Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58602, marzo 2024 (Publicado Mar. 01, 2024)

Variation of the diet of the sea urchin

(Diadema mexicanum (Diadematoida: Diadematidae))

according to its size in the Eastern Tropical Pacific

Andrea Bogantes-Retana1; https://orcid.org/0009-0008-4302-4578

José Barquero-Jackson1; https://orcid.org/0009-0002-6690-614X

Mario Vargas-Guerrero1; https://orcid.org/0000-0001-9649-1075

Juan José Alvarado1,2,3 *; https://orcid.org/0000-0002-2620-9115

1. Escuela de Biología, Universidad de Costa Rica; andrea.bogantesretana@ucr.ac.cr, jose.barquerojackson@ucr.ac.cr,

mario.vargasguerrero19@ucr.ac.cr, juan.alvarado@ucr.ac.cr (*Correspondence).

2. Centro de Investigación en Ciencias del Mar y Limnología, Universidad de Costa Rica, 2060-11501 San José,

Costa Rica.

3. Centro de Investigación en Biodiversidad y Ecología Tropical (CIBET), Universidad de Costa Rica, 2060-11501 San

José, Costa Rica.

Received 23-I-2023. Corrected 14-IX-2023. Accepted 27-IX-2023.

ABSTRACT

Introduction: The sea urchin Diadema mexicanum, due to its bioerosion activity, is considered of ecological

importance. This phenomenon could negatively or positively affect coral reef ecosystems. The bioerosion process

varies according to the abundance and size of the sea urchin.

Objective: Juvenile organisms possess different metabolic needs compared to adults, so knowing their stomach

content according to size allows us to quantify the selection of substrate bioeroded.

Methods: To determine this, D. mexicanum individuals were collected in 12 sites from January 2009 to September

2010 along the Eastern Tropical Pacific coast. The stomach content was categorized in Carbonated Fraction (CF),

Non-Carbonated Fraction (NCF), and Organic Matter (OM). Stomach content was analyzed according to a)

juvenile (< 2.5 cm) or adult (> 2.5 cm) stage and b) locality.

Results: Juveniles presented the following stomach content average percentages: 20.7 % OM, 12 % NCF and

67.9 % CF; and adults: 11.4 % OM, 14.8 % NCF and 73.8 % CF. Based on a Wilcoxon test and a Kendall linear

regression, the following results were obtained. The carbonated fraction in the stomach increased by 0.47 units

on average for every cm of growth (p < 0.05). OM consumed by D. mexicanum increases only 0.05 units for

every cm of growth (p < 0.05). We found a difference of stomach content depending on the site (p < 0.05) and

life stage (p < 0.05). Localities like Huatulco and Coco presented significant differences that could be related to

local oceanographic conditions.

Conclusions: We relate these changes of the stomach fractions to the necessity of the juvenile sea urchins for

nutrients to maintain their growth. The amount of OM is crucial for the development of early stages, meaning

that there is a difference in substrate selection associated with growth.

Key words: organic matter; coral reefs; stomach content; carbonates; growth; bioerosion.

https://doi.org/10.15517/rev.biol.trop..v72iS1.58602

SUPPLEMENT

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58602, marzo 2024 (Publicado Mar. 01, 2024)

INTRODUCTION

Sea urchins of the genus Diadema can

conquer different habitats like coral reefs and

rocky grounds, due to their generalist diet

(Benítez-Villalobos et al., 2015). Even though,

sea urchin Diadema mexicanum (A. Agassiz,

1863) are mainly herbivores and feed mostly

on algae, it is also common to see them feeding

on living and dead corals (Cabanillas-Terán

et al., 2016; Glynn & Morales, 1997; Tribollet

& Golubic, 2011). Added to this, this species

plays an important role in the Eastern Tropical

Pacific (ETP) due to its bioeroding action on

coral reefs (Alvarado et al., 2016a), which has

intensified in El Niño events (Eakin, 2001).

When feeding, D. mexicanum scrapes the

surface where the food is located, sometimes

causing bioerosion to the substrate (Benítez-

Villalobos et al., 2008; Hutchings, 2011).

Grazing made by sea urchins can be advanta-

geous in some specific cases, as it happens

for algae, whose development and abundance

gets restricted, helping corals to easily obtain

light and space (Herrera-Escalante et al., 2005;

McClanahan et al., 1996). Similarly, they also

have an impact on rocky reefs, because they

control organisms that grow over them, howev-

er high densities of this sea urchins could lead

to a negative impact, due to the high abrasion

they cause, changing the reef structure (Alves et

al., 2003; Eakin, 2001).

Feeding of this sea urchin is related to

many dynamic processes of the ecosystem and

its composition. Gut content found inside the

sea urchin can be divided in three categories:

organic matter (OM), non-carbonated frac-

tion (NCF) and carbonated fraction (CaCO3).

This depends on what the sea urchins feed on

and the substrate in which they obtained their

food. Food availability in the zone and food

preference will consequently influence the gut

content (Alvarado et al., 2015).

Due to this, knowing the amount of matter

that the sea urchins are consuming according to

RESUMEN

Variación de la dieta del erizo de mar (Diadema mexicanum (Diadematoida: Diadematidae))

según su tamaño en el Pacífico Tropical Oriental

Introducción: El erizo de mar Diadema mexicanum, por su actividad de bioerosión, es considerado de impor-

tancia ecológica. Este fenómeno podría afectar negativa o positivamente a los ecosistemas de arrecifes de coral. El

proceso de bioerosión varía según la abundancia y el tamaño del erizo de mar.

Objetivo: Los organismos juveniles poseen diferentes necesidades metabólicas en comparación con los adultos,

por lo que conocer el contenido estomacal según el tamaño, nos permite cuantificar la selección de sustrato

bioerosionado.

Métodos: Para determinar esto, se recolectaron individuos de D. mexicanum en 12 sitios desde enero de 2009

hasta septiembre de 2010 a lo largo de la costa del Pacífico Tropical Oriental. El contenido estomacal se clasificó en

Fracción Carbonatada (FC), Fracción No Carbonatada (NCF) y Materia Orgánica (MO). El contenido estomacal

se analizó según a) estadio juvenil (< 3 cm) o adulto (> 3 cm) y b) localidad.

Resultados: Los juveniles presentaron los siguientes porcentajes promedio del contenido estomacal: 20.7 % OM,

12 % NCF y 67.9 % CF; y adultos: 11.4 % OM, 14.8 % NCF y 73.8 % CF. Con base en una prueba de Wilcoxon y

una regresión lineal de Kendall, se obtuvieron los siguientes resultados. La fracción carbonatada en el estómago

aumentó en promedio 0.47 unidades por cada cm de crecimiento (p < 0.05). La MO consumida por D. mexicanum

aumenta solo 0.05 unidades por cada cm de crecimiento (p < 0.05). Encontramos una diferencia en el contenido

estomacal según el sitio (p < 0.05) y el estadio de vida (P < 0.05). Localidades como Huatulco y Coco presentaron

diferencias significativas que podrían estar relacionadas con las condiciones oceanográficas locales.

Conclusiones: Relacionamos estos cambios de la composición porcentual del contenido estomacal con la necesi-

dad de los erizos de mar juveniles de nutrientes para mantener su crecimiento. La cantidad de MO es crucial para

el desarrollo de las primeras etapas, lo que significa que existe una diferencia en la selección de sustrato asociada

con el crecimiento.

Palabras clave: materia orgánica; arrecifes de coral; contenido estomacal; carbonatos; crecimiento; bioerosión.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58602, marzo 2024 (Publicado Mar. 01, 2024)

their stage of development is important, since it

makes it possible to quantify their selection of

bio-eroded substrate. Taking this into account,

determining whether the location of D. mexi-

canum influences stomach content can be a

relevant factor to slow down coral reef degra-

dation. Here, we thereby determine if there is a

difference in the gut content of D. mexicanum

according to the study site and development

stage and establish if there is a correlation

between their gut content and their age. We

predict that there is going to be a difference

between stomach contents of D. mexicanum

according to their age and locality. We expect

there to be a significant correlation between the

sea urchin size and the stomach content type.

MATERIALS AND METHODS

This study was carried out in 12 localities

with coral reefs in the Eastern Tropical Pacific

(ETP) (Fig. 1), which included continental,

peninsular and insular environments, both pro-

tected and non-protected areas (Alvarado et al.,

2016a, Alvarado et al., 2016b).

Diet composition was determined by col-

lecting the evacuated gut content (EGC), and

organic matter (OM), calcium carbonate frac-

tion (CaCO3) and non-carbonated fraction

(NCF) were analyzed. To obtain the ECG, 30

individuals per locality were collected (50 in

Coiba and Las Perlas), from January 2009 to

September 2010, and placed in 10 L plastic

containers with continuous ventilation, letting

them evacuate for 24 hours (sensu Glynn, 1988;

Reyes-Bonilla & Calderón-Aguilera, 1999).

The evacuated material by each individual

sea urchin was dried in an oven at 60 ºC for

24 hours. The samples were weighed in a top

loading balance (0.001 g), and then combusted

for 6 hours at 550 ºC to burn the OM. The OM

starts burning at 200 ºC and gets completely

burned away at 550 ºC, the carbonates are not

affected (Griffin et al., 2003). After cooling,

the samples were weighed again, and the dif-

ference in mass was the organic matter present

in the material evacuated (Carreiro-Silva &

McClanahan, 2001). The remaining fraction

represents the inorganic fraction that consisted

of calcium carbonate (CaCO3) and insoluble

residues (rock fragments, quartz grains, sponge

spicules, diatoms, radiolarians and silt). The

inorganic fraction was digested in 10 % hydro-

chloric acid and after the dissolution of CaCO3

filtered using pre-weighed fiberglass filters.

The weight of the residual material retained on

the filter corresponds to the non-carbonated

fraction (NCF). The difference between the

inorganic fraction weight and the NCF was

CaCO3 (Carreiro-Silva & McClanahan, 2001).

All sea urchins were measured with a caliper,

and it was established that a size greater than

2.5 cm corresponds to an adult organism,

while those less than or equal to said size

were considered juveniles according to Benítez-

Villalobos et al. (2015).

A Wilcoxon test (W) was conducted to

determine the difference in stomach content

between size groups. The difference in stomach

content between localities was analyzed using a

non-parametric Kruskal-Wallis. Finally, a lin-

ear regression model with a Kendall correlation

was made to obtain the correlations between

their different stomach fractions (g) and their

size (cm). All these analyses were performed

using R studio (v4.2.2.) (R Core Team, 2023).

RESULTS

The EGC of 160 juvenile and 210 adults of

D. mexicanum were analyzed. The organic mat-

ter (OM) (W = 11 694, p < 0.001), carbonated

fraction (CaCO3) (W = 3 980.5, p < 0.001) and

non-carbonated fraction (NCF) (W = 4224.5,

p < 0.001) varied between both sizes. Juveniles

presented an average of 0.3708 ± 0.1745 g of

CaCO3, 0.1141 ± 0.0795 g of OM and 0.0606 ±

0.075 g of NCF, while adults presented 1.3527

± 1.2244 g of CaCO3, 0.1956 ± 0.2563 g of OM

and 0.2553 ± 0.2579 g of NCF on average (Fig.

2). Also, the carbonated fraction increased 0.47

g on average for each cm of growth of D. mexi-

canum (R= 0.5690, p < 0.05, Fig. 3), while the

organic matter only increased 0.05 g per cm (R

= 0.2630, p < 0.05, Fig. 4).

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58602, marzo 2024 (Publicado Mar. 01, 2024)

Overall, Coco’s Island presented the high-

est average of the three fractions of the gut con-

tent (CaCO3 = 2.2519 ± 1.1802 g, OM = 0.5380

± 0.5293g, NCF = 0.7525 ± 0.2909 g). Coiba had

the lowest averages of CaCO3 (0.4179 ± 0.2710),

while the lowest value of OM was presented in

Pulmo (0.0892 ± 0.0281 g) and the lowest aver-

age of NCF was obtained in Huatulco (0.0418

± 0.6633 g). Also, significant differences were

obtained between CaCO3 (χ2 = 144.9, df = 11,

Fig. 1. Diadema mexicanum study localities along in the ETP. A. Isla Espíritu Santo; B. Cabo Pulmo; C. Islas Marietas; D.

Carrizales; E. Ixtapa-Zihuatanejo; F. Bahías de Huatulco; G. Los Cóbanos; H. Bahía Culebra; I. Isla del Caño; J. Isla del Coco;

L. Isla Coiba; M. Archipiélago de Las Perlas.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58602, marzo 2024 (Publicado Mar. 01, 2024)

Fig. 2. A. Percentage of the stomach content of Diadema mexicanum according to its development stage. The error bars

represent the standard deviation; B. % Gut content per size frequencies of test’s (cm).

Fig. 3. Correlation of Diadema mexicanum between its size and the carbonated fraction, per individual.

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58602, marzo 2024 (Publicado Mar. 01, 2024)

p < 0.001), OM (χ2 = 135.66, df = 11, p < 0.001)

and NCF (χ2 = 213.67, df = 11, p < 0.001) by

locality (Fig. 5).

DISCUSSION

The amount of carbonates per individ-

ual per size class (Fig. 2) was similar to the

ones observed for Diadema savigny (Audouin,

1809), Echinothrix diadema (Linnaeus, 1758)

and Echinostrephus molaris (Blainville, 1825) in

French Polynesia (Bak, 1990) or for D. antilla-

rum in Barbados (Scoffin et al., 1980) (Table 1).

Also, similar to the values found by Herrera-

Escalante et al. (2005) for D. mexicanum in

Huatulco, 0.47 g CaCO3 ind-1 for sea urchins

Fig. 4. Correlation of Diadema mexicanum between its size and the organic matter, per individual.

Fig. 5. Percentage of the stomach content of D. mexicanum according to the collection sites. The error bars represent the

standard deviation.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58602, marzo 2024 (Publicado Mar. 01, 2024)

smaller than 3 cm, 1.41 g CaCO3 ind-1 for

urchins between 3-5 cm and 2.96 g CaCO3 ind-1

for urchins between 5 and 7 cm of test diameter.

Hawkins (1981) and Hawkins and Lewis

(1982) found a change in the percentage com-

position of organic matter among sea urchins

bigger than 3.5 cm, as we found. The percent-

age of encrusting coralline algae in the gut

content of D. antillarum changes between sizes

(Hawkins & Lewis, 1982). In sea urchins small-

er than 3.5 cm, these algae represent between

70–80 %, while epilithic or endolithic algae rep-

resent between 5 % and 20 %. In sizes over 3.5

cm, encrusting coralline algae become a minor

element of the gut content (5–20 %), while epi-

lithic algae represent between 50 and 75 %. Sea

urchins smaller than 3.5 cm present a higher

growth rate (3.4 mm month-1) than sea urchins

above this size (1.5 mm month-1) (Hawkins &

Lewis, 1982). When sea urchins grow, their diet

varies from encrusting coralline algae (with

high organic matter content) to epilithic algae

(with low organic matter content). The high-

est growth rates in small sea urchins require

a higher quality diet with an organic content

richer than the diet of sea urchins over 3.5 cm.

Additionally, sea urchins that eat encrusting

coralline algae possess an absorption efficiency

ranging between 26–72 %, while urchins that

eat other algae possess an efficiency between

1 % and 24 % (Hawkins, 1981). In the ETP, 51 %

of sea urchins are under 4 cm (Fig. 4). Also,

in seven of the studied localities, between 53

% and 100% of the collected individuals were

under 4 cm, highlighting the abundance of

young urchins. It seems that small individuals

prefer calcareous algae, which give them the

necessary energy requirements to grow fast and

reach adulthood.

Regarding the development of the sea

urchins, it has been seen that their growth and

gonad development do not occur at the same

time (Lawrence, 2000). On the contrary, usu-

ally these individuals focus on one process or

another, both requiring nutrients, both limited

by food availability (Lawrence, 2000). The tran-

sition from a larval state to a juvenile has not

been studied deeply, and this process involves

a drastic change in the urchin’s diet (Fadl

et al., 2018). There is a period of time, spe-

cifically at the beginning of this process, where

the urchin is deprived of nutrients, which is

related to the development of Aristotle’s lantern

(Fadl et al., 2018).

What the sea urchins eat during the first

juvenile stages is unknown and the change of

stage can lead to a different diet (Fadl et al.,

2018). Also, it has been proven by experiments

that sea urchins with a more calcareous diet do

not get to change into an adult stage, meaning

they never develop their gonads to a point of

sexual maturity (Meidel & Scheiblingl, 1999).

This implies that the idea and presence of the

organic matter and proper nutrients are neces-

sary during juvenile development stages, which

means that a diet based on more organic matter

in the early stages is to be expected (Meidel &

Scheiblingl, 1999).

In the case of the general increase of the

stomach content related to size, D. mexicanum

gonads grow in proportion to their size (López-

Pérez & López-López, 2016). The gonads size

not only depends on the increase in number

and size of gametes, but also depends on the

phagocytes and the nutrient storage needed

for the start of gametogenesis. These nutrients

need to be recovered with food since individu-

als who do not eat or do not have a good diet

tend to either have smaller gonads or not have

them at all (Muthiga & McClanahan, 2007).

Table 1

Average carbonate grams per individual (g CaCO3 ind-1)

in Barbados (D. antillarum; Scoffin et al., 1980), French

Polynesia (D. savigny, E. diadema, Echinostrephus molaris;

Bak, 1990) and in ETP (D. mexicanum; this research).

Class interval Barbados French Polynesia ETP

[1.00, 2.00) 0.273 0.01 0.277

[2.00, 3.00) 0.507 0.04 0.404

[3.00, 4,00) 1.292 0.16-0.36 0.705

[4.00, 5.00) 1.490 0.71-1.06 1.150

[5.00, 6.00) 2.264 1.87-3.03 1.290

[6.00, 7.00) 4.32-6.81 2.478

[7.00, 8.00) 3.886

[8.00, 9.00) 2.728

Average 1.165 1.185-1.885 1.435

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58602, marzo 2024 (Publicado Mar. 01, 2024)

Then, the increase in size could be related

to a strategy for the urchin to prepare for a

reproductive stage. An example of this has been

seen in the green sea urchin, Strongylocentro-

tus droebachiensis (O.F. Müller, 1776), which

presents a mobilization of nutrients from the

nutritive phagocytes, indicating a new game-

togenesis, surrounding germ cells with the

released nutrients (Benítez-Villalobos et al.,

2015). Also, it has been seen that the size is

directly proportional to the amount of carbon-

ates consumed (López-Pérez & López-López,

2016), which is supported by the non-paramet-

ric test done (Kruskal, p < 0.001).

The size of the sea urchins can increase

due to external factors not directly related to

nutritive requirements, which is the case for the

genus Diadema, where it has been seen that, in

some occasions, when the population density

is low, the individual size increases (Benítez-

Villalobos et al., 2008). This happens because

sea urchins are considered density-dependant,

where whenever there are fewer individuals, the

resource availability increases, leading to a bet-

ter general diet (Benítez-Villalobos et al., 2008).

Another case where this happens is depending

on the substrate of the localities (López-Pérez

& López-López, 2016). Generally, the size and

density of the organisms changes according

to the size of the site, for example, places with

bigger rocks tend to have bigger sea urchins

(López-Pérez & López-López, 2016).

Lastly, coral reefs are very susceptible to

environmental changes, which can create dif-

ferences between them throughout the Eastern

Tropical Pacific (Alvarado et al., 2016a). D.

mexicanum lives in these ecosystems, which

could have been modified by El Niño of 1982-

1983, which generated a high mortality rate

in the corals, and subsequently an increase in

macroalgae growth, that populated the site,

considerably increasing their coverage (Alvara-

do et al., 2016a). This phenomenon is impor-

tant because the bioerosion of D. mexicanum

is approximately twice as high in dead coral

substrate (Glynn, 1988), which influences con-

siderably, because the sea urchins arrive at these

affected places in search of food and this leads

to a localized abrasion of the calcareous depos-

its (Herrera-Escalante et al., 2005).

Another factor that goes hand in hand

with the disturbances in the reefs of the ETP

zone is that these are very susceptible to erosive

changes due to their little development, mean-

ing any damage would be more drastic. The

higher bioeresion rate could also be attributed

to D. mexicanum generally found in groups

(Herrera-Escalante et al., 2005). The feeding of

urchins can also have an impact on carbonate

levels and algal cover of coral reefs (Alvarado

et al., 2016a). Variations in the ecosystems and

conditions, like the ones described above, can

cause differences in feeding, so, a change can

be observed in the type of stomach content in

relation to the location.

As a recommendation, for other studies

like this one, it is important to note that adult

sea urchins have high nutrient stages, where

they seem to prepare for their reproductive

stage and spawning (Benítez-Villalobos et al.,

2015). This is an important consideration since

the season for the data collection can influence

the results. Another aspect to consider is that

some of the areas of study were protected areas

and that not all of them have the same level of

conservation (Alvarado et al., 2016a). This is

important since it has been reported that areas

with overfishing, unprotected areas or less pro-

tected areas, usually present higher densities of

sea urchins and a more noticeable bioerosion

effect (Graham et al., 2011).

In conclusion, it seems that the life stage

of the sea urchin does influence the stomach

content, and the juveniles tend to consume a

higher percentage of organic matter related to

the necessity of the early-stage sea urchins for

nutrients to maintain their growth. The amount

of OM is crucial for the development during

this stage, meaning that there is a difference in

substrate selection associated with growth.

Aside from this, the locality, which relates

to the kind of substrate and the availability of

nutrients is key to the diet of D. mexicanum. At

last, there is an important correlation between

the size of the urchin and their stomach content,

which states that whenever the size increases,

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58602, marzo 2024 (Publicado Mar. 01, 2024)

all of the stomach content increases too, being

most noticeable in the case of the carbon-

ated fraction. Also, the percentage distribution

of the stomach content significantly differs,

where it is seen that the carbonated fraction

has double the percentage of consumption in

the case of juveniles compared to adults. All of

this could suggest that in case of a situation of

D. mexicanum overpopulations, the adults are

going to be causing more damage to the ecosys-

tem and mostly to corals, leading to a possible

disbalance of carbonate levels and algal covers,

so controlling the adult population is advised.

Ethical statement: the 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 sec-

tion. A signed document has been filed in the

journal archives.

ACKNOWLEDGMENTS

We acknowledge the following persons

that collaborated during the development of

this work: C. Fernández, O. Breedy, C. Sánchez,

S. Martínez, E. Gómez, A. Planas, V. Flores, O.

Norzagaray, L.E. Calderón-Aguilera, A. Ayala, J.

Carrión, L. Hernández, G. Ramírez, V. Vargas,

J. Ramírez, and the Bezy, Sánchez-Camacho

and García-Zuñiga families. We also thank

the following institutions, organizations and

companies: Centro de Investigación en Cien-

cias del Mar y Limnología (CIMAR, Univer-

sidad de Costa Rica), Universidad Autónoma

de Baja California Sur (UABCS), Laborato-

rio de Sistemas Arrecifales (LSA), Centro de

Investigaciones en Ciencias Marinas (CICI-

MAR), Universidad de Guadalajara, Centro de

Investigación Científica y Educación Superior

de Ensenada (CICESE), Universidad del Mar,

Ministerios del Ambiente y Recursos Natura-

les-El Salvador, Universidad de El Salvador,

Smithsonian Tropical Research Institute, Liquid

Jungle Lab, Charles Darwin Foundation, Hotel

Pacífica, Mero Divers, Vallartec, Fundarrecife,

and Reserva Biológica Isla del Caño, Parque

Nacional Isla del Coco and Parque Nacional

Los Cóbanos park rangers, MY Adventure

crew, Instituto Costarricense de Turismo, Siste-

ma Nacional de Áreas de Conservación-Costa

Rica (SINAC), Autoridad Nacional del Ambi-

ente- Panamá (ANAM), Hotel Punta Maren-

co Lodge and Águila de Osa Inn. A special

acknowledgement for their economic support

for this research to Vicerrectoría de Investig-

ación-Universidad de Costa Rica, Ministerio de

Ciencia y Tecnología de Costa Rica (MICIT),

Consejo Nacional para Investigaciones Cientí-

ficas y Tecnológicas de Costa Rica (CONICIT),

Consejo Nacional de Ciencia y Tecnología de

México (CONACYT), Fonds Français pour

l’Environnement Mondial (FFEM), Ecodesar-

rollo Papagayo and Grupo Adelante.

REFERENCES

Alvarado, J., Cortés, J., Guzman, H., & Reyes-Bonilla,

H. (2016a). Bioerosion by the sea urchin Diade-

ma mexicanum along Eastern Tropical Pacific coral

reefs. Marine Ecology, 37(5), 1088–1102. https://doi.

org/10.1111/maec.12372

Alvarado, J., Cortés, J., Guzman, H., & Reyes-Bonilla, H.

(2016b). Distribution, size and diet of Diadema mexi-

canum (Echinoidea) along the Eastern Tropical Paci-

fic coral reefs. Aquatic Biology, 24, 151–161. https://

doi.org/10.3354/ab00645

Alvarado, J. J., Reyes-Bonilla, H., & Benítez-Villalobos, F.

(2015). Diadema mexicanum, erizo de mar clave en

los arrecifes coralinos del Pacífico Tropical Oriental:

lo que sabemos y perspectivas futuras (Diadematoida:

Diadematidae). Revista de Biología Tropical, 63(S2),

135–157. http://dx.doi.org/10.15517/rbt.v63i2.23140

Alves, F., Chícharo, L., Serrao, E., & Abreu, A. D. (2003).

Grazing by Diadema antillarum (Philippi) upon

algal communities on rocky substrates. Scientia

Marina, 67(3), 307–311. https://doi.org/10.3989/

scimar.2003.67n3307

Bak, R. P. M. (1990). Patterns of echinoid bioerosion in two

Pacific coral reef lagoons. Marine Ecology Progress

Series, 66, 267–272.

Benítez-Villalobos, F., Gómez, M. D., & Pérez, R. L. (2008).

Temporal variation of the sea urchin Diadema mexi-

canum population density at Bahias de Huatulco,

Western Mexico. Revista de Biología Tropical, 56(S3),

255–263. https://doi.org/10.15517/rbt.v56i3.27140

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58602, marzo 2024 (Publicado Mar. 01, 2024)

Benítez-Villalobos, F., Ávila-Poveda, O. H., Díaz-Martínez,

J. P., & Bravo-Ruiz, A. R. (2015). Gonad development

stages and reproductive traits of Diadema mexicanum

(Echinodermata: Echinoidea) from Oaxaca, Mexi-

co. Invertebrate Reproduction & Development, 59(4),

237–249. http ://dx.doi.org/10.1080/07924259.2015

.1108935

Cabanillas-Terán, N., Loor-Andrade, P., Rodríguez-Barre-

ras, R., & Cortés, J. (2016). Trophic ecology of sea

urchins in coral-rocky reef systems, Ecuador. PeerJ, 4,

e1578. https://doi.org/10.7717/peerj.1578

Carreiro-Silva, M., & McClanahan, T. R. (2001). Echinoid

bioerosion and herbivory on Kenyan coral reefs: the

role of protection from fishing. Journal of Experimen-

tal Marine Biology and Ecology, 262, 133–153. https://

doi.org/10.1016/S0022-0981(01)00288-X

Eakin, C. M. (2001). A tale of two ENSO events: carbonate

budgets and the influence of two warming disturban-

ces and intervening variability, Uva Island, Panama.

Bulletin of Marine Science, 69(1), 171–186.

Fadl, A. E. A., Mahfouz, M. E., El-Gamal, M. M. T., &

Heyland, A. (2018). Onset of feeding in juvenile sea

urchins and its relation to nutrient signalling. Inver-

tebrate Reproduction & Development, 63(1), 11–22.

https://doi.org/10.1080/07924259.2018.1513873

Glynn, P. W. (1988). El Niño warming, coral mortality and

reef framework destruction by echinoid bioerosion in

the Eastern Pacific. Galaxea, 7(2), 129–160. https://

doi.org/10.1007/s00227-017-3175-0

Glynn, P. W., & Morales, G. E. L. (1997). Coral reefs of

Huatulco, West Mexico: reef development in upwe-

lling Gulf of Tehuantepec. Revista de Biología Tropical,

45(3), 1033–1047.

Graham, J. E., Banks, S. A., Bessudo, S., Cortés, J., Guz-

mán, H. M., Henderson, S., Martinez, C., Rive-

ra, F., Soler, G., Ruiz, D., & Zapata, F. A. (2011).

Variation in reef fish and invertebrate communi-

ties with level of protection from fishing across

the Eastern Tropical Pacific seascape. Global Eco-

logy and Biogeography, 20(5), 730–743. https://doi.

org/10.1111/j.1466-8238.2010.00642.x

Griffin, S. P., García, R. P., & Weil, E. (2003). Bioero-

sion in coral reef communities in southwest Puer-

to Rico by the sea urchin Echinometra viridis.

Marine Biology, 143, 79–84. https://doi.org/10.1007/

s00227-003-1056-1

Hawkins, C. M. (1981). Efficiency of organic matter absorp-

tion by the tropical echinoid Diadema antillarum

Philippi fed non-macrophytic algae. Journal of Expe-

rimental Marine Biology and Ecology, 49, 245–253.

https://doi.org/10.1016/0022-0981(81)90074-5

Hawkins, C. M., & Lewis, J. B. (1982). Ecological ener-

getics of the tropical sea urchin Diadema antilla-

rum Philippi in Barbados, West Indies. Estuarine,

Coastal and Shelf Science, 15, 645–669. https://doi.

org/10.1016/0272-7714(82)90077-4

Herrera-Escalante, T., López-Pérez, R. A., & Leyte-Morales,

G. E. (2005). Bioerosion caused by the sea urchin

Diadema mexicanum (Echinodermata: Echinoidea)

at Bahías de Huatulco, Western Mexico. Revista

de Biología Tropical, 53(S3), 263–273. https://doi.

org/10.15517/rbt.v53i3.26784

Hutchings, P. (2011). Bioerosion. In: G, Gabioch, P. Davies,

T. J. Done, E. Guschler, I. G. Macintyre, R. Wood, C.

D. Woodroffe, & D. Hopley (Eds), Encyclopedia of

Modern Coral Reefs: Structure, form, and Process (pp.

139–156). Springer.

Lawrence, J. M. (2000). Conflict between somatic and gona-

dal growth in sea urchins: a review [Technical Inform].

Florida Sea Grant College Program.

López-Pérez, A., & López-López, D. A. (2016). Impacto

bioerosivo de Diadema mexicanum en arrecifes de

coral del Pacífico sur mexicano. Ciencias marinas,

42(1), 67–79. https://doi.org/10.7773/cm.v42i1.2586

McClanahan, T. R., Kamukuru, A. T., Muthiga, N. A.,

Gilagabher, M., & Obura, D. (1996). Effect of sea

urchin reductions on algae, coral, and fish popula-

tions. Biological Conservation, 10, 136–154. https://

doi.org/10.1046/j.1523-1739.1996.10010136.x

Meidel, S. K., & Scheibling, R. E. (1999). Effects of food

type and ration on reproductive maturation and

growth of the sea urchin Strongylocentrotus droeba-

chiensis. Marine Biology, 134, 155–166. https://doi.

org/10.1007/s002270050534

Muthiga, N. A., & McClanahan, T. R. (2007). Ecology of

Diadema. In J. M. Lawrence (Ed.), Edible Sea Urchins:

Biology and Ecology (pp. 205–219). Elsevier.

R Core Team (2023). R: A language and environment

for statistical computing [Computer software]. R

Foundation for Statistical Computing. https://www.R-

project.org/

Reyes-Bonilla, H., & Calderón-Aguilera, L. E. (1999).

Population density, distribution and consumption

rates of three corallivores at Cabo Pulmo reef, Gulf of

California. Marine Ecology, 20, 347–357. https://doi.

org/10.1046/j.1439-0485.1999.2034080.x

Scoffin, T. P., Stearn, C. W., Boucher, D., Frydl, P., Hawkins,

C. M., Hunter, J. G., & MacGeachy, J. K. (1980). Cal-

cium carbonate budget of fringing reef of the West

coast of Barbados. Part II. Erosion, sediments and

internal structure. Bulletin of Marine Sciences, 30,

475–508

Tribollet, A., & Golubic, S. (2011). Reef Bioerosion: Agents

and Processes. In Z. Dubinsky, & N. Stambler (Eds.),

Coral Reefs: An Ecosystem in Transition (pp. 435–449).

Springer.