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Keywords:

  • myliobatoids;
  • muscle cephalic;
  • gills

Abstract

  1. Top of page
  2. Abstract
  3. METHODOLOGY
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSIONS
  7. Acknowledgements
  8. APPENDIX A
  9. LITERATURE CITED

This article describes the anatomy of the dorsal and ventral cephalic musculature of Gymnura marmorata, G. micrura, Aetobatus narinari, Myliobatis californica, M. longirostris, Rhinoptera steindachneri, Mobula munkiana, and M. thurstoni. It was observed that muscles of the dorsal cephalic region showed little variation among species, with the exception of the dorsal longitudinal bundles and the cucullaris muscle. The ventral cephalic musculature showed wider differences, mainly in the depressor hyomandibulae, coracomandibularis, and mandibular adductor muscles. M. munkiana and M. thurstoni revealed a significant muscle reduction, while M. californica, M. longirostris, A. narinari, and R. steindachneri showed a significant development of the ventral cephalic musculature. The species in this comparative study were clearly grouped based on their feeding habits. Data gathered on the muscle arrangements correspond to other taxonomy studies conducted on these groups. However, the results of this study agree only partially with those from previously described phylogenetic models. Therefore, further phylogenetic research is recommended. Anat Rec Part A 271A:259–272, 2003. © 2003 Wiley-Liss, Inc.

Batoids (commonly known as rays) are a group of cartilaginous fish with a characteristic dorsoventral flatness. They have enlarged pectoral fins (often wing-shaped), which are attached to the head, near to the fifth or sixth ventral gill openings. Currently, this group includes 16 families and more than 500 living species of rays worldwide. Most of these are marine, and a few live in freshwater (Last and Stevens, 1994).

Compagno (1977) divided batoids into five monophyletic groups: rhinobatoids (guitarfishes), rajoids (skates), pristoids (sawfishes), torpedinoids (torpedo or electric rays), and myliobatoids (stingrays, and cownose and devil rays). Myliobatoids have been taxonomically positioned (Nishida, 1990; Nelson, 1994), as suborder Myliobatoidei, including two superfamilies: Dasyatoidea and Myliobatoidea.

The superfamily Myliobatoidea contains some of largest batoid species, including nine genuses and 59 species. This superfamily is integrated by the families Gymnuridae and Myliobatidae, which Nishida (1990) gathered into a monophyletic group. In both families, the postorbital process has an anterior position in the orbital region.

The muscles of the head and gill skeleton in batoids and myliobatoids are more complex than in any other elasmobranchii. They also show a significant variation, mainly in the ventral cephalic region, which is the most widely known.

Studies on batoid musculature are scarce (De Andres et al., 1987; Miyake, 1988; Miyake et al., 1992). During the last decade, however, characteristics of the dorsal and ventral cephalic musculature (Nishida, 1990; McEachran et al., 1996; Lovejoy, 1996) have been examined in phylogenetic projects. The objective of this work was to describe the anatomy of the cephalic dorsal and ventral musculature of myliobatoids, as a basis for future phylogenetic genus research.

METHODOLOGY

  1. Top of page
  2. Abstract
  3. METHODOLOGY
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSIONS
  7. Acknowledgements
  8. APPENDIX A
  9. LITERATURE CITED

Specimens of the following Myliobatoidea species were included in this study: Gymnura marmorata, G. micrura (butterfly ray), Aetobatus narinari (spotted duck-billed ray and spotted eagle ray), Myliobatis californica (eagle ray), M. longirostris (eagle ray), Rhinoptera steindachneri (cownose ray), Mobula munkiana (devil ray), and M. thurstoni (bentfin devilray). The specimens used are described in Appendix A. The collection areas were located along the main Mexican coastal fishery centers in the Gulf of Mexico, Gulf of California, and the Pacific Ocean. Myliobatids are commonly captured in shrimp trawlers or dragnets. In larger organisms (such as Mobula) that are used for human consumption, only the medial region, which is discarded by fishermen, was collected. This region includes the cranial and branchial regions, and the vertebral column. It should be noted that the species described herein are under no special protection status, and thus are being exploited with no control. This type of study can help to assess the current situation of these organisms, and improve their future management.

The largest specimens (>900 mm DW) were dissected in the field, and specimens <900 mm DW were fixed in formaldehyde 10%, to be later transported to the laboratory. Dissections were conducted with conventional techniques, focusing on the dorsal and ventral cranial musculature for the anatomical description (Fig. 1). For each muscle the following characteristics were analyzed: form, disposition, fiber orientation, origin, and insertion. The terminology used herein is based on De Andrés et al. (1987), Nishida (1990), Miyake et al. (1992), and Wilga and Motta (1998).

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Figure 1. Dorsal view of the cephalic musculature: (a) Rhinoptera steindachneri, and (b) Mobula munkiana. Ventral view of the cephalic musculature: (c) R. steindachneri (level 2), and (d) M. munkiana (level 2). AM, adductor mandibulae; CA, coracoarcualis; CM, coracomandibular; DC1, dorsal constrictor 1; DLB, dorsal longitudinal bundles; DR, depressor rostri; LHM, levator hyiomandibulae; TS, superficial transverse.

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RESULTS

  1. Top of page
  2. Abstract
  3. METHODOLOGY
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSIONS
  7. Acknowledgements
  8. APPENDIX A
  9. LITERATURE CITED

Muscles of the Dorsal Cephalic Region

Precranial muscle (PM).

This paired muscle was present only in G. micrura (Fig. 2a) and G. marmorata (Fig. 2b). It originates on the mid-line, where it fuses with its antimere (symmetrical opposed or homotypical muscle). Each section runs caudolaterally until it inserts in the lateral corner of the neurocranium, under the preorbital process on the nasal capsules.

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Figure 2. Dorsal view of the cephalic musculature: (a) Gymunura micrura, (b) Gymnura marmorata, (c) Myliobatis californica, and (d) Myliobatis longirostris. AM, adductor mandibulae; AML2, adductor mandibulae lateralis 2; CC, cucullaris; CHD, constrictor hyoideus dorsalis; DC, dorsal constrictors; DC1–DC5, dorsal constrictors 1–5; DLB, dorsal longitudinal bundles; ELF, endolymphatic foramen; EPE, ethmoideo-parethmoidalis; FON, fontanelle; HM, hyomandibular cartilage; LF, lymphatic foramen; LHM, levator hyomadibulae; LS, levator spiracularis; N, neurocranium; PM, precranial muscle; S, synarcual.

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Ethmoideo-parethmoidalis muscle (EPE).

In all taxa, this muscle originates from the anterolateral part of the neurocranium, and runs caudally until it inserts in the propterygium (Fig. 2). Together with the mesopterygium, metapterygium, and scapulacoracoid cartilages, the propterygium integrates a part of the pectoral girdle. This muscle is not visible in A. narinari, R. steindachneri, M. munkiana, and M. thurstoni, because it is under the neurocranium.

Dorsal longitudinal bundles (DLB).

This muscle originates in the rostrodorsal side of the scapulacoracoid cartilage. In G. micrura (Fig. 2a) and G. marmorata (Fig. 2b), it runs anteriorly and inserts in the otic region, well behind the only pair of lymphatic foramina. In M. californica (Fig. 2c) and M. longirostris (Fig. 2d), this structure is inserted close to the perilymphatic foramina. In A. narinari (Fig. 3a), it runs rostrally and inserts just behind the fontanelle. In R. steindachneri (Fig. 3b), M. thurstoni (Fig. 3c), and M. munkiana (Fig. 3d), this muscle inserts in the rostral portion of the postorbital process, next to the fontanelle. In R. steindachneri (Fig. 3b), the DLB is formed by fibers oriented in two directions: rostral fibers, with a diagonal orientation; and caudal fibers, longitudinally oriented. In M. thurstoni (Fig. 3c) and M. munkiana (Fig. 3d), the muscular bundle is split. Fiber orientation is diagonal in the rostral bundle, and longitudinal in the caudal bundle. This is similar to R. steindachneri. In R. steindachneri, M. munkiana, and M. thurstoni, the caudal bundle muscle fibers insert with fibers of connective tissue on the caudal region of the first muscular bundle. In these species, the DLB has split in two, thus allowing to talk about a rostral and a caudal DLB.

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Figure 3. Dorsal view of the cephalic musculature: (a) Aetobatus narinari, (b) Rhinoptera steindachneri (level 1 on the left side displays pectoral muscles; the right side shows level 2), (c) Mobula thurstoni, and (d) Mobula munkiana. For abbreviations, see Fig. 1.

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Levator hyomandibulae muscle (LHM).

In all of the rays examined, this muscle originates on the lateral wall of the neurocranium otic region. It runs rostrolaterally and inserts in the mid-dorsal region of the hyomandibular cartilage in G. marmorata (Fig. 2a), G. micrura (Fig. 2b), and A. narinari (Fig. 3a). In the Myliobatis species (Figs. 2c and d) and in M. munkiana (Fig. 3d), the muscle narrows and runs up to the tip of the hyomandibular cartilage. In M. thurstoni (Fig. 3c), the anterior portion of this muscle is on the rostral DLB.

Levator spiracularis muscle (LS).

This muscle arises just below the origin of the levator hyomandibulae muscle (Fig. 2a and b). It runs anterolaterally and inserts in the distal tip of the hyomandibular cartilage. As it is located under the postorbital processes, this muscle may not appear in some of the figures in this work.

Superficial dorsal constrictor muscles 1–5 (DC1–DC5).

These muscles consist of five paired muscles covering the dorsal branchial region. They originate anteriorly and run caudally, inserting into membranes located between constrictor muscles. In A. narinari (Fig. 3a), M. californica (Fig. 2c), and M. longirostris (Fig. 2d), they have fused into a muscular bundle. R. steindachneri has five pairs of dorsal constrictors, but only the first one can be observed, because the rest are covered by the pectoral girdle muscles (Fig. 3b). A similar arrangement is found in M. thurstoni (Fig. 3c), where the dorsal constrictors 1–3 are partially visible. In M. munkiana (Fig. 3d), even when these muscles are fused, a slight separation between them can be observed.

Constrictor hyoideus dorsalis (CHD).

In all taxa examined, this muscle originates on the dorsal constrictor 1 and runs anteroventrally, until it inserts in a septum located between the CHD and the constrictor hyoideus ventralis (Figs. 2 and 3).

Cucullaris muscle (CC).

This muscle originates on the anterior face of the scapulacoracoid cartilage and runs medially, inserting in the dorsal longitudinal bundles. In some species, such as G. marmorata (Fig. 2a), M. californica (Fig. 2c), and R. steindachneri (Fig. 3b), it is triangular, while in others, such as M. longirostris (Fig. 2d) and G. micrura (Fig. 2b), it is rectangular. In M. longirostris it extends under the dorsal constrictors. This muscle was not observed in A. narinari, M. thurstoni, and M. munkiana.

Muscles of the Cephalic Ventral Region

Depressor rostri muscle (DR).

This paired muscle originates from a strong fascia in the mid-ventral region. In G. marmorata (Fig. 4a) and G. micrura (Fig. 5a), the depressor rostri inserts directly into the propterygium, while in the rest of the species it inserts directly through an aponeurosis in the lateral part of the nasal capsules. In both species, the fibers of each muscle have a differential orientation that makes them look as two muscles, which are fused to their antimere in the mid-line. In M. longirostris and M. californica, fibers of this muscle have a single orientation. In M. californica (Fig. 6a), the right and left depressor rostri muscles are together, while in M. longirostris (Fig. 6d) they are slightly separated. In A. narinari (Fig. 7a) and R. steindachneri (Fig. 8a), muscle fibers have two orientation. In the Mobula species, these muscles have a single orientation and are clearly separated (Fig. 9).

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Figure 4. Ventral view of the cephalic musculature in Gymnura marmorata: (a) level 1, (b) level 2, (c) level 3, and (d) level 4. AML1, adductor mandibulae lateralis 1; AMM, adductor mandibulae medialis; BH, basihyal cartilage; CA, coracoarcualis; CB, coracobranchiales; CH, coracohyoideus; CHM, coracohyomandibularis; CHV, constrictor hyoideus ventralis; CM, coracomandibular; DH, depressor hyomandibulae; DR, depressor rostri; F, fascia; MK, Meckelian cartilage; NS, nostril; SB, suborbitalis; VC1– VC5, ventral constrictors 1–5.

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Figure 5. Ventral view of the cephalic musculature in Gymnura micrura: (a) level 1, (b) level 2, (c) level 3, and (d) level 4. For abbreviations, see Fig. 3.

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Figure 6. Ventral view of the cephalic musculature in Myliobatis californica: (a) level 1, (b) level 2, and (c) level 3; and Myliobatis longirostris: (d) level 1, (e) level 2, and (f) level 3. VS, ventral constrictors; Y, Y muscle; Z, Z muscle. For other abbreviations, see Fig. 3.

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Figure 7. Ventral view of the cephalic musculature in Aetobatus narinari: (a) level 1, (b) level 2, and (c) level 3. For abbreviations, see Figs. 3 and 5.

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Figure 8. Ventral view of the cephalic musculature in Rhinoptera steindachneri: (a) level 1, (b) level 2, (c) level 3, and (d) level 4. M, M muscle; TS, superficial transverse. For other abbreviations, see Figs. 3 and 5.

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Figure 9. Ventral view of the cephalic musculature in Mobula munkiana: (a) level 1, and (b) level 2; and Mobula thurstoni: (c) level 1, and (d) level 2. For other abbreviations, see Figs. 3, 5, and 7.

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Superficial transverse (ST) muscle and superficial ventral constrictors (VC1–VC5).

This muscle was previously described by De Andrés et al. (1987) in Mobula. Both M. thurstoni (Fig. 9a) and M. munkiana (Fig. 9c) have a muscle that may correspond to the ST muscle. It originates on the fascia located in the mid-ventral region, and runs anterolaterally until it inserts on one side of the depressor rostri muscle. In A. narinari (Fig. 7a), M. californica (Fig. 6a), and M. longirostris (Fig. 6d), the superficial VCs are fused, forming a muscular bundle that can be mistaken for the ST muscle. At first glance, it appears that constrictors are fused in R. steindachneri (Fig. 8a). However, a detailed dissection of the muscle revealed the existence of a very thin muscle layer originating in the medial region, which runs anterolaterally. This muscle may correspond to the ST described by De Andrés et al. (1987). When this muscle was removed, the superficial VC1–VC5 muscles could be observed (Fig. 8b). In Mobula thurstoni (Fig. 9a) and M. munkiana (Fig. 9c), the ST muscle and the superficial VCs are clearly separated, the latter being reduced. In G. marmorata (Fig. 4a) and G. micrura (Fig. 5a), only the superficial VC1–VC5 can be observed.

Coracoarcualis muscle (CA).

This muscle originates in the anteroventral face of the scapulacoracoid cartilage. It runs rostrally and inserts in a strong fascia on the coracomandibularis muscle. The length of this muscle is variable. In A. narinari (Fig. 7a), it is reduced and reaches the fifth gill slit. In G. marmorata (Fig. 4b), G. micrura (Fig. 5b), M. californica (Fig. 6a), M. longirostris (Fig. 6d), Rhinoptera steindachneri (Fig. 8a), and M. thurstoni (Fig. 9a), it reaches the fourth gill slit. In M. munkiana, this muscle is longer than in all other species, and reaches the second gill slit (Fig. 9c).

Coracomandibular muscle (CM).

This muscle has diverse origins, but in all organisms it runs rostrally and inserts in the Meckelian cartilage. In A. narinari (Fig. 7b), it is inserted with a pair of tendons. In all other species, it inserts directly on the cartilage. In M. californica (Fig. 6b), M. longirostris (Fig. 6e), A. narinari (Fig. 7b), and R. steindachneri (Fig. 8b), this muscle originates in the anterodorsal face of the scapulocoracoid cartilage. In M. munkiana (Fig. 9c), G. marmorata (Fig. 4b), and G. micrura (Fig. 5b), it originates in the membrane where the coracoarcualis muscle inserts. In M. thurstoni (Fig. 9b), the muscle originates in a strong fascia located at the level of the superficial VC3.

Suborbitalis muscle (SB).

This muscle originates in the dorsal part of the palatoquadrate cartilage. It runs caudoventrally on this cartilage until it inserts through a small tendon on the mandibulae lateralis 2 adductive muscle. In A. narinari (Fig. 7b), this muscle is reduced, whereas it is more developed in G. marmorata (Fig. 4b), G. micrura (Fig. 5b), M. californica (Fig. 6c), M. longirostris (Fig. 6e), and R. steindachneri (Fig. 8b). This structure was not observed in M. munkiana or M. thurstoni.

Adductor mandibulae medialis muscle (AMM).

This is a paired digastric muscle that Wilga and Motta (1998) described as quadratomandibularis medial. In M. californica (Fig. 6b), M. longirostris (Fig. 6d), and R. steindachneri (Fig. 8a), it originates on the medial part of the Meckelian cartilage and runs laterally, surrounding the mouth. Forming the commisure, it turns anteromedially and inserts in the palatoquadrate. In A. narinari (Fig. 7a), each muscle fuses with its antimere in the medial region of the palatoquadrate cartilage. In G. marmorata (Fig. 4a) and G. micrura (Fig. 5a), this muscle is small and inserts in the lateral region of the Meckelian cartilage. It was not identified in M. thurstoni and M. munkiana.

Mandibular adductive muscles (AM, AML1, and AML2).

These muscles show different degrees of development. In G. marmorata (Fig. 4b) and G. micrura (Fig. 5b), two lateral muscles are clearly observed, corresponding to the AML1 and AML2 of Nishida (1990), and to the quadratomandibularis anterior, medial, and deep of Wilga and Motta (1998). In A. narinari (Fig. 7b), both muscles were also observed, but there is a third muscle, which is well developed. It originates in the palatoquadrate, on one side of the AML2, and runs laterally until it inserts in the opposite side, on the palatoquadrate cartilage. Miyake et al. (1992) described this muscle as the adductor mandibulae. This same muscle was observed in R. steindachneri (Fig. 7b), where it is well developed, and in M. californica (Fig. 6b) and M. longirostris (Fig. 6e). In the latter two species, the muscle splits in the lateral region. The AML1 and AML2 muscles were not observed in R. steindachneri (Fig. 8). In M. thurstoni (Fig. 9b) and M. munkiana (Fig. 9d), only one AM muscle was found.

Quadratomandibularis ventral (QV).

This muscle originates in the superior region of the palatoquadrate cartilage and runs caudally until it inserts in the ventral edge of the Meckelian cartilage. Together with the AML1 and AML2, it covers the mandible articulation. This structure was found only in G. marmorata (Fig. 4c) and G. micrura (Fig. 5c), but it was also described by Motta and Wilga (1995) in the lemon shark (Negaprion brevirostris).

Coracohyoideus muscle (CH).

This muscle is located under the coracomandibularis muscle. In G. marmorata (Fig. 4c) and G. micrura (Fig. 5c), it originates in the medial portion, on a membrane at the level of the ventral constrictor 3, and runs anteriorly until it inserts in the ventral surface of the basihyal cartilage. In G. micrura, it is fused to its antimere for its entire length, while in G. marmorata it is fused only in the anterior end. In all other species, it originates in the anterodorsal face of the scapulacoracoid cartilage. In M. californica (Fig. 6c) and M. longirostris (Fig. 6f), it inserts in a membrane located just behind muscle “Z” in the medial region. In A. narinari (Fig. 7c) and R. steindachneri (Fig. 8c), it expands more rostrally behind muscle “Y,” and in M. munkiana (Fig. 9d) it expands up to the fourth ventral constrictor. M. thurstoni (Fig. 9b) has a muscle originating in a membrane, at the level of the fourth ventral constrictor, that runs anteriorly until it inserts in the adductor mandibulae muscle. Given its position, this muscle may be the coracohyoideus.

Coracohyomandibularis muscle (CHM).

This muscle was observed only in G. marmorata (Fig. 4d) and G. micrura (Fig. 5d). It originates in the mid-line ventral, on the basihyal cartilage. In G. micrura, this muscle expands toward the caudal region; some fibers originate at the level of the ventral constrictor 4, and other fibers lie underneath the first hypobranchial cartilage. It runs rostrolaterally and inserts with a tendon on the posterior edge of the Meckelian cartilage.

Depressor hyomandibulae (DH).

This muscle originates in the medial part of the membrane covering the coracomandibularis muscle, and runs laterally until it inserts on the ventral edge of the hyomandibular cartilage. This muscle is strongly developed in G. marmorata (Fig. 4b), G. micrura (Fig. 5b), and R. steindachneri (Fig. 8b). In M. californica (Fig. 6b), it is slightly smaller, while in M. longirostris (Fig. 6e) and A. narinari, it is quite reduced. This muscle was not observed in M. thurstoni or M. munkiana.

Constrictor hyoideus ventralis (CHV).

In all taxa, this muscle originates on the ventral constrictor 1 and runs anteroventrally, until it inserts in a septum located between the CHV and the CHD.

Coracobranchiales muscles (CB).

These muscles originate from the anteroventral face of the pectoral girdle, underneath the coracomandibularis muscle. They run rostrally and insert at the level of the first gill slit.

Y muscle (Y).

This muscle was first described by Miyake et al. (1992). It was found in M. californica (Fig. 6c) and M. longirostris (Fig. 6f), under the AM muscle, between the first interbranchial septa. This muscle extends anterodorsally up to the posterior edge of the Meckelian cartilage. In A. narinari (Fig. 7c), the “Y” muscle is relatively thin, while in R. steindachneri (Fig. 8c), it is quite thick. This muscle is absent in all other species.

Z muscle (Z).

This structure was described by Miyake et al. (1992) in R. steindachneri as a small muscle located in the interbranchial septa. In the present study, it was found that in R. steindachneri this “muscle” is a segment of the ventral superficial constrictors, hidden by the upper muscular layer. In M. californica (Fig. 6c), M. longirostris (Fig. 6f), and A. narinari, this muscle appears to be a part of the ventral superficial constrictors and is not fused. In all other taxa, this muscle is absent.

M muscle (M).

In the current study, this structure is termed the M muscle. This muscle was found only in R. steindachneri (Fig. 8d). It is a paired, flat muscle located on the basal plate of the neurocranium, posterior to the nasal capsules. It originates on the mid-ventral region of the neurocranium, just below the nasal capsules, and runs laterally until it inserts in the neurocranium lateral portion, near the articulation of the nasal capsules to the antorbital cartilage. This structure is not homologous to any previously described muscle.

DISCUSSION

  1. Top of page
  2. Abstract
  3. METHODOLOGY
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSIONS
  7. Acknowledgements
  8. APPENDIX A
  9. LITERATURE CITED

As regards its position, size, and shape, the dorsal cephalic musculature was consistent in all taxa examined. However, differences were observed in two muscles. The dorsal longitudinal bundles are inserted behind the linfatic foramina in G. micrura and G. marmorata. This arrangement is considered to be a plesiomorphic characteristic. In other organisms, such as M. longitostris, M. californica, and A. narinari, the insertion point of this muscle is behind the fontanella. However, in M. munkiana, M. thurstoni, and R. steindechnari, it tends to increase in size by an anterior expansion, until it inserts in the neurocranium orbital region. This development in the muscle size can be considered as a synapomorphy. In R. steindachneri, this muscle is slightly divided in two bundles, which are more evident in M. munkiana and M. thurstoni.

Another variation in the dorsal region, the absence of cucullaris muscle, was observed in A. narinari, M. thurstoni, and M. munkiana, which may be considered to be a derived characteristic.

The ventral cephalic musculature showed significant differences: 1) The depressor hyomandibulae is reduced (M. californica, M. longirostris, and A. narinari), and even absent (M. munkiana and M. thurstoni). Loss of this muscle is considered to be a derived characteristic. 2) The quadratomandibularis muscle was found only in G. micrura and G. marmorata. We consider that the presence of this muscle is a plesiomorphic characteristic, while its absence in all other taxa examined is a derived characteristic. 3) The mandibular adductor muscles (M. longirostris, M. californica, A. narinari, and R. steindachneri), tend to increase their size which is considered to be a derived characteristic. 4) In M. thurstoni and M. munkiana, the dorsal and ventral superficial constrictor muscles tend to reduce their size, while in A. narinari, M. californica, and M. longirostris tend to fuse. Fusion of these muscles is considered to be a synapomorphy. 5) The coracomandibularis muscle showed high variability. In M. californica, M. longirostris, A. narinari, and R. steindachneri, this muscle originates in the pectoral girdle. In G. micrura, G. marmorata, M. thurstoni, and M. munkiana, it is shorter, originating in the membrane where the coracoarcualis muscle inserts. 6) The Y muscle was found in M. californica, M. longirostris, A. narinari, and R. teindachneri. The presence of the Y muscle is considered to be a synapomorphy. 7) In M. californica, M. longirostris, A. narinari, and R. steindachneri, the Z muscle was observed. We propose that the Z muscle is a part of the superficial ventral constrictors.

At the interspecific ground, low variation was found among the species of the genus Gymnura, while a higher variation was observed in the species of the genus Mobula and Myliobatis.

In general, differences in the ventral region musculature are related to the feeding habits of these organisms. The muscular arrangement of G. micrura and G. marmorata is similar to that described for Rhinobatos lentiginosus (Wilga and Motta, 1998). The common diets of all three species are based on small fish, crustacean, and mollusks (Bigelow and Schroeder, 1953).

A. narinari, M. californica, M. longirostris, and R. steindachneri subsist chiefly on hard-shelled mollusks, but their diet also includes crustaceans (Bigelow and Schroeder, 1953). The need to be strong enough to break the food shells may explain why the mandibular adductor and coracomandibular muscles are more developed in these species. These muscles play an active role in mandibular elevation and depression. Although they are present in all species included in this study, they are significantly stronger in A. narinari, M. californica, M. longirostris, and R. steindachneri. The coracomandibular muscle is the first muscle triggered during lower mandible depression movement, supported by mandibular and hyomandibular depressors. The mandibular adductor muscle plays a role in lower jaw elevation movement, and upper jaw protrusion (Wilga and Motta, 1998).

M. munkiana and M. thurstoni are filtering species that feed mainly on small crustaceans, especially mysids and euphausiids (Notobartolo-di-Sciara, 1987). A significant reduction of the ventral cephalic musculature is found in these species, while the depressor hyomandibulae and coracohiomandibularis muscles are absent. As these organisms keep their mouth open for long periods to filter their food, they need no strength to close their mandibles and triturate preys. This explains the absence of such muscles, as the coracomandibularis alone can perform this function. A significant development of the adductor mandibulae muscle was also observed. This muscle plays a role in mandibular elevation by allowing the mouth to be open for the filtering operation. A reduction of the adductor mandibulae lateralis 1 and 2, and the superficial ventral constrictor muscles was also observed.

The muscular arrangement in G. micrura and G. marmorata is similar to that reported by Wilga and Motta (1998) for Rhinobatos lentiginosus. The coracohyomandibularis muscle, which is considered to be a plesiomorphic structure, was observed only in these organisms. Such results agree with the phylogenetic model developed by Nishida (1990) (Fig. 9a), Lovejoy (1996) (Fig. 10b), and McEachran et al. (1996) (Fig. 10c). It should also be noted that the ventral quadratomandibularis muscle was detected only in G. marmorata and G. micrura, and has only been described previously by Motta and Wilga (1995) in lemon sharks (Negaprion brevirostris).

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Figure 10. Phylogeny of Myliobatoidei, according to: (a) Nishida (1990), (b) Lovejoy (1996), and (c) McEachran et al. (1996).

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Phylogenetic studies of these groups, including those conducted by Lovejoy (1996), Shirai (1996), and McEachran et al. (1996), considered a large number of taxa (urolophids, dasyatids, rajids, myliobatids, and even some sharks). Therefore, characteristics of the dorsal and ventral cephalic musculature are too general. In contrast, Nishida (1990) worked specifically on the phylogeny of the suborder Myliobatoidei. For his analysis (Fig. 10a), he used two muscles of the dorsal cephalic region: 1) the precranial muscles found only in gymnurids (also detected in the current study), and 2) the dorsal longitudinal bundle (reported as a long muscle inserted at the orbital region), which is considered to be a synapomorphy.

As regards the ventral cephalic muscles, this study revealed characteristics that were not described by Nishida (1990). The superficial transverse muscle has only been described by De Andres et al. (1987) in Mobula; however, in the present study it was also observed in Rhinoptera. It is proposed that this muscle and the dorsal longitudinal bundle are two synapomorphies that are shared by Rhinoptera and Mobula, and support phylogenies obtained by other authors.

This analysis has considered characteristics shared by mylobatids (Myliobatis-Aetobatus) and Rhinoptera, including: 1) the Y muscle found only in these species; 2) the Z muscle found only in these species; 3) a highly developed coracomandibular muscle; and 4) a highly developed adductor mandibular muscle. It can be concluded that myliobatids and Rhinoptera share more characteristics than Rhinoptera and Mobula, which suggests that Rhinoptera is the myliobatids' sister group. It should be noted, however, that these results are based only on the muscular arrangement, whereas previous reports were concerned with internal and external morphological characteristics.

CONCLUSIONS

  1. Top of page
  2. Abstract
  3. METHODOLOGY
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSIONS
  7. Acknowledgements
  8. APPENDIX A
  9. LITERATURE CITED

Major variations were found in the arrangement of the ventral musculature of the myliobatoids examined, whereas the dorsal musculature was more constant. The highest number of plesiomorphic characteristics was observed in G. micrura and G. marmorata, while M. thurstoni and M. munkiana presented the highest number of derived characteristics. The comparative study clearly grouped the species according to their feeding habits. The muscle data are in agreement with the group taxonomy reported by Nelson (1994), based on Nishida (1990). The phylogeny proposed in this work has a partial correspondence to previous models; therefore, it is recommended that the current results should be used for future phylogeny research.

Acknowledgements

  1. Top of page
  2. Abstract
  3. METHODOLOGY
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSIONS
  7. Acknowledgements
  8. APPENDIX A
  9. LITERATURE CITED

I thank Dr. Sh. P. Applegate and Dr. J. Musick for their comments and suggestions on this document. I also express my gratitude to Héctor M. Montes-Domínguez for his valuable help in the field and laboratory.

APPENDIX A

  1. Top of page
  2. Abstract
  3. METHODOLOGY
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSIONS
  7. Acknowledgements
  8. APPENDIX A
  9. LITERATURE CITED

Specimens Examined

  • Superfamily Myliobatoidea

  • Family Gymnuridae

    • Gymnura marmorata: two specimens collected in Mazatlán, Sinaloa (298 mm total length (TL), 222 mm disc length (DL), 369 mm disc width (DW); and 240 mm TL, 185 mm DL, 317 mm DW).

    • Gymnura micrura: three specimens collected in Alvarado, Veracruz (149 mm TL, 118 mm DL, 214 mm DW; 155 mm TL, 112 mm DL, 218 mm DW; and 279 mm TL, 403 mm DL, 219 mm DW).

  • Family Myliobatidae

  • Subfamily Myliobatinae

    • Myliobatis californica: two specimens collected in Bahia Kino, Sonora (1031 mm TL, 476 mm DL, 715 mm DW; and 1,230 mm TL, 591 mm DL, 900 mm DW)

    • Myliobatis longirostris: two specimens collected in Bahia Kino, Sonora (1,370 mm TL, 437 mm DL; and 1,095 mm TL, 603 mm DW).

    • Aetobatus narinari: one specimen collected in San Blas, Nayarit (1,380 mm TL, 561 mm LD).

  • Subfamily Rhinopterinae

    • Rhinoptera steindachneri: three specimens collected in Boca del Cielo, Chiapas (1,350 mm TL, 550 mm DL, 830 mm DW; 1,229 mm TL, 515 mm DL, 838 mm DW; and 1089 mm TL, 530 mm DL, 876 mm DW).

  • Subfamily Mobulinae

    • Mobula munkiana: one specimen collected in Salina Cruz, Oaxaca (1,350 mm TL, 960 mm DW) and one collected in Caleta de Campor, Michoacán (1,116 mm TL, 675 mm DL, 1,015 mm DW).

    • Mobula thurstoni: one specimen collected in La Ventana, Baja California Sur (1,601 mm TL, 1033 mm DL, 1694 mm DW), and one collected in Bahia Kino, Son. (1,040 mm TL, 650 mm DL).

LITERATURE CITED

  1. Top of page
  2. Abstract
  3. METHODOLOGY
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSIONS
  7. Acknowledgements
  8. APPENDIX A
  9. LITERATURE CITED
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  • Compagno LJV. 1977. Phyletic relationships of living sharks and rays. Amen Zool 17: 303322.
  • De Andrés A, García GJM, Muñoz-Chápuli R. 1987. Ventral musculature in elasmobranchs: some functional and phylogenetic implications. In: Proceedings of the Fifth Congress of European Ichthyologists, Stockholm. p 5763.
  • Last PR, Stevens JD. 1994. Sharks and rays of Australia. Australia: CSIRO.
  • Lovejoy NR. 1996. Systematics of myliobatid elasmobranchs: with emphasis on the phylogeny and historical biogeography of neotropical freshwater stingrays (Potamotrygonidae: Rajiformes). Zool J Lin Soc 117: 207257.
  • McEachran JD, Miyake T, Dunn KA. 1996. Interrelationships of the batoid fishes (Chondrichthyes: Batoidea). In: StiassnyMLJ, ParentiLR, Johnson, GD, editors. Interrelationships of fishes. New York: Academic Press. p 6384.
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  • Miyake T, McEachran JD, Hall BK. 1992. Edgeworth's legacy of cranial muscle development with an analysys of muscles in the ventral gill arch of batoid fishes (Chondrichthyes: Batoidea). J Morphol 212: 213256.
  • Motta PJ, Wilga CD. 1995. Anatomy of the feeding apparatus of the lemon shark, Negaprion brevirostris. J Morphol 226: 309329.
  • Nelson JS. 1994. Fishes of the world. 3rd ed. New York: John Wiley & Sons, 600 p.
  • Nishida K. 1990. Phylogeny of the suborder Myliobatoidei. Mem Fac Fish Hokkaido Univ 37: 1108.
  • Notobartolo-di-Sciara. 1987. Natural history of the rays of the genus Mobula in the Gulf of California. Fish Bull 86: 4566.
  • Shirai S. 1996. Phylogenetic interrelationships of the Neoselachians (Chondrichthyes: Euselachii). In: StiassnyMLJ, ParentiLR, JohnsonGD, editors. Interrelationships of fishes. New York: Academic Press. p 934.
  • Wilga CD, Motta PJ. 1998. Feeding mechanism of the Atlantic guitarfish Rhinobatos lentiginosus: modulation of kinematic and motor activity. J Exp Biol 201: 31673184.