Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58993, marzo 2024 (Publicado Mar. 01, 2024)

Study of histopathology on Arbacia lixula (Arbaciidae: Arbacioida)

and Paracentrotus lividus (Parachinidae: Camarodonta)

with bald sea urchin disease symptoms in Gran Canaria Island, Spain

Raibel Núñez-González1*; https://orcid.org/0000-0001-6088-3042

María José Caballero2; https://orcid.org/0000-0002-2575-0997

Daniel Padilla2; https://orcid.org/0000-0002-6678-5029

José Luis Martín Barrasa2, 3; https://orcid.org/0000-0002-3280-9838

José Juan Castro Hernández1; https://orcid.org/0000-0001-9577-5957

1. Instituto Universitario EcoAqua, University of Las Palmas de Gran Canaria, 35017 Tafira, Spain;

raibel.nunez101@alu.ulpgc.es (*Correspondence), jose.castro@ulpgc.es

2. Institute for Animal Health and Food Safety (IUSA), Veterinary School, University of Las Palmas de Gran Canaria,

35413 Arucas, Spain; mariajose.caballero@ulpgc.es, daniel.padilla@ulpgc.es, joseluis.martin@ulpgc.es

3. Experimental Animal Facility, Research Unit, Hospital Universitario de Gran Canaria, Dr. Negrín, Las Palmas de Gran

Canaria, Spain.

Received 27-VI-2023. Corrected 06-XII-2023. Accepted 03-I-2024.

ABSTRACT

Introduction: Sea urchin diseases have been documented in several locations worldwide, with reported occur-

rences of bacterial, protozoan, fungal, and algal infections.

Objective: This study aimed to investigate pathogen agents in populations of Arbacia lixula and Paracentrotus

lividus along the coast of Gran Canaria Island (Central-East Atlantic, Spain).

Methods: Sampling was conducted at San Cristobal beach, on the Northeast side of the island, where sea urchins

were manually collected from depths of 1-3 m during June, July, and October 2022. Swab samples were taken

from the external and internal areas of the lesions and cultured on various media plates.

Results: Eight different pathogen agents, including bacteria and fungi, were identified, with Vibrio alginolyticus

being the most frequently observed bacteria in all diseased sea urchin samples. Additionally, ciliated protozoans

were found within the tests, potentially acting as opportunistic parasites.

Conclusions: This research provides a unique perspective on bald sea urchin disease by identifying a significant

number of associated pathogens, including Candida, previously unreported in diseased organisms. Furthermore,

the study highlights the presence of an inflammatory response in tissues with bacterial colonies, offering crucial

insights into understanding this sea urchin disease.

Key words: rocky shore; Vibrio; sea urchin mortality; Canary Islands; Webbnesia.

RESUMEN

Estudio de histopatología en Arbacia lixula (Arbaciidae: Arbacioida) y Paracentrotus lividus

(Parachinidae: Camarodonta) con síntomas de la enfermedad del erizo desnudo

en la Isla de Gran Canaria, España

Introducción: Las enfermedades en los erizos de mar han sido descritas en muchas localidades alrededor del

mundo, y se han asociado con la presencia de infecciones por bacterias, protozoarios, hongos y algas.

https://doi.org/10.15517/rev.biol.trop..v72iS1.58993

SUPPLEMENT

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58993, marzo 2024 (Publicado Mar. 01, 2024)

INTRODUCTION

Sea urchin diseases have been described

around the globe, particularly those that caused

several mass mortalities, including those that

occurred in the 80´ with Diadema antillarum

(Philippi, 1845) in the Caribbean Sea (Lessios,

1988), and Strongylocentrotus droebachiensis

(O.F. Müller, 1776) in Nova Scotia, Canada

(Jones et al., 1985). In both cases, the infection

agents were not deeply described. In addition,

sea urchin diseases have been reported between

2001 and 2020 in some regions of Webbnesia:

Madeira (Portugal), and Tenerife and La Palma

in Canary Islands (Spain), mainly in Diadema

africanum (Rodríguez, Hernández, Clemente &

Coppard, 2013), but in other species as Paracen-

trotus lividus (Lamarck, 1816), Arbacia lixula

(Linnaeus, 1758), and Sphaerechinus granularis

(Lamarck, 1816) (Clemente et al., 2014; Dyková

et al., 2011; Girard et al., 2011; Gizzi et al., 2020;

Hernández et al., 2020; Salazar-Forero et al.,

2022), and it is important to highlight that there

are no reports of mass mortalities or diseases in

Gran Canaria Island.

In recent times, some authors have report-

ed the pathogenic action of different infec-

tious agents in sea urchins, such as bacteria,

protozoan, fungi, and algae, being bacteria the

most common agent appearing in all diseases

(Dyková et al., 2011; Gizzi et al., 2020; Grech

et al., 2019; Grech et al., 2022; Hernández et

al., 2020; Hewson et al., 2023; Jangoux, 1987;

Salazar-Forero et al., 2022; Shaw et al., 2024;

Shimizu et al., 1995; Wang et al., 2013b; Wang

et al., 2023). In the case of bacteria, one of the

groups most frequently described in marine

habitats is that of the Vibrio genus, which

increases its concentration during the tempera-

ture rise and produces blooms (Mira-Gutiérrez

& García-Martos, 1998). Within the Vibrio

genus, Vibrio alginolyticus (Miyamoto et al.,

1961) is the most abundant and halotolerant

species in temperate marine ecosystems (Mira-

Gutiérrez & García-Martos, 1998).

Several authors around the globe have

reported Vibrio spp. in diseased tissues of

some sea urchin’s species, such as D. africa-

num, Strongylocentrotus intermedius (A. Agas-

siz, 1864), and P. lividus (Becker et al., 2008;

Clemente et al., 2014; Gizzi et al., 2020; Grech

et al., 2022; Salazar-Forero et al., 2022; Shimizu

et al., 1995; Wang, Chang et al., 2013; Wang,

Feng et al., 2013; Wang et al., 2023). However,

there is some controversy because the same

bacteria are isolated from healthy sea urchins,

leading to their classification as opportunistic

rather than primary pathogens. For this rea-

son, it is essential to resort to histopathologi-

cal studies to visualize tissue alterations and

to complement the diagnosis of this disease

(Virwani et al., 2021).

Different protozoan species have been

described in some echinoderms as infection

Objetivo: Este estudio tuvo como finalidad investigar sobre los agentes patógenos que afectan a las poblaciones de

Arbacia lixula y Paracentrotus lividus a lo largo de la costa de la Isla de Gran Canaria (Atlántico Centro-Oriental,

España).

Métodos: El muestreo fue llevado a cabo en la playa de San Cristóbal, al noreste de la isla, dónde los organismos

fueron capturados entre 1-3 metros de profundidad, durante junio, julio y octubre del año 2022. Se tomaron

muestras en la zona interna y externa de la lesión en cada organismo, y se cultivaron en varios medios de cultivo.

Resultados: Fueron identificados ocho agentes patógenos diferentes, incluyendo bacterias y hongos, y sien-

do Vibrio alginolyticus la bacteria más frecuentemente observada en todas las muestras de erizos enfermos.

Además, se observaron protozoarios ciliados dentro de los caparazones, actuando potencialmente como parásitos

oportunistas.

Conclusiones: Esta investigación proporciona una perspectiva única sobre la enfermedad del erizo desnudo

al identificar un número significativo de patógenos asociados, incluida Candida, que no se había reportado

previamente en organismos enfermos. Además, el estudio destaca la presencia de una respuesta inflamatoria

en tejidos con colonias bacterianas, lo que ofrece información crucial para comprender esta enfermedad de los

erizos de mar.

Palabras clave: costas rocosas; Vibrio; mortalidad de erizos de mar; Islas Canarias; Webbnesia.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58993, marzo 2024 (Publicado Mar. 01, 2024)

agents. For example, Hernández et al. (2020)

reported that the mass mortality events of D.

africanum in Madeira and the Canary Islands

were associated with anomalous southwest

storms that resuspended bottom sediment and

favored the appearance of paramoebas pro-

moting paramoebiasis. Also, Scheibling and

Lauzon-Guay (2010) described how the amoe-

bic disease has been producing sea urchin mas-

sive mortalities in the North Atlantic Ocean,

because of intense tropical cyclones near warm

coastlines, which has facilitated the spread of

the disease. Furthermore, Jangoux (1987) in

his echinoderm diseases review described the

presence of the ciliate Orchitophrya stellarum

(Cépède, 1907) which parasites the gonads

of Asterias rubens (Linnaeus, 1758). Finally,

Virwani et al. (2021) reported the presence

of ciliates and encysted metazoan parasites in

diseased test tissues on Tripneustes ventricosus

(Lamarck, 1816) from St. Kitts, Caribbean Sea.

It is crucial to emphasize that certain authors

have associated the increase of pathogen bac-

teria with the rising seawater temperature.

Indeed, the collaborative work of Garrabou et

al. (2022) showed that the increase in seawater

temperature in the Mediterranean Sea between

2015–2019 is the cause behind the mass mortal-

ity of 23 taxa and seven phyla, with the shallow

water echinoderms, distributed between 0 and

10 m depth, included in this list.

In this context, this work aimed to char-

acterize the infection agents and describe the

histopathology and disease observed in Arbacia

lixula and Paracentrotus lividus populations on

the coast of Gran Canaria Island (Northeast

Atlantic, Spain).

MATERIALS AND METHODS

Study area: This study was conducted on

San Cristobal beach, on the northeast coast of

Gran Canaria Island (Canary Islands, Spain;

27º45´N 15º45´W) (Fig. 1). This urban beach

of the capital city of Las Palmas of Gran Canar-

ia, the most populated area of the island, is a

highly anthropogenic coast close to the La Luz

harbor, one of the most important ports in

Fig. 1. San Cristobal beach location, where sea urchins (Paracentrotus lividus and Arbacia lixula) were collected (Gran

Canaria Island, Spain).

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58993, marzo 2024 (Publicado Mar. 01, 2024)

the northwest Africa area because of its great

influence on fish products and goods traffic

of the region.

Field survey: Diseased and apparently

healthy individuals of the sea urchins of Arba-

cia lixula and Paracentrotus lividus were manu-

ally collected between 1 and 3 m depth, with

temperatures over 23 °C, according to data col-

lected by the State Ports Buoy Network, Gov-

ernment of Spain, for the eastern area of Gran

Canaria (Ministerio de Transporte, Movilidad

y Agenda Urbana- Puertos del Estado, 2022).

All individuals were larger than 4 cm in test

diameter and were collected with basic apnea

equipment in June, July, and October 2022.

After being collected, the live sea urchins were

transported to the laboratory in a small box

with seawater.

Additionally, one visual census was carried

out to count the number of complete sea urchin

tests in an area of 30 m2 (two parallel transects

of 15 m2) to estimate test density (Fig. 2A, Fig.

2B); some sea urchins with the presence of ill-

ness marks, and tests suspected that they could

have been broken due to fishing activity or

predation were discarded.

Laboratory: Tissue samples were taken on

the external and internal face of lesions, scrap-

ing the test surface with a sterilized swab, and

in the external and internal face of the healthy

sea urchin. The samples were then placed on

plates with different culture media (Blood agar,

MacConkey agar, Baird Parker and Sabouraud

agar (Pronadisa, Laboratorios Conda, Madrid,

Spain)). The culture plates were incubated at 25

ºC during 7 days of aerobiosis. Strains obtained

Fig. 2. A. Sea urchin tests around the sampling area; B. test of a recently dead sea urchin with areas of the test showing the

presence of disease; C. healthy sea urchins: black sea urchin in the upper part of the image is Arbacia lixula and the two in

the lower area (greenish and purple) are Paracentrotus lividus; D. and H. A. lixula individuals with the presence of external

test damage caused by disease; E. and I. A. lixula organism with the presence of internal test damage caused by the disease;

F. and J. P. lividus individuals with the presence of external test damage caused by the disease; G. and K. P. lividus specimens

with the presence of internal test damage caused by the disease.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58993, marzo 2024 (Publicado Mar. 01, 2024)

from culture were identified through mass

spectrometry, employing MALDI-TOF tech-

nique (Autoflex III, Bruker Daltonics GmbH).

This method is a standard tool in clinical

microbiology due to its rapid and depend-

able microorganism identification capabilities

(Siller-Ruiz et al., 2017), creating a spectrum

based on the protein profile using a complete

database of more than 16 000 strains covering

more than 5 000 species and more than 1 000

genera of marine microorganisms (Bizzini &

Greub, 2010; Croxatto et al., 2012).

Samples of the test, gonad, and tube feet

from diseased and healthy sea urchin were

fixed in formaldehyde (4 %) for 48 hours. Test

samples were decalcified for 5 minutes. After

that, all samples were dehydrated with graded

ethanol and xylene series, and embedded in

paraffin using a routine histological process.

Serial cross sections (4 µm) were made and

stained with Hematoxylin and Eosin (H&E)

and Gram stains. The slides were mounted and

examined with a light microscope (Olympus

BX51TF, Japan).

Analysis: The frequency of appearance

of the infection agent in the organisms was

represented using ggplot2 package (Wickham,

2016) in R v4.2.3 (R Core Team, 2023), and the

map was graphed using QGIS software (QGIS.

org, 2023).

RESULTS

Description of samples: The counting of

192 complete sea urchin tests in 30 m2, resulted

in a density of 3.84 dead sea urchins/m2. In

general, all the complete tests showed marks

associated with diseases (Fig 2A, Fig. 2B).

Overall, the signals of disease in both sea

urchin species were bare test surfaces, without

spines or pedicellaria, and discoloration of the

test in comparison with the healthy calcarean

tissue (Fig. 2D). Additionally, it was observed

that when the disease was advanced, the test in

the affected area was weakened. In the case of

A. lixula, the affected area was in cream color

with brown-reddish zones (Fig. 2H, Fig. 2I)

compared to the blackish color of the healthy

test. For P. lividus, the affected area was in a

greenish color (Fig. 2F, Fig. 2G) compared to

the dark red color of the healthy test. In the

last phases of the disease, lesions resulted in the

perforation of the test (Fig. 2J, Fig. 2K), expos-

ing the coelomic cavity. In addition, the inside

of the injured area was darkened to different

degrees (Fig. 2E, Fig. 2G, Fig. 2I, Fig. 2K).

Microscopically, an inflammatory reaction

composed mainly of coelomocytes and pig-

ment cells, was observed at the edge of the

injured areas from diseased sea urchins (Fig. 3,

inset I). In the affected spines, groups of gram-

negative bacterial colonies (Fig. 4A, Fig. 4B),

were observed. Moreover, ciliate protozoan

(Fig. 4C) inside the sea urchin test and meta-

zoans inside the pedicellaria were found in

affected sea urchins (Fig. 4D). Neither bacterial

colonies nor the presence of parasitic forms

was observed in the apparently healthy sea

urchins collected.

Analysis of infection agents: A total of 17

sea urchins, 13 sick (7 of Arbacia lixula and 6

of Paracentrotus lividus), and four apparently

healthy individuals of both species were sam-

pled. The infection agents vary between species

and health conditions, but Vibrio alginolyticus

was the most frequent bacteria in sick speci-

mens of both species on the internal or external

side of the tests. The other microorganism

which appeared in both species was Candida

sp. Variations among species considering other

infection agents were found: in case of sick A.

lixula, Acinetobacter johnsonni, Pseudomonas

frederiksbergensis and Vibrio myliti were found.

However, on P. lividus we found Vibrio harveyi

and Pseudomonas rhodesiae (Fig. 5). On the

other hand, no infection agents in healthy A.

lixula internal tissues and P. lividus external tis-

sues were found, even though V. alginolyticus

was detected in external tissues of A. lixula.

Comparing the infection agents on sea

urchins reported in the bibliography in dif-

ferent areas of the globe, some authors

describe the presence of Vibrio in samples of

P. lividus, S. intermedius, D. africanum and

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58993, marzo 2024 (Publicado Mar. 01, 2024)

Strongylocentrotus purpuratus, but V. alginolyti-

cus was only reported in an association with D.

africanum and S. purpuratus (Table 1).

DISCUSSION

The present study provides fundamental

pathology data for two species of common sea

urchins in Gran Canaria, P. lividus and A. lixula,

with a particular focus on visually infected indi-

viduals. Test lesions were found to be a preva-

lent feature among reports of urchin diseases,

establishing a description of the morphological

representation of this condition. Diseased sea

urchins present bare surfaces in the test asso-

ciated with tissue necrosis, loss of spines and

tube feet, and some greenish or brownish areas

in the most compromised tissue, features that

have been associated with bald sea urchin dis-

ease (Bauer & Young, 2000; Becker et al., 2008;

Clemente et al., 2014; Dumont et al., 2004;

Hernández et al., 2020; Hughes et al., 1985;

Virwani et al., 2021).

The samples of sick sea urchins collected

in San Cristobal beach were consistent with the

description of bald sea urchin disease. All the

affected organisms exhibited varying degrees of

infection, manifesting the described character-

istics associated with this disease. In the case of

P. lividus, the bald surface had a greenish color

and in A. lixula, it had a brown-reddish color;

in both cases the test presented loss of spines

and tube feet, and in advanced disease condi-

tion, it also included epidermal tissue loss and

perforation of the test.

Fig. 3. Histological test preparation with the general view of the injured area. A. ST: sick tissue, b: bacteria colony, P: non-

affected spine base, I: inflammation area with coelomocytes and pigment cell in the edge of lesion (scale bar = 500 μm); B.

close-up of the area in the box of Fig. 3A, showing inflamed areas with a high concentration of coelomocytes (dark purple

cells) (scale bar = 50 μm).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58993, marzo 2024 (Publicado Mar. 01, 2024)

The presence of protozoans and metazoans

in different tissues has been reported in previ-

ous works (Francis-Floyd, 2020; Grech et al.,

2022), and specifically the presence of amoe-

bas has been described in several works as an

infection agent in sea urchin diseases (Dyková

et al., 2011; Hernández et al., 2020; Jones et al.,

1985; Salazar-Forero et al., 2022; Scheibling &

Lauzon-Guay, 2010). In our study, we found

different protozoa and metazoan species in

diseased sea urchin tests, spines, and tube feet,

while other authors described them just in the

rigid structures (spines and test). According to

Jones et al. (1985), infiltration of protozoan is

frequently observed in the organic matrices of

spines but the notable impacts of the disease

are primarily evident in the spine bases. The

presence of these microorganisms associated

with echinoderms, has been extensively docu-

mented by multiple authors (Jangoux, 1987),

and in some cases, they have been considered

commensal in the gut of sea urchins because

they inhabit the digestive systems of certain

echinoids without causing disease (Grech et

al., 2022). In our samples, we found that these

organisms were proximate to diseased tissues,

suggesting they might function as opportunis-

tic pathogens rather than the primary cause of

the disease.

Considering the presence of bacteria with-

in the lesions, numerous studies have reported

several bacterial species consistent with bald

sea urchin disease; in the Pacific Ocean, Vibrio

genus was reported in S. intermedius sick sea

urchin in Japan and China (Wang, Feng et al.,

2013; Wang et al., 2023). In the Mediterranean

Sea, bacteria were present in lesions of P. l iv i -

dus and A. lixula (Maes & Jangoux, 1984), and

Vibrio genus in P. lividus (Becker et al., 2008;

Grech et al., 2022). In the Canary and Madeira

archipelagos, V. alginolyticus was reported in

affected tissues of D. africanum, A. lixula, and

Fig. 4. Histological test preparation with the presence of pathogen organisms: (A) bacteria colony in the injured spine base,

cross-sections stained with H&E (scale bar = 100 µm); (B) bacteria colony stained with Gram stain, denoting their gram-

negative characterization (red color) (scale bar = 100 µm); (C) Ciliate protozoa inside the test (scale bar = 50 µm); (D)

Metazoan inside the pedicellaria (scale bar = 200 µm).

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58993, marzo 2024 (Publicado Mar. 01, 2024)

P. lividus (Clemente et al., 2014; Gizzi et al.,

2020; Salazar-Forero et al., 2022), and in S.

purpuratus grown in aquariums (Shaw et al.,

2024); this species was frequent in almost all

the samples of healthy and sick individuals in

our study, inside and outside the diseased tis-

sue. Additionally, the second most abundant

bacterial species found both in our study and

in other studies was V. h ar v e y i in P. lividus

samples, which coincides with the finding of

Wang, Feng et al. (2013) in hatcheries in China.

Furthermore, Shaw et al. (2024) reported the

presence of Acinetobacter sp. in S. purpuratus

hatcheries consistent with our findings in dis-

eased tissues of A. lixula. We also found other

pathogen agents in diseased tissues of both spe-

cies (Table 1) that together could be producing

the signal of the disease.

Importantly, while it is true that many of

these bacteria, such as V. algynoliticus and V.

harveyi, can be found in the marine environ-

ment, we can assert that, when present within

the internal region of the diseased tissue, they

serve as contributors to the development of the

disease. Moreover, Shaw et al. (2024) highlight-

ed that diseased sea urchins could be exposed

to great abundance, concentration, or diversity

of opportunistic microorganisms, potentially

intensifying the pathogenic effects.

Our research has effectively established a

histopathology association between the pres-

ence of bacterial colonies in the injured areas

and an accompanying inflammatory response

in the affected tissue. This evidence strongly

suggests that these bacterial colonies could be

the causative agents of the disease.

The presence of V. alginolyticus on the

external tissues of healthy A. lixula is expected

because this is one of the most frequent bacteria

in marine ecosystems. Similarly, the presence of

other unidentified bacteria within the tests of

both sea urchin species is an expected result as

it is widely recognized that the coelomic fluid

of sea urchins harbors a diverse bacterial com-

munity. Indeed, Clemente et al. (2014) report-

ed that in some instances, individuals harbor

pathogens in their coelomic fluid without

exhibiting any outward signs of disease. Even

upon experimental injection with a pathogen-

containing suspension, the individuals did not

contract the disease throughout the duration of

the infection experiments, indicating that the

Fig. 5. Frequency of appearance of the infection agent in Arbacia lixula and Paracentrotus lividus organisms, both healthy

and sick.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58993, marzo 2024 (Publicado Mar. 01, 2024)

Tabl e 1

Comparison between the infectious agents reported in different species of sea urchin.

Author Sampling year Locality Sea urchin species Pathogen agent

Jones et al., (1985) 1982 Nova Scotia Strongylocentrotus

droebachiensi

Paramoeba

Maes and Jangoux

(1984)

1984 Mediterranean Sea and

North Atlantic, France

Echinus esculentus,

Sphaerechinus granularis,

Psammechinus miliaris

Arbacia lixula and

Paracentrotus lividus

Bacterial infection

Shimizu et al., (1995) 1990-1992 Fisheries Breeding

Center, Japan

Strongylocentrotus

intermedius

Vibrio and Aeromonas

Becker et al., (2008) 2006 Atlantic coast, Brittany,

France

Paracentrotus lividus 5 Alphaproctobacteria, 8 Gammaprotobacteria and 1 Fusobacteria.

Some were identified as Vibrio sp., Colwellia sp., Stappia sp.,

Bacteroidetes sp. and Cytophagales sp.

Girard et. al., (2011) 2003 Tenerife, Spain Paracentrotus lividus Bald sea urchin disease related with global climate warming

Dyková et al., (2011) 2010 Tenerife, Spain Diadema africanum Neoparamoeba branchiphila

Wang, Feng et al.

(2013)

2009-2010 Heishijiao

Hatchery, China

Strongylocentrotus

intermedius

Vibrio splendidus, V. shilonii, V. harveyi, Pseudoalteromonas

tetraodonis, Shewanella aquimarina

Clemente et al,

(2014)

2009-2010 Madeira Island

(Portugal) to the Canary

Islands (Spain)

Diadema africanum Vibrio alginolyticus.

Virwani et al. (2021) 2017-2018 St. Kitts, Caribbean Sea Tripneustes ventricosus Ciliates and encysted metazoan parasites

Hernández et al.,

(2020)

Since 2001 Tenerife and La Palma,

Spain

Diadema africanum Paramoeba branquiphila

Gizzi et al., (2020) 2018 Madeira, Portugal Diadema africanum In the coelomic fluid: Aeromonas salmonicida and non-identified

β-hemolítica (gram-negative) bacteria species (as V. alginolyticus)

Grech et al., (2022) 2019 Sardinia (Italy) Paracentrotus lividus Vibrio splendidus, protozoa and metazoan observed too

Salazar-Forero et al.,

(2022)

2020 After Filomena Storm.

Tenerife, Spain

Diadema africanum Neoparamoeba brachiphula, Vexillifera minutissima, Vibrio

alginolyticus

Sphaerechinus granularis Neoparamoeba brachiphila, Vexillifera minutissima

Paracentrotus lividus

Arbacia lixula

Federico et al., (2023) 2019-2020 Napoli (Italy) Paracentrotus lividus Vibrio anguillarum, Aeromonas salmonicida, Tenacibaculum spp.

Wang et al. (2023) 2020 Sea urchin farm in

Weihai, Shandong

Province, China

Strongylocentrotus

intermedius

Vibrio coralliilyticus

Hewson et al., (2023) 2022 Saba (Caribbean

Netherlands) and St.

John (USVI)

Diadema antillarum Philaster spp (ciliate)

Zirler et al., (2023) 2022 Levantine coast of

Greece and Turkey

Diadema setosum Infection agents were not described

Shaw et al., (2024) –Southern California Sea

Urchin

Company (Corona del

Mar, CA)

Strongylocentrotus

purpuratus

Many different pathogenic bacteria, including V. alginolyticus, V.

coralliilyticus, Flexibacter sp., Acinetobacter sp., Tenacibaculum sp.,

Colwellia sp., Flexibacteraceae, Rhodobacterales, Cohaesibacter

gelatinilyticus, Stappia, Psychrobacter,

Staphylococcus, and Saprospiraceae

Our study 2022 Gran Canaria, Spain Arbacia lixula Acinetobacter johnsonii

Pseudomonas frederiksbergensis

Vibrio alginolyticus

Vibrio myliti

Candida

Paracentrotus lividus Pseudomonas rhodesiae

Vibrio alginolyticus

Vibrio harveyi

Candida

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58993, marzo 2024 (Publicado Mar. 01, 2024)

presence of this diversity of bacteria is not nec-

essarily related to the appearance of the disease.

Furthermore, it is important to mention

that in our samples the detected pathogen agent

varied according to the individual despite the

lesions showed having the same characteris-

tics. This result coincides with that reported

by Becker et al. (2008). The diverse symptoms

associated with this disease suggest that pathol-

ogy can vary significantly between individuals,

because of the presence of different oppor-

tunistic infection agents, producing different

levels of the bald sea urchin disease (Shaw et

al., 2023). Finally, the histological work of Beck-

er et al. (2008) revealed that bacteria infect-

ing Paracentrotus lividus test were confined to

the central zone, whereas the peripheral zone

exhibited a high concentration of cells that

function as a barrier and the surrounding tis-

sues remained unaffected, impeding the spread

of the infection.

The presence of Candida in A. lixula and P.

lividus affected surfaces represents a new record

in sea urchins’ infection agents. There is only

one previous work that reports other species of

fungi in sea urchin spines in the Pacific Ocean,

but those fungi were not considered as patho-

gens (Dabrowa et al., 1964). This information

shows a novel perspective on the bald sea

urchin disease, adding new possible pathogens

that cause this disease.

Even with all the infectious agents described

above, it is important to highlight that these

diseases seem to have a multifactorial origin,

influenced by physiological and environmental

factors (temperature variation, adverse factors,

and plankton blooms), and life cycles in trophic

networks (Federico et al., 2023). These adverse

characteristics in the conditions agree with the

season of our study, with the highest tempera-

tures reported in Gran Canaria Island during

2022, and with the reproductive season of the

sea urchin species in the area (Núñez-González

et al., unpublished data). According to what was

described above, the presence of these patho-

genic agents could be inducing the weakening

of the organism. First for the immune system,

but then because of diminished adhesion to

the substrate due to the external lesions and

loss of the tube feet that affect the normal

behavior of the sea urchin (Girard et al., 2011),

and make them prone to being attacked by

predators (Hughes et al., 1985). In addition to

these physiological effects, our study reveals the

presence of an inflammatory response within

the affected tissues where bacterial colonies

are present, providing crucial insight into the

understanding of this sea urchin disease.

In this sense, we highlight the importance

of histopathology as the primary tool for com-

prehending the impact of pathogens, not only

on tissues but also on the overall development

of sea urchins in their natural habitat. The

utilization of histopathology enables a com-

prehensive assessment of the effects caused by

these pathogens.

Finally, the exhaustive review of Feehan &

Scheibling (2014) and Sweet (2020) indicated

that research about disease patterns in marine

key species, such as sea urchins, could be affect-

ed by climate change and other human-induced

pressures, such as pollution and fishing activi-

ties which affect the top-down control exerted

by predators. While the species of the study are

not frequently consumed by the inhabitants

of Gran Canaria Island, they hold significant

value as bait for fishing some species of fish. It is

crucial to enhance our understanding of disease

dynamics in marine ecosystems and recognize

the role that disease plays in driving alterations

within these ecosystems.

The effect of the disappearance of coastal

sea urchins can produce important changes in

ecosystem dynamics, as the case reported by

Sangil & Hernández (2022), where the decrease

in D. africanum population implied a rapid

recovery of non-crustose macroalgae in the

Canary Archipelago. However, the impact of

species’ disappearance in our study remains

unexplored and should be worthy of further

studies. We emphasize the need to continue

monitoring marine species and to gain insight

into the development of these diseases within

marine ecosystems, to provide new methods

for the efficient management and governance

of coastal resources. By doing so, we can

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58993, marzo 2024 (Publicado Mar. 01, 2024)

implement conservation measures to safeguard

these species for future generations.

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

The authors gratefully thank the Govern-

ment of the Canary Islands, for providing the

scientific permit Nº: 168/2020 - Tomo: 1, Libro:

401, Date: 10/06/2020, to collect all the samples

for this study. We also thank Sarah Piaugeard

for helping during the sampling campaigns,

Eleinis Ávila-Lovera for helping us to improve

the manuscript, and Sam C. for helping us cor-

rect English grammar.

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