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Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 438-451, March 2021 (Published Mar. 10, 2021)

Redescription of the sea urchin Eucidaris thouarsii (Cidaroida: Cidaridae)

based on material from the Mexican Pacific

Mariana P. Ruiz-Nava

Carlos A. Conejeros-Vargas

Francisco A. Solís-Marín

1. Licenciatura en Biología, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México, Av.

De Los Barrios 1, Hab. Los Reyes Ixtacala, Barrio de los Árboles, Tlalnepantla, Estado de México, México;

mpaola.ruiznava@gmail.com (*Correspondence).

2. Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Av. Ciudad Universitaria,

Coyoacán, Ciudad de México, México; conejeros@ciencias.unam.mx

3. Colección Nacional de Equinodermos “Dra. Ma. Elena Caso Muñoz”, Laboratorio de Sistemática y Ecología de

Equinodermos, Instituto de Ciencias del Mar y Limnología, UNAM, Av. Ciudad Universitaria, Coyoacán, Ciudad de

México, México; fasolis@cmarl.unam.mx

Received 15-VII-2020. Corrected 21-X-2020. Accepted 06-XI-2020.

ABSTRACT

Introduction: Eucidaris thouarsii is a cidaroid sea urchin found from the Gulf of California to Ecuador. Its

taxonomy is based on general descriptions of test shape, primary and secondary spines, the Aristotle’s lantern,

apical system, and peristome. Objective: To redescribe E. thouarsii with detailed descriptions, adding new

taxonomic characters. Methods: We examined and reidentified 792 specimens, measuring and analyzing in

detail structures of taxonomic value. Results: The horizontal diameter of the test ranges from 2.8 to 48.45

mm; the peristome corresponds to 40-60 % of that diameter, proportionally bigger than the apical system; the

interambulacral areas are four times larger than the ambulacral areas. The variation of the pedicellariae is shown

with scanning electron microscopy. The specimens of the Mexican oceanic islands are markedly different when

compared to those of the mainland. Conclusions: Eucidaris thouarsii has five well differentiated second-

ary spines, and also specific regionalization; the apical system varies according to the size of the Horizontal

Diameter of the Test; the globiferous pedicellariae have intraspecific differences; and the tridentate pedicellariae

are specifically regionalized.

Key words: cidaroids; secondary spines; pedicellariae; morphology; taxonomy.

Ruiz-Nava, M.P., Conejeros-Vargas, C.A., & Solís-

Marín, A.A. (2021). Redescription of the sea urchin

Eucidaris thouarsii (Cidaroida: Cidaridae) based

on material from the Mexican Pacific. Revista de

Biología Tropical, 69(S1), 438-451. DOI 10.15517/

rbt.v69iSuppl.1.46383

Historically, the genus Eucidaris has been

recognized since Pomel’s description in 1883,

when he also proposed the division of the genus

Cidaris Leske, 1778 due to the great number of

species that it contained and the great varia-

tion in their morphological characters. The

taxonomic character that he used to sepa-

rate Eucidaris from the rest of its congeners

was the presence of uncrenulated tubercles,

in addition to the characteristics of the genus

Cidaris (Leske, 1778). Latterly, Mortensen

(1928) described the genus thus: organisms

with short primary spines, of the same size as

the horizontal diameter of the test (HDT); the

primary spines sometimes are robust and thick,

and the areolas are small and not sunken. The

DOI 10.15517/rbt.v69iSuppl.1.46383

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Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 438-451, March 2021 (Published Mar. 10, 2021)

area occupied by the peristome is generally

larger than the area corresponding to the apical

system. It has large globiferous pedicellariae,

without a terminal tooth in the valves, small

globiferous pedicellariae without a terminal

tooth, and tridentate pedicellariae. However,

the constancy of forms in all genera makes the

distinction between them and their species very

difficult (Agassiz & Desor, 1846), and the sum

of small differences between the characters is

needed for the identification of species.

Originally, only three species were includ-

ed in the description of the genus Eucidar-

is; however, it possesses five living species:

Eucidaris australiae Mortensen, 1950; E.

galapagensis Döderlein, 1887; E. metularia

(Lamarck, 1816); E. tribuloides (Lamarck,

1816) and E. thouarsii (Valenciennes in Agas-

siz & Desor, 1846). According to Mortensen

(1928), the genus dates back to the Miocene.

Eucidaris is a pantropical genus: that is, its

species are distributed in shallow waters (< 570

m), between the tropics and with an adjacent

but not superimposed distribution (Lessios,

Kessing, Robertosn, & Paulay, 1996). The

problems in identifying characters to diagnose

the species within Eucidaris have given rise

to confusion about the validity of E. galapa-

gensis as a species, rather than as a variation

of E. thouarsii, since the differences between

them are discreet; nevertheless, molecular stud-

ies have shown that both species are valid (Les-

sios, Kessing, Robertosn, & Paulay, 1999).

Eucidaris thouarsii was described by

Valenciennes (L. Agassiz & Desor, 1846) as

follows: “…sea urchin with narrow ambula-

cral areas, made up of four lines of granules,

whose two internal parts are barely developed.

Tubercle base broad. Intermediate granules

between the rows, narrow, quite apparent,

not very tight. Sub-cylindrical spines, swol-

len, very granular...”. As the description was

made in 1846 and the genus Eucidaris was

described in 1883, the original name of the

species was Cidaris thouarsii; this is probably

the reason for the historical taxonomic confu-

sions within the genus Eucidaris. For example,

Döderlein (1887) considered Eucidaris as a

subgenus, and H.L. Clark (1907) described

specimens using its original name (Cidaris

thouarsii), without considering the existence of

the genus Eucidaris.

The most exhaustive work on the descrip-

tion of the species is from Mortensen (1928),

who was very meticulous in describing the

arrangement of the interambulacral plates, the

shape of the pedicellariae and the prima-

ry spines ornamentation. Just over twenty-

five years later, Caso (1953) synonymized

Hesperocidaris asteriscus H.L. Clark, 1948

with Eucidaris thouarsii, considering that the

descriptions of both taxa were morphologically

interconnected; however, in her doctoral thesis

in 1961 she considered both species as valid.

Due to the different changes in the identi-

fication of diagnostic characters that Eucidar-

is thouarsii has undergone from its original

description to the most recent studies, the aim

of this paper is to redescribe this species, add-

ing and distinguishing the main characters

that facilitate the specific determination of

specimens of E. thouarsii, and to provide an

extended diagnosis for the species, including

the variation of some characters on different

sizes of them.

MATERIALS AND METHODS

A total of 792 specimens were analyzed

using an OLYMPUS® SZX7 stereoscopic

microscope. We followed the descriptions by

Mortensen (1928) and Caso (1976) to prop-

erly identify the specimens; additionally, we

reviewed the photographs of the material type

available in the database of the Natural History

Museum of Paris. The characters in table 1

were used to perform the specimen examina-

tion. Finally, 16 specimens were chosen (that

were in good condition without apparent regen-

eration or fractures) and in which the details

of the structures could be better observed

and were photographed in the Laboratorio de

Microscopia y Fotografia de la Biodiversidad

of the Instituto de Biologia (IB-UNAM), with

a Leica DFC490 multifocal microscope. The

areas photographed were the peristome, the

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apical system, the ambulacral and inter-ambu-

latory areas, as well as the ornamentation of the

primary spines and the different morphotypes

of the secondary spines.

To identify the pedicellariae, specimens of

different sizes were selected and preparations

were made for Scanning Electron Microscopy

(SEM) by extracting these structures from dif-

ferent areas (ambitus, peristome, apical system

and below the lamellae). After a dehydration

train with gradual alcohol changes (70 %, 80 %

and absolute), the samples were covered with

ionized gold in the Laboratorio de Biodivers-

idad Animal II of the IB-UNAM, and the nec-

essary photographs were taken to illustrate the

most important characteristics and variations of

the pedicellariae who were not described previ-

ously in other works.

For the morphometric analyses the follow-

ing morphometric measurements were taken

from each organism: height and width of the

test, the length of the longest primary spine at

the ambitus, the diameter of the peristome and

the diameter of the apical system. All measure-

ments were taken in millimeters with a TRU-

PER digital Vernier caliper. The measurements

were taken in triplicate in each specimen to

obtain an average of the individual sizes, and

recorded in Microsoft Excel spreadsheet. We

performed a linear regressions analysis using

SigmaPlot14 in order to corroborate the cor-

relation between the primary spine (at the level

of the ambitus) and the horizontal diameter of

the test, between the height of the test and the

horizontal diameter of the test, and between the

diameter of the peristome and the diameter of

the apical system.

RESULTS

According to the bibliographic revision

and the International Code of Zoological

Nomenclature in the Chapter 11, Article 50,

the taxonomic authority of Eucidaris thouarsii

corresponds to Valenciennes, 1846, published

in the work from L. Agassis & Dessor “Cata-

logue raisonné des familles, des genres, et

des espèces de la classe des échinodermes.”.

Knowing this, the correct way to cite this spe-

cies is Eucidaris thouarsii (Valenciennes in L.

Agassis and Dessor, 1846).

Systematics:

Order Cidaroida Claus, 1880

Superfamily Cidaroidea Gray, 1825

Family Cidaridae Gray, 1825

Subfamily Cidarinae Gray, 1825

Genus Eucidaris Pomel, 1883

Eucidaris thouarsii

(Valenciennes in L. Aggasiz & Desor, 1846)

Eucidaris thouarsii (Valenciennes, 1846 in

L. Agassiz & Desor, 1846)

TABLE 1

Characters and abbreviations used to examine and redescribe Eucidaris thouarsii. Asterisk (*)

indicates the characters that are described in detail herein

Character Abbreviation Character Abbreviation

Test height TH Maximum length of the primary spine MLPS

Horizontal diameter of the test HDT Secondary spines* SP*

Peristome diameter PD Primary tubercles PT

Apical system diameter ASD Secondary tubercles ST

Coronal plates CP Interambulacral plates IP

Genital plates GP Ambulacral plates AP

Ocular plates OP Ambulacral pores Apo

Periproct plates* PP* Tube feet ossicles* TFO*

Genital pores GPo Globiferous* pedicellariae GPe*

Madreporite M Tridentate* pedicellariae TP*

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Cidaris thouarsii Valenciennes in L. Agas-

siz & Desor, 1846: 326; A. Agassiz, 1863:

301; Agassiz, 1872-1874: 98-99, 213, 385-386;

Lockington, 1875-1876: 152; H.L. Clark, 1902:

526; H.L. Clark, 1907: 185-186.

Cidaris (Eucidaris) thouarsii Döderlein,

1887: 18-20.

Eucidaris thouarsii H.L. Clark, 1913: 220;

H.L. Clark, 1923: 157; H.L. Clark, 1940: 347;

H.L. Clark, 1948: 226, 229-230; Mortensen,

1921: 22-24; Mortensen, 1928: 393-398;

Boone, 1926: 8; Boone, 1933: 80-81; Ziesen-

henne, 1937: 231; A.H. Clark, 1939: 12; A.H.

Clark, 1946: 2; Caso, 1961: 222-226; Caso,

1962: 29; Birkeland, Mayer, Stames, & Buford,

1975: 68; Maluf, 1988: 142; Conejeros-Vargas,

2015: 153-156.

Type material: Syntypes: National Museum

of Natural History (Paris) MNHN-IE-2014-397,

Galapagos Island; MNHN-IE-2013-10447,

MNHN-IE-2013-10448, MNHN-

IE-2013-10449, MNHN-IE-2013-10450.

Type locality: California Noboux and

Galapagos (H.L. Clark, 1948; Caso, 1978).

Distribution: Along the Mexican Pacific

coast, the mainland islands and the Revilla-

gigedo Archipelago.

Material examined*: Baja California

Norte ICML-UNAM 4.3.82; ICML-UNAM

4.3.83; ICML-UNAM 4.3.84. Baja Califor-

nia Sur ICML-UNAM 4.3.1; ICML-UNAM

4.3.2; ICML-UNAM 4.3.14; ICML-UNAM

4.3.15; ICML-UNAM 4.3.16; ICML-UNAM

4.3.17; ICML-UNAM 4.3.18; ICML-UNAM

4.3.19; ICML-UNAM 4.3.21; ICML-UNAM

4.3.22; ICML-UNAM 4.3.26; ICML-UNAM

4.3.31; ICML-UNAM 4.3.77; ICML-UNAM

4.3.79; ICML-UNAM 4.3.80; ICML-UNAM

4.3.81; ICML-UNAM 4.3.95; ICML-UNAM

4.3.96; ICML-UNAM 4.3.100; ICML-

UNAM 4.3.101; ICML-UNAM 4.3.102;

ICML- UNAM 4.3.103; ICML-UNAM 4.1.6;

ICML-UNAM 4.1.9; ICML-UNAM 4.1.22;

ICML-UNAM 4.1.25; ICML-UNAM 4.1.26;

ICML-UNAM 4.1.27; ICML-UNAM 4.1.61;

ICML-UNAM 4.1.62; ICML-UNAM 10932

ICML-UNAM 10941; ICML-UNAM 10945;

ICML-UNAM 10950; ICML-UNAM 10961;

ICML-UNAM 10964; ICML-UNAM 10967;

ICML-UNAM 10970; ICML-UNAM 10974.

Clarion Island ICML-UNAM 4.1.10. Clip-

perton Island ICML-UNAM 4.1.0. Colima

ICML-UNAM 4.3.78; ICML-UNAM 4.3.88;

ICML-UNAM 4.3.93; ICML-UNAM 4.3.94.

Galapagos Islands ICML-UNAM 4.1.1. Guer-

rero ICML-UNAM 4.3.3; ICML-UNAM

4.3.4; ICML-UNAM 4.3.5; ICML-UNAM

4.3.6; ICML-UNAM 4.3.7; ICML-UNAM

4.3.12; ICML-UNAM 4.3.13; ICML-UNAM

4.3.20; ICML-UNAM 4.3.23; ICML-UNAM

4.3.24; ICML-UNAM 4.3.27; ICML-UNAM

4.3.86; ICML-UNAM 4.3.86; ICML-UNAM

4.3.104; ICML-UNAM 4.1.41; ICML-UNAM

4.1.7; ICML-UNAM 4.1.28; ICML-UNAM

4.1.16; ICML-UNAM 4.1.17; ICML-UNAM

4.1.18; ICML-UNAM 10667. Jalisco ICML-

UNAM 4.3.0; ICML UNAM 4.3.8. Michoacán

ICML-UNAM 4.3.67; ICML-UNAM 4.3.87;

ICML-UNAM 4.3.89; ICML-UNAM 4.3.90;

ICML-UNAM 4.3.9; ICML-UNAM 4.3.92;

ICML-UNAM 4.3.105; ICML-UNAM 4.3.106;

ICML-UNAM 4.3.107; ICML-UNAM 4.3.108;

ICML-UNAM 4.3.109; ICML-UNAM 4.3.110;

ICML-UNAM 4.1.13; ICML-UNAM 4.1.23;

ICML-UNAM 4.1.24; ICML-UNAM 4.1.29;

ICML-UNAM 4.1.36; ICML-UNAM 4.1.37;

ICML-UNAM 4.1.38; ICML-UNAM 4.1.39;

ICML-UNAM 4.1.40; ICML-UNAM 4.1.50;

ICML-UNAM 4.1.51; ICML-UNAM 4.1.52;

ICML-UNAM 4.1.53; ICML-UNAM 10593;

ICML-UNAM 4.1.30; ICML-UNAM 4.1.31;

ICML-UNAM 4.1.32; ICML-UNAM 4.1.33;

ICML-UNAM 4.1.34; ICML-UNAM 4.1.35;

ICML-UNAM 4.1.46; ICML-UNAM 4.1.47;

ICML-UNAM 4.1.48; ICML-UNAM 4.1.49;

ICML-UNAM 9943; ICML-UNAM 9967;

ICML-UNAM 10063; ICML-UNAM 10087;

ICML-UNAM 10105; ICML-UNAM 10122;

ICML-UNAM 10136; ICML-UNAM 10157.

Nayarit ICML-UNAM 4.3.97; ICML-UNAM

4.3.98. ICML-UNAM 4.1.19; ICML-UNAM

4.1.20; ICML-UNAM 4.1.21; ICML-UNAM

10031. Oaxaca ICML-UNAM 4.3.85; ICML-

UNAM 4.3.99. Revillagigedo Archipelago

ICML-UNAM 4.3.9; ICML-UNAM 4.3.10;

ICML-UNAM 4.1.2; ICML-UNAM 4.1.3;

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ICML-UNAM 4.1.4; ICML-UNAM 4.1.5;

ICML-UNAM 4.1.8; ICML-UNAM 4.1.11;

ICML-UNAM 4.1.12; ICML-UNAM 4.1.15;

ICML-UNAM 4.1.54; ICML-UNAM 4.1.55

ICML-UNAM 4.1.56; ICML-UNAM 4.1.57;

ICML-UNAM 4.1.58; ICML-UNAM 4.1.59;

ICML-UNAM 4.1.60; ICML-UNAM 18369;

ICML-UNAM 18370; ICML-UNAM 18371.

Sinaloa ICML-UNAM 4.3.29; ICML-UNAM

4.3.30; ICML-UNAM 4.3.32; ICML-UNAM

4.3.33; ICML-UNAM 4.3.34; ICML-UNAM

4.3.35; ICML-UNAM 4.3.36; ICML-UNAM

4.3.37; ICML-UNAM 4.3.38; ICML-UNAM

4.3.39; ICML-UNAM 4.3.40; ICML-UNAM

4.3.41; ICML-UNAM 4.3.42; ICML-UNAM

4.3.43; ICML-UNAM 4.3.44; ICML-UNAM

4.3.45; ICML-UNAM 4.3.46; ICML-UNAM

4.3.47; ICML-UNAM 4.3.48; ICML-UNAM

4.3.49; ICML-UNAM 4.3.50; ICML-UNAM

4.3.51; ICML-UNAM 4.3.52; ICML-UNAM

4.3.53; ICML-UNAM 4.3.54; ICML-UNAM

4.3.55; ICML-UNAM 4.3.56; ICML-UNAM

4.3.57; ICML-UNAM 4.3.58; ICML-UNAM

4.3.59; ICML-UNAM 4.3.60; ICML-UNAM

4.3.61; ICML-UNAM 4.3.62; ICML-UNAM

4.3.63; ICML-UNAM 4.3.64; ICML-UNAM

4.3.65; ICML-UNAM 4.3.66; ICML-UNAM

4.3.68; ICML-UNAM 4.3.69; ICML-UNAM

4.3.70; ICML-UNAM 4.3.71; ICML-UNAM

4.3.72; ICML-UNAM 4.3.73; ICML-UNAM

4.3.74; ICML-UNAM 4.3.75; ICML-UNAM

4.3.76; ICML-UNAM 4.3.11; ICML-UNAM

4.1.45. Sonora ICML-UNAM 4.3.25; ICML-

UNAM 4.3.28; ICML-UNAM 4.1.42; ICML-

UNAM 4.1.43; ICML-UNAM 4.1.44.

*Note: the material is sorted by location.

Diagnosis (modified from Mortensen,

1928): Robust, relatively short primary spines

with blunt or truncated distal ends, rough orna-

mentation. Secondary spines of five different

type well defined and regionalized. Two types

of pedicellariae: large abundant globiferous,

small globiferous with long peduncle and ter-

minal teeth, and tridentate pedicellariae. Plates

of apical system covered with tubercles. Inter-

ambulacral tubercles arranged in regular series,

adradially to them each plate has a secondary

tubercle. Ambulacral pores of approximately

same size.

Redescription: The test is wider than tall,

with the oral and aboral poles depressed;

their sizes range from 2.8 to 48.45 mm in the

Horizontal Diameter of the Test (HDT); the

peristome membrane extends beyond the level

of the test, with this feature visible even in the

specimens of smaller sizes (2.88 mm) (Fig. 1A,

1B, 1C, 1D, 1E,1F ). The ambulacral areas are

composed of two parallel rows of ambulacral

plates, each consisting of a pair of ambula-

cral pores, a secondary tubercle, and milliary

tubercles. The interambulacral areas are four

times larger than the ambulacral areas, made

up of two rows of four to nine coronal plates,

each one with one areole and a hemispheri-

cal mamelon with a perforation in the center;

around the areole there are a series of ST and

milliary tubercles continuing in the direction of

the interradial zone (Fig. 1G1H, 1I, 1J).

The peristome ranges from 40 to 66 % of

the HDT (proportionally bigger compared to

the apical system diameter) and is covered by a

membrane with irregular plates in the interam-

bulacral areas, ornamented by a series of two

or three tubercles where secondary spines are

inserted, and globiferous pedicellariae; the two

rows of AP overlap as they approach the oral

opening (Fig. 2A, 2B, 2C, 2E, 2F). The apical

system is composed of several small periproc-

tal plates around the anal pore and ten large

peripheral plates covered by milliary tubercles,

five corresponding to the genital plates (one

of them corresponds to the madreporite) and

five to the ocular plates; the arrangement of

the genital plates results in a star shape (Fig.

2G). The ocular plates are triangular, elongated

with a perforation in the center of the base,

almost on the groove; they connect at their

base with the ambulacral area and on the sides

with the genital plate (GP). The genital plates

are trapezoid, longer than wide with the varia-

tion in this character shown in the different

sizes of this species: in the smallest organisms

(sizes 2.8 to 14 mm) (Fig. 2H, 2I) the plates

are slightly triangular; as test size increases, it

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Fig. 1. Size variations of Eucidaris thouarsii. A, D. Apical view. B, E. Oral view. C, F. Lateral view. G-H. Lateral view

from naked tests, showing the arrangement of the ambulacral and the interambulacral areas. A-C, G ICML-UNAM 4.3.80;

D-F ICML-UNAM 4.3.105; H ICML- UNAM 4.3.19; I ICML-UNAM 4.3.33; J ICML-UNAM 4.3.28.

can be seen that the plates lose the upper angle,

resulting in truncated GP in large specimens

(> 30 mm) (Fig. 2J, 2K, 2L), acquiring the

trapezoid shape. The genital perforation, nor-

mally in the center of the plate, can sometimes

be very close to the distal edge; in the genital

perforations a series of SP is found covering

the genital pores. The madreporite, the largest

genital plate, is distinguished by being covered

with small perforations; in some cases, it is

bulky and occasionally moves the arrangement

of the apical system. The grooves between ocu-

lar plates and genital plates are very evident in

small specimens (from 2.88 to 13 mm), but in

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the larger ones (< 13 mm) the grooves are thin,

difficult to distinguish with the naked eye, and

covered by a dense layer of secondary spines.

The periproctal plates near the base of the geni-

tal plates are pentagonal and those next to the

anus are quadrangular.

The primary spines at the level of the

ambitus are semi-cylindrical, narrow at their

base, the same size or slightly shorter than

the HDT; they are composed of four parts: the

necklace, the milliary ring, the shaft and the

crown. The milliary ring is less than 1 mm

tall and composed of a series of longitudinal

ridges; the axis of the spine is ornamented by

irregular semi-spherical tubercles that run in

rows towards the distal part - as they approach

the terminal part of the spine the tubercles are

elongated, forming ridges that result in a ter-

minal crown, the number of ridges not being

directly related to the size of the specimen.

The terminal crown is only visible in the most

conserved spines and agglomerations of gran-

ules or ridges can be seen in the center of the

crown in the direction of the base of the spine.

The secondary spines (SP) can be divided into

five morphs as follows, specifically located on

the test:

[1] Lamellae; are the largest secondary

spines (5 mm), characterized by being semi-

rectangular, with rounded tips; shortly before

the terminal part there is a slight crescent-

shaped depression, resulting in a spatula shape

(Fig. 3A). This type is found around the areo-

las, in the secondary tubercles, thus forming a

protective barrier for the insertion area of the

primary spines. Next to the lamellae, towards

the interradial suture is the second morph,

[2] smaller (between 2 and 3 mm in length),

robust and wider towards the distal part (Fig.

3B). Interspersed with this is the third morph,

[3] semi-rhomboid, and two sizes (from 1 to

1.5 mm), the smallest bordering the interradial

suture (Fig. 3C). These spines are also arranged

on the surface of all the plates of the apical

system on milliary tubercles, the largest in two

specific areas: on the genital plates around the

pores and covering them; and bordering all the

plates. The former is more evident at the edge

of the entire apical system. The fourth morph

[4] is located one per ambulacral plate in the

terminal part thereof; they are thin, almost as

tall as the second morph (2 to 2.5 mm), rectan-

gular in shape and located in two parallel rows

(Fig. 3D). In the membrane of the peristome

there are elongated, irregular plates where the

fifth morph [5] is inserted: they are elongated

and thin with a wide and spatulate tip, and

completely cover the surface of the plates of

the peristome membrane; their height ranges

from 2 to 2.5 mm (Fig. 3E).

There are globiferous and tridentate pedi-

cellariae. The globiferous pedicellariae are of

two different morphs, their sizes ranging from

1 to 3 mm and it is possible to distinguish them

by the size of the stem and the valves. The first

type has a thin stem, with the insertion of the

neck into the stem being found in the center of

the axis, or displaced (Fig. 4B, 4C). In general,

the valves are wide at their base and narrow

towards the distal region (triangular shape);

from dorsal view, three parts can be observed,

the intermediate one being smooth until it

reaches the distal end, where the terminal tooth

can be seen, while the parts that correspond to

the left and right edges of the tooth are perfo-

rated (Fig. 4C). From ventral view, the articular

zone is located in the proximal part, where a

semicircular base that can be reduced or as

wide as the width of the articular zone can be

observed; in this part there are also two to three

lateral edges. The valve is divided in half by the

apophysis, which rises above the edge of the

valve, and can run to the middle or three quar-

ters of the inner face; on the rest of the surface

small perforations continue towards the edges.

In the distal part, a triangle is formed that at its

base has two teeth higher and sharper than the

rest, one for vertex A and B; in C the terminal

tooth is in the form of a hook with a blunt or

claw-like tip, although within the variations,

the tooth can be separated from this triangular

formation. The periphery of the valve is ser-

rated; in the proximal part the teeth are short

and as the distal area approaches, they are

more evident (Fig 4E, 4F). There are two other

variations within this first type of pedicellariae.

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Fig 2. Arrangement of the peristome and the apical system. A. Diagram of the ambulacral plates on the peristome membrane

in yellow and the overlapping ambulacral plates in red. B-F. Shows the changes present on different sizes. G. Diagram of

the apical system. Abbreviations. M. Madreporite, GP. Genital plate, OP. Ocular plate, PP. Periproctal plate. GPo. Genital

pore. H-I. From specimens of sizes 2.8 to 14 mm (HDT). J-L. From specimens larger than 30 mm (HDT). B. ICML-UNAM

4.3.101; C. ICML-UNAM 4.3.27; D. ICML-UNAM 4.1.36; E. ICML-UNAM 4.1.51; F-L. ICML-UNAM 4.1.41; G. ICML-

UNAM 4.3.19; H.ICML-UNAM 4.1.46; I. ICML-UNAM 4.1.50; J.ICML-UNAM 4.3.89; K. ICML-UNAM 4.3.108.

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Firstly, sharper peripheral teeth from the middle

of the valve to the distal area; in the terminal

part it is not possible to distinguish a consistent

triangle, nor is there a terminal tooth; the shape

of the valve is more elongated, and the articular

zone is continuous to the striae of the insertion

zone (Fig. 4G). Secondly, the periphery of the

valve towards the terminal part is interrupted,

forming a slight fan that returns to its original

line (Fig. 4H). The second form of globiger-

ous pedicellariae corresponds to those with the

thickest stem with robust valves covered by a

brown pigmented epithelium; in the external

view only complete perforations of half of the

valve to the distal area can be observed on the

lateral parts, while in the rest of the body of

the valve there are very small perforations and

some superficial ones; before the terminal part,

the valve becomes slender. In the internal view

of the valve, the same structures differentiated

in size can be found, and the insertion zone is

continuous along the width of the base. In the

lateral view, the process is higher towards the

middle part of the valve, the teeth are small

and sharp at the periphery, while those that are

arranged on the terminal area are larger (Fig.

4I, 4J, 4K). Regarding its regionalization, this

type of pedicellariae is distributed at the apical

system, peristome, ambulacral areas and in the

interradial suture; the pedicellariae covered by

epithelium are located towards the membrane

of the peristome and at the edges of the apical

system. The valves of the tridentate pedicel-

lariae are approximately 1 mm long, with a

long and thin stem; the neck is located in the

center of the stem, and the valves become

thinner towards the distal part. In the external

view, the valves are smooth where the lateral

perforations are barely visible; in the internal

view, the insertion base is semicircular, with

continuous irregularly shaped grooves stacked,

forming a cusp that covers the first fifth part

of the valve (Fig 5L). At the base of the valve

two protrusions can be seen on each side; on

the periphery of the structure very small and

irregular teeth can be found. Its distribution

over the organism is limited, between the

muscle fibers of the primary spines and the

lamellae that cover them.

The ambulacral tube feet are also of two

types and are regionalized on the surface of the

test: in the section corresponding to the ambi-

tus-peristome they are of robust body and with

a suction disc in the terminal part; in the ambi-

tus-apical system area, the tube feet are of a

finger-like type, without suction disc. There are

Fig. 3. Secondary spines. A. lamellae, located around the areolae. B. smaller than the lamellae, in the interradial suture.

C. semi rhomboid shape, bordering the interradial suture. D. the thinner spines, in the ambulacral plates. E. located in the

peristome. A-E. ICML-UNAM 4.3.5.

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Fig. 4. Pedicellariae present in Eucidaris thouarsii. A. Diagram with the parts that compose the valves of a globiferous

pedicellaria. B-C. Globiferous pedicellariae stems. D-K. Globiferous pedicellariae. L. Valve of tridentate pedicellariae.

M-N. Tubefeet osscicles.

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two variations of tube feet ossicles (TFO). The

first variation corresponds to those with suction

disc and big spiny rods, which are sometimes

interconnected in the distal part (Fig. 4M). The

second variation corresponds to the finger-like

ambulacral feet which has the same shape but

not the interconnected rods (Fig. 4N).

In the correlation between the test height

and the HDT (Fig. 5A), the Revillagigedo

Archipelago specimens are separate from

specimens from the mainland. The correlation

between the largest primary spines and the

HDT (Fig. 5B) shows that the primary spines

are larger, or of the same size as the HDT. The

correlation between the diameter of the api-

cal system and the diameter of the peristome

(Fig. 5C) shows that the apical system is

smaller than the peristome, suggesting that they

grow proportionally.

DISCUSSION

A total of 20 morphological characters

were analyzed, 15 of which had been previ-

ously reported (Döderlein, 1887; Mortensen,

1928) and five of which (periproct plates, sec-

ondary spines, tube feet ossicles, globiferous

pedicellariae and tridentate pedicellariae) are

new proposals to diagnose Eucidaris thouar-

sii morphologically. In addition, it has been

demonstrated that, while mainland specimens

show variations in the apical system accord-

ing to the HDT, oceanic island specimens

show variations in the other characters that

were exmained in this study as well. Many of

the previous taxonomical descriptions (Agas-

siz & Desor, 1846; Döderlein, 1887; Clark,

1907; Mortensen, 1928) were made using a

single or few specimens (2-5), where a slightly

Fig. 5. Morphometric analyses of the relationship between

characters. A. HDT-Height of the test. B. HDT- Maximum

length of the primary spine. C. Peristome diameter-Apical

system diameter.

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different character was often pointed out as the

basis for new species or variety description,

without considering the intraspecific varia-

tion. The species of the genus Eucidaris are

distinguished by having cylindrical primary

spines that are the same size or shorter than the

horizontal diameter of the test, as well as hav-

ing globiferous pedicellariae. In this redescrip-

tion of E. thouarsii, we present a better and

more explicit diagnosis, because although in

the description of E. tribuloides (sister species

from the Gulf of Mexico) it is mentioned that

the interporiferous areas are narrow and the

color of the species is distinct, it is important to

point out that the addition of specific measure-

ments in the descriptions allows us to be much

clearer when identifying species.

Mortensen (1928) mentioned that the

shape of the primary spines lacks taxonomi-

cal validity when distinguishing cidaroid taxa;

nonetheless, H.L Clark (1913) and Caso (1978)

utilized the number of coronal crests to distin-

guish Eucidaris thouarsii from Hesperocidaris

asteriscus. We agree with Mortensen (1928)

in rejecting this character because it is not

constant in all the primary spines at the ambit

level of one organism; these differences may be

due to regeneration or probably associated with

ontogenetic growth or size of the specimens

(Ebert, 1988).

Although Mortensen (1928) mentioned the

presence of different morphotypes of second-

ary spines; in this paper we describe five differ-

ent types of secondary spines and their specific

regionalization, which are present in all sizes

of the specimens analyzed. This suggests that

such characters do not have variations related

with the species itself, nor to the ontogeny of it.

Among the works that describe E. thouar-

sii, the work of Döderlein (1887) stands out,

where he states that within the characters to

clearly identify E. thouarsii is the height and

horizontal diameter of the test (possible cor-

relation between both measures to reaffirm

its hemispherical shape); this was verified

through linear regression (Fig. 5A), resulting

in a positive correlation (R

= 0.937) between

HDT and the height of the test. In this study a

clear separation of the specimens belonging to

the oceanic islands (Clipperton and Revilla-

gigedo archipelago) can be differentiated when

comparing them with the mainland organisms

(Fig. 5A, data inside the ellipse), indicating

that the specimens belonging to the oceanic

islands are bigger and more spherical compared

to the continental specimens, that are smaller

and more flattened. The morphological varia-

tions identified in the oceanic island organ-

isms could represent a new species; something

similar happened with the E. thouarsii speci-

mens from the Ecuadorian coast and from the

Galapagos Islands that were later identified as

Eucidaris galapagensis.

Döderlein (1887) provided valuable infor-

mation regarding the apical system of the

species, proposing the shape of the apical

system plates as a diagnostic character and

emphasizing the triangular shape of the genital

and ocular plates. In this paper we identified

this character only in the specimens ranging

from 4.88 to 10 mm in horizontal diameter. As

the diameter of the test increases, the genital

plates change with it, being trapezoidal, or even

quadrangular (Fig. 3) when the specimens are

larger (> 40 mm); Döderlein’s idea works only

for small specimens (< 20 mm).

Coppard, Kroh and Smith (2012) sug-

gested that tridentated pedicellariae are associ-

ated with cleaning functions in the organism.

E. thouarsii possess tridentate pedicellariae

only below the lamellae and above the muscle

fibers of the primary spines. Coppard et al.

(2012) suggest that the particular location of

this pedicellariae is due to the fact that it is the

space where the muscle and collagen fibers

that give mobility to the primary spines are

located; pedicellariae keep this area free of any

external agent that could impede the mobility

of such structures.

Further investigations regarding the mor-

phological variation of E. thouarsii from oce-

anic islands need to be done in order to test if

its molecular composition and ecology differs

from those of mainland specimens. It is neces-

sary to study the morphological variation of

pedicellariae within the family Cidaridae, in

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order to corroborate its validity as a diagnostic

character to distinguish between genera.

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 Alicia Durán

(ICML, UNAM) for her technical support.

To Susana Guzmán Gómez (IB, UNAM) for

her technical support with the multifocal pho-

tography. To Berenit Garfias (IB, UNAM) for

her technical support with the Scanning Elec-

tron Microscopy. CACV (scholarship holder

666781) thanks the National Council for Sci-

ence and Technology (CONACyT) for the doc-

toral scholarship 722925. Finally, the authors

would like to thank Matthew Lovegrove,

Andrea Caballero-Ochoa and Luis E. Flores

for the valuable comments when reviewing the

English version of this manuscript.

RESUMEN

Redescripción del erizo de mar Eucidaris thyarsii

(Cidaroida: Cidaridae) basado en material

del Pacífico mexicano

Introducción: Eucidaris thouarsii es una especie

de erizo de mar, cidárido presente desde el Golfo de

California hasta Ecuador. Su taxonomía está basada en

descripciones generales de la forma de la testa, espinas

primarias y secundarias, la linterna de Aristóteles, el siste-

ma apical y peristoma. Objetivo: Redescribir E. thouarsii

con descripciones detalladas, añadiendo nuevos caracteres

taxonómicos. Método: Examinamos y reidentificamos 792

ejemplares, midiendo y analizando a detalle estructuras

de valor taxonómico. Resultados: El diámetro horizontal

de la testa va de 2.8 a 48 mm; el peristoma corresponde

entre el 40-60% del diámetro horizontal de la testa, pro-

porcionalmente más grande que el sistema apical; el área

interambulacral es cuatro veces más grande que el área

ambulacral. La variación en los pedicelarios se muestra

con microscopía electrónica de barrido. Los ejemplares de

las islas oceánicas mexicanas son claramente diferentes,

comparados con los de la costa. Conclusiones: Eucida-

ris thouarsii tiene cinco tipos bien definidos de espinas

secundarias que se encuentran regionalizadas en la testa, el

sistema apical varía de acuerdo con el diámetro horizontal

de la testa, los pedicelarios globíferos tienen diferencias

intraespecíficas y los pedicelarios tridentados estas especí-

ficamente regionalizados.

Palabras clave: cidáridos; morfología; pedicelarios;

morfología, taxonomía.

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