from the two regions, with
the infusion of genetic variability onto the South Coast.
Furthermore, interactions with nonfamilial groups may
result in an exchange and relocation of individuals.
The former appears to be responsible for genetic ex-
change between populations of bottlenose dolphins
(Duffield and Wells 1991) and pods of pilot whales
(Amos et al. 1991), where roving male groups make
frequent movements between female groups, during
which mating occurs.
Alternatively, there may be two distinct populations
of bottlenose dolphins on the south-east African coast:
a KwaZulu/Natal population, consisting predominantly
of animals that reside in home ranges, and an Eastern
Cape population, a proportion of which makes an an-
nual northward migration onto the KwaZulu/Natal
south coast. At that time, animals from both popula-
tions are caught in shark nets on that coast. With no
means of differentiating "residents" from "migrants" in
the sampling procedure, all samples were analysed as
having originated in KwaZulu/Natal. This may have
generated a "pseudo-structure" in the genotype fre-
quency data, confounding the actual lack of structure
and suggesting subdivision of the population. The use
of defined home ranges by bottlenose dolphins has
been described in coastal populations off Argentina
(Wlirsig and Wlirsig 1979), Texas (Shane 1980) and
Florida (Shane 1990). Additionally, both short-term
and seasonal shifts in distribution in response to prey
movements have been described for coastal popula-
tions of bottlenose dolphins (see Shane et at. 1986 for
review).
South-east African bottlenose dolphins follow a
1996 Goodwin et al.: Genetic Variation in Bottlenose Dolphins
predominantly summer breeding pattern, which sug-
gests that the winter migration would not result in pro-
lific breeding between dolphins from the Eastern Cape
and those from the KwaZulu/Natal south coast. Fur-
thennore, it is assumed that both "resident" and "mi-
grant" dolphins constitute the elevated catch on the
South Coast during winter (Cockcroft 1990). This
suggests the latter of the two scenarios as the most
plausible explanation for the present findings. The for-
mer cannot be excluded, however, because insufficient
data are available to support a true subdivision of the
KwaZulu/Natal population as a result of gene flow be-
tween South Coast and Eastern Cape groups.
The extent of interaction or subdivision between dol-
phin populations from the KwaZulu/Natal and Eastern
Cape coasts would be more effectively resolved with
the combined use of more sensitive molecular genetic
techniques and coordinated field observations.
Molecular DNA analysis is currently being completed;
it assesses the possibility of there being two genetically
discrete populations of T. truncatus on the South-East
African coast. Furthennore, photo-identification mark
and recapture data are being collected simultaneously
with biopsies for future genetic analysis of free-ranging
bottlenose dolphins.
ACKNOWLEDGEMENTS
We owe gratitude to our colleague, Dr G. Campbell,
for assistance in the laboratory, and to Drs G. 1. B. Ross
(Australian Biological Resources Study, Canberra,
Australia) and P. Hale (University of Queensland,
Australia) for extremely helpful comments on an earlier
draft of this paper.
LITERATURE CITED
AMOS, B., BARRETI, J. and G. A. DOVER 1991 - Breeding
system and social structure in the Faroese pilot whale as re-
vealed by DNA fingerprinting. Rep. into Whalg Commn
Spec. Issue 13: 255-268.
ANDERSEN, L. W. 1988 - Electrophoretic differentiation among
local populations of the long-finned pilot whale,
Globicephala melaena, at the Faroe Islands. Can. J. Zool.
66: 1884-1892.
ARCHIE, J. W. 1985 - Statistical analysis of heterozygosity data:
independent sample comparisons. Evolution 39(3):
623-637.
BAIRD, D. 1971 - Seasonal occurrence of the pilchard Sardinops
ocellata on the east coast of South Africa. Investl Rep.
Div. Sea Fish. S. Afr. 96: 19 pp.
BALLANCE, L. T. 1990 - Residence patterns, group organization,
and surfacing associations of bottlenose dolphins in Kino
Bay, Gulf of California, Mexico. In The Bottlenose Dolphin.
Leatherwood, S. and R. R. Reeves (Eds). San Diego;
231
Academic Press: 267-283.
COCKCROFr, V. G. 1990 - Catches of dolphins in the Natal
shark net~, 1980-1988. S. Afr. J. Wildl. Res. 20: 44-51.
COCKCROFr, V. G. 1992 - Incidental capture of bottlenose dol-
phins (Tursiops truncatus) in shark nets: an assessment of
some possible causes . .I. Zool .. Lond. 226: 123-134.
COCKCROFr, V. G., DE KOCK, A. c., LORD, D. A. and G. J.
B. ROSS 1989 - Organochlorines in bottlenose dolphins
Tursiops truncatus from the east coast of South Africa.
S. Afr . .I. mar. Sci. 8: 207-217.
COCKCROFr, V. G. and G. J. B. ROSS 1990 - Bottlenose dol-
phins in Natal shark nets, 1980 through 1987: catch rates
and associated contributing factors. In Cetaceans and
Cetacean Research in the Indian Ocean Sanctuary.
Leatherwood, S. and G. P. Donovan (Eds). Mar. Mamm.
tech. Rep. 3: 115-127.
COCKCROFr, V. G., ROSS, G. J. B. and V. M. PEDDEMORS
1990 - Bottlenose dolphin Tursiops truncatus distribution
in Natal's coa~tal waters. S. Afr . .I. mar. Sci. 9: 1-10.
COCKCROFr, V. G., ROSS, G. J. B. and V. M. PEDDEMORS
1991 - Distribution and status of bottlenose dolphin
Tursiops truncatus on the south coast of Natal, South Africa.
S. Afr . .I. mar. Sci. 11: 203-209.
DAN IELS D6TIIR , A. K., DUKE, E. 1., JOYCE, P. and A.
ARNASON ]991 - Preliminary studies on genetic varia-
tion at enzyme loci in fin whales (Balaenoptera physalus)
and sei whales (Balaenoptera borealis) from the North
Atlantic. Rep. into Whalg Commn Spec. Issue 13: 115-124
DOS SANTOS, M. E. and M. LACERDA 1987 - Preliminary ob-
servations of the bottlenose dolphin (Tursiops truncatus) in
the Sado estuary (Portugal). Aquat. Mamm. 13: 65-80.
DUFFIELD, D. A. and R. S. WELLS 1991 - The combined appli-
cation of chromosome, protein and molecular data for the
investigation of social unit structure and dynamics in
Tursiops truncatus. Rep. into Whalg Commn Spec. Issue 13:
155-169.
GARRATI, P. [AI. 1980 - Dolphins home in on Natal ski-boaters.
Ski-scene Sept./Oct. 1980: p. 21.
HARRIS, H. and D. A. HOPKINSON 1976 - Handbook of
Enzyme Electrophoresis in Human Genetics. Amsterdam;
Elsevier: Non-consecutive numeration.
HEYDORN, A. E. E, with BANG, N. D., PEARCE, A. E,
FLEMMING, B. w., CARTER, R. A., SCHLEYER, M. H.,
BERRY, P. E, HUGHES, G. R., BASS, A. J., WALLACE, J.
H., VAN DER ELST, R. P., CRAWFORD, R. J. M. and P.
A. SHELTON 1978 - Ecology of the Agulhas Current re-
gion: an assessment of biological responses to environmen-
tal parameters in the south-west Indian
Ocean. Trans. R. Soc. S. Afr. 43(2): 151-190.
LEVENE, H. 1949 - On a matching problem arising in genetics.
Ann. math. Statist. 20: 91-94.
Lt, C. C. and D. G. HORVITZ 1953 - Some methods of estimating
the inbreeding coefficient. Am . .I. hum. Genet. 95: 107 -117.
MITION, J. B., ZELENKA, D. 1. and P. A. CARTER 1994 -
Selection of breeding stock in pigs favours 6PGD heterozy-
gotes. Heredity 73: 177-184.
MURPHY, R. w., SITES, J. w., BUTH, D. G. and C. H. HAU-
FLER 1991 - Proteins I: isozyme electrophoresis. In
Molecular Systematics. Hillis, D. M. and C. Moritz (Eds).
Sunderland; Sinauer Associates: 45-126.
NEI, M. 1978 - Estimation of average heterozygosity and genetic
distance from a small number of individuals. Genetics 89:
583-590.
PEDDEMORS, V. M. 1995 - The aetiology of bottlenose dolphin
capture in shark nets off Natal, South Africa. Ph.D. thesis,
University of Port Elizabeth: 138 pp.
ROSS, G. J. B., COCKCROFr, V. G. and D. S. BUTTERWORTH
1987 - Offshore distribution of bottlenosed dolphins in
Natal coastal waters and Algoa Bay, Eastern Cape. S. AjI: J.
232 South African Journal of Marine Science 17
Zool. 22(1): 50-56.
ROSS, G. J. B., COCKCROFr, V. G., MELTON, D. A. and D. S.
BUTTERWORTH 1989 - Population estimates for bot-
tlenose dolphins Tursiops truncatus in Natal and Transkei
waters. S. Afr. J. mar. Sci. 8: 119-129.
SCOTT, M. D., WELLS, R. S. and A. B. IRVINE 1990 - A long-
term study of bottlenose dolphins on the west coast of
Rorida. In The Boltlenose Dolphin. Leatherwood, S and R.
R. Reeves (Eds). San Diego; Academic Press: 235-244.
SELANDER, R. K., SMITH, M. H., YANG, S. Y., JOHNSON, W.
E. and J. B. GENTRY 1971 - Biochemical polymorphism
and systematics in the genus Peromyscus. 1. Variation in the
old-field mouse (Peromyscus polionotus). Stud. Genetics
Univ. Texas 6 7103: 49-90.
SHANE S. H. 1980 - Occurrence, movements and distribution of
bottlenose dolphin, Tursiops truncatus, in southern Texas.
Fishery Bull., Wash. 78: 593-601.
SHANE, S. H. 1990 - Behaviour and ecology of the bottlenose
dolphin at Sanibel Island, Florida. In The Bottlenose
Dolphin. Leatherwood, S. and R. R. Reeves (Eds). San
Deigo; Academic Press: 245-265 ...
SHANE, S. H., WELLS, R. S. and B. WURSIG 1986 - Ecology,
behavior and social organisation of the bottlenose dolphin: a
review. Mar. mamm. Sci 2: 34-63.
SHIMURA, E. and K-I. NUMACHI 1987 - Genetic variability
and differentiation in the toothed whales. Scient. Rep.
Whales Res. Inst. 38: 141-163.
1996
SWOFFORD, D. L. and G. J. OLSEN 199] - Phylogeny recon-
struction. In Molecular Systematics. Hillis, D.M. and C.
Moritz (Eds). Sunderland; Sinauer Assoc.: 4] 1-501.
SWOFFORD, D. L. and R. B. SELANDER 1981 - BIOSYS-I: a
FORTRAN program for the comprehensive analysis of elec-
trophoretic data in population genetics and systematics. J.
Heredity 72: 28]-283.
WADA, S. ]988 - Genetic differentiation between two fOnTISof
short-finned pilot whales off the Pacific coast of Japan.
Scient. Rep. Whales Res. Inst. 39: 9]-101.
WADA, S. and K-I NUMACHI 1991 - Allozyme analyses of genet-
ic differentiation among the populations and species of
Balaenoptera. Rep. into Whalg Commn Spec. Issue 13:
]25-154.
WEIR, B. S. and C. C. COCKERHAM 1984 - Estimating F-
Statistics for the analysis of population structure. Evolurion
38: 1358-1370.
WORKMAN, P. L. and J. D. NISWANDER 1970 - Population
studies on southwestern Indian tribes. 2. Local genetic dif-
ferentiation in the Papago. Am. J. hum. Genet. 22: 24-49.
WRIGHT, S. 1978 - Evolution and the Genetics of Populations,
Vol 4. Tn Variability Within and Among Natural Populations.
Evolution and the Genetics of Populations 4. Chicago;
.. University Press: ?80 pp.
WURSIG, B. and M. WURSIG 1980 - Behavior and ecology of
the bottlenose dolphins, Tursiops truncatus, in the South
Atlantic. Fishery Bull .. Wash. 77: 399-412.