Journal of Mammalogy, 83(1):125–134, 2002
SKULL SHAPE AND SIZE DIVERGENCE IN DOLPHINS OF THE
GENUS SOTALIA: A TRIDIMENSIONAL
MORPHOMETRIC ANALYSIS
EMYGDIO LEITE
DE
ARAUJO MONTEIRO-FILHO,* LEANDRO RABELLO MONTEIRO,
SÉRGIO FURTADO DOS REIS
AND
Departamento de Zoologia, Setor de Ciências Biológicas, Universidade Federal do Paraná,
Caixa Postal 19020, 81531-970 Curitiba, Paraná, Brazil (ELAMF)
Instituto de Pesquisas Cananéia, Rua João Salim, Lote 26–Quadra Y, Parque Xangrilá,
13098-106 Campinas, São Paulo, Brazil (ELAMF)
Laboratório de Ciências Ambientais, Universidade Estadual do Norte Fluminense, Avenida Alberto
Lamego 2000, Horto, 28015-620 Campos dos Goytacazes, Rio de Janeiro, Brazil (LRM)
Departamento de Parasitologia, Instituto de Biologia, Universidade Estadual de Campinas,
Caixa Postal 6109, 13083-970, Campinas, São Paulo, Brazil (SFR)
A study of cranial shape in dolphins of genus Sotalia was done using 104 specimens (92
from localities along the Brazilian coast and 12 from the Amazon River basin). Twentytwo cranial landmarks, assumed to be homologous, were selected for analysis. The first 2
principal components of aligned coordinates explained 40.6% of the total variation in cranial shape. Although no sexual dimorphism was detected (P 5 0.811), shape differences
among populations of Sotalia were highly significant (P , 0.000001). The 1st and 2nd
principal components of shape showed that the Sotalia population from the Amazon basin
differed in cranial shape from marine populations. Based on differences in geometric shape,
a discriminant analysis of 3 linear measurements between landmarks provided an equation
that classified skulls as belonging to Amazonian or marine populations. Based on these
results and evidence from several other divergent character systems and life history attributes, we suggest the use of Sotalia guianensis for marine dolphins and S. fluviatilis for
Amazonian dolphins.
Key words:
dolphins, geographic variation, geometric morphometrics, skull shape, Sotalia
The genus Sotalia (Cetacea: Delphinidae) was described in 1866 by Gray (see
Hershkovitz 1966), based on a skull from
French Guyana, and the specimen was
named Sotalia guianensis (see van Bénéden
1864 in Hershkovitz 1966). About the same
time, 2 new species were described, with S.
fluviatilis (see Gervais and Deville 1853 in
Hershkovitz 1966; 5S. pallida 5S. tucuxi)
applied to dolphins from the Amazon basin
(northern Brazil), and S. brasiliensis van
Bénéden 1875 to dolphins restricted to
Guanabara bay (Baı́a de Guanabara), Rio de
Janeiro State, southeastern Brazil (Hershkovitz 1966).
These species names and areas of occurrence were accepted until reports confirmed
the presence of Sotalia along the coast of
several Brazilian states and in other Central
and South American countries (e.g., Bossenecker 1978; Carvalho 1963; da Silva
and Best 1996; Husson 1978; SimõesLopes 1988). Sotalia is now known to have
an extensive distribution along the Atlantic
coast of Central and South America and in
the Amazon (da Silva and Best 1994,
1996). These dolphins are commonly observed inshore, in rivers, bays, and estuar-
* Correspondent: [email protected]
125
126
JOURNAL OF MAMMALOGY
ies, where they follow the original distribution of mangroves, from Honduras (da
Silva and Best 1996) to the state of Santa
Catarina in southern Brazil (Simões-Lopes
1988).
The external morphology of marine and
freshwater Sotalia is similar, although there
are differences in their habitat usage. Based
on these observations, Rice (1977) suggested the existence of only 1 species, S.
fluviatilis, with 2 subspecies: S. f. fluviatilis
in the Amazon and S. f. guianensis in marine waters. Based on a study of 59 skulls
from marine and freshwater dolphins, Borobia (1989) subsequently strengthened the
argument for only 1 species. In this case,
conventional multivariate morphometrics
confirmed the size variation noticed before,
but the scores for specimens of the 2 populations overlapped considerably in the second principal component (shape component) and could explain only 6% of the total
variation in the distance measurements of
skulls.
With the acceptance of Sotalia as a
monotypic genus, some authors (Best and
da Silva 1984; da Silva and Best 1994,
1996) have used information obtained from
dolphins in the Amazon to make generalizations about various aspects of the biology of Sotalia, mainly because the tucuxi
(S. f. fluviatilis) is the most studied of the
Sotalia dolphins (Alcuri and Busnell 1989;
Best and da Silva 1984; Caldwell and Caldwell 1970; da Silva 1990; da Silva and Best
1996; Harrison and Brownell 1971; Magnusson et al. 1980; Zam et al. 1970). Such
generalizations suggest that morphological
evidence for the assignment of taxa in Sotalia requires reexamination using more
powerful, recently developed methods.
Considering that morphological structures in an organism have 2 components
(size and shape), and that shape is the most
informative for defining biological entities
in nature (Atchley et al. 1992; Patton and
Brylski 1987), we evaluate in this study
whether the component of shape differences
between Amazonian and marine Sotalia is
Vol. 83, No. 1
really negligible, as has been suggested by
multivariate analysis of distance measurements and, therefore, insufficient to justify
the recognition of more than a single biological entity. To address this question, we
applied the recently developed method of
geometric morphometrics (Bookstein 1991;
Kendall 1984; Rohlf 1996, 1998), which allows the analysis of geometrical shape in
biological structures.
MATERIALS
AND
METHODS
Samples.—The 104 specimens (Appendix I)
used were from collections held by the Laboratório de Mamı́feros Aquáticos, Universidade
Federal de Santa Catarina (LAMAQ/UFSC),
Universidade Federal do Paraná (UFPR), Instituto de Pesquisas Cananéia (IPeC), Museu de
Zoologia, Universidade de São Paulo (MZUSP),
Museu de História Natural, Universidade Estadual de Campinas (ZUEC), Museu Nacional
(MN/UFRJ), and Projeto Mamirauá. The specimens were grouped based on geographic origin
as marine south (n 5 32), marine southeast (n
5 47), marine northeast (n 5 13), and Amazonian (n 5 12).
Twenty-two landmarks (Fig. 1), assumed to
be homologous in all specimens, were defined
for the dolphin skulls as follows: 1 5 rostral tip,
2 and 12 5 anteriormost point of the notch in
the maxilla, 3 and 11 5 intersection between the
frontal bone and zygomatic process, 4 and 10 5
intersection between the parietal bone and frontal–interparietal suture, 5 and 9 5 posteriormost
point on the curve of the parietal, 6 and 8 5
posteriormost point on the curve of the occipital
condyle, 7 5 posteriormost point on the edge of
the supraoccipital, 13 5 midpoint of the nasal
bone suture, 14 5 anteriormost point of the suture between the frontal and interparietal bones,
15 and 22 5 dorsalmost point on the pterygoidal
notch, 16 and 21 5 point in the suture between
the frontal and alisphenoid bones, 17 and 20 5
ventralmost point of the basioccipital crest, and
18 and 19 5 ventralmost point of the paraoccipital process.
The skulls were photographed in 3 views
(dorsal, lateral, and ventral) at an angle of 908
from each other (dorsal and ventral views were
1808 apart). The pictures were digitized with a
flatbed scanner and superimposed with the constraint that landmarks 1 and 7 were at the same
February 2002
MONTEIRO-FILHO ET AL.—SHAPE ANALYSIS OF SOTALIA SKULLS
FIG. 1.—Cranial landmarks defined for the lateral, dorsal, and ventral views of the skull of
Sotalia. See text for description of landmarks.
coordinate position in the 3 pictures of each
specimen (these 2 landmarks could be identified
in all views). The 2-dimensional coordinates
were combined in such a way that the y-dimension in the lateral view (the dorsoventral axis)
corresponded to the z-dimension in the dorsal
and ventral data sets. This combination produced a 3-dimensional data set of skull landmarks. Skull size was calculated as the centroid
size of landmark configurations (Bookstein
1991) which corresponded to the square root of
the summed squared distances between each
landmark and the configuration centroid (average point in each landmark constellation).
Morphometric methods.—The landmark configurations were superimposed by an orthogonal
least squares technique known as Procrustes superimposition (Rohlf and Slice 1990; Slice
1996). This technique translates, scales, and rotates the landmark configurations so as to minimize the summed squared distances between
corresponding landmarks. In the generalized
least squares superimposition (GLS), a mean
127
shape is iteratively estimated and all specimens
in the sample are superimposed on the mean.
In 3-dimensional objects, 7 nuisance parameters are removed from the coordinates after superimposition: 3 axes of translation, 1 scale
(centroid size), and 3 angles of rotation. Although this information is removed, the set of
coordinates retains the same number of dimensions (3p, where p 5 number of landmarks),
whereas the real dimensionality of the data set
should be 3p 2 7. One way to solve this problem
is to reduce the dimensionality of the set of superimposed landmark coordinates using a multivariate technique (Dryden and Mardia 1998).
We used principal component analysis to remove the extra dimensions from the aligned coordinates (the last 7 principal components have
eigenvalues equal to 0) and to search for biologically interesting phenomena in the directions of
major variation within shape space. The eigenvectors can be depicted in figure space as estimated shapes (icons) with high scores in both
positive and negative directions (Dryden and
Mardia 1998). The principal components of superimposed coordinates are equivalent to other
variance-maximizing rotations of shape variables commonly used in morphometric studies,
such as relative warp analysis (Rohlf 1999).
We used the first 2 principal components of
the Sotalia sample, with sexes and geographic
origin combined as shape variables in multivariate analyses of variance (MANOVA). As there
were too many skulls with no information on
sex, the interaction between sex and geographic
origin could not be evaluated, and the analyses
had to be performed separately for each factor,
instead of using a 2-way model. To test for sexual dimorphism and geographic effects on size,
we performed analyses of variance (ANOVA)
on centroid size, classifying the samples by sex
and locality.
To assess the relative importance of localized
versus global shape changes, we performed a
generalized affine least squares superimposition
(GALS). This technique superimposes the landmark configurations after removing the nuisance
parameters from the coordinates and stretches
and compresses the configurations in orthogonal
directions (affine transformations). The number
of dimensions after the affine superimposition is
smaller than those of after the orthogonal superimposition. For 3-dimensional objects, there are
3p 2 12 dimensions (the 7 nuisance parameters
128
JOURNAL OF MAMMALOGY
Vol. 83, No. 1
plus 5 uniform dimensions). The coordinates resulting from this superimposition were used in
a 2nd principal components analysis. The difference between the ordinations obtained using
the results of orthogonal superimposition and the
affine superimposition reveals the effect of discarding uniform components and of performing
the analysis in a localized shape subspace
(Bookstein 1996).
RESULTS
The first 2 principal components of the
superimposed coordinates (orthogonal least
squares) explained 40.6% of the total shape
variation in the sample. The MANOVA
performed on the 2 principal components
classified on the basis of sex was not significant (Wilks’ lambda 5 0.98458, d.f. 5
2, 27, P 5 0.810748), whereas that performed on the same components classified
on the basis of geographic origin (marine
south, marine southeast, marine northeast,
and Amazonian) was highly significant
(Wilks’ lambda 5 0.093936, d.f. 5 6, 198,
P , 0.0000001). The ANOVA for sexual
dimorphism on centroid size was not significant (F 5 0.253083, d.f. 5 1, 128, P 5
0.618847), whereas the ANOVA for geographic effects on size was highly significant (F 5 38.56772, d.f. 5 3, 100, P ,
0.0000001). As no sexual dimorphism in
skull shape or size was observed (either because there was none or because the information available was incomplete), we analyzed only geographic variation.
The scatterplot for the first 2 principal
components (Fig. 2) from GLS showed 2
groups of samples, marine and Amazonian.
The 1st principal component depicted a major shape difference between the Amazonian and marine specimens. Morphologically, there were differences in shape between the 2 populations (Fig. 3). In Amazonian specimens, the rostrum and the
occipital condyle pointed downwards relative to the anteroposterior axis of the skull,
whereas in marine specimens the rostrum
and the condyle were aligned along this
axis. Consequently, the skulls of Amazo-
FIG. 2.—Scatterplot of the first 2 principal
components from the generalized least squares
for marine (south, southeast, and northeast) and
Amazonian (Amazon) samples of Sotalia.
nian specimens look arched with the concavity on the ventral side; the region of the
zygomatic process was relatively larger in
marine specimens than in Amazonian ones.
The braincase was relatively larger in marine than in Amazonian specimens, and the
distance between the anterior notch of the
maxilla (landmarks 2 and 12) and the nasal
bone (landmark 13) was relatively greater
in Amazonian specimens.
The ordination of specimens on the first
2 principal components from the GALS (results not shown) was similar to that obtained with orthogonally superimposed coordinates. The first 2 principal components
from GALS accounted for about the same
percentage of sample variation as the GLS
principal components (41%), but the latter
concentrated more variation in the 1st axis.
The scatterplot between the 1st principal
component from GLS and centroid size
(Fig. 4) showed an allometric pattern between Amazonian and marine populations.
However, this allometric pattern between
groups was not an extrapolation of the within-group pattern. An analysis of covariance
of the scores of the 1st principal component
from GLS, classified by locale and using
centroid size as a covariate, was still significant (F 5 103.047, d.f. 5 3, 99, P ,
0.0000001, test of parallelism: P 5 0.995).
A discriminant analysis (classifying by 2
groups: marine and Amazonian) was done
February 2002
MONTEIRO-FILHO ET AL.—SHAPE ANALYSIS OF SOTALIA SKULLS
129
FIG. 3.—Effect of the 1st principal component of shape on the mean landmark configuration of
skulls of Sotalia. The center column represents the mean shape, the right column represents the
estimated shape for positive scores on PC1 (magnified 3 times), and the left column represents the
estimated shape for negative scores on PC1 (magnified 3 times). The top row represents the skulls
in lateral view, the middle row represents the skull in dorsal view, and the bottom row represents
the skull in frontal view.
FIG. 4.—Scatterplot for the 1st principal component from generalized least squares versus
centroid size for marine (south, southeast, and
northeast) and Amazonian (Amazon) samples of
Sotalia.
on linear measurements between landmarks
(obtained from the 3-dimensional coordinates) in the skulls. We used 3 distances
that, judging from the results of the geometric analysis, were expected to reflect the
shape differences between the 2 populations: distance between landmarks 1 and 7
(D1,7; basicranial axis length), distance between landmarks 1 and 13 (D1,13; tip of the
snout to nasal bone), and distance between
landmarks 16 and 21 (D1,16; skull width).
To avoid confusion in the analysis by the
large size differences between groups, we related each distance to basicranial axis length
using the ratios (D1,13)/(D1,7) and (D16,21)/
(D1,7) as variables. As expected, the discriminant analysis using the two ratios was highly significant (Wilks’ lambda 5 0.407675, F
5 73.37318, d.f. 5 2, 101, P , 0.000001),
and the marine specimens had higher scores
130
JOURNAL OF MAMMALOGY
than the Amazonian ones on the discriminant axis. The percentage of correct classifications was very high. For the marine
specimens, only 2 out of 92 were incorrectly classified. The entire sample of 12
Amazonian specimens was correctly classified. The structural coefficients for the ratios on the discriminant axis were: (D1,13)/
(D1,7) 5 20.80625 and (D16,21)/(D1,7) 5
0.59578. Thus, the allometric pattern for
discriminant structural coefficients indicated that, although the marine specimens
were larger than Amazonian specimens, the
former had a relatively larger skull width at
the base and a relatively smaller length
from the tip of the snout to the nasal bone
(all relative to skull length). The classification functions obtained were
Marine:
Score 5 21,965.46 1 4,433.26
1D 2
D1,13
1,7
1 1,083.90
1D 2
D16,21
1,7
Amazonian:
Score 5 22,101.22 1 4,660.07
1D 2
D1,13
1,7
1 977.16
1 D 2.
D16,21
1,7
The 2 scores were calculated for each
specimen, and specimens were then
grouped according to their highest classification scores. Using these functions, it was
possible to identify whether a Sotalia skull
belonged to a marine or Amazonian specimen based only on 3 skull measurements.
These classification functions may be useful
for researchers who use museum specimens
of unknown geographic origin.
DISCUSSION
Our results provide new insights into the
pattern of skull shape and size variation in
Vol. 83, No. 1
the genus Sotalia. The only factor that influences shape divergence among specimens was geographic origin. The lack of
sexual dimorphism in the skull dimensions,
although not confirmed here because of
lack of information on the sex of some
specimens, has been observed earlier in this
group (Borobia 1989).
Like other small cetaceans, such as Stenella (Perrin et al. 1981, 1987, 1991) and
Delphinus (Evans 1994; Perrin et al. 1985),
the genus Sotalia is a subject of taxonomic
controversy at species level. Initially, 8 species of Sotalia were described (which included Sotalia and Sousa). A century and a
half later only 1 species is accepted, although doubts remain, and subspecific
names have been attributed to Amazonian
(S. fluviatilis fluviatilis) and marine (S. f.
guianensis) dolphins (cf. Rice 1977). Borobia (1989), who recognized only 1 species based on a conventional multivariate
morphometric analysis of linear distances,
suggested that Amazonian and marine specimens differed only in size.
Geographic differences in size have been
reported earlier in Sotalia (Mitchell 1975)
and do not support the creation of taxonomic boundaries between closely related organisms (Atchley et al. 1992; Patton and
Brylski 1987). In contrast, shape variation
is a more reliable and richer source of information about biological processes. When
defined as the geometric properties of an
object that are invariant to the effects of
rotation, translation, and scaling (Dryden
and Mardia 1998), the shape of biological
structures is best studied using geometric
methods that are unaffected by these confounding effects. Traditional morphometric
methods, such as principal components of
distance measurements, are confounded by
size differences among specimens (Rohlf
and Bookstein 1987) and cannot be reliably
used to determine shape differences between biological entities.
The 1st principal component from the
generalized least squares superimposition
showed a large amount of shape variation
February 2002
MONTEIRO-FILHO ET AL.—SHAPE ANALYSIS OF SOTALIA SKULLS
between marine and Amazonian specimens.
There was also considerable overlap among
marine specimens of different geographic
origins (south, southeast, and northeast), indicating that these specimens are morphologically uniform. The same result was obtained for the first 2 principal components
of the GALS, indicating that differences in
global shape were not important for discerning between the two groups of specimens. On the other hand, the description of
shape differences uncovered large- and
small-scale localized shape differences between the two groups.
The differences in shape between the
skulls of marine and Amazonian dolphins
were large. The alignment of the rostrum
and occipital condyle differed markedly between the 2 groups of dolphins. In marine
dolphins, the opening of the foramen magnum is located further posterior, whereas in
Amazonian dolphins this opening is directed downwards. This variation in the position of the foramen magnum suggests that
in marine dolphins the cranium would be in
line with the vertebral column, whereas in
Amazonian dolphins the cranium would
point downwards.
This difference in skull shape may reflect
a functional distinction between marine and
Amazonian dolphins. The downward inflection of skulls in Amazonian dolphins may
be associated more with the need to scan
river beds which are frequently littered with
tree trunks and branches that might cause
dolphins to strand, rather than with the type
of food taken, as only 11% of the fish consumed are bottom-dwellers (da Silva 1983).
On the other hand, for marine dolphins,
about 60% of the fish and crustaceans (e.g.,
shrimps) consumed are bottom-dwellers
(M. R. Oliveira, in litt.), and diving toward
the bottom during fishing activities is common (Monteiro-Filho 1992, 1995), with no
risk of stranding.
When 2 groups of closely related organisms differ in size and shape, it is important
to establish whether the differences in shape
reflect heterochronic phenomena alone,
131
such as hypermorphosis (Alberch et al.
1979), in which the 2 groups of organisms
share a common linear growth trajectory
but with 1 group attaining a larger size and,
consequently, a different shape. One could
argue that the relatively larger braincase
and smaller skull size seen in Amazonian
specimens are evidence that these dolphins
have retained early ontogenetic features of
shape and size (neotenic differentiation), or
that marine dolphins attain a larger size and
different shape (hypermorphosis).
Examination of the size and shape vectors for the skulls of marine and Amazonian
Sotalia indicates that, although the 2 groups
differ in size and shape, the within-group
major axes of variation are not linearly related (i.e., they do not correspond to simple
linear extensions of each other), as would
be expected if skull shape differentiation in
these groups could be attributed only to hypermorphosis. On the other hand, the pattern of size and shape differentiation between the two groups suggests a static intraspecific allometric pattern (Cheverud
1982) that has no simple heterochronic basis. A thorough study on skull shape differentiation between Amazonian and marine Sotalia and its ontogenetic basis would
require the inclusion of young individuals
in the sample, but young specimens are uncommon in museum samples.
The geometric descriptors and multivariate statistical analyses used here revealed
a substantial morphological discontinuity in
cranial shape between Amazonian and marine dolphin populations. There are, in addition, several other character systems in
which the Amazonian and marine groups
differ markedly: size of adults, with smaller
dolphins living in river systems and larger
ones living in the sea (Borobia 1989;
Mitchell 1975); social organization, with a
polyandrous system for Amazonian dolphins (Best and da Silva 1984) and a family
organization for marine dolphins (Monteiro-Filho 2000); presence of only 1 (left)
functional ovary and a gestation time of
10–10.3 months in Amazonian dolphins
132
JOURNAL OF MAMMALOGY
(Best and da Silva 1984; Harrison and
Brownell 1971) compared with both ovaries being functional and a gestation time
of 11.3–12 months in marine dolphins (Rosas and Barreto, in press); seasonal testicular activity in Amazonian dolphins and
continuous testicular activity in marine dolphins (F. Rosas, in litt.); significant differences between the mitochondrial DNA sequences of marine and Amazonian populations (M. Furtado-Neto, in litt.); and dissimilar echolocation clicks between the 2
populations (Kamminga et al. 1993).
This evidence strongly suggests that morphogenetic mechanisms and evolutionary
processes have acted independently on marine and Amazonian dolphins, leading to
the currently observed distinct patterns of
morphological, ecological, and behavioral
traits. We consider this evidence to indicate
that Sotalia is not monotypic, and suggest
the use of separate names to designate the
2 groups currently recognized as Sotalia
fluviatilis. Based on priority, the names
should be Sotalia guianensis for marine
dolphins and S. fluviatilis for Amazonian
dolphins.
RESUMO
Um estudo da forma craniana em golfinhos do gênero Sotalia foi realizado utilizando 104 espécimens (92 oriundos de localidades costeiras e 12 da Bacia do Rio Amazonas), sendo utilizados vinte e dois marcos
anatômicos considerados homólogos. Os 2
primeiros componentes principais explicaram 40.6% da variação de forma craniana.
Não foi detectado dimorfismo sexual (P 5
0.811), entretanto a diferença de forma entre as populações foi altamente significativa
(P , 0.000001). Os dois primeiros componentes de forma do crânio mostraram que
os Sotalia da Bacia Amazônica diferem da
população marinha. Baseado nas diferenças
de forma geométrica, uma análise discriminante de 3 medidas lineares gerou uma
equação que classifica os crânios como sendo da Bacia Amazônica e da população
marinha. Com base nesses resultados e em
Vol. 83, No. 1
outras caracterı́sticas da história natural
destes animais, nós sugerimos o uso de Sotalia guianensis para os golinhos marinhos
e S. fluviatilis para os golfinhos da Bacia
Amazônica.
ACKNOWLEDGMENTS
We thank M. Marmontel (Sociedade Civil
Mamirauá), J. A. de Oliveira, L. B. F. Oliveira,
and L. O. Salles (Museu Nacional, Rio de Janeiro), M. de Vivo (Museu de Zoologia, Universidade de São Paulo, São Paulo), and P. C.
Simões-Lopes (Laboratório de Mamı́feros Aquáticos, Universidade Federal de Santa Catarina)
for allowing access to specimens, and M. Furtado-Neto, F. C. W. Rosas and M. R. Oliveira
for their observations. We thank F. C. W. Rosas
and K. D. K. A. Monteiro who provided critical
and insightful comments, J. R. Somera who
helped with the line drawings, E. P. Lessa who
provided thoughtful comments that greatly improved the clarity of the manuscript, and S. Hyslop for reviewing the English of the manuscript.
This work was funded by the Conselho Nacional
de Desenvolvimento Cientı́fico e Tecnológico
(CNPq), Fundação de Amparo à Pesquisa do Estado de São Paulo (grant number 99/06845-3),
and Instituto de Pesquisas Cananéia. ELAMF
and SFR are partially supported by research fellowships from CNPq. Work by LRM is funded
by the Fundação Estadual do Norte Fluminense.
LITERATURE CITED
ALBERCH, P., S. J. GOULD, G. F. OSTER, AND D. B.
WAKE. 1979. Size and shape in ontogeny and phylogeny. Paleobiology 5:296–317.
ALCURI, G., AND R. BUSNELL. 1989. Unicité fonctionnelle des clics sonar et des sifflements dans les émissions acoustiques d’ún dauphin amazonien Sotalia
fluviatilis Gervais et Deville. Comptes Rendus de
L’Academie de Sciences 308:379–384.
ATCHLEY, W. R., D. E. COWLEY, C. VOGL, AND T.
MCLELLAN. 1992. Evolutionary divergence, shape
change, and genetic correlation structure in the rodent mandible. Systematic Biology 41:196–221.
BEST, R. C., AND V. M. F. DA SILVA. 1984. Preliminary
analysis of reproductive parameters of the boutu,
Inia geoffrensis and the tucuxi, Sotalia fluviatilis, in
the Amazon river system. In Reports of the International Whaling Commission, Special Issue 6:361–
369.
BOOKSTEIN, F. L. 1991. Morphometric tools for landmark data: geometry and biology. Cambridge University Press, London, United Kingdom.
BOOKSTEIN, F. L. 1996. Combining the tools of geometric morphometrics. Pp. 131–151 in Advances in
February 2002
MONTEIRO-FILHO ET AL.—SHAPE ANALYSIS OF SOTALIA SKULLS
morphometrics (L. F. Marcus, M. Corti, A. Loy, G.
Naylor, and D. E. Slice, eds.). Plenum, New York.
BOROBIA, M. 1989. Distribution and morphometrics of
South American dolphins of the genus Sotalia.
M.Sc. thesis, McGill University, Montreal, Quebec,
Canada.
BOSSENECKER, P. J. H. 1978. The capture and care of
Sotalia guianensis. Aquatic Mammal Science 6:13–
17.
CALDWELL, D. K., AND M. C. CALDWELL. 1970. Echolocation-type signals by two dolphins, genus Sotalia.
Quarterly Journal of the Florida Academy of Sciences 33:124–131.
CARVALHO, C. T. 1963. Sobre um boto comum no litoral do Brasil. (Cetacea: Delphinidae). Revista
Brasileira de Biologia 23:263–276.
CHEVERUD, J. M. 1982. Relationships among ontogenetic, static and evolutionary allometry. American
Journal of Physical Anthropology 59:139–149.
DA SILVA, V. M. F. 1983. Ecologia alimentar dos golfinhos da Amazônia. M.Sc. thesis, Instituto Nacional
de Pesquisas da Amazônia/Universidade do Amazonas, Manaus.
DA SILVA, V. M. F. 1990. Botos mitológicos hóspedes
da Amazônia. Ciência Hoje 11:14–18.
DA SILVA, V. M. F., AND R. C. BEST. 1994. Tucuxi
Sotalia fluviatilis (Gervais, 1853). Pp. 43–69 in
Handbook of marine mammals (S. H. Ridgway and
R. Harrison, eds.) 5:1–416.
DA SILVA, V. M., AND R. BEST. 1996. Sotalia fluviatilis.
Mammalian Species 527:1–7.
DRYDEN, I. L., AND K. V. MARDIA. 1998. Statistical
shape analysis. John Wiley & Sons, New York.
EVANS, W. E. 1994. Common dolphin, white-bellied
porpoise Delphinus delphis Linnaeus, 1758. Pp.
191–224 in Handbook of marine mammals (S. H.
Ridgway and R. Harrison, eds.). Academic Press,
London, United Kingdom 5:1–416.
HARRISON, R. J., AND R. L. BROWNELL. 1971. The gonads of the South American dolphins, Inia geoffrensis, Pontoporia blainvillei, and Sotalia fluviatilis.
Journal of Mammalogy 52:413–419.
HERSHKOVITZ, P. 1966. Catalog of living whales.
Smithsonian Institution Press, Washington, D.C.
HUSSON, A. M. 1978. The mammals of Suriname. E.
J. Brill, Leiden, The Netherlands.
KAMMINGA, C., M. T. VAN HOVE, F. J. ENGELSMA, AND
R. P. TERRY. 1993. Investigations on cetacean sonar
X: a comparative analysis of underwater echolocation clicks of Inia spp. and Sotalia spp. Aquatic
Mammal Science 19:31–43.
KENDALL, D. G. 1984. Shape-manifolds, procrustean
metrics, and complex projective spaces. Bulletin of
the London Mathematical Society 16:81–121.
MAGNUSSON, W. E., R. C. BEST, AND V. M. F. DA SILVA.
1980. Numbers and behaviour of Amazonian dolphins, Inia geoffrensis and Sotalia fluviatilis fluviatilis, in the Rio Solimões, Brazil. Aquatic Mammals
Science 8:27–32.
MITCHELL, E. 1975. Review of biology and fisheries
for smaller cetaceans. Journal of Fisheries and Research Board of Canada 32:875–1240.
MONTEIRO-FILHO, E. L. A. 1992. Pesca associada entre
golfinhos e aves marinhas. Revista Brasileira de
Zoologia 9:29–37.
133
MONTEIRO-FILHO, E. L. A. 1995. Pesca interativa entre
o golfinho Sotalia fluviatilis guianensis e a comunidade pesqueira de região de Cananéia. Boletim do
Instituto de Pesca, São Paulo 22:15–23.
MONTEIRO-FILHO, E. L. A. 2000. Group organization
of the dolphin Sotalia fluviatilis guianensis in an estuary of southeastern Brazil. Ciência e Cultura 52:
97–101.
PATTON, J. L., AND P. V. BRYLSKI. 1987. Pocket gophers
in alfalfa fields: causes and consequences of habitatrelated body size variation. American Naturalist 130:
493–506.
PERRIN, W. F., P. A. AKIN, AND J. V. KASHIWADA. 1991.
Geographic variation in external morphology of the
spinner dolphin Stenella longirostris in the eastern
Pacific and implications for conservation. Fishery
Bulletin 89:411–428.
PERRIN, W. F., E. D. MITCHELL, J. G. MEAD, D. K.
CALDWELL, AND P. J. H. VAN BREE. 1981. Stenella
clymene, a rediscovered tropical dolphin of the Atlantic. Journal of Mammalogy 62:583–598.
PERRIN, W. F., M. D. SCOTT, G. J. WALKER, AND V. L.
CASS. 1985. Review of geographical stock of tropical dolphin (Stenella spp. and Delphinus delphis) in
the eastern Pacific. NOAA Technical Report, National Marine Fisheries Services 28:1–28.
PERRIN, W. F., ET AL. 1987. Revision of the spotted
dolphins, Stenella spp. Marine Mammal Science 3:
99–170.
RICE, D. W. 1977. A list of the marine mammals of
the world. 3rd ed. NOAA Technical Report, National
Marine Fisheries Services 711:1–15.
ROHLF, F. J. 1996. Morphometric spaces, shape components, and the effects of linear transformations.
Pp. 117–129 in Advances in morphometrics (L. F.
Marcus, M. Corti, A. Loy, G. Naylor, and D. E.
Slice, eds.). Plenum, New York.
ROHLF, F. J. 1998. On the application of geometric
morphometrics to studies of ontogeny and phylogeny. Systematic Biology 47:147–158.
ROHLF, F. J. 1999. Shape statistics: procrustes superimpositions and tangent spaces. Journal of Classification 16:197–223.
ROHLF, F. J., AND F. L. BOOKSTEIN. 1987. A comment
on shearing as a method for ‘‘size correction.’’ Systematic Zoology 36:356–367.
ROHLF, F. J., AND D. E. SLICE. 1990. Extensions of the
Procrustes method for the optimal superimposition
of landmarks. Systematic Zoology 39:40–59.
ROSAS, F. C. W., AND A. BARRETO. In press. Reprodução e crescimento. In Biologia e ecologia do botocinza, Sotalia guianensis (E. L. A. Monteiro-Filho,
ed.).
SIMÕES-LOPES, P. C. 1988. Ocorrência de uma população de Sotalia fluviatilis Gervais 1853, (Cetacea,
Delphinidae) no limite sul de sua distribuição, Santa
Catarina, Brasil. Biotemas 1:57–62.
SLICE, D. E. 1996. Three-dimensional generalized resistant fitting and the comparison of least squares
and resistant fit residuals. Pp. 179–200 in Advances
in morphometrics (L. F. Marcus, M. Corti, A. Loy,
G. Naylor, and D. E. Slice, eds.). Plenum, New
York.
ZAM, S. G., D. K. CALDWELL, AND M. C. CALDWELL.
1970. Some internal parasites from freshwater ce-
134
JOURNAL OF MAMMALOGY
taceans from the upper Amazon river. Investigations
on Cetacea 2:250–251.
Submitted 25 August 2000. Accepted 29 May 2001.
Associate Editor was Joseph A. Cook.
APPENDIX I
Specimens examined.—The 104 specimens
used were obtained from the following collections: Laboratório de Mamı́feros Aquáticos,
Universidade Federal de Santa Catarina (LAMAQ/ UFSC: 1073; 1079; 1082; 1083; 1087;
1104; 1108; 1114; 1117; 1130; 1175; 1180;
1203; 1208; 1218; 1219; 1222; 1226), Universidade Federal do Paraná (UFPR: 011; 014; 020;
027; 029; 031; 033; 052; 113; 114; 134),Instituto
de Pesquisas Cananéia (IPeC:008; 010; 012;
Vol. 83, No. 1
013), Museu de Zoologia, Universidade de São
Paulo (MZUSP: 9417; 9611; 9821; 10230;
10232; 10403; 18874; 18923; 18943; 18944;
18948; 18949; 19541; 19913; 23801; 23802;
23809; 23810; 23811; 23812; 23813; 24811;
24812; 26852; 26853; 26855; 26856; 26857;
26858; 26859; 26860; 26863; 26866; 26867;
26868; 26870; 26871; 27521; 27522; 27523;
27560; 27561; 27591; 27592; 27653; 27654;
27830; 27831; 27997; 27998; 27999; 28000;
28181; 28182; 28183; 28184;), Museu Nacional
(MN/UFRJ: 001; 004; 009; 010; 014; 124), and
Projeto Mamirauá (EEMSF 9502; 9507; 9508;
9509; 9510; 9514; RDSMSF 97; 97/2; and 1
specimen not numbered). The specimens were
grouped by geographic origin as marine south (n
5 32), marine southeast (n 5 47), marine northeast (n 5 13), and Amazonian (n 5 12).