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Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 202-218, March 2021 (Published Mar. 30, 2021)

Reproduction of the sea urchin Tripneustes depressus (Camarodonta:

Toxopneustidae) in Bahía de La Paz, Baja California Sur, Mexico

Ailet Vives

Tamara Rubilar

2,3

María Dinorah Herrero-Pérezrul

Bertha Patricia Ceballos-Vázquez

1. Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Av. Instituto Politécnico Nacional s/n,

Playa Palo de Santa Rita, La Paz, Baja California Sur, México; ailetvives@gmail.com, dherrero@ipn.mx,

bceballo@ipn.mx (*Correspondence).

2. Laboratorio de Química de Organismos Marinos, Instituto Patagónico del Mar. Facultad de Ciencias Naturales y

Ciencias de la Salud. Universidad Nacional de la Patagonia San Juan Bosco. Bvld. Brown, Puerto Madryn, Chubut,

Argentina; tamararubilar@gmail.com

3. Laboratorio de Oceanografía Biológica, Centro para el Estudio de Sistemas Marinos. Bvld. Brown, Puerto Madryn,

Argentina; tamararubilar@gmail.com

Received 30-VI-2020. Corrected 25-X-2020. Accepted 06-XI-2020.

ABSTRACT

Introduction: Sea urchin gonads (roe or uni) are considered a culinary delicacy worldwide. However, only

a few species are considered edible and commercialized. The sea urchin Tripneustes depressus has generated

the interest of producers in Baja California Sur, Mexico, due to the quality of its gonads. A biological basis

for designing a management strategy is key to consider its commercial exploitation. Objective: To determine

the reproductive season of T. depressus through description of the gonad stages and reproductive cycle, and

to establish its relationship with environmental factors. Methods: We collected monthly samples (October

2016-September 2017), recording in-situ temperature and photoperiod. We evaluated a sample of 1 055 speci-

mens for demographic characteristics, using total weight (g) and test diameter (cm). We also did a histological

analysis of gonads from 178 individuals. Results: Average test diameter was 9.70 ± 0.03 cm (5-12.50 cm). Based

on the proportion into the gonad of sexual (gametes) and somatic (nutritive phagocytes) cells, we propose five

gonad stages (growing, premature, mature, spawning, and intergametic) for both sexes. There were two times

of the year when gonads were heaviest and closely corresponded to the growing stage, coinciding with the

highest proportions of nutritive phagocytes. Gonad development (growing and premature stages) peaks in the

months with the longest daylight periods, with spawning in the shortest daylight periods. Conclusions: Gonad

wet weight and adjusted gonad weight are good indicators of the reproductive season of T. depressus. The low-

est gonad wet weights were matched the spawning peak in the shortest daylight period (January and March).

Key words: reproductive season; adjusted gonad weights; gonadal stages; urchin roe; Echinoidea.

Vives, A., Rubilar, T., Herrero-Pérezrul, M.D., &

Ceballos-Vázquez, B.P. (2021). Reproduction of

the sea urchin Tripneustes depressus (Camarodonta:

Toxopneustidae) in Bahía de La Paz, Baja California

Sur, Mexico. Revista de Biología Tropical, 69(S1),

202-218. DOI 10.15517/rbt.v69iSuppl.1.46353

Sea urchins are ecologically important

due to their major impact on community struc-

ture and dynamics in shallow subtidal zones

(Harrold & Pearse, 1987; Toro-Farmer, Can-

tera, Londono-Cruz, Orozco, & Neira, 2004).

In addition, their gonads are consumed as

food, making of sea urchins a valuable fishery

resource (Montealegre & Gómez, 2005; Law-

rence, 2007).

Knowledge about the reproductive cycle

of sea urchins is key for understanding their

life history. Sea urchin gonads contain not only

DOI 10.15517/rbt.v69iSuppl.1.46353

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reproductive cells, but also nutritive phago-

cytes, thus serving also as nutrient storage

organs (Walker, 1982; Unuma, 2002; Walker,

Lesser, & Unuma, 2013; Unuma, Murata,

Hasegawa, Sawaguchi, & Takahashi, 2015).

This makes the gametogenic cycle more com-

plex; the cycle begins with fully developed

nutritive phagocytes and changes in the epi-

thelium and germ cells, which differentiate

into male and female gametes that then ripe

until being released along with the decrease of

nutritive phagocytes (Walker, Unuma, & Less-

er, 2007), showing an alternating abundance

of the somatic and reproductive cell types.

Besides, factors such as temperature, photo-

period, hydrodynamics, food availability, and

diet composition influence the reproductive

cycle and development of echinoids (Ridder &

Lawrence, 1982; McBride, Pinnix, Lawrence,

Lawrence, & Mulligan, 1997; Fernandez &

Pergent, 1998; Spirlet, Grosjean, & Jangoux,

2000; Vaitilingon, Rasolofonirina, & Jangoux,

2005; Lawrence, 2007).

Currently, only two sea urchin species

are commercially exploited in Mexico, Meso-

centrotus franciscanus (=Strongylocentrotus

franciscanus) (red sea urchin) and Strongy-

locentrotus purpuratus (Pacific purple sea

urchin), both restricted to Baja California. In

Baja California Sur, Tripneustes depressus

is one of the most common sea urchins and

along with its large size and the fact that its

gonads have been recently rated as of good

quality (Vives, 2018), generating the inter-

est of local fishing cooperatives to market it.

However, it is necessary at least to generate

biological information and made an appropri-

ate population analysis base and a management

strategy before thinking about the commercial

exploitation of T. depressus, in fact it would

be more appropriate to think about developing

its aquaculture. In this sense, the objective of

our study is to generate biological knowledge

of T. depressus determining its reproductive

season through description of the gonad stages

and the reproductive cycle, besides establish

its relationship with environmental factors, and

to provide information on some demographic

characteristics in a natural population from the

southwestern part of Bahía de la Paz.

MATERIALS AND METHODS

Specimen collection: Monthly samplings

were carried out from October 2016 to Sep-

tember 2017 at El Tecolote beach (Fig. 1), in

the southwestern part of Bahía de la Paz, Baja

California Sur State, Mexico (24°20’9” N &

110°13’48” W). Samples were collected at 1-5

m depth, according to the known distribution

of T. depressus in the study area. Temperature

(°C) was measured in situ at the time of collec-

tion with a mercury thermometer; photoperiod

data for the study period were obtained from

Timeanddate (2017).

Sample processing: To evaluate demo-

graphic characteristics based on average test

diameter and total body weight, between 80

and 100 specimens from all size classes (5-12.5

cm in test diameter) found in each monthly

sample were measured with a vernier caliper

and weighed with a digital scale, to the nearest

1 mm or 0.01 g, respectively.

To characterize the reproductive cycle,

15 specimens were randomly selected from

each monthly sample, except in January and

December; their gonads were excised and

weighed (to the nearest 0.0001 g), fixed in

Finefix for 48 hours, and preserved in 70 %

alcohol. Gonads were subsequently processed

using conventional histological techniques and

5 µm-thick sections were cut and stained with

haematoxylin-eosin (Humason, 1979). From

the histological analysis, specimens were first

sexed, since these did not show any apparent

differences either in external morphology or

gonad color to determine sex macroscopically.

Afterward, gonad stages were identified based

on the proportion of sexual cells (gametes)

and somatic phagocytic cells (nutritive phago-

cytes), using the scale proposed by Unuma et

al. (2015) modified for this species. Five stages

were considered: growing, premature, mature,

spawning, and intergametic. Histograms of

the monthly frequency of the different gonad

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stages were plotted to identify the reproductive

cycle of this species.

The test diameter (D) and total body

weight (W) of specimens were used to calcu-

late a condition index (CI) using the following

formula: CI = W*100/D

. The gonad index

(GI) of each specimen was calculated as the

percentage ratio of gonad wet weight to total

body weight (Meidel & Scheibling, 1998);

these values were used to assess the potential

use of the index as an indicator of reproductive

activity in this species (Sánchez-España, Mar-

tínez-Pita, & García, 2004). Additionally, due

to the proven allometric relationship between

gonad wet weight and test diameter in sea

urchins (Ebert, Hernandez, & Russell, 2011),

a temporal pattern of the gonad cycle was

evaluated testing the average gonad wet weight

(AGW) as described below.

Statistical analyses: A temporal pattern of

the gonad cycle was evaluated by using a GLM

two-way ANCOVA, with test diameter as the

covariate and sex and months as factors; with

this, it was possible to determine (eliminating

the effect of the body size), whether regressions

of the average gonad wet weight (AGW) for

each individual test diameter differed between

months and sexes (Packard & Boardman, 1999).

Since our data did not follow a normal distri-

bution (Sokal & Rohlf, 1995), non-parametric

tests were used for the analyses. The Kruskal-

Wallis method was used to test for differences

between sexes and between reproductive stages

in each of the variables examined. The Spear-

man’s rank correlation coefficient was used to

examine the correlation between test diameter

and total body weight, and between gonad wet

weights and the environmental variables. All

the analyses were carried out using the soft-

ware Statistica v.8.0; a significance level α =

0.05 was used for all tests.

RESULTS

Demographic characteristics: The results

from the 1 055 specimens sampled showed that

total body weight ranged from 72 to 912 g,

with a mean (± standard error) of 411.72 ± 4.25

g, median of 422 g, and mode of 445 g; 60 %

of specimens weighed between 318 and 516

Fig. 1. Location of the study area in Bahía de la Paz, Baja California Sur State, Mexico.

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g. There were significant differences between

months (KW: H = 317.24, P < 0.0001) in

total body weight; the lightest specimens were

recorded in October and December and the

heaviest from April to September.

Test diameter ranged between 5 and 12.50

cm, with a mean (± standard error) of 9.79 ±

0.03 cm. Most specimens (52 %) had a test

diameter between 9 and 11 cm. The monthly

frequency distributions of test diameter were

unimodal (Fig. 2); the smallest specimens were

recorded from October to December.

A significant correlation (rs = 0.27,

P < 0.05) between test diameter and total

weight was detected. There were significantly

more females than males (0.7M:1.4F) in the

178specimen sample that was sexed (χ2 = 5.75,

P < 0.05). We found no significant differences

between males and females in test diameter,

total body weight, or CI (P > 0.05), Table 1.

Fig. 2. Monthly frequency distributions of test diameter (cm) of Tripneustes depressus

in Bahía de La Paz, BCS, Mexico (N = 1 055).

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Gonad description: The sea urchin

T. depressus, has five lobe-shaped gonads

attached internally to the test. Each gonad lobe

has an elongated shape pointed towards the

oral end and rounded towards the aboral end;

granular appearance that resembles a bunch of

grapes; color ranging from yellowish to brown-

ish; texture varying from flaccid to turgid.

Gonad female stages:

Growing stage: Higher proportion of nutri-

tive phagocytes than germ cells. The acini

showed previtellogenic oocytes towards the

periphery, while the rest of the acinus was filled

with nutritive phagocytes (Fig. 3A).

Premature stage: Pre-vitellogenic and

vitellogenic oocytes were present at the

Fig. 3. Gonad female stages of T. depressus from Bahía de La Paz, BCS, Mexico: A. Growing stage. B. Premature stage. C.

Mature stage. D. Spawning stage. E. Intergametic stage. NP: nutritive phagocytes. PO: previtellogenic oocytes. RO: residual

oocytes. VO: vitellogenic oocytes. Scale bar = 100 µm.

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periphery of the acinus. Vitellogenic oocytes

started to appear within the acinus. Nutri-

tive phagocytes were still abundant, but some

empty spaces could be found (Fig. 3B).

Mature stage: Higher proportion of germ

cells than nutritive phagocytes. Vitellogenic

oocytes filled the center of the acinus, whereas

previtellogenic oocytes, when present, were

found in small amounts at the periphery. Nutri-

tive phagocytes were restricted to the periphery

of acini (Fig. 3C).

Spawning stage: Nutritive phagocytes

make a smaller proportion and with no nutri-

tional content. Partially empty acini may show

residual vitellogenic oocytes (Fig. 3D).

Intergametic stage: This stage represents

the recovery period before the next gametogen-

ic development. Acini are almost empty, show-

ing nutritive phagocytes and residual oocytes

undergoing resorption (Fig. 3E).

Gonad male stages:

Growing stage: Nutritive phagocytes

occurred in higher proportion than germ cells.

Spermatocytes and spermatogonia restricted to

the periphery of the acinus. Nutritive phago-

cytes filled the rest of the acinus (Fig. 4A).

Premature stage: Active spermatogenesis

was observed at the periphery of the acinus;

spermatozoa started accumulating at the center

of the acinus. Nutritive phagocytes remain

abundant, but some empty spaces appear

(Fig. 4B).

Mature stage: Spermatogenic cells were

evident in higher proportion than nutritive

phagocytes. Spermatozoa almost fill the acinus.

Spermatogenic development centers can be

found at the periphery of the acinus. Nutritive

phagocytes occurred in low proportion, restrict-

ed to the periphery of the acinus (Fig. 4C).

Spawning: Nutritive phagocytes occurred

in a small proportion and empty of nutri-

tional content. Partially empty acini contained

different quantities of spermatozoa in the

lumen (Fig. 4D).

Intergametic stage: This stage represents

the recovery period, prior to the onset of

gametogenic development. The acini mainly

contain nutritive phagocytes. Residual sper-

matozoa inside the acinus are undergoing

resorption (Fig. 4E).

Reproductive cycle: Fig. 5A shows the

frequency distribution of the gonad develop-

ment stages of both sexes combined over the

study period. The growing and intergametic

stages occurred for most of the year and cor-

responded to stages of reproductive inactivity

and recovery. Gamete development and growth

in this species seem to take place in two sea-

sons. The main season starts between April

and August and peaks in June; the second and

shorter season takes place from September to

December, peaking in October. Spawning takes

place between January and March, with a small

secondary event in August. The gonads enter

an intergametic stage after spawning and prior

to starting a new cycle; this stage was most

frequently seen from January to April.

Gonad weight and Gonad index: Both,

gonad wet weight (GWW) and adjusted gonad

weight (AGW) presented similar results

(Table 1). Both values were significantly higher

in males than females (KW: H = 11.779, P =

0.0006; GLM: F = 39.97, P < 0.0001). Monthly

variations of GWW and AGW followed a simi-

lar trend in both, males and females and also

displayed a similar seasonal variation (Fig. 5C,

5D) with significant different values among

months (KW: H = 122.22, P < 0.0001; GLM: F

= 47.73, P < 0.0001). In the same sense, males

showed gonad index values significantly higher

than females (KW: H = 14.274, P = 0.0002).

The highest GI values were recorded in Octo-

ber and December 2016, with high values also

recorded between May and September 2017;

the lowest values occurred from January to

March 2017 (Fig. 5B). The heaviest gonads

(both GWW and AGW) were found in two

periods, October-December 2016 and May-

September 2017, and the lightest, from Janu-

ary to March 2017 (Fig. 5C, 5D). However,

monthly variations followed a similar trend in

the two sexes.

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Environmental variables: Temperature

ranged from 17 ºC (January) to 30 ºC (October)

over the study period (Fig. 6A). The number

of daylight hours ranged between 10 and 13 h

per day, with the lowest values recorded from

November to January and the largest from May

to August (Fig. 6B). Gonad index values were

significantly correlated with temperature (rs =

0.68, P < 0.05) but not with photoperiod (rs =

0.17, P > 0.05). In contrast, gonad wet weight

Fig. 4. Gonad male stages of T. depressus from Bahía de La Paz, BCS, Mexico: A. Growing stage. B. Premature stage.

C. Mature stage. D. Spawning stage. E. Intergametic stage. NP: nutritive phagocytes. RS: residual spermatozoa. SC:

spermatocyte. SZ: spermatozoa. Scale bar = 100 µm.

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was significantly correlated with photoperiod

(rs = 0.41, P > 0.05) but not with temperature

(rs = 0.76, P < 0.05).

Gonad wet weight and GI were the

only morphometric variables that showed

statistically significant (P < 0.05) differences

between some gonad stages; in particular,

values between the growing stage and the

premature, spawning, and intergametic stages

(Table 2).

Fig. 5. A. Reproductive cycle of Tripneustes depressus as shown by the monthly frequency of gonad stages. B. Gonad index.

C. Gonad wet weight. D. Adjusted gonad weight. Vertical bars are the standard errors.

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Fig. 6. Variation of environmental variables over the study period at Bahía de La Paz, BCS. A. In-situ temperature. B.

Daylight hours per day; vertical bars denote the monthly range of daylight hours, the dashed line marks the 12 h daylight

photoperiod that would be expected at the equator.

TABLE 1

Statistics (mean ± standard error, range in parentheses) of the morphometric variables recorded, per sex and for

the total sample for Tripneustes depressus in Bahía de la Paz, Mexico

Variable

Total

N = 1055

Females

N = 73

Males

N = 105

Kruskal-Wallis

H P

Total weight (g) 411.72 ± 4.25 (72-912) 425.04 ± 17.73 404.04 ± 14.56 2.20 0.138

Test diameter (cm) 9.79 ± 0.03 (5.0-12.3) 9.96 ± 0.10 9.82 ± 0.09 2.36 0.1245

Condition index (%) 44.38 ± 0.52 (8.79-150.88) 41.52 ± 1.24 41.33 ± 1.04 1.19 0.2745

Gonad wet weight (g) 28.65 ± 2.33 38.51 ± 1.85 11.78 0.0006*

Gonad index (%) 7.45 ± 0.61 10.66 ± 0.66 14.27 0.0002*

GLM

F P

Adjusted gonad weight (g) 27.53 ± 4.31 34.70 ± 3.96 39.97 0.0001*

*Variables with significant differences between females and males.

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DISCUSSION

The specimens examined in our study

were adult, mostly intermediate-sized (9-11 cm

in diameter) individuals. Large specimens were

highly abundant in our sample, while small

individuals (< 5 cm) were absent. The absence

of juveniles may be due to various causes,

including predation, variability in the avail-

ability of food and refuge (Ebert, 1967; Sala &

Zabala, 1996), a different distribution than that

of adults (Fernandez, Caltagirone, & Johnson,

2001; Tomas, Romero, & Turon, 2004), or the

behavior of its growth rate (Sonnenholzner,

Touron, & Panchana-Orrala, 2018).

Mortality by predation in the early juve-

nile stages is considered the main bottleneck

in echinoid populations (Tegner & Dayton,

1981; McClanahan & Muthiga, 1989; Sala,

1997; López et al., 1998). In this sense, the

availability of refuge for juvenile sea urchins

is a key factor in the rate of predation (Roberts

& Ormond, 1987; Hixon & Beets, 1993), since

hiding and protection in crevices becomes

in the main strategy to avoid this predation.

In species like Echinometra mathaei, smaller

individuals are more susceptible to predation

than adults (Hart & Chia, 1990). Himmel-

man (1988), suggests that the juveniles of

Strongylocentrotus droebachiensis wait for ref-

uges until reaching a certain size, after which

they begin to move actively looking for food.

Botsford, Smith, and Quinn (1994) indicate

that the mortality rate increases when refuges

from predators are limited. In species such as

S. franciscanus and Echinometra vanbrunti,

when they reach a certain size, they are forced

to abandon their refuges, being more vulner-

able to predation (Tegner & Dayton, 1981;

González-Peláez, 2004). In this regard, also

has been reported that species such as S.

purpuratus and T. depressus show cannibal-

istic behaviors of medium-sized individuals

on small individuals in conditions of starving

or low food availability, which could directly

affect the presence of juveniles (Sonnenhol-

zner, Montaño-Moctezuma, & Searcy-Bernal,

2011; Sonnenholzner et al., 2018). However, in

our study area there is a great food availability.

The food availability of juvenile E. vanbrunti

TABLE 2

Means (± standard error) of the morphometric variables recorded, per sex and gonad stage.

Values with different letters are significantly different (P < 0.05)

Variable

Gonad stages Kruskal-Wallis

Growing Premature Mature Spawning Intergametic H P

Total weight, g

Female 399.14 ± 32.2 344.94 ± 81.5 551.70 ± 95.0 452.16 ± 39.9 450.57 ± 21.0 3.85 0.4269

Male 404.81 ± 24.0 365.63 ± 32.8 428.0* 439.43 ± 24.8 438.95 ± 18.2 4.41 0.2208

Test diameter, cm

Female 9.88 ± 0.2 9.56 ± 0.4 10.80 ± 0.7 9.90 ± 0.3 10.08 ± 0.1 3.38 0.4957

Male 9.98 ± 0.1 9.41 ± 0.2 10.3* 9.96 ± 0.3 9.95 ± 0.1 4.91 0.1776

Condition Index, %

Female 39.70 ± 2.6 35.62 ± 5.1 42.90 ± 0.3 45.83 ± 1.2 43.51 ± 1.3 1.74 0.7840

Male 39.80 ± 1.8 40.98 ± 2.4 39.2* 44.69 ± 2.0 44.05 ± 0.5 0.71 0.8712

Gonad wet weight, g

Female 38.51 ± 3.3c 29.53 ± 8.1bc 51.12 ± 14.5c 11.69 ± 4.4ab 20.74 ± 3.2a 24.28 0.0001

Male 46.22 ± 2.3b 29.60 ± 3.6a 15.0* 22.93 ± 3.8a 39.39 ± 4.2ab 20.15 0.0002

Gonad index (%)

Female 10.52 ± 0.8c 10.12 ± 2.8bc 9.00 ± 1.8bc 2.60 ± 0.8a 4.83 ± 0.7ab 33.14 0.0001

Male 13.25 ± 1.1b 9.22 ± 1.3a 3.5* 5.45 ± 1.1a 8.95 ± 0.9a 20.83 0.0001

* This stage was not included in the analyses because only one mature male was found.

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in Panama can be another limiting factor, so

that spawning in populations occurs at the time

of upwelling (Lessios, 1981).

Juveniles and adults can also present dif-

ferent distribution. For P. lividus migrations

of small or medium-sized sea urchins have

been described (Haya de la Sierra, 1990; Fer-

nandez et al., 2001; Tomas et al., 2004), while

the adults are more sedentary and capable of

spending several months in confined spaces

(Dance, 1987). However, there are reports that

juvenile settlements in other species occur

where adults live (Cameron & Schroeter, 1980;

Tegner & Dayton, 1981).

Tropical species such as T. depressus,

large-size, short time to maturity, fast growth

rates, high reproductive effort, high respiration

rates, high feeding capacity and short life span

(Lawrence & Agatsuma, 2013), present a low

and highly variable survival rate of juveniles,

which may be an adaptation of their life strat-

egy (Stearns, 1976). In this sense, it has been

reported that the proliferation densities of T.

depressus in Ecuador can decrease rapidly or

disappear completely at monthly intervals, con-

trary to slow-growing temperate species (Son-

nenholzner et al., 2018), to which it contributes

in largely the absence of juveniles.

For all these reasons, the low recruitment

rate played a determining role in the distribu-

tion of the size structure found in T. depressus

in this study.

The average test diameter in the study

population was 9.79 ± 0.03 cm. This value is

similar to that reported for this same species

(9.74 ± 0.02 cm) at Punta Arenas de la Ventana,

Mexico (González-Peláez, 2001). In contrast,

larger average test diameters were reported in

two regions of the Galapagos Islands: 11.50

± 0.08 cm (Luna, 2000) and the largest of

12.50 cm reported by Sonnenholzner, Moreira,

and Panchana-Orrala (2019). The monthly fre-

quency of test diameter in T. depressus showed

a unimodal distribution, indicating that indi-

viduals could be of the same age, suggesting

that this species reproduces massively. In this

sense, Sonnenholzner et al. (2019) suggested

that T. depressus presents an initial natural

differentiation in the body size of small and

large individuals of the same cohort.

The average body wet weight of T. depres-

sus was 411.72 ± 4.25 g, higher than the figure

reported (347.6 ± 4.31 g) by González-Peláez

(2001) for the same species. Individual body

wet weight was highly variable and showed

no discernible pattern. This may be due to

various factors, including food availability,

coelomic fluid, and gonadal weight, therefore

these values have to be considered under this

information. In this study, the total body weight

was used for computing both the CI and the GI;

in addition, gonad wet weight was also used

for calculating the GI. Therefore, as discussed

below, the GI values are implicitly biased

given the dual nature of the gonad, and due to

the allometric relationship between the gonad

wet weight and the test diameter (Ebert et al.,

2011). Thus, we found that neither IC nor GI

are good indicators for the reproductive season

in T. depressus. GWW and AGW were both

better indicators of the reproductive status of

the population, since no significant differences

were found in the test length between months

or sex studied (note that this could be different

if the variation in the body size of the sample

studied is more extensive).

Sea urchin gonads, unlike those of other

organisms, also play a role as reserve organs

regardless of sex. Nutritive phagocytes, present

inside the gonad, store the nutrients necessary

for initiating gametogenesis and supply them to

germ cells (Walker, 1982; Walker et al., 2013;

Unuma 2002; Unuma et al., 2015). Gonad wet

weight is commonly used as an indicator of

reproductive status. However, due to their dual

role as nutrient reserve organs in sea urchins,

gonads may show high weight values even in

the intergametic stage due to the accumulation

of nutrients in storage cells (Kenner & Lares,

1991; Kelly, 2000; Unuma & Walker, 2009).

In T. depressus, GWW and AGW were signifi-

cantly higher in males in our study. This pattern

has also been reported for Abatus cavernosus

from the Argentinian Patagonia (Gil, Zaixso,

& Tolosano, 2009). However, the opposite

pattern (i.e., heavier gonads in females) has

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been reported for many other species such

as S. droebachiensis (Meidel & Scheibling,

1999), Holopneustes purpurascens (William-

son & Steinberg, 2002), and Arbacia dufresnii

(Epherra et al., 2015).

The lightest gonads in male and female

T. depressus were found between January and

March (winter), and the heaviest from April to

September (spring-summer), although some

high values were also observed from October

to December. This trend was consistent with the

pattern shown by gonad stages. In this sense,

when gonads were heaviest, the frequency of

individuals in growing stage was high. Grow-

ing stage presented the highest proportion of

nutritive phagocytes. Additionally, in females

there was high gonad wet weight during grow-

ing and mature stages (no significant different

weights); this could not be appreciated in males

because only one mature male was found. In

this last female gonad stage, instead of nutritive

phagocytes, the highest proportion of gametes

provided the most weight. Therefore, gonad

wet weight illustrates the dual nature of this

organ in sea urchins. Once the reproductive

cycle was understood, the GWW and AGW

are useful to determine the reproductive season

(spawning period) in sea urchins due to its

timely development; i.e. spawning period is

characterized by lower GWW an AGW, result-

ing from weight loss associated with gamete

release, together with a low proportion of nutri-

tive phagocytes.

We observed that spawning peaked from

January to March (winter), with a smaller peak

in August. This finding differs from previous

studies on this same species. González-Peláez

(2001) reported a single spawning period from

May to August in Punta Arena, Bahía de La

Ventana, BCS, Mexico. For this same locality,

Álvarez-López (2017) reported that spawn-

ing occurred most of the year, except for

December, although he described two major

spawning seasons, one in October-November

and the other from April to June. Meanwhile,

the T. depressus population from the Gala-

pagos Islands (Ecuador) shows two or three

spawning periods per year. This is consistent

with the fact that sea urchin species inhabit-

ing in temperate zones exhibit a well-defined

reproductive cycle, whereas tropical species

show no apparent periodicity in spawning

(Luna, 2000). Sonnenholzner et al. (2018)

suggest that T. depressus has continuous, non-

discrete and synchronous gametogenic activity

throughout the year, with two peaks of gonadal

development for reproduction. This continuous

reproduction pattern with peaks in winter and

summer has been reported for other species of

the genus such as T. ventricosus off the coast

of Florida (McPherson, 1965) and T. gratilla in

Madagascar, Kenya and the Philippines (Muth-

iga, 2005; Toha et al., 2017).

Populations of the same species often

show differences in their spawning periods,

and significant interannual differences may

also occur within the same population (Pearse

& Cameron, 1991; Byrne, Andrew, Worthing-

ton, & Brett, 1998). The lack of a well-defined

spawning season seems to be common when

food is highly available and environmental

conditions are favorable (Kennedy & Pearse,

1975; Pearse, Pearse, & Davis, 1986; Bay-

Schmith & Pearse, 1987; Pearse & Cameron,

1991; Guillou & Michel, 1993). The partial

release of gametes (different spawning periods)

would ensure that at least part of the offspring

would coincide with favorable environmental

conditions (Calvo, Morriconi, & Orler, 1998).

Because of this characteristic, T. depressus

has been considered as an opportunistic spe-

cies that uses available resources to reproduce

(Lawrence & Agatsuma, 2013).

Gametic development is regulated by

endogenous factors such as the nutritional state

of the individual, which influences gonadal pro-

duction (Meidel & Scheibling, 1998; Walker &

Lesser, 1998; Garrido & Barber, 2001), as well

as by various environmental factors including

photoperiod, light intensity, and temperature

(Pearse et al., 1986; Bay-Schmith & Pearse,

1987; McClintock & Watts, 1990; Kelly, 2001;

Mercier & Hamel, 2009). Our results show

that gonad wet weight in T. depressus was

not correlated with temperature. Temperature

functions as a trigger of reproductive events

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in many sea urchin species (James, Heath, &

Unwin, 2007). Many authors have reported that

high temperatures could boost gonad develop-

ment and maturation, and low temperatures,

the onset of gametogenesis (Espinoza, Reyes,

Himmelman, & Lodeiros, 2008; González-

Irusta, 2009). Lara-Rueda (2004) found a posi-

tive correlation between temperature and the

gonad cycle in E. vanbrunti. However, there

is also evidence showing that gonad growth

in P. lividus and S. droebachiensis is related to

decreasing temperatures (Herrero-Barrencua,

2008; James & Siikavuopio, 2012). Moreover,

in species such as S. purpuratus no direct cor-

relation was found between gonad cycle and

temperature (Cochran & Engelmann, 1975),

similar to our findings for T. depressus in this

study. Nevertheless, Gil (2015) concluded that,

although temperature is not the key driving fac-

tor for the onset of gametogenesis or spawning

in Pseudechinus magellanicus, it is essential

for oocytes to reach their maximum develop-

ment during the winter maturation.

Finally, the T. depressus gonad wet weight

was significantly correlated with photoperiod,

another factor known to influence the repro-

ductive cycle. We found that gonad develop-

ment (growing and premature stages) occurs

in the months with the longest daylight peri-

ods, whereas spawning takes place during the

season with the shortest daylight periods. Sea

urchins can detect light intensity through their

podia, which have innervated terminal discs

containing photosensitive pigments (Lesser,

Carleton, Böttger, Barry, & Walker, 2011).

Longer daylight periods have been found to

be associated with the onset of gametogenesis

in P. magellanicus and Evechinus chloroticus

(Brewin, Lamare, Keogh, & Mladenov, 2000;

Gil, 2015). However, experimental studies on

other species of sea urchins have shown that

gametogenesis is restrained in long days and

favored in short days (Pearse & Cameron,

1991). Direct lighting and changes in day length

are correlated with sea temperature in tropical

shallow-waters, and both factors can affect

sexual reproduction in marine invertebrates

(Coma, Ribes, Gili, & Zabala, 2000; Shpigel,

McBride, Marciano, & Lupatsch, 2004; Far-

hadian, Yusoff, & Arshad, 2014). This topic has

yet to be investigated in T. depressus.

Gonad wet weight and adjusted gonad

weight were found to be good indicators of the

reproductive season of T. depressus. The lowest

gonad wet weights were recorded in correspon-

dence with the shortest daylight and the spawn-

ing peak (January and March).

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 acknowledgments

section. A signed document has been filed in

the journal archives.

ACKNOWLEDGMENTS

This research was funded by Instituto

Politécnico Nacional (SIP projets 20170262,

20195021, 20200693). Ailet Vives received a

scholarship from Consejo Nacional de Ciencia

y Tecnología; the results here presented are part

of her thesis. Thanks to Sánchez-Salazar for the

English translation.

RESUMEN

Reproducción del erizo de mar Tripneustes depressus

(Camarodonta: Toxopneustidae) en Bahía de La Paz,

Baja California Sur, México

Introducción: Las gónadas de erizo de mar (huevas

o uni) se consideran un manjar culinario en todo el mundo.

Sin embargo, solo unas pocas especies se consideran

comestibles y se comercializan. El erizo de mar Tripneustes

depressus ha generado el interés de productores de Baja

California Sur, México, por la calidad de sus gónadas.

Una base biológica es clave para diseñar una estrategia de

manejo para T. depressus para considerar su explotación

comercial. Objetivo: Determinar la época reproductiva

de T. depressus a través de la descripción de los estadios

de las gónadas y del ciclo reproductivo, y establecer su

relación con factores ambientales. Métodos: Recolecta-

mos muestras mensuales (octubre de 2016 a septiembre de

2017), registrando in-situ la temperatura y el fotoperiodo.

Evaluamos una muestra de 1055 especímenes para las

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características demográficas, utilizando el peso total (g)

y el diámetro de testa (cm). También hicimos el análisis

histológico de las gónadas de 178 individuos. Resultados:

El diámetro de la testa promedio fue de 9.70 ± 0.03 cm

(5-12.50 cm). Con base en la proporción en la gónada de

células sexuales (gametos) y somáticas (fagocitos nutriti-

vos), proponemos cinco estadios gonádicos (crecimiento,

prematuro, maduro, desove e intergamético) para ambos

sexos. Hubo dos épocas del año en que las gónadas eran

más pesadas y se correspondían estrechamente con la etapa

de crecimiento, coincidiendo con las proporciones más

altas de fagocitos nutritivos. El desarrollo de las gónadas

(etapas de crecimiento y prematuro) alcanza su punto

máximo en los meses con los periodos de luz más largos,

con desove en los periodos de luz más cortos. Conclusio-

nes: El peso húmedo de las gónadas y el peso ajustado de

las gónadas son buenos indicadores de la temporada repro-

ductiva de T. depressus. Los pesos húmedos más bajos de

las gónadas coincidieron con el pico de desove en el perío-

do con luz diurna más corto (enero y marzo).

Palabras clave: temporada reproductiva; pesos de gónadas

ajustados; estadios gonadales; hueva de erizo; Echinoidea.

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