Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e59007, marzo 2024 (Publicado Mar. 01, 2024)

Predators of the sea urchin Diadema mexicanum

(Diadematoida: Diadematidae) at the Eastern Tropical Pacific coral reefs

José Carlos Hernández1*; https://orcid.org/0000-0002-1539-1783

Beatriz Alfonso1; https://orcid.org/0000-0003-2152-8122

Ana Gloria Guzmán-Mora2

Juan José Alvarado3,4; https://orcid.org/0000-0002-2620-9115

1. Departamento de Biología Animal, Edafología y Geología, Universidad de La Laguna, Canary Islands, Spain;

jocarher@ull.es (*Correspondence), balfonso@ull.edu.es

2. Conservation International, Costa Rica; aguzman@conservation.org

3. Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Universidad de Costa Rica, San Pedro, San José,

Costa Rica; juan.alvarado@ucr.ac.cr

4. Centro de Investigación en Biodiversidad y Ecología Tropical (CIBET), Universidad de Costa Rica, San Pedro, San José,

Costa Rica.

Received 02-II-2023. Corrected 22-XI-2023. Accepted 04-XII-2023.

ABSTRACT

Introduction: The coral reefs of Isla del Coco National Park are some of the most pristine ecosystems on Earth.

The sea urchin Diadema mexicanum (Diadematoida: Diadematidae) is a common inhabitant with a pivotal role

in the ecology of this unique ecosystem.

Objective: In this study, we identified the predominant predators of D. mexicanum and estimated the predatory

consumption rates. We also determined predation rates at different sea urchin sizes and at sites with contrasting

refuge availability.

Methods: We use field video recording observations and tethering experiments.

Results: The balistid Sufflamen verres and the labrid Bodianus diplotaenia were identified as predators of small

and medium size D. mexicanum; the labrids Thalassoma grammaticum and B. diplotaenia (juvenile) and the

tetraodontid Arothron meleagris were attempted predators; and Canthigaster punctatissima and Holacanthus

passer were scavengers. Larger sea urchins (> 30 mm) were also preyed upon during the tethering experiments.

Furthermore, a clear effect of the site on survival of the different sea urchins’ sizes was noted. No difference in

the sea urchin predator biomass was found among sites, which highlights the importance of site complexity on

survival. At high and medium complexity sites, large individuals had better survival, while at the low complex-

ity site, there was almost no differences in survival rates among the three size classes. Our results also show

that a high abundance of these predatory fishes, above 0.04 ind m-2, guarantees a low sea urchin density. Below

this threshold, a higher variability in sea urchin density is observed Despite not being registered with the video

recordings, lobsters were observed once preying upon a large sea urchin individual.

Conclusions: This study identifies a keystone fish guild with high predation rate for Diadema in the National

Park, which suggests that protective actions have positively benefited predatory fish and lobster populations.

Key words: Balistidae; Labridae; lobsters; Isla del Coco; video; tethering experiment.

https://doi.org/10.15517/rev.biol.trop..v72iS1.59007

SUPPLEMENT

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e59007, marzo 2024 (Publicado Mar. 01, 2024)

INTRODUCTION

Several species of sea urchins play an

important role in the ecology of coral reefs, and

its grazing activity is crucial to prevent mac-

roalgae overgrowth on corals and to facilitate

coral recruitment (Sammarco, 1982; Edmunds

& Carpenter, 2001). However, when the sea

urchin population increases, its voracious activ-

ity can destroy the coral framework, limiting

coral reef biodiversity (Bak, 1994; Alvarado et

al., 2016a). Therefore, factors that can cause

boom–bust changes in the sea urchin den-

sity are important for maintaining the health

of the coral reefs (Knowlton, 2001; Muthiga &

McClanahan, 2020). Deteriorating health of the

world’s coral reefs threatens global biodiversity

and ecosystem function as well as the liveli-

hood of millions of people living in the tropics

(Hoegh-Guldberg et al., 2007).

Among the factors that control varia-

tions in the sea urchin population density,

anthropogenic influences contribute most fre-

quently, and these included increased primary

productivity through eutrophication, ocean

warming, disease, overfishing, and species

introduction (Uthicke et al., 2009; Hernández,

2017). A remarkable sea urchin abundance

fluctuation occurred in 1983 and 1984 due to

the Caribbean-wide mass mortality of the sea

urchin Diadema antillarum (Lessios, 1988).

This event provides an excellent study case

to evaluate the key role of sea urchins in

changes in macroalgal cover and subsequent

coral reef deterioration. However, long before

the mass mortality, the Caribbean coral reefs

were subjected to intense fishing, and this

reduced predatory control over D. antillarum,

which were extremely abundant (Jackson, 1997;

Jackson et al., 2001). At that time, the den-

sity of D. antillarum was sufficiently high to

influence characteristics such as community

composition and reef grow (Ogden, 1977; Bak

et al., 1984). Therefore, although catastrophic

RESUMEN

Depredadores del erizo de mar Diadema mexicanum (Diadematoida: Diadematidae)

en los arrecifes de coral del Pacífico Tropical Oriental

Introducción: Los arrecifes de coral del Parque Nacional Isla del Coco son uno de los ecosistemas más prístinos

de la Tierra. El erizo de mar Diadema mexicanum (Diadematoida: Diadematidae) es un habitante común con un

papel ecológico esencial en este ecosistema único.

Objetivo: En este estudio, identificamos los depredadores predominantes de D. mexicanum y estimamos las tasas

de consumos predatorias. También determinamos las tasas predatorias de diferentes tamaños de erizo de mar en

sitios con disponibilidad de refugio contrastante.

Métodos: Utilizamos grabaciones de video de campo y experimentos de marcaje.

Resultados: El pez ballesta Sufflamen verres y el lábrido Bodianus diplotaenia fueron identificados como depreda-

dores de tamaños pequeños y medianos de D. Mexicanum; los lábridos Thalassoma grammaticum y B. diplotaenia

(juvenil) y el tetraodóntido Arothron meleagris fueron intento de depredadores; y Canthigaster punctatissima y

Holacanthus passer fueron carroñeros. Los erizos de mar de gran tamaño (> 30 mm) también fueron depredados

durante el experimento de marcaje. Además, se encontró un efecto claro del sitio en la supervivencia de los dife-

rentes tamaños de erizo de mar. No se encontraron diferencias en la biomasa de los depredadores del erizo de mar

entre sitios, lo que señala la importancia de la complejidad del sitio en la supervivencia. En sitios con complejidad

estructural alta y media, los individuos grandes tuvieron mejor supervivencia, mientras que en sitios de compleji-

dad baja apenas hubo diferencias en las tasas de supervivencia entre los tres tamaños. Nuestros resultados también

muestran que una alta abundancia de peces depredadores, por encima de 0.04 ind m-2, asegura bajas densidades

de erizos de mar. A pesar de no ser registrado durante las grabaciones de video, se observó en una ocasión a una

langosta depredando sobre un erizo de gran tamaño.

Conclusiones: Este estudio identifica el grupo de peces clave con grandes tasas de depredación sobre Diadema en

el Parque Nacional, lo que sugiere que las medidas de protección han beneficiado positivamente las poblaciones

de peces depredadores y langostas.

Palabras clave: Balistidae; Labridae; langostas; Isla del Coco; vídeo; experimentos de marcaje.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e59007, marzo 2024 (Publicado Mar. 01, 2024)

events can quickly alter coral reefs, predatory

control upon sea urchins was found to be a key

ecological process in the functioning of coral

reefs (McClanahan, 1988; McClanahan, 1995).

A recent global metanalysis study showed

that predators’ impact on the sea urchin popula-

tions was higher in tropical coral reefs compared

to temperate regions (Sheppard-Brennand et

al., 2017). However, the same authors also high-

lighted that there is an important role of the

predator and prey identity, which can modulate

or alter this relationship. Therefore, identifying

the key sea urchin predators and quantifying

predation rates seems to be essential to deter-

mine the conservation status of the coral reefs

and to propose specific fishing restrictions

that will ensure a correct predator–sea urchin

balance for a healthy reef. The predator–prey

interaction can also be limited by the environ-

mental context (e.g., climatic events or habitat

complexity) (Steneck et al., 2002; Shears et al.,

2008; Clemente et al., 2010; Tebbett & Bell-

wood, 2018). Thus, field ecology studies should

also consider these regional and habitat charac-

teristics to better explain the observed spatial

and temporal predatory patterns.

The sea urchin Diadema mexicanum A.

Agassiz, 1863 is one of the best-studied echi-

noid species in the Eastern Tropical Pacific

(ETP) area (Alvarado et al., 2015). It is distrib-

uted from the Gulf of California (Paz-García

et al., 2016) to the Islas Galapagos (Glynn et

al., 2015). Different investigations have helped

to determine its key role as an herbivore and

bioeroder in the dynamics of ETP coral reefs

(Alvarado et al., 2016a; Cabanillas-Terán et

al., 2016; López-Pérez & López-López, 2016;

Obonaga et al., 2017). Although its role as a

herbivore has partially been studied (Benítez-

Villalobos & Valencia-Méndez, 2015), D. mexi-

canum is well known due to its bioerosive

activity, a loss of coral cover and reef framework

were observed after the El Niño 1982/1983 and

1997/1998 events (Eakin, 1996; Eakin, 2001;

Glynn, 1988). The 1982/1983 El Niño event

caused intense coral bleaching, which pro-

duced up to 80 % to 100 % mortality in some

areas of the ETP (Glynn, 1984). This left space

for colonization of turf-forming seaweeds that

served as food for a variety of herbivorous

organisms, thus favoring an increase in their

populations. Additionally, bioerosion of the

coral reefs in some areas of the ETP increased

the sea urchin populations of Eucidaris thouar-

sii (L. Agassiz & Desor, 1846), Eucidaris galapa-

gensis Döderlein, 1887, and D. mexicanum by

up to 60 % to 80 % (Eakin, 1996; Eakin, 2001;

Glynn, 1988; Guzman, 1988; Guzman & Cortés,

1992). The coral reefs of Isla del Coco, Costa

Rica were negatively affected by both El Niño

and the intense bioerosive activity of Diadema

after El Niño (Alvarado et al., 2012; Guzman

& Cortés, 1992; Guzman & Cortés, 2001). The

effect was such that it was estimated that the

coral reef recovery would take one century

(Guzman & Cortés, 1992). However, in less

than 30 years, the live coral coverage returned

to values that were close to those before the

1982–1983 El Niño. Concurrent with the coral

reef recovery, the sea urchin density decreased

to values where their bioerosive activity was at

a minimum (Alvarado et al., 2012; Alvarado

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

Beita et al., 2016).

Isla del Coco has the most diverse coral

reefs in the ETP (Alvarado et al., 2016b). How-

ever, one of the greatest threats to the ecological

integrity of this World Heritage Site was ille-

gal fishing until 2001 when the management

efforts increased. In 2001, the marine protected

area (MPA) limits of Isla del Coco increased

from 15 km to 22 km around the island where

extraction of any marine resource, any dam-

age to the fauna or flora, as well as commer-

cial, industrial, and agricultural activities were

completely prohibited in the National Park

waters. A buffer zone of 7 km within this 22-km

MPA, was also implemented, were regulated

extraction of fish resources may be permitted.

Another remarkable event was the use of coast-

guard boats since 2003 for surveillance purpos-

es (Alvarado et al., 2016b; Cajiao 2005; Decreto

N° 43368). This strengthening of the protective

measures resulted in an increase in the control

and surveillance of illegal activities such as

fish and lobster poaching (López-Garro et al.,

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e59007, marzo 2024 (Publicado Mar. 01, 2024)

2016), during subsequent years, which led to

an increase in fish apex predators (e.g. sharks,

jacks, and groupers) (Friedlander et al., 2012).

Currently, the National Park is considered to be

one of the five best MPAs in the world (Edgar

et al., 2014; Strain et al., 2018), and it has one

of the highest top predator biomasses among

coral reefs (Alvarado et al., 2016a; Alvarado et

al., 2016b; Fourriére et al., 2016; Friedlander et

al., 2012; White et al., 2014).

Although the increase in fish assemblages

coincides with a reduction in D. mexicanum

densities, no previous studies have identified

the key predators or predatory consumption

rates of this diadematid in the ETP. However,

fishing restrictions that were implemented in

the National Park may have benefited this fish

(predator) abundance, and thus, controlled

the sea urchin population. Other authors have

previously found that the fishing restrictions

inside the marine reserves in the neighboring

archipelago of the Islas Galapagos limits sea

urchin populations through top-down control

(Dee et al., 2012; Sonnenholzner et al., 2009;

Witman et al., 2017).

The Isla del Coco National Park is an inter-

esting place because it biogeographical features

together with fishing restrictions in this park

seem to favor predatory guild abundances.

However, prey and predator identity have an

important role in determining variations in

strength of the interaction. Therefore, to identi-

fy predators and quantify their influence on key

sea urchin populations, it is crucial to be able

to determine subsequent effects on coral reef

ecosystem structures and functions. Addition-

ally, knowledge of predators and how predation

rates vary among ETP coral reef locations is of

primary interest for management and conser-

vation strategies in the context of anthropogen-

ic changes to predator communities through

overfishing. Currently, the fishes Arothron

meleagris (Anonymous, 1798), Arothron hispi-

dus (Linnaeus, 1758) (Tetradontidae), Diodon

holocanthus Linnaeus, 1758 (Diodontidae),

Bodianus diplotaenia (Gill, 1862) (Labridae),

Pseudobalistes naufragium (Jordan & Starks,

1895), and Balistes polylepis Steindachner, 1876

(Balistidae) have been proposed as predators

of D. mexicanum and other sea urchins in the

ETP, but there is no data to support this theory

(Eakin 2001; Glynn et al., 1972; Guzman, 1988;

Sonnenholzner et al., 2009).

As stated previously, the Isla del Coco

seems to meet the requirements for a suitable

place for predators, at least in a biogeographical

and historical context. However, other smaller

scale factors must be taken into consideration

such as habitat architecture or individual sea

urchin size, which are among the most impor-

tant factors that limit predation (Clemente et

al., 2007; McClanahan & Shafir, 1990; Sala et al.,

1998). The presence of shelter or larger-sized

individuals can increase sea urchin survival

(Clemente et al., 2007; McClanahan, 1995).

Therefore, the presence of a predator alone does

not always ensure low sea urchin densities and

other factors must be taken into consideration

(Steneck, 2020; Tebbett & Bellwood, 2018).

This work aimed to evaluate the following

three parameters: (1) identify D. mexicanum

predators and their predation rates using video

recordings; (2) determine the effects of site

and sea urchin sizes on sea urchin predation

using tethering experiments; and (3) discuss

the potential key role of these predators on the

recent decrease in the sea urchin population.

MATERIALS AND METHODS

Study area: Isla del Coco is located in the

ETP, and it is 503 km off the southwest shore

of Costa Rica. In 1978, Isla del Coco National

Park was created, and it was established as an

official MPA 10 years later. The protected area

consists of 209 506 hectares, of which 98 % is

a marine environment (Alvarado, Beita et al.,

2016). In this study, two field experiments were

performed with the aim of identifying the key

predators of the sea urchin D. mexicanum and

to evaluate the effects of site/location and sea

urchin size on urchin survival. The experi-

ments were conducted in December 2016 at

three sites on the northern shore of the island

because it had the most favorable conditions

for scientific diving. The sites chosen were the

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e59007, marzo 2024 (Publicado Mar. 01, 2024)

Bays of Ulloa (5°33’5.20” N, 87°1’56.80” W),

Chatham (5°33’9.20” N, 87°2’27.50” W), and

Weston (5°33’8.20” N, 87°3’3.20” W). Each

of these bays have a contrasting coral habi-

tat complexity that allowed evaluation of the

protective effects of different types of sites on

D. mexicanum individuals.

Predators type identification: To identify

key D. mexicanum predators and estimate their

consumption rates, daylight video observations

were performed using three cameras per site

that recorded for 30 minutes. Three sizes of sea

urchin were offered as bait at each camera: (1)

small size, < 20 mm; (2) medium size, 20–30

mm; and (3) large size, > 30 mm. Sea urchins

were tethered to nylon and offered as bait to

possible predators. A thin metal wire was used

to maintain the fixed position of the sea urchins

in front of the camera. Videos were recorded

using a GoPro Hero 4 (San Mateo, California,

USA) with a weighted tripod. The predation

experiments were performed at a depth of 6 to

12 m at each site.

After the experiments, all video recordings

were examined in our lab, and the fish species

and their behavior were recorded. We identi-

fied the fish species that interacted with the

sea urchins and counted the type of interaction

with the sea urchin to calculate the average

behavior that was displayed by the different

species of fish. Then, we expressed these val-

ues as percentages. We defined three types of

predators depending on their behavior towards

the sea urchins, as follows: (1) predators, which

were species that broke open the sea urchin test;

(2) attempted predators, which were species

that bit but failed to open the test; and (3) scav-

engers, which were those that were fed on sea

urchin remains that were left by other preda-

tors. We also use the term “keystone guild”

(McClanahan, 1995) to refer to the group of

identify predators.

Diadema mexicanum survival: The effects

of site and sea urchin test diameter (TD) sizes

on survival were determined using the tether-

ing experiments. For each site, we quantified

the habitat complexity as the ratio l/L, where

L was the actual distance between two points

and l was the linear distance between such

points (Nichols et al., 2015). A chain was

placed directly along the substrate (L), and that

measurement was compared to the total linear

distance (l). Three sites with contrasting habitat

complexity (HC) were used: (1) Ulloa, which

had a low HC (< 0.5 m); (2) Chatham, which

had a medium HC (0.5–1 m); and (3) Weston,

which had a high HC (> 1 m).

The experimental design consisted of three

10 m transects per site with ten sea urchins per

transect. Transects were placed between 6 and

12 m at each site. The three sea urchin TD sizes

were distributed randomly along the transect

(small TD size, < 20 mm; medium TD size,

20–30 mm; and large TD size, > 30 mm, with

ten sea urchins in each size class). Using a tag-

ging gun and following the protocol of Hereu

(2005), each sea urchin was marked by insert-

ing a nylon anchor in a 2–3 mm hole that was

drilled near the top of the urchin in the inter-

ambulacrum. The nylon was 1 m long, and it

was tied transverse to the main transect, which

facilitated sea urchin movement. Survival of the

sea urchins was checked daily for 5 days at each

transect and site.

Fish and D. mexicanum surveys: Fish sur-

veys were performed at three depths (shallow,

4–8; intermediate, 9–12; and deep, 13–16 m)

with three 10-m long transects that were paral-

lel to the coast, and there were 10 m separating

each transect. To determine the fish composi-

tion at the reef, the sizes of all the fish that were

observed from the transect line were counted

and estimated within 2.5 m on each side of the

transect (width) and 5 m above (10 m × 5 m ×

5 m), forming an imaginary tunnel. The size of

each fish was estimated and classified into the

following categories (in cm): (1) < 5; (2) 5–10;

(3) 10–15; (4) 15–20; (5) 20–25; (6) 25–50; (7)

50–100; (8) 100–150; (9) 150–200; (10) 200–

250; and (11) 250–300. The length frequency

of each species was transformed into biomass

according to Alvarado, Beita et al. (2016).

D. mexicanum surveys were also performed

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e59007, marzo 2024 (Publicado Mar. 01, 2024)

at the three depths, which were mentioned

above, for the fish surveys. The abundance was

recorded at the three depths levels using three

10 × 2 m transects with 10 m of separation

between transects.

Historical sea urchin and fish predator

abundance trends: For a complete temporal

trend of sea urchin abundance and predators

at Isla del Coco, we used all of our observed

data and our survey data (2016). D. mexica-

num data from 1987 and 1990 were taken

from Guzman & Cortés (1992) and Lessios et

al. (1996), respectively. For the fish predators

(Sufflamen verres (Gilbert & Starks, 1904) and

B. diplotaenia) and D. mexicanum abundances,

the 2006, 2008, and 2011 data were taken from

the Reef Life Survey (RLS) repository (Edgar &

Stuart-Smith, 2014). Using these data, we tried

to reconstruct the historical abundance trends.

The RLS D. mexicanum and predator data were

also used for the historical trend. Sites that

were sampled during these previous visits to

the Islands have been specified within each

figure legend.

Data analysis: We recorded the action

that was displayed by each fish species and

expressed it as a percentage of the behavior

that was shown per species during the experi-

ment for all sites. The consumption rate based

on video observations was calculated using the

number of urchins that were eaten during the

experiment and expressed as a percentage of

daily consumption ratio. The effects of the site

and sea urchin size were analyzed using a mul-

tivariate analysis of variance (PERMANOVA)

using the PRIMER v7 and PERMANOVA +

(Anderson et al., 2008) statistical package. The

analysis consisted of a two-factor design, as fol-

lows: (1) site (fixed, three levels); and (2) size

(fixed, three levels) using the Euclidean dis-

tances in a raw data matrix and 5 000 permuta-

tions. When appropriate, a posteriori pairwise

comparisons were performed using permuta-

tions (Anderson, 2005). The effects of site and

Fig. 1 Percentage of fish behaviour exhibited per species during the experiments ± standard error. Predator, species that break

open the sea urchin test, S. verres and B. diplotaenia (adult). Attempted predators, species that bite but fail to open the test,

B. diplotaenia (juvenile), grammaticum and A. meleagris. Scavengers, those that were feeding on sea urchin remains left by

predators, C. puntatissima and H. passer. Black: predators; Dark grey: attempted predators; Light grey: scavengers.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e59007, marzo 2024 (Publicado Mar. 01, 2024)

predator type on the fish biomass data were also

analyzed using a PERMANOVA. The analysis

consisted of a two-factor design, as follows: (1)

site (fixed, three levels); and (2) fish behavior

(fixed, three levels) using the same data proce-

dure as described above.

A correlation between sea urchin survival

in the tethering experiments and the consump-

tion rates that were obtained during video

observations was performed. Finally, a regres-

sion analysis between the total density of fish

predators and D. mexicanum density was per-

formed using curvilinear regression analyses

of the abundance data in SPSS 25 (IBM Corp.

Released 2017. IBM SPSS Statistics for Win-

dows, Version 25.0. Armonk, NY: IBM Corp.).

RESULTS

Two species of fish, the Balistidae S. verres

and the Labridae B. diplotaenia, were identified

as predators of sea urchins that were up to 30

mm in size with 30 % and 66 % of predator

behavior, respectively, during the video record-

ing experiment at all sites. The tetraodontid A.

meleagris and the labrids Thalassoma grammat-

icum Gilbert, 1890 and B. diplotaenia (juvenile)

were attempted predators. The latter showed

the highest percentage of attempting behav-

ior (75 %). Finally, Canthigaster punctatissima

(Günther, 1870) and Holacanthus passer Valen-

ciennes, 1846 were identified as scavengers with

an average of 30 % scavenging behavior (Fig. 1).

There was a significant effect of the inter-

action term “site × sea urchin size” on D.

mexicanum survival (Table 1). In the pairwise

comparison results, small and medium size

urchins (20 and 20–30 mm, respectively) were

highly preyed upon at all sites. Nearly six of

the small D. mexicanum (< 20 mm) individual

urchins per day were consumed compared

to medium-sized sea urchins, of which two

urchins were consumed per day. Sea urchins

>30 mm were not eaten by predatory fish. At

Ulloa, with a low habitat complexity (<0.5 m),

many small- and medium-sized sea urchins

were preyed upon, whereas at Chatham, small

sea urchin consumption was significantly lower

than that of medium and larger sea urchins.

At Weston, in which the habitat complexity

was > 0.5 m, survival rates of large sea urchins

were significantly different from small and

medium size sea urchins (Fig. 2, Table 1).

There was a significant correlation between

survival in the tethering experiments and con-

sumption rates that were obtained based on

Fig. 2. Effect of the interaction of factors “Site” and “Test Diameter Size” on the survival of sea urchin D. mexicanum. Results

of pairwise analysis is displayed for each site.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e59007, marzo 2024 (Publicado Mar. 01, 2024)

video observation, particularly in high com-

plexity habitats (R2 = 0.9) (Fig. 3). Larger

D. mexicanum urchins (> 30 mm) were also

preyed upon during the tethering experiments,

particularly in Ulloa, where the sea urchin

survival rate decreased to 10 % on day 2;

however, in Chatham and Weston, the sur-

vival was > 60 % (Fig. 4). One individual of the

lobster species Panulirus penicillatus (Olivier,

1791) was observed between 7 and 8 a.m. in

Chatham holding a large sea urchin individual,

which was more likely removed from the teth-

ering experiments during the night. However,

no recordings of this event were noted in the

daylight hour videos, and this may indicate that

predation upon large sea urchin individuals by

these lobsters occurs during the night.

No significant differences were found in

the predator fish biomass among sites, either

among fish behavior or the interaction term

(Table 2). Finally, a negative logarithmic

regression described the relationship between

predators and D. mexicanum abundance, but

it was not significant (F = 2.205, p = 0.154,

Fig. 5). We used the combined S. verres and B.

diplotaenia abundance data in the regression

analysis. Abundance of fish predators instead

of the biomass was used in this analysis because

no fish size data is stored in the RLS repository.

A decrease in D. mexicanum abundance

was observed from 1987 to 2016. More recently,

from 2006 to 2016, an increase in predatory

abundance (S. verres and B. diplotaenia) was

observed (Fig. 6).

DISCUSSION

Six species of fish were observed to have

interacted with the sea urchin D. mexicanum,

and they can be considered to be members

of a keystone guild. The Balistidae S. verres

and the Labridae B. diplotaenia (adult) were

Tabl e 1

PERMANOVA analysis of site and sea urchin size effect on survival of D. mexicanum based on raw data matrix with two fixed

factors “Site” (three levels; Ulloa, Chatham and Weston) and “Test Diameter Size” (small TD size < 20 mm, medium TD size

=20–30mm and large TD size > 30mm).

PERMANOVA

Source of variation df SS MS Pseudo-F p(perm)

Site 2 2495.1 1247.5 1.676 NS

TD Size 2 19712 9856.2 13.245 < 0.01

Site x TD Size 4 12326 3081,4 4.141 < 0.01

Residual 81 60274 744.12

Total 89 92556

Pairwise comparisons

Within level “Ulloa” of factor “Site” tp (perm)

Large vs. medium 1.539 NS

Large vs. small 1.599 NS

Small vs. medium 2.350 < 0.05

Within level “Chatham” of factor “Site”

Large vs. medium 1.974 NS

Large vs. small 3.209 < 0.01

Small vs. medium 2.425 NS

Within level “Weston” of factor “Site”

Large vs. medium 3.145 < 0.01

Large vs. small 3.782 < 0.01

Small vs. medium 0.556 NS

Estimates for pairwise comparisons of the interaction “Site x TD Size”. NS: not significant; P < 0.05, P < 0.01.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e59007, marzo 2024 (Publicado Mar. 01, 2024)

predators. The Labridaes T. grammaticum and

B. diplotaneia (juvenile) and the Tetraodon-

tidae A. meleagris were attempted predators.

Finally, the Tetraodontidae C. puntatissima and

the Pomacanthidae H. passer were identified

as scavengers. Recent observations in the Gulf

of California (three sites near Cabo San Lucas,

October 2018) at the northern-most site for D.

mexicanum also revealed that both S. verres and

B. diplotaenia preyed upon D. mexicanum (size

Fig. 3. Correlation between percentage daily survival of tethering experiment and consumption rate of video observation

experiment. Log-lineal trend equation and R2 value for each site are provided.

Tabl e 2

PERMANOVA analysis of site and predator type on predators’ biomass based on raw data matrix with two fixed factors “Site”

(three levels; Ulloa, Chatham and Weston) and “Predator type” (predators, attempted predator, scavenger).

PERMANOVA

Source of variation df SS MS Pseudo-F p(perm)

Site 2 2712.4 1356.2 1.024 NS

Predator type 2 5260.9 2630.4 1.986 NS

Site x Predator type 4 3289.5 822.38 0.621 NS

Residual 41 54289 1324.1

Total 49 74292

Estimates for pairwise comparisons of the interaction “Site x Predator type”. NS: not significant. P > 0.05.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e59007, marzo 2024 (Publicado Mar. 01, 2024)

range, 30 to 44 mm test diameter) (S. Ling, per-

sonal communication, 2021). These field obser-

vations are particularly valuable for our study

because they confirm the role of these fishes in

most of the D. mexicanum geographical range.

Therefore, these fishes can be considered to

be part of a “keystone guild” for all of the ETP

coral reefs.

Our results also show that a high abun-

dance of these predatory fishes, above 0.04 ind

m-2, guarantees a low sea urchin density. Below

this threshold, a higher variability in sea urchin

density is observed (Fig. 5). However, this rela-

tionship must be viewed with caution because

it is not significant. It is likely that other sea

urchin predators must be included in the equa-

tion to obtain a better fit. Habitat architecture

and the sea urchin size add to the complexity of

this relationship. For example, the survival was

higher at Weston where some of the medium

and largest sea urchins survived during the 5

days of the experiment, while at Ulloa, the sur-

vival was very low, and a dramatic decrease in

survival was observed starting on the first days

of the experiment for all sea urchin sizes. Addi-

tionally, no significant difference in fish preda-

tor biomass was found among sites. Therefore,

it is more likely that the differences that were

found in survival are mainly due to the con-

trasting complexity of the habitat architecture

that is found between sites (Fig. 4). Weston is

a bay with an impressive Porites lobata habi-

tat architecture, which provides refuge to D.

mexicanum. Conversely, the Ulloa site consists

Fig. 4. Percentage of D. mexicanum size classes survival during five days of tethering experiment in each site. Habitat

complexity in (a) Ulloa, (b) Chatham and (c) Weston.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e59007, marzo 2024 (Publicado Mar. 01, 2024)

Fig. 5. Logarithmic negative regression of fish predators’ abundances (S. verres and B. diplotaenia ) on D. mexicanum density

at Isla del Coco. Grey dots show the data obtained from the Reef Life Survey (RLS) repository (years 2006, 2008 and 2011;

sites: Atrevido, Iglesias Bay, Inutil Bay, Wafer Bay, Dos Amigos, Isla Manuelita, Manuelita Afuera, Isla Pájara, Punta Giessler,

Punta Leonel, Punta María, Punta Presidio, Ulloa, Roca Sucia, Roca Sumergida, Rodolitos, Silverado Norte) and black dots

show the data obtained in this study (Chatham Bay, Weston Bay, Ulloa Bay).

Fig. 6. Historical abundance trend of predatory fish and D. mexicanum from 1987 to 2016 at several sites at Isla del Coco.

Data shown on the graph include the Guzmán & Cortés, 1992 D. mexicanum data (year 1987; sites: Punta Presidio, Chatham

Bay, Punta Pacheco), Lessios et al., 1996 (year 1990; site: Chatham Bay), the Reef Life Survey (RLS) (years 2006, 2008 and

2011; sites: Atrevido, Iglesias Bay, Inutil Bay, Wafer Bay, Dos Amigos, Isla Manuelita, Manuelita Afuera, Isla Pájara, Punta

Giessler, Punta Leonel, Punta María, Punta Presidio, Ulloa, Roca Sucia, Roca Sumergida, Rodolitos, Silverado Norte)

predatory and D. mexicanum data and the data obtained in 2016 survey.

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e59007, marzo 2024 (Publicado Mar. 01, 2024)

of a mix of small P. lobata corals and sandy

patches, which may facilitate predation upon

the sea urchins. Habitat architecture influences

on predation has been previously studied, and

it has been found to be a very important factor

that reduces predator success upon Diadematid

species (Carpenter, 1984; Clemente et al., 2007;

Levitan & Genovese, 1989; Ling & Johnson,

2012; Vance & Schmitt, 1979).

Consistent with other coral reef studies

(McClanahan & Muthiga, 2020; Muthiga &

McClanahan, 2020; Young & Bellwood, 2012),

the most common daylight predators of adult

sea urchins were fish. In our case, only two

fish, a triggerfish and a hogfish, were observed

to prey upon the urchins. This result should

be interpreted with caution because only 4.5

hours could be recorded due to the logistics of

the field work that was performed at Isla del

Coco National Park. It is more likely that other

triggerfish species that were observed in the

area were also able to prey upon D. mexicanum.

However, based on the videos, we can state

with certainty that the mortality of small and

medium-sized sea urchins that was recorded

in the tethering experiment was mainly due

to the above-mentioned fish predators. This

result is also confirmed by the high correlation

that is found between the daily survival that

was estimated by the tethering experiment and

the consumption rate that was estimated using

video observations. The low numbers of preda-

tory fish species coincide with observations

in the temperate rocky reefs of the Mediter-

ranean Sea (Sala, 1997) and at the subtropical

Canary Islands (Clemente et al., 2011). How-

ever, many fish predators have been identified

in the coral reefs of the Red Sea (Fricke, 1971),

East Africa (McClanahan, 1995; McClanahan,

2000), and the Great Barrier Reef (Young &

Bellwood, 2012). These numbers seem to show

a clear pattern of increasing predator trophic

redundancy toward the tropics, as previously

suggested in the metanalysis by Sheppard-

Brennand et al. (2017).

The most common effective predators

of Diadematids are fishes that belong to the

families Balistidae, Labridae, Diodontidae, and

Tetraodontidae, all of which possess power-

ful jaw morphologies that are designed for

predation upon hard invertebrates (Turingan

& Wainwright, 1993; and references therein).

However, other families have also been listed as

predators, attempted predators, or scavengers

of Diadema remains, such as Scaridae, Spari-

dae, Batrachoidinae, Carangids, Ostraciidae,

and Haemulidae. Triggerfishes and hogfishes,

which have been identified as predominant

predators in the Caribbean (Randall et al.,

1964), the Red Sea (Fricke, 1971), East Afri-

ca (McClanahan, 2000), the Easter Atlantic

Archipelagos (Clemente et al., 2010), the Great

Barrier Reef (Young & Bellwood, 2012), and

now at the ETP, Isla del Coco, are always

included among the most voracious types of

fish. Both fish species displayed contrasting

feeding techniques. While the hogfish, B. diplo-

taenia, engulfs small sea urchin sizes at once or

bangs medium size individuals on rocks/corals

until the spines are removed, the triggerfish, S.

verres, can break the sea urchin with a powerful

bite. These feeding behaviors of these two fish

coincide with previously published reports for

fishes that prey upon D. africanum (Clemente et

al., 2010). The triggerfish also acted as a domi-

nant predator, excluding other fishes, while

preying on D. mexicanum.

In the Caribbean and the Canary Islands,

other fish species, such as some haemullids

(Anisotremus surinamensis, Haemulon mac-

rostomum) or the sparid Pagrus auriga are

frequently seen with purple dots on their lips

and surrounding mouth structures, indicating

Diadema spine pricks (Randall et al., 1964; and

J. C. Hernández author’s personal observations,

August, 2017). These species have night-time

feeding habits and/or live in deeper waters

where less experimentation has been done.

Therefore, Diadema consumption has only

been corroborated based on the predators’

stomach contents (Clemente & Hernández,

2007; Randall et al., 1964). These previous

observations emphasize the possibility that

other fish predators could also be predators of

D. mexicanum; however, due to the inherent

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e59007, marzo 2024 (Publicado Mar. 01, 2024)

limitation of our experimental design, we did

not detect any other predatory behaviors.

The cause of the largest-sized sea urchin

mortality remains unknown, but we suspect

that predation by lobsters during the night

could be responsible for large sea urchin

mortality. The lobster P. penicillatus was also

observed once preying upon a large sea urchin

individual during the first hours of the day.

However, lobster predation was not observed

during the daylight video recordings; therefore,

this observation must be viewed with caution.

Among the macroinvertebrates, two gastro-

pod species of the genus Cassis, the starfish

Coscinasterias tenuispina (Lamarck, 1816), and

the spiny lobster Panulirus argus (Latreille,

1804) were observed to prey upon species of

the genus Diadema (Clemente & Hernández,

2007; Levitan & Genovese, 1989; Randall et al.,

1964). The crucial predatory role of lobsters

upon large Diadematid sea urchins has been

demonstrated (Ling et al., 2009), which sup-

ports our hypothesis of lobster predation in

Isla del Coco. Ling et al. (2009) also confirmed

that predation occurred only at night when

sea urchins left their day-time shelters. Thus,

our observation of the spiny lobster P. penicil-

latus preying upon D. mexicanum is interesting

because this lobster is probably the only species

that is capable of preying on the largest sea

urchins. However, due to this lobster’s noctur-

nal habits, our experimental video approach

did not allow observation of its consumption

rates and behaviors. Additionally, Diadematid

sea urchins show homing behaviors that can

also help them to avoid fish predators during

the day. For example, in the Caribbean, D.

antillarum have a nocturnal foraging behavior

that allows them to escape trigger fish preda-

tion (Carpenter, 1984); this finding is similar

to observations for Centrostephanus coronatus

(Verrill, 1867) in California to avoid hogfish

predation (Nelson & Vance, 1979) or for C.

rodgersii in southern Australia (Andrew &

Underwood, 1993). Thus, the lobsters that

share nocturnal feeding habits have a higher

probability of consuming urchins as prey.

The fishing restrictions, due to implemen-

tation of the MPA, may have favored predatory

control over D. mexicanum populations, which

is also supported by the historical trends (Fig.

6). However, we also believe that in highly com-

plex environments such as that found at the Isla

del Coco reefs, lobsters may play a crucial func-

tional role by preying on the largest sea urchins

due to the natural capacity of the lobsters to

creep through the habitat crevices and holes

at night. A diverse predatory guild, including

fish predators of small- and medium-sized sea

urchins in addition to lobsters that prey upon

large sea urchins may help to ensure a healthy

coral reef in which the bioerosion-related sea

urchin activity is controlled.

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.

ACKNOWLEDGEMENTS

The present investigation would not have

been possible without the support of the follow-

ing people in the field: S. Mena, M. Espinoza, E.

Ochoa, C. Salas, J. M. Camargo, J. C. Azofeifa,

C. Sanchez, and J. Cortés. Likewise, the work

was strengthened by the support of Undersea

Hunter Group, colleagues from CIMAR and

ACMIC officials. A special thanks to Conserva-

tion International for believing in this type of

research. This project was supported financially

by Conservation International and CIMAR. It

also had the endorsement of SINAC through

resolution 2016-I-ACMIC-022 and is registered

with the UCR Foundation (3013-001) and in

the Vice-Rector for Research of the University

of Costa Rica (808-B6-520). We would like to

finish with a special mention to Scott Ling who

suggested us to use the Reef Live Survey data

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e59007, marzo 2024 (Publicado Mar. 01, 2024)

and also shared with us interesting field obser-

vations he has made at Cabo San Lucas.

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