Joa 228 877
Joa 228 877
Joa 228 877
REVIEW ARTICLE
Abstract
Extraocular muscles are classically grouped as four rectus and two oblique muscles. However, their description
and potential associations with species behavior are limited. The objective was to characterize extraocular
muscles in four Myliobatoidei rays from diverse habitats with divergent behaviors. Heads (10 per species) of
Dasyatis hypostigma, Gymnura altavela, Mobula thurstoni and Pteroplatytrygon violacea were decalcified and
dissected to characterize and describe extraocular muscles. Principal component analysis (PCA) was used to
evaluate relationships between muscle length and species; for P. violacea, D. hypostigma and G. altavela, these
were qualitatively and quantitatively consistent with the general pattern of extraocular muscles in vertebrates.
In contrast, for M. thurstoni, the two oblique muscles were completely fused and there was a seventh
extraocular muscle, named m. lateral rectus b (both were apparently novel findings in this species). There were
also significant differences in eye disposition in the chondrocranium. The PCA axis 1 (rectus muscles) and PCA
axis 2 (oblique muscles) accounted for 98.47% of data variability. Extraocular muscles had significant
differences in length and important anatomical differences among sampled species that facilitated grouping
species according to their life history. In conclusion, extraocular muscles are not uniform in all vertebrate
species, thereby providing another basis for comparative studies.
Key words: Dasyatis; Gymnura; Mobula; morphology; Pteroplatytrygon.
A B A B
C D
C D
C D
Table 1 EYL, extraocular muscles length and width in studied rays Axes 1 and 2 from the PCA explained 98.47% of data vari-
(10 individuals for each species). ability (Fig. 7). The first axis was associated with the rectus
muscles and the second with oblique muscles (Table 2). The
Gymnura Dasyatis Pteroplatytrygon Mobula
G. altavela juveniles had the lowest values, whereas they
altavela hypostigma violacea thurstoni
were highest for M. thurstoni, and were intermediate for
three adult G. altavela specimens, D. hypostigma and
EYL (mm) 12.8 2.3 13.9 0.8 28.5 1.3 31.1 1.4
Length (mm) P. violacea (Fig. 7). Muscle length differed significantly
SR 15.3 7.7 17.3 0.6 17.2 1.4 46.7 0.8 among sampled species (Fig. 8).
LR 19.8 5.4 20.2 0.7 26.5 0.5 57.2 0.6
IR 17.5 1.5 24.1 0.8 24.5 0.7 55.2 1.1
MR 19.0 6.0 23.4 0.7 21.6 0.5 63.2 1.1 Extraocular muscles
IO 13.0 3.9 24.4 0.7 26.4 0.7 32.8 0.9
SO 11.8 5.8 25.5 0.8 22.7 1.1 32.4 0.9 SR
LRb 27.1 1.1
Width (mm) The SR was triangular in D. hypostigma (Figs 1A and B, and
SR 4.4 0.9 6.3 0.5 7.3 0.8 12.1 0.6 6B), but fusiform in other species. The insertion point was
LR 3.7 1.1 6.4 0.5 6.0 0.0 14.1 0.7 posterior to the EB in G. altavela (Figs 2A and 6C) and
IR 3.7 0.6 5.7 0.5 5.0 1.0 10.8 0.6 D. hypostigma, but anterior to EB in P. violacea (Figs 3C
MR 4.2 1.3 4.5 0.5 5.0 0.0 8.2 0.6 and D, and 6A) and M. thurstoni (Figs 4A–D and 6). The ITD
IO 5.2 2.4 15.3 0.6 10.9 0.6 15.1 0.9
fixation line varied among all four species: straight in
SO 9.5 2.6 15.0 0.6 16.6 0.7 17.2 0.6
G. altavela; concave in D. hypostigma; convex in P. violacea;
LRb 8.4 0.8
and oblique in M. thurstoni. There were no differences in
EYL, eye length; IO, m. inferior oblique; IR, m. inferior rectus; LR, muscle length between D. hypostigma and G. altavela. The
m. lateral rectus; LRb, m. lateral rectus b; MR, m. medial rectus; highest proportions were in M. thurstoni, whereas
SO, m. superior oblique; SR, m. superior rectus. Mean SD in mm. P. violacea had the lowest (Fig. 8A; one-way ANOVA,
F3,36 = 41.9; P < 0.01).
eyeballs, with the former being slightly smaller (Table 1). In
P. violacea, the eyeball was smaller than M. thurstoni but
IR
bigger than the other two species (Table 1). Furthermore,
there were differences between M. thurstoni and the other The IR was fusiform in all species. The insertion
three species regarding angulation of SO and SR in relation point was ventral to the EB and adjacent to the IO insertion
to the midline (Fig. 6). The SR angle ranged from slightly in G. altavela (Fig. 2C and D) and M. thurstoni (Figs 4A,
smaller or larger than the SO angle with an almost equilat- B and D, and 5), whereas in D. hypostigma (Fig. 1C) and
eral shape or much larger, giving a scalene shape (Fig. 6). P. violacea (Fig. 3D) it was between the optical nerve and
clade of Myliobatidae (Nishida, 1990; Lovejoy, 1996; ular muscles in frontal- and lateral-eyed animals (man, cat,
McEachran et al. 1996; Shirai, 1996; Dunn et al. 2003; De guinea pig and rabbit) was examined by orientation of
Carvalho et al. 2004; McEachran & Aschliman, 2004; Claeson semicircular canals; there were marked differences in inser-
et al. 2010; Aschliman et al. 2012; Naylor et al. 2012). Thus, tion points and line action angulation of the superior mus-
the completely fused oblique muscles in M. thurstoni repre- cles (SR and SO) on the globe between them (Simpson &
sented a condition derived from that with just the fused ori- Graf, 1981). Although semicircular canals have apparently
gin and separated insertions for D. brevis, D. pastinaca and not been studied in rays, the pattern of insertion and mus-
T. torpedo (Oliva, 1967; Nishida, 1990: fig. 44C), but appar- cle path had considerable modifications, with apparent
ently autapomorphic for that single examined species of associations to muscle function and animal habitat. Modi-
Mobula. Such characteristics should be considered in future fied insertions and muscle path of vertical extraocular mus-
phylogenetic studies, ideally with inclusion of additional cles were indicative of requirements for producing specific
species. compensatory eye movements, and resulted in disparate
Evidence of up to seven extraocular muscles and the con- secondary kinematic actions. The muscle paths of SO and SR
dition of two abducens-innervated eye muscles in placo- in M. thurstoni resembled the rabbit, with the ray eyes posi-
derms (as an outgroup of all extant gnathostomes) would tioned more laterally, similar to that species. However, in
support homology between those of the lamprey and the the three other species, muscle paths resembled the guinea
external rectus and retractor bulbi of tetrapods (Fritzsch pig, with eyes positioned slightly forward compared with
et al. 1990; Young, 2008). other species (Simpson & Graf, 1981: 23; fig. 1). Comparing
The accessory lateral rectus muscle (aLR) is a well-known the angle among studied ray species, rabbit and guinea pig,
abducens-innervated muscle, with a potential role in stra- the SR tended to form an acute angle (56–65 °). However,
bismus in monkeys (Spencer & Porter, 1981; Schnyder, 1984; in humans and cats, this angle tends to be obtuse (23–25 °),
Boothe et al. 1990; Narasimhan et al. 2007) and humans almost parallel to the body axis, in species with eyes
(Von Lu € dinghausen et al. 1999; Liao & Hwang, 2014). Typi- strongly positioned forward.
cally, the aLR is very small, inconsistently located, often The association of recti muscles on the first axis and obli-
superior to the optic nerve, medial to the LR and inserts at que muscles on the second axis of the PCA (Fig. 8) indicated
the posterior half of the eye ball, approximately between the importance of the size of the recti muscles to these rays,
LR and SR (Schnyder, 1984: fig. 1; Liao & Hwang, 2014). as the bottom-dwelling G. altavela juveniles had smaller
Schnyder (1984) proposed that the aLR represented a negative values, whereas pelagic M. thurstoni had higher
residual retractor bulbi (RB) from lower vertebrates, but positive values. Three G. altavela individuals, D. hypostigma
Narasimhan et al. (2007) refuted it by comparing their ori- both bottom-dwelling rays and pelagic P. violacea
gins, because aLR originates on the LR and in lower verte- remained in the middle of the PCA axis with negative val-
brates, the RB has four broad heads originating at the optic ues, separated without overlap. Furthermore, the slightly
foramen. higher values and close position to D. hypostigma in Axis 1,
According to Narasimhan et al. (2007), the aLR originated P. violacea had shorter extraocular muscle lengths related
on the orbital surface of the deep LR belly in monkeys. Liao to eyeball diameter compared with the other species. Varia-
& Hwang (2014) described a similar condition in humans, tion in muscle length in G. altavela was attributed to a com-
with aLR and LR originating from the same tendon, and bination of juveniles and adults. These differences in muscle
that it may have a muscle belly or exist simply as a fibrous path angulation and size of recti and oblique muscles have
band. Both descriptions implied that aLR does not have its a role in eyeball rotation, providing different visual fields
own source, but that it actually appeared as an appendix LR among studied species (McComb & Kajiura, 2008).
(accessory). Both aLR and LR were equally innervated In Myliobatiformes, the pectoral girdle has four distinct
although, in aLR, innervation was to single fibers (Schnyder, articular regions constituted by three condyles and a facet
1984). (Da Silva & De Carvalho, 2015) and a diverse general loco-
The LRb in M. thurstoni was similar to topography of motor behavior (Rosenberger, 2001). Stingrays such as Dasy-
mammalian aLR. Notwithstanding the similarites, these atis species have pectoral fin skeletal structures with
muscles are considered non-homologous, as LRB was larger reduced calcification and joint staggering (Schaefer & Sum-
and had its own origin. Although innervation of LRb was mers, 2005); they move with an undulatory swimming
not confirmed, due to the proximity of its origin with the mode (Rosenberger, 2001) and feed mainly on benthic prey
LR, it was probably innervated by the same nerve (VI). (Jacobsen & Bennett, 2013). The joint-staggering pattern
Future studies are needed to confirm its innervation in was lost in P. violacea, and the chains of calcification on its
M. thurstoni and to determine whether LRb is present in robust radials are very broad and highly mineralized (Schae-
any other Myliobatiformes. fer & Summers, 2005) allowing an oscillatory swimming
The origin of recti and oblique muscles in the four species mode (Rosenberger, 2001). These changes allow it to move
studied was posterior and anterior to the orbit, respectively, away from the bottom to open, clear water. The oscillatory
in agreement with Nishida (1990). The geometry of extraoc- swimming mode and abiotic factors such as light and
visibility could have allowed new angles to the visual field life history. The presence of LRb and fusion of oblique mus-
and favored the development of its eyeball, leading to a cle in other Mobulid species need to be investigated.
shift in the kind of prey captured. It feeds on fish, cephalo- Extraocular muscles were not extraordinarily uniform in all
pods, pteropods and small crustaceans (Ve ras et al. 2009; vertebrates and, therefore, could be used in future compar-
Jacobsen & Bennett, 2013). Despite extraocular muscles in ative anatomical, functional and evolutionary studies in var-
P. violacea and D. hypostigma being smaller and having ious species that, until now, have not been well
similar sizes (Table 1) when related to EYL (Fig. 3), compara- characterized.
tively, the P. violacea values are smaller, as its EYL is almost
twice that of D. hypostigma.
The butterfly rays (Gymnuridae) have a crustal calcifica- Acknowledgements
tion pattern on pectoral fin skeletal structure with cross- The authors thank: Ulisses L. Gomes (UERJ), Marcelo R. de Carvalho
bracing radials (Schaefer & Summers, 2005). Its semi-oscilla- (IB USP), Arani N. B. Mariana and Pedro P. Bombonato (UFMV USP)
tory swimming mode allows both undulate/bottom and for inspiration and extensive discussions; Marcelo Machado (UFPR)
oscillatory/column water swimming (Rosenberger, 2001) or and Andre Casas (UFAC) for help with dissection and extensive dis-
delivery of physical blows to stun prey before ingestion in cussions regarding results; and two anonymous reviewers who sug-
gested substantial revisions. The authors also thank Dr John
an ambush feeding strategy (Jacobsen et al. 2009; Jacobsen
Kastelic, University of Calgary, Alberta, Canada, for English edition
& Bennett, 2013). Gracile and flexible jaws with large
on manuscript. This work was partially supported by CAPES (Coor-
gape allow engulfment of food much larger than the ~o de Aperfeicßoamento de Pessoal de Nıvel Superior, Brazil)
denacßa
resting mouth opening (Dean et al. 2007). Furthermore, to C.M.C. by a doctorate grant and post-doc grant (proc.
M. thurstoni shares the same crustal calcification pattern #8739/13-7).
with cross-bracing radials (Schaefer & Summers, 2005), but
with an oscillatory mobuliform swimming mode that con-
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