Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 89-100, March 2021 (Published Mar. 30, 2021)

Ontogenetic variation of the odontophore of Luidia superba

(Asteroidea: Paxillosida) and its taxonomic implications

Magdalena De los Palos-Peña

https://orcid.org/0000-0002-9667-8670

Francisco Alonso Solís-Marín

; https://orcid.org/0000-0001-5729-3316

Alfredo Laguarda-Figueras

Alicia Durán-González

1. Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, México;

mdelospalos@ciencias.unam.mx (*Correspondence).

2. Laboratorio de Sistemática y Ecología de Equinodermos, Instituto de Ciencias del Mar y Limnología, Universidad

Nacional Autónoma de México, México; fasolis@cmarl.unam.mx; laguarda@cmarl.unam.mx;

aliciad@cmarl.unam.mx

Received 17-VI-2020. Corrected 14-IX-2020. Accepted 05-X-2020.

ABSTRACT

Introduction: The sea star odontophore is the structure positioned between the paired oral ossicles, with which

they articulate through proximal and distal processes. The internal anatomy structures may be used as taxonomic

characters for a precise differentiation between species, so it is necessary to describe the structures variation

throughout growth. Objective: To describe the odontophore shape and variation of Luidia superba A. H.

Clark, 1917 from specimens of the Gulf of California deposited in the Echinoderm National Collection, ICML

UNAM. Methods: A total of 735 specimens were examined to describe the external characters, from which 55

selected specimens, within a range of R = 14 mm and R = 210 mm, were dissected to extract the odontophores

and analyzed with geometric morphometrics. Results: Scanning electronic microscopy (SEM) images of the

odontophores showing the variations in shape throughout growth are presented. Differences in shape between

size groups were confirmed with a Canonical Variables Analysis (P < 0.05). Conclusions: There are three main

groups in this size ranges where specialization of the stereom can be observed through the ontogenetic series;

the variation in shape of the odontophore shown here is a precedent for the use of internal anatomy as new

taxonomic characters of identification.

Key words: Ossicles; morphology; oral frame; internal anatomy; geometric morphometrics; Scanning Electron

Microscopy.

De los Palos-Peña, M., Solís-Marín, F.A., Laguarda-

Figueras, A., & Durán-González. A. (2021).

Ontogenetic variation of the odontophore of Luidia

superba (Asteroidea: Paxillosida) and its taxonomic

implications. Revista de Biología Tropical, 69(S1),

89-100. DOI 10.15517/rbt.v69iSuppl.1.46330

The genus Luidia Forbes, 1839 is com-

posed of infaunal organisms; they usually

inhabit shallow waters and reefs on the conti-

nental shelf, although some species can extend

to the upper batial zone. They are generally

more active and agile than other starfish, and

feed primarily on small mollusks and other

echinoderms. They are characterized by having

5-11 quite long arms, which narrow distally

(Downey, 1973; A.M. Clark & Downey, 1992;

Benavides-Serrato, Borrero-Pérez, & Díaz-

Sánchez, 2011).

Species of this genus are distributed in

all oceans from the tropics to high temperate

latitudes. Some species have a wider distribu-

tion, while others have a more restricted one

DOI 10.15517/rbt.v69iSuppl.1.46330

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 89-100, March 2021 (Published Mar. 30, 2021)

(Sladen, 1889; A.M. Clark & Downey, 1992;

Puppin-Gonçalves, Rocha, Alencar, Moraes,

Araújo & Freire, 2020). The known morpho-

logical characteristics of the organisms that are

associated with the particulate nature of the

substrate they inhabit are mainly the shape and

arrangement of the ambulacral feet and paxil-

lae. These organisms are buried in the substrate,

so it has been suggested that the rounded tip of

the feet is adapted to push between the particles

of the substrate and contribute to an efficient

movement (Blake, 1989; Lawrence, 2013).

Organisms of this genus are intraoral feed-

ers, which may be related to their presence

in particulate substrates where most of the

available food corresponds mainly to infaunal

organisms, such as foraminifera. They do not

have the ability to separate the small infauna

from the sediment while feeding; the car-

diac stomach is very large, which gives them

the ability to ingest very large prey (Hulings

& Hemlay, 1963; Jangoux 1982a; Jangoux

1982b; Lawrence, 2013). The mouth frame is

composed of ten pairs of oral and circumoral

muscles and five unpaired interradial odonto-

phores. This was described by Viguier in 1878,

and he suggested that more precise characters

may be derived from the oral frame and the

internal anatomy. The odontophore is made

up of symmetrical, paired, distal, and proxi-

mal processes which articulate with the inner

surface of the oral plates and an actinal keel

to which the fibers of the odontophore-oral

muscle attach (Gale, 2011).

Luidia superba A.H. Clark, 1917 is the

largest species of the genus in the Pacific, and

the largest specimen so far reported (R = 415

mm) was collected in Galapagos (Downey

& Wellington, 1978) and deposited in the

United States National Museum, Smithsonian

Institution (USNM E18920). This species is

distributed from the Gulf of California to Peru

(Alvarado & Solís-Marín, 2013). Although no

studies have been conducted on the feeding

habits of this species, it is known that other

members of the genus are effective preda-

tors, so it is necessary to carry out studies on

their anatomy and the intraspecific latitudinal

variation that exists among specimens of the

Gulf of California to Peru. It is likely that a

successful predator, such as a luidid, needs a

developed oral system, since the five pairs of

interradial muscles, five radial pairs, the five

transverse actinal muscles on the circumorals,

and the five odontophore-oral muscles (Fig. 1)

close the peristome by contracting.

The odontophore plays an important role

in the oral frame, since together with the

oral ossicles, are responsible for the opening

movement of the mouth, which allows organ-

isms feeding. Blake (1973) described that the

ontogenetic variation is greater than variation

between conspecific individuals of similar size,

and that there is variation in age and size of the

various ossicles of an arm series, but he did not

discuss this for the oral ossicles. It is necessary

to describe the variation of the odontophore

throughout its growth, especially in species that

have a wide range of sizes such as this one.

Studies on ossicle morphology are common

in other echinoderm groups, such as ophiuroids

(Thuy & Stöhr, 2016; Hendler, 2018; Alitto,

Granadier, Christensen, O’Hara, Domenico &

Borges, 2020). For asteroids, the taxonomic

usefulness of the individual elements and inter-

pretations of evolutionary relationships have

not been completely explored. The goal of this

study is to describe the ontogenetic variation of

the odontophore shape of Luidia superba in the

Gulf of California from specimens deposited

in the Echinoderm National Collection, Insti-

tuto de Ciencias del Mar y Limología, Univer-

sidad Nacional Autónoma de México (ICML,

UNAM) as a first approach to evaluate the

possibility of using it as a taxonomic character

for differentiation at specific level.

MATERIALS AND METHODS

Specimen examination: We examined all

the available specimens of L. superba depos-

ited in the Echinoderm National Collection

ICML (UNAM) and the National Museum

of Natural History, Smithsonian Institution

(USNM), Washington D. C. (735 specimens

in total). Organisms were observed using a

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 89-100, March 2021 (Published Mar. 30, 2021)

stereoscopic microscope Olympus SZX7 and

measured using a digital caliper (TRUPER

Caldi-6MP), the following measurements were

taken: R, r, arm length (L

) and arm width at the

base (B

). They were also photographed using

a multifocal microscope LEICA Z16 APOA

at the Laboratorio Nacional de Microscopía

y Fotografía de la Biodiversidad (Instituto de

Biología, UNAM). After reviewing the exter-

nal characters of the available material to make

the description, 55 of the Echinoderm National

Collection (ICML-UNAM) specimens were

selected to represent the size range that this

species reaches in the Gulf of California; the

selected specimens range from R = 14 mm to

R = 210 mm. We used the anatomical conven-

tions to describe ossicle orientation and nomen-

clature described by Gale (2011) and Fau and

Villier (2018): doda: distal oral/odontophore

articulation on the oral; odom: odontophore-

oral muscle; poda: proximal odontophore-oral

articulation (Fig. 1).

Scanning Electron Microscopy (SEM):

A small cut was made on the actinal face of

the disc to remove one of the five pairs of oral

plates and an odontophore. Arms are desig-

nated by Carpenter’s system, with “A” being

the arm opposite the madreporite and the other

rays being designated “B”, “C”, “D”, and “E”

clockwise when viewed from the oral side

(O’Neill, 1989; Lawrence, 2013). To standard-

ize the odontophore selected per specimen, the

pair of plates found in the interradium between

arms “C” and “D” (the arms between which the

madreporite is found) was taken in each speci-

men. The dissection of the selected specimens

was carried out using the method described

by Fau and Villier (2018): specimens were

prepared in a dilute solution of NaClO (house-

hold bleach) followed by several rinsings with

tap water and alcohol (70%); they were then

dried, mounted and gold-coated on a SEM stub

at the Laboratorio Nacional de Microscopía

y Fotografía de la Biodiversidad (Instituto de

Biología, UNAM) and at the National Museum

of Natural History SEM Laboratory (USNM).

Geometric morphometrics: The SEM

images of the actinal view of the odontophore

were analyzed using geometric morphometrics

with specialized software: TPSUtil, TPSDig,

CoordGen, PCAGen, CVAGen. A TPS file was

built with the images. Subsequently, 14 land-

marks and eight semi-landmarks were digitized

to define the perimeter of the plate, giving a

total of 22 marks; the eight semilandmarks

are the ones defining de odontophore “waist”.

A Procrustes fit was performed and then a

Principal Component Analysis (PCA) in order

to simplify the description of the variation

between ossicles and a Canonical Variables

Analysis (CVA) to explore the morphological

differences between five ontogenetic catego-

ries (Table 1). The categories are made up of

11 specimens each, which were defined based

on the available material of each size between

Fig. 1. Scanning electron microscopy (SEM) image of

the odontophore in actinal view (ICML-UNAM 1647).

In green: insertion of poda (proximal odontophore-

oral articulation); in pink: insertion of the muscle odom

(odontophore-oral muscle); in blue: insertion of doda

(distal oral/odontophore articulation).

TABLE 1

List of categories, size range and number

of specimens per category

Category Size interval (r mm) # Specimens

1 14.07-40.13 11

2 42.93-51.96 11

3 52.61-80.12 11

4 84.03-130.5 11

5 138.7-210.5 11

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14-210 mm, in other words, from the smallest

to the largest size available from the Gulf of

California material. P values were calculated

using a MANOVA permutation test based on

1 000 permutations.

RESULTS

Systematics

Luidia superba A. H. Clark, 1917 (Fig. 2

A-F)

Luidia superba A. H. Clark (1917): 171;

Caso (1943): 37; (1961): 41; (1979): 205;

(1994): 36; Downey & Wellington (1978): 375;

Granja-Fernández et al. (2015): 91; Alvarado et

al. (2009): 3; Alvarado & Solís-Marín (2013):

547; Martín-Cao-Romero et al. (2017): s171.

Luidia (Alternaster) superba: Maluf

(1991): 348; Solís-Marín et al. (2005): 125;

Benítez-Villalobos et al. (2008): 78; Honey-

Escandón et al. (2008): 59.

Diagnosis (Modified from Clark, 1917):

R = 205 mm, r = 30 mm, R/r = 6.8. Five or

six arms relatively stout gradually tapering

to a blunt extremity; superomarginal paxillae

squared, correspond to the inferomarginals;

four rows of lateral paxillae on each side of the

arm; in the third row, every third or fourth pax-

illae is much enlarged and bears a stout conical

central spine; the central third of the arm is

occupied by small, irregular, rounded paxillae,

many of which may bear a spine too; infero-

marginal plates bear three long stout spines,

the lowest being the longest, and on the actinal

surface there are three to five spines much

shorter and decreasing in size toward the ambu-

lacral groove; actinal intermediate plates have

a single prominent median spine; adambulacral

plates bear four spines; oral plates narrow with

11 gradually decreasing spines situated along

the median suture and four similar spines situ-

ated along the furrow margin; no pedicellariae.

Description: Five arms, R = 15.38-415

mm, r = 2.96-49 mm, R/r = 4.02-9.59, aver-

age R/r = 5.94. Small disk, five long flattened

arms that taper slightly to a rounded tip (L

12.01-363 mm; B

= 3.83-48 mm). Paxillae of

the center of the disk rounded with six to nine

central spinelets surrounded by 18 to 20 slender

peripheral ones (Fig. 2A); 15 to 19 paxillae

transversally, in the middle section of the arm

very small and irregular paxillae, mixed with

some enlarged ones that occasionally bear a

central conical spine (Fig. 2C), these enlarged

paxillae are irregularly distributed on the arm;

lateral paxillae squared in shape. Three to

four rows of lateral paxillae on each side of

the arm (Fig. 2E); lateral paxillae square with

rounded edges; superomarginal paxillae similar

in shape, slightly larger, with 30 stout central

spinelets approximately and up to 40 peripheral

spinelets; madreporite small, rounded and hid-

den in the interradius between the first three

rows of lateral paxillae, there may be a couple

of adjacent bigger paxillae that surround it; ter-

minal plate rounded, almost completely abacti-

nal, covered with fine granules; inferomarginal

plates long and narrow, with three long spines

and three to five smaller ones on the actinal

surface of the plate (Fig. 2F); three adambula-

cral spines and there may be a fourth small one

behind the last one (Fig. 2D); eight to ten oral

spines, central ones longer; six to eight suboral

smaller spines which decrease in size toward

the distal section of the plate; no pedicellariae.

Material examined: Holotype USNM-

36948, Albatross st. 2797 Panama, (8°6’29.8”

N & 78°50’59.9” W) 60 m; USNM-36948,

one specimen, Panama (8°6’29.8” N &

78°50’59.9” W) 60 m; USNM-E18920, two

specimens, Galapagos Islands, Ecuador (?)

9-18 m; USNM-E41830, one specimen, Gala-

pagos islands (?) depth?; SONORA: ICML-

UNAM 2582, one specimen, (26°38’00” N &

112°31’00” W) depth?; ICML-UNAM 4419,

two specimens, (30°59’00” N & 114°3’1” W)

95 m; ICML-UNAM 2342, one specimen,

(27°55’00” N & 111°0’00” W) depth?; ICML-

UNAM 4426, two specimens, (30°0’9” N &

112°54’60” W) 103 m; ICML-UNAM 3569, 15

specimens, (26°51’04” N & 110°6’3” W) 48 m;

ICML-UNAM 4239, 33 specimens, (28°20’0”

N & 111°35’0” W) 30 m; ICML-UNAM 4414,

two specimens, (26°58’16” N & 110°3’25” W)

19.5 m; ICML-UNAM 4388, one specimen,

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 89-100, March 2021 (Published Mar. 30, 2021)

(26°51’3” N & 110°6’5” W) 47.7 m; ICML-

UNAM 4238, 320 specimens, (28°20’0” N

& 111°35’0” W) 29.9-31 m; ICML-UNAM

3555, ten specimens, (26°51’4” & 110°6’3”

W) 53 m; ICML-UNAM 4244, six specimens,

(28°16’16” N & 111°36’79” W) 57 m; ICML-

UNAM 4423, 24 specimens, (26°51’4” N &

110°6’3” W) 19.5 m; ICML-UNAM 4197, 23

specimens, (26°51’4” N & 110°6’3” W) 47.7 m;

ICML-UNAM3627, one specimen, (26°51’4”

N & 110°6’3” W) 23 m; ICML-UNAM 4208,

22 specimens, (28°20’0” N & 111°35’0” W)

57 m; ICML-UNAM 4211, 182 specimens,

(28°20’0” N & 111°35’0” W) 58 m; ICML-

UNAM 3621, five specimens, (28°20’0” N &

111°35’0” W) 54 m; ICML-UNAM 1647, eight

Fig. 2. Luidia superba A.H. Clark, 1917. (ICML-UNAM 3569). A-B. Actinal and abactinal view. A. Central paxillae. B.

Detail of oral plates and odontophore (SEM). C. Paxillae central spine. D. Detail of adambulacral plates. E. Detail of lateral

and superomarginal paxillae, marginal spines. F. Detail of inferomarginal spines.

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 89-100, March 2021 (Published Mar. 30, 2021)

specimens, Mazatlán, Mexico (22°40’00” N &

105°55’00” W) depth?; ICML-UNAM 4399,

25 specimens, Gulf of California (29°27’14” N

& 112°29’10” W) 40 m; ICML-UNAM 3002,

one specimen, Colima, Mexico (19°7’00” N &

104°21’00” W) depth?; ICML-UNAM 4410,

14 specimens, Baja California Sur, Gulf of Cal-

ifornia (26°58’82” N & 111°53’60” W) 64.2

m; ICML-UNAM 4425, six specimens, Baja

California Sur, Gulf of California (26°58’82”

N & 111°53’60” W) 64.2 m; ICML-UNAM

4429, eight specimens, Tiburon Island, Gulf of

California (29°27’14” N & 112°29’10” W) 40

m; ICML-UNAM 4406, four specimens, Tibu-

ron Island, Gulf of California (29°27’14” N &

112°29’10” W) 40 m; ICML-UNAM 4422, two

specimens, San Miguel Cape, Baja California,

Mexico (28°8’24” N & 112°46’21” W) 48 m;

ICML-UNAM 7523, one specimen, Rosario,

Oaxaca, Mexico (15°54’1” N & 95°41’30” W)

depth?; ICML-UNAM 4582, six specimens,

Baja California Sur, Mexico (26°59’9.7” N &

111°53’26.9” W) 63.3 m; ICML-UNAM 7779,

one specimen, Gulf of Tehuantepec, Oaxaca,

Mexico (16°18’0” N & 95°10’0” W) depth?;

ICML-UNAM 1646, one specimen, Mazatlán,

Mexico (22°40’0” N & 105°55’0” W) depth?;

ICML-UNAM 4577, one specimen, Del Car-

men Island, Gulf of California (25°58’14” N

& 111°7’23” W) 37 m; ICML-UNAM 4218,

one specimen, Santa María, Sinaloa, Mexico

(25°7’0” N & 108°20’0” W) 22.8 m; ICML-

UNAM 2562, one specimen, Los Angeles Bay,

Baja California N, Mexico ( ? ) depth?.

Geographic and bathymetric distribution:

Mexico: Gulf of California, Sinaloa, Oaxaca,

Gulf of Tehuantepec; Panama; Colombia; Gala-

pagos, Ecuador, and Peru. From 3 to 250 m

(Clark, 1989; Alvarado & Solís-Marín, 2013).

Fig. 3. PCA plot. Variance explained by the two first components.

The number of significant eigenvalues is 1. X

=8.2861, 4.2862.

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Remarks: The holotype has six arms; how-

ever, Downey and Wellington (1978) reported

that this is not normal for the species, since

the ones observed and collected in Galapagos

have five arms. All the examined specimens

in the present study have five arms as well.

Clark (1917) mentioned that the Albatross st.

2797 was in Colombia but according to the

geographic coordinates, it is in Panama.

Geometric morphometrics: PCA results

showed that more than 50% of the vari-

ance (0.007999) is explained by the first two

components (PC 1= 0.4241; PC2 = 0.1918)

(Fig. 3). Differences in shape of the odonto-

phore between size groups were confirmed

with CVA (P < 0.05) and the deformation grid

exhibited the differences along the odonto-

phore keel based on landmark and semi-land-

mark displacement vectors. As shown in Fig. 4,

the shape of the odontophore undergoes the

greatest change in the curvature of the lateral

notch of the plate (keel) due to the elongation

that occurs throughout growth. The result from

the MANOVA test (P = 0.000999) based on 1

000 permutations (Variance error = 0.005774)

and the variance explained by groups was

=0.006009, so that groups explain 51 % of the

total variance. The CVA (Table 2) together with

the Mahalanobis distances showed two distinct

canonical variables (p scores = 6.5859 e-08,

0.0156715) (Table 3), which means there are

three significantly distinct groups (Fig. 5). Of

the five different categories, two, three and four

form a single significant group, which sepa-

rates organisms into three size ranges from R

= 14.02-40.13 mm (Fig. 6A), R = 42.93-130.5

mm (Fig. 6B), and R = 138.7-210 mm (Fig.

6C). The three significantly different groups

were named: S (small specimens), M (medium

specimens), L (large specimens).

DISCUSSION

Using a comparative morphological

approach, we provide evidence of three size

groups in which the odontophore varies sig-

nificantly in this species. This study quantified

Fig. 4. CVA Deformation grid and vectors showing relative strength of differences

in Procrustes-superimposed odontophore shape along CVA axis 1.

TABLE 2

Geometric morphometrics results for the age groups,

MANOVA results: canonical axes (λ), chi square (X

freedom degrees (DF) and p values

MANOVA (CVA)

1 λ = 0.0002 X

= 272.89 DF = 160 P = 6.5859

2 λ = 0.0079 X

= 152.31 DF = 117 P = 0.015671

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 89-100, March 2021 (Published Mar. 30, 2021)

the main morphological differences observed

between small, medium, and large specimens

of Luidia superba. As mentioned by Gale

(2015), the odontophore is one of the defining

characters of the post-Palaeozoic Neoasteroi-

dea. Viguier (1878) discussed the classification

of asteroids and proposed to use the shape of

the oral plates and the odontophore to separate

taxa, mentioning that Astropecten Gray, 1840,

Luidia Forbes, 1839 and Ctenodiscus Müller &

Troschel, 1842 form a natural group. This was

the first and only approach to a classification

based on this character and was only recently

explored by some authors (Gale, 2011; Fau &

Villier, 2018; Fau & Villier, 2019) for certain

groups of asteroids.

Fau and Villier (2018) described the com-

plete ontogenetic development of the skeleton

of Zoroaster fulgens Thompson, 1873 using

SEM imaging and discussed how the ossicles

grow in asteroids though the addition of extra-

cellular calcite deposits. They described that

younger ossicles not only have different shapes

compared with older, homologous ossicles, but

also lack differentiated structures like muscle

insertions. The results obtained in this study

are similar to that observed in theirs, since the

odontophore shows a much simpler general

shape in the S group. Also, while dissecting

specimens, these are the first ones to lose all

the tissue, which could suggest that the latter is

softer, and that the ossicle lack a developed or

TABLE 3

Mahalanobis distance between a priori group means

1 2 3 4 5

0.000000 6.898565 13.114938 13.654911 18.854568

6.898565 0.000000 6.485488 8.021896 12.693379

13.114938 6.485488 0.000000 8.487616 10.550907

13.654911 8.021896 8.487616 0.000000 5.331041

18.854568 12.693379 10.550907 5.331041 0.000000

Fig. 5. CVA plot for 55 specimens of L. superba. Categories 1-5 are separated in colors,

the three distinct groups showed by the analysis are shown in boxes (I, II, III).

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specialized stereom to allow greater adherence.

The gradually specialization of the stereom can

be observed through the ontogenetic series.

Our results allowed us to confirm that, as

size of the specimen increases, different areas

of specialized stereom start to appear (Fig. 5B),

for example in the odontophores keel, where

the odontophore muscle (odom) inserts. In this

case, CVA showed shape is significantly dif-

ferent only between three main groups named

small, medium, and large. Stereom becomes

thinner where muscles are inserted, so the

keel becomes one of the most fragile parts

of the plate. The results of our study contrast

with those observed by Turner and Dearborn

(1972) in Ctenodiscus crispatus Bruzelius,

1805, since, despite the fact that it is also a

member of Paxillosida Perrier, 1884, they

reported only slightly ontogenetic variation in

the odontophore. This only highlights the need

for further studies of this important character.

It must be considered that the odonto-

phore may be indicative of the feeding habits

of a species, so the odom may be stronger in

some species due to their feeding needs and

the size of their preys. This means that the

stereom around the keel could be more or less

thin. Luidiids are characterized by being effi-

cient predators (Lawrence, 2013) and Luidia

superba is a species that shows a large size

range, which, based on the stomach content

of reviewed specimens, suggests that they

are capable of ingesting exceptionally large

prey, such as other echinoderms or mollusks.

Therefore, despite standardizing the size of the

sampled specimens (i.e. specimens in group M)

to make a comparison, the possibility that the

change in shape is due to other non-ontogenetic

Fig. 6. Variation in shape in the three size groups defined from the CVA results. The shape varies on the sides of the keel

and in the elongation of the proximal and distal processes. A. Small specimens, (S). B. Medium specimens (M). C. Large

specimens (L).

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 89-100, March 2021 (Published Mar. 30, 2021)

variables, such as feeding and burrowing habits

or the habitat, is not ruled out.

It has been proven that new identification

characters can be derived from the internal

anatomy (Fau & Villier, 2018), but it is neces-

sary to develop more studies of this type in all

taxa to establish odontophore as a new valid

taxonomic character in any order of asteroids.

Research has tended to focus on external

anatomy rather than internal anatomy; work-

ing with external morphological characters

has resulted in various taxonomic problems

between species, specially in some groups with

highly variable characteristics such as paxil-

losids. Although quantitative studies based

on traditional ossicle morphometry can be

performed (Lawrence et al., 2018), it is com-

plicated to define species based on spination

and ossicles whose shape can be affected by the

environment or suffer changes due to habitat

conditions. Moreover, the search for internal

morphological characters has become neces-

sary and represents some advantages accord-

ing with what has been explored in other

echinoderms, such as ophiuroids (Thuy &

Stöhr, 2016; Hendler, 2018; Alitto, Granadier,

Christensen, O’Hara, Domenico & Borges,

2020) as they have shown to be conserved and

support robust studies, for example, they may

be used for phylogenetic works (Gale, 2011;

Thuy & Stöhr, 2016). Blake (1973) developed

the first and only detailed study on the ossicle

morphology of the genus Luidia. However,

he focused his study mainly on the ossicles

of the arm and discussed the disadvantage of

working with internal anatomy, due to the use

of highly destructive methods. In his study,

he did not include the oral frame ossicles for

this same reason, and it should be noted that

he mentioned that he had rare material that

should be preserved as complete as possible.

In this sense, this is the greatest challenge we

face, since we do not always have the neces-

sary number of specimens to perform that kind

of studies, therefore, there is still a lot to be

done. The lack of more studies on the internal

anatomy of this genus, confirm that the varia-

tion in the shape of the odontophore shown

here is a precedent for the use of ossicles as

additional new taxonomic characters for iden-

tification at specific level. The odontophore

may be used as an additional character but it

is necessary to conduct studies that compare

the structure among other species of Luidia.

Our results on L. superba suggest that more

phylogenetic characters can be derived from

internal anatomy, and more studies are required

for character definition. Regarding the use of

Geometric Morphometrics to analyze the odon-

tophore ontogeny, we suggest to use a greater

number of ossicles and, consequently, more

landmarks and semilandmarks in order to cover

most of the ossicle perimeter and to explore

other views, such as the lateral or the abactinal,

for further studies.

Ethical statement: authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We would like to thank Ma. Esther Diupo-

tex Chong for her technical support at the ENC,

ICML, UNAM. To Susana Guzmán Gómez

for her technical support with the multifocal

photography. To Cirene Gutierrez for the mor-

phometric analysis advice. To CONACYT for

the scholarship (number 929010) and to Dave

Pawson, William Moser, and the Smithsonian

staff for their support. To Berenit Mendoza

Garfias and Pietro Tardelli for the SEM photo-

graphs. Finally, the authors would like to thank

M. G. Lovegrove and A. A. Caballero-Ochoa

for the valuable comments on the manuscript’s

English and scientific content.

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 89-100, March 2021 (Published Mar. 30, 2021)

RESUMEN

Variación ontogenética del odontóforo de

Luidia superba (Asteroidea: Paxillosida)

y sus implicaciones taxonómicas

Introducción: El odontóforo es la estructura posicio-

nada entre las placas orales pareadas con las que se articula

a través de procesos proximales y distales. Las estructuras

de la anatomía interna se pueden usar como caracteres

taxonómicos para la diferenciación más precisa entre espe-

cies, por lo que es necesario describir la variación de las

estructuras a lo largo del crecimiento. Objetivo: Describir

la forma y la variación del odontóforo de Luidia superba A.

H. Clark, 1917 de ejemplares del Golfo de California depo-

sitados en la Colección Nacional de Equinodermos, ICML

UNAM. Métodos: Se revisaron un total de 735 ejemplares

para describir los caracteres externos y de las cuales se

seleccionaron 55 ejemplares, dentro de un intervalo de R

= 14 mm a R = 210 mm, de los cuales se extrajeron los

odontóforos y fueron analizados utilizando morfometría

geométrica. Resultados: Se presentan imágenes de micros-

copía electrónica de barrido (MEB) de los odontóforos que

muestran las variaciones de la forma durante el crecimien-

to. Se confirmaron diferencias significativas de la forma

entre los grupos de tallas mediante un CVA (p< 0.05).

Conclusiones: Se observa especialización del estereoma a

lo largo de la serie ontogenética; la variación en la forma

del odontóforo aquí mostrada es precedente para el uso de

estructuras de la anatomía interna como nuevos caracteres

de identificación.

Palabras clave: Osículos; morfología, zona oral, anatomía

interna; morfometría geométrica; Microscopía Electrónica

de Barrido.

REFERENCES

Alitto, R.A., Granadier, G., Christensen, A.B., O’Hara, T.,

Di Domenico, M., & Borges, M. (2020). Unravelling

the taxonomic identity of Ophiothela Verrill, 1867

(Ophiuroidea) along the Brazilian coast. Journal

of the Marine Biological Association of the United

Kingdom, 100(3), 413-426.

Alvarado, J.J., Solís-Marín F.A., & Ahearn, C.G. (2009).

Echinoderm (Echinodermata) diversity in the Pacific

coast of Central America. Marine Biodiversity, 40(1),

45-56.

Alvarado, J.J., & Solís-Marín, F.A. (2013). Echinoderm

Research and diversity in Latin America. Berlin Hei-

delberg: Springer-Verlag.

Benítez-Villalobos, F., Castillo-Lorenzano, F.E., & Gon-

zález-Espinosa, G.S. (2008). Listado taxonómico

de los equinodermos (Echinodermata: Asteroidea y

Echinoidea) de la costa de Oaxaca en el Pacífico sur

mexicano. Revista de Biología Tropical, 56(3), 75-81.

Benavides-Serrato, M., Borrero-Pérez G.H., & Díaz-Sán-

chez, C.M. (2011). Equinodermos del Caribe colom-

biano I: Crinoidea, Asteroidea y Ophiuoridea. Serie

de Publicaciones Especiales de Invemar, 22, 384.

Blake, D.B. (1973). Ossicle morphology of some recent

asteroids and description of some West American

fossil asteroids. University of California Publications

in Geological Sciences, 104.

Blake, D.B. (1989). Asteroidea: Functional morphology,

classification, and phylogeny. In M. Jangoux & J.M.

Lawrence (Eds.), Echinoderms Studies 3 (pp. 179-

186). Rotterdam: Balkema publishers.

Bruzelius, N. (1805). Dissertatio sistens species cognitas

asteriarum, quamr. sub praesidio A.J. Retzii. exhibet

N. Bruzelius. (pp.1-37). Lundae (formerly know as

Retzius, R.J.).

Caso, M.E. (1943). Contribución al conocimiento de los

astéridos de México (Master’s thesis). Facultad de

Ciencias, Universidad Nacional Autónoma de Méxi-

co, Mexico.

Caso, M.E. (1961). Los Equinodermos de México (Docto-

ral thesis). Facultad de Ciencias, Universidad Nacio-

nal Autónoma de México, Mexico.

Caso, M.E. (1979). Los Equinodermos de la Bahía de

Mazatlán, Sinaloa. Anales del Centro de Ciencias del

Mar y Limnología, Universidad Nacional Autónoma

de México, 6(1), 197-368.

Caso, M.E. (1994). Estudio morfológico, taxonómico,

ecológico y distribución geográfica de los asteroideos

colectados durante las campañas oceanográficas Cor-

tés 1, 2, 3. Anales del Instituto de Ciencias del Mar

y Limnología, Universidad Nacional Autónoma de

México,12, 1-111.

Clark, A.M. (1989). An index of names of recent Asteroi-

dea-Part 1: Paxillosida and Notomyotida. In M. Jan-

goux & J.M. Lawrence (Eds.), Echinoderm studies 3

(pp. 225-347). Rotterdam: Balkema publishers.

Clark, A.M., & Downey, M.E. (1992). Starfishes of the

Atlantic. London, UK: Chapman & Hall.

Clark, A.H. (1917). Two new astroradiate echinoderms

from the Pacific coast of Colombia, and Ecuador.

Proceedings of the Biological Society of Washington,

30,171-174.

Downey, M.E. (1973). Starfishes from the Caribbean and

the Gulf of Mexico. Smithsonian Contributions to

Zoology, 126, 1-158.

Downey, M. E., & Wellington, G.M. (1978). Rediscovery

of the giant sea-star Luidia superba A.H. Clark in

the Galapagos Islands. Bulletin of Marine Science,

28(2), 375-376.

100

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 89-100, March 2021 (Published Mar. 30, 2021)

Fau, M., & Villier, L. (2018). Post-metamorphic ontogeny

of Zoroaster fulgens Thompson, 1873 (Asteroidea:

Forcipulatacea). Journal of Anatomy, 233, 644-665.

Fau, M., & Villier, L. (2019). Comparative anatomy and

phylogeny of the Forcipulatacea (Echinodermata:

Asteroidea): insights from ossicle morphology. Zoo-

logical Journal of the Linnean Society, 20, 1-32.

Forbes, E. (1839). On the Asteriadae of the Irish Sea.

Memoirs of the Wernerian Society, 8, 114-143.

Gale, A. (2011). The phylogeny of post-Palaeozoic Asteroi-

dea (Neoasteroidea, Echinodermata). Special Papers

in Palaeontology, 85, 5-112.

Gale, A. (2015). Evolution of the odontophore and the

origin of the neoasteroids. In S. Zamora & I. Rábano

(Eds.), Progress in echinoderm palaeobiology (pp.

67-69). Madrid: Instituto Geológico y Minero de

España.

Granja-Fernández, R., Solís-Marín, F.A., Benítez-Villalo-

bos, F., Herrero-Pérezrul, M.D., & López-Pérez, A.

(2015). Checklist of echinoderms (Echinodermata)

from the Southern Mexican Pacific: a historical

review. Revista de Biología Tropical, 63(2), 87-114.

Gray, J.E. (1840). A synopsis of the genera and species of

the class Hypostoma (Asterias, Linnaeus). Annals of

the Magazine of Natural History, 6, 275-290.

Hendler, G. (2018). Armed to the teeth: a new paradigm

for the buccal skeleton of brittle stars (Echinoder-

mata: Ophiuroidea). Contributions in Science, 526,

189-311.

Hulings, N.C., & Hemlay D.W. (1963). An investigation of

the feeding habits of two species of sea stars. Bulletin

of Marine Science of the Gulf and Caribbean, 13,

354-359.

Honey-Escandón, M., Solís-Marín, F.A., & Laguarda-

Figueras, A. (2008). Equinodermos (Echinodermata)

del Pacífico Mexicano. Revista de Biología Tropical,

56 (3), 57-73.

Jangoux, M. (1982a). Food and feeding mechanisms:

Asteroidea. In M. Jangoux & J.M. Lawrence (Eds.),

Echinoderm Nutrition (pp. 117– 159). Rotterdam:

Balkema publishers.

Jangoux, M. (1982b). Digestive systems: Asteroidea. In M.

Jangoux & J.M. Lawrence (Eds.), Echinoderm Nutri-

tion (pp. 235 – 248). Rotterdam: Balkema publishers.

Lawrence, J.M. (2013). Luidia. In J.M. Lawrence (Ed.),

Starfish. Biology and ecology of the Asteroidea

(pp. 109-119). Baltimore: Johns Hopkins University

Press.

Lawrence, J.M., Cobb, J.C., Herrera, J.C., Duran-Gonza-

lez, A., & Solís-Marín, F.A. (2018). Morphological

comparison of Astropecten cingulatus and a new

species of Astropecten (Paxillosida, Astropectinidae)

from the Gulf of Mexico. Zootaxa, 4407(1), 86-100.

Maluf, L.Y. (1991). Echinoderm fauna of the Galápagos

Islands. Chapter 16. In M. J. James (Ed.), Galápa-

gos Marine Invertebrates (pp. 345-367). New York:

Springer Sciences.

Martín-Cao-Romero, C., Solís-Marín, F.A., Caballero-

Ochoa, A.A., Hernández-Díaz, Y.Q, López, L., &

Zúñiga-Arellano, B. (2017). New echinoderm rema-

ins in the buried offerings of the Templo Mayor of

Tenochtitlan, Mexico City. Revista de Biología Tro-

pical, 65(1), 168-179.

Müller, J. & Troschel, F.H. (1842). System der Asteriden.1.

Asteriae. 2. Ophiuridae. Vieweg: Braunschweig, 134

pp.

O’Neill, P. (1989). Structure and mechanics of starfish

body wall. Journal of Experimental Biology 147,

53– 89.

Perrier, E. (1884). Mémoire sur les étoiles de mer recuei-

lliés dans la mer des Antilles et le golfe du Mexi-

que: durant les expéditions de dragace faites sous

la direction de M. Alexandre Agassiz. Archives

(Muséum national d’histoire naturelle (France)). 2.

sér., 6,127-276.

Puppin-Gonçalves, C.T., Rocha, M.A.L., Alencar, C.E.,

Moraes, S.A., Araújo, P.V., & Freire, F.A. (2020).

Niche modeling remarks of Luidia senegalensis

(Lamarck, 1816) (Asteroidea, Luidiidae) after 30

years of its first capture in the northeastern Brazilian

coast. Latin american journal of aquatic research,

48(3), 497-505.

Sladen, W.P. (1889). The Asteroidea. Report on the scien-

tific results of voyage of H. M. S. “Challenger”.

Zoology, 30, 1-935.

Solís-Marín F.A., Laguarda-Figueras, A., Durán-González,

A., Ahearn, C.G., & Torres-Vega, J. (2005). Equi-

nodermos (Echinodermata) del Golfo de California,

México. Revista de Biología Tropical, 5(3), 123-137.

Thuy B, Stöhr S. (2016). A new morphological phylogeny

of the Ophiuroidea (Echinodermata) accords with

molecular evidence and renders microfossils accessi-

ble for cladistics. PLoS One, 11 (5), e0156140.

Turner, R.L., & Dearborn, J.H. (1972). Skeletal morpholo-

gy of the mud star, Ctenodiscus crispatus (Echinoder-

mata: Asteroidea). Journal of Morphology, 138(2),

239-262.

Viguier, C. (1878). Classification des Stellerides. Comptes

rendus hebdomadaires des séances de l’Académie des

sciences, 86, 681-683.