487

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 000-000, March 2021 (Published Mar. 10, 2021)

Área de Conservación Guanacaste Echinoderms,

North Pacific of Costa Rica

José Leonardo Chacón-Monge

1,2,3

Juan Carlos Azofeifa-Solano

Juan José Alvarado

1,2,3

Jorge Cortés

1,2

1. Centro de Investigación en Ciencias del Mar y Limnología, Universidad de Costa Rica, San Pedro, San José, Costa

Rica; jose.chaconmonge@ucr.ac.cr (*Correspondence), juan.azofeifa@ucr.ac.cr, juan.alvarado@ucr.ac.cr,

jorge.cortes@ucr.ac.cr

2. Escuela de Biología, Universidad de Costa Rica, San Pedro, San José, Costa Rica

3. Centro de Investigación en Biodiversidad y Ecología Tropical, Universidad de Costa Rica, San Pedro, San José,

Costa Rica

Recibido 29-VII-2020. Corregido 20-X-2020. Aceptado 27-X-2020.

ABSTRACT

Introduction: The study of the marine diversity of the North Pacific of Costa Rica began with isolated foreign

expeditions in the 1930s and was systematically developed in the mid-1990s by the Center for Research in

Marine Sciences and Limnology, Universidad de Costa Rica, as consequence there are now a total of 1 479

reported species in this region. Objective: Present an update to the echinoderm richness of the Guanacaste

Conservation Area. Methods: We sampled 25 localities exhaustively and estimated similarity between sites

based on the family richness and environmental heterogeneity. Results: We found 61 taxa, which represent 26

% of the echinoderm reported species for the country’s Pacific coast. Of these, 43 species are new records for

the Guanacaste Conservation Area, and seven for Costa Rica and Central American Pacific coasts. We found

three morpho-species that do not match to available descriptions of the Eastern Tropical Pacific echinoderm

species. We also found the holothuroid Epitomapta tabogae, and the ophiuroid Ophioplocus hancocki, previ-

ously thought endemic to Panama and the Galapagos Islands, respectively. The proximity of the sampled sites

and the redundancy of certain families may explain why we did not find important differences among localities.

Conclusions: The echinoderm richness of this conservation area is at least 20 % higher than previously reported,

reaching similar levels to those in other high diversity sites of the Eastern Tropical Pacific.

Key words: Murciélago Islands; Santa Elena; coastal upwelling; scientific collections; taxonomy; Echinodermata.

Chacón-Monge, J.L., Azofeifa-Solano, J.C., Alvarado,

J.J., & Cortés, J. (2021). Área de Conservación

Guanacaste Echinoderms, North Pacific of Costa

Rica. Revista de Biología Tropical, 69(S1), 487-500.

DOI 10.15517/rbt.v69iSuppl.1.46391

The North Pacific region of Costa Rica is

divided into two conservation areas, managed

by the Ministry of Environment and Energy,

Tempisque and Guanacaste. These two con-

servation areas cover part of the province of

Puntarenas and all of Guanacaste (Alvarado,

Cortés, Esquivel, & Salas, 2012). The Área de

Conservación Guanacaste (ACG), is northern-

most Costa Rica’s protected area and borders

Nicaragua. The ACG marine protected area

comprises 430 km

and 150 km of protected

coastline, and it includes 732 ha of Santa Elena

Bay Management Marine Area, and the Marine

Sector of Guanacaste National Park, including

DOI 10.15517/rbt.v69iSuppl.1.46391

488

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 000-000, March 2021 (Published Mar. 10, 2021)

the archipelago of the Murciélago Islands (Fig.

1). This region is subjected to strong seasonali-

ty, with a dry season that runs from December

to April, a first rainy season from May to June,

and a second from August to October. During

the dry season, the influence of northeast trade

winds increases, causing a seasonal tropical

upwelling, that exposes shallow coastal habi-

tats to cold, nutrient-rich, lower pH, and high

oxygenated waters (Alfaro & Cortés, 2012;

Cortés, Samper-Villarreal & Bernecker, 2014;

Lizano & Alfaro, 2014; Cortés, 2016).

Entirely, ACG is managed as a mega park

and operates as a conservation enterprise (Jan-

zen, 2000; Janzen & Hallwachs, 2016; Janzen

& Hallwachs, 2020). Being a world’s reference

in management as a conservation and restora-

tion area, therein remains the latest relict of

the uninterrupted and protected landscape that

integrates the more endangered and complexes

neotropical habitats (e.g., open ocean, shores,

hard and softs bottoms, rhodolites, algae beds,

and coral reefs, wetlands, mangroves, dry,

rainy and cloud forests) (WHC, 2013; Janzen

& Hallwachs, 2016; Janzen & Hallwachs,

2019). These spatial and biologic connection

becomes a sanctuary at many natural scales

(physics and organics), that engages the deep

sea and surface ocean, salty, and freshwater

systems, that extends from the rugose Pacific

shore and dry forest, to the cloud mountains, at

the Atlantic basin (SINAC, 2013; WHC, 2013;

Janzen & Hallwachs, 2016; Janzen & Hallwa-

chs, 2020). ACG was declared as a UNESCO

World Heritage site, highlighting its geogra-

phic, socio-cultural and biological importance,

in administrating and secure the preservation

of the natural resources, as well as shelter the

genetic diversity to perpetuity (Cortés & Joyce,

2020; Janzen & Hallwachs, 2020).

The management areas of the ACG marine

sector include zones with different protection

status and use categories, as areas for absolute

protection, for public, especial, and sustai-

nable use (SINAC, 2013). There are fishing

regions for semi-industrial and artisanal fishe-

ries (Villalobos-Rojas, Herrera-Correa, Gari-

ta-Alvarado, Clarke & Beita-Jiménez, 2014).

Many beaches, shores, reefs, and islets are

available for tourism, where the main acti-

vities are surfing, beach visitation, snorke-

ling, scuba, and sportfishing activities. Other

areas are oriented to conservation, education,

and or investigation due to their remarkable

attributes and importance to sustain marine

diversity, productivity, and to avoid ecological

Fig. 1. Área de Conservación Guanacaste showing sampling sites. Blue dots represent peninsular

sample sites, whereas the red ones represent archipelago sample sites.

489

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 000-000, March 2021 (Published Mar. 10, 2021)

degradation (SINAC, 2013; Villalobos-Rojas

et al., 2014). Despite that, there are pressures

like overfishing or illegal extraction of species

for aquarium and as for delicatessen (i.e., sea

cucumbers) (Toral-Granda, 2008; Villalobos-

Rojas et al., 2014). Altogether, these conditions

open up opportunities for marine conservation

management, and to establish the framework

for accurate strategies and policies, that should

be regionally implemented in order to maintain

the ecosystemic services and sustainability,

for wild and as well for human communities,

inside and beyond of protected areas (Janzen,

2000; Janzen & Hallwachs, 2016; Janzen &

Hallwachs, 2020).

The study of marine diversity in the ACG

started in the 1930s with zoological speci-

mens’ scientific collection, during international

expeditions (Cortés, 2017). However, it was

not until the mid-1990’s when the Center for

Research in Marine Sciences and Limnology

(CIMAR) of the Universidad de Costa Rica

(UCR) leads the systematic exploration of

marine environments and organisms of ACG

(Cortés, 2017). The BioMar-ACG Project, was

established to increase the knowledge of mari-

ne biodiversity in ACG. Beginning operations

in 2015, with an inter-institutional partnership

between CIMAR, the Museo de Zoología (MZ-

UCR) and the Herbario de Biología (USJ) of

the Universidad de Costa Rica, the Sistema

Nacional de Áreas de Conservación (SINAC),

and the Guanacaste Dry Forest Conservation

Fund (GDFCF) (Cortés & Joyce, 2020). Accor-

ding to the literature, there are 594 species of

marine organisms listed for ACG, of which

crustaceans, mollusks, and cnidarians, are the

richest groups (Cortés, 2017). Until now, only

15 echinoderm species have been included in

scientific publications for ACG (Cortés, 2017).

That compilation does not include ophiuroids,

although its presence is known because of

direct observations at field, samplings, and spe-

cimen collections (Granja-Fernández, Pineda-

Enríquez, Solís-Marín & Laguarda-Figueras,

2020). Is expected that, by redirecting sampling

effort, the improvement in technology, as by

the survey of deeper waters or new habitats, the

echinoderm representativeness in ACG might

increase (Cortés, 2017; Cortés & Joyce, 2020).

Recording and publishing marine biodi-

versity of echinoderms with precise taxono-

mic identifications is necessary to improve

research and management efforts in this Marine

Protected Area, and to properly evaluate the

natural response of anthropogenic impacts on

these ecosystems (Worm et al., 2006; Costello,

Michener, Gahegan, Zhang & Bourne, 2013).

An update of the research and study of echi-

noderms is presented under the BioMar-ACG

Project, to complement the ACG marine bio-

diversity baseline compilation (Cortés, 2017).

The taxonomic affinity of the collection sites

was compared, according to the area that they

belong (peninsula or archipelago), and the affi-

nity between sample sites, based on the family

richness and their environmental heterogeneity

(area, depth, and substrate).

MATERIALS AND METHODS

Sampling: Five field trips (July

2018-August 2019) were carried out to record

the richness of echinoderms in ACG, by scuba

diving. Three of the expeditions visited the

Murciélago Islands archipelago, and two visi-

ted the Santa Elena Peninsula and the surroun-

dings of Cuajiniquil Bay. A total of 25 sample

sites were visited (Fig. 1); 14 in the peninsular

area (P: north of the Santa Elena Peninsula)

and 11 in the archipelago (A: south of the Santa

Elena Peninsula). We recorded geographical

coordinates, depth, and substrate type at each

site (Table 1). The sampling sites were selected

using the criteria and the local knowledge of

the parataxonomists, BioMar-ACG Project’s

crew, and the scientific team. Echinoderms

were collected at each site between, over, and

under different substrates (algae, rocks, corals,

debris, and sand). At least one specimen of each

morpho-species found was collected, as a taxo-

nomic voucher of the site echinoderm richness.

Sample preparation and identification:

Collected specimens were deposited in plastic

containers and transferred in seawater-filled

490

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 000-000, March 2021 (Published Mar. 10, 2021)

buckets to the laboratory, then classified and

separated into groups by locality and taxono-

mic affinity. The organisms were relaxed with

menthol, magnesium chloride, and alcohol

solutions, in trays with filtered seawater. Each

specimen was identified to the lowest possi-

ble taxonomic category, based on specialized

literature for the region (Lessios, 2005; Solís-

Marín, Arriaga-Ochoa, Laguarda-Figueras,

Frontana-Uribe & Durán-González, 2009;

Granja-Fernández et al., 2014; Solís-Marín et

al., 2014; Borrero-Pérez & Vanegas-González,

2019; Granja-Fernández, Pineda-Enríquez,

Solís-Marín & Laguarda-Figueras, 2020) and

TABLE 1

Echinoderm sampling sites of the BioMar-ACG project, North Pacific of Costa Rica

Sector Code Sampling site Substrate Lat. (N) Long.(W)

Archipelago Arc El Arco, Isla San José, Murciélago Islands Boulders 10º51’07” 85º55’03”

BNe Bajo Negro, Murciélago Islands Boulders 10º49’58” 85º53’32”

BPo Bajo Pochote, Isla San José, Murciélago

Islands

Boulders 10º51’22” 85º55’27”

CBP Close to Bajo Pochote, Murciélago Islands Boulders, sand and

gravel bottom

10º51’22” 85º55’24”

Cha Mata de Chagüite, Santa Elena Peninsula Boulders, sand and

gravel bottom

10º52’30” 85º53’19”

ICc Isla Cocinera, Murciélago Islands Rocky reef 10º51’24” 85º54’05”

ICo Isla Colorada, Murciélago Islands Boulders 10º50’16” 85º52’42”

IGo Isla Golondrina, Murciélago Islands

Rocky and Pocillopora

spp. Reef

10º51’18” 85º56’26”

IPe Isla Pelada, Murciélago Islands Boulders 10º52’00” 85º53’54”

ISJ Isla San José, Murciélago Islands Boulders 10º51’10” 85º54’38”

SPe San Pedrito, Murciélago Islands Boulders, sand and

gravel bottom

10º51’16” 85º57’09”

Peninsula 4x4 Playa 4x4, Cuajiniquil Boulders 10º56’09” 85º42’27”

Ace Aceituno, Santa Elena Peninsula Boulders, sand and

gravel bottom

10º53’14” 85º54’23”

BTh Bahía Thomas, Cuajiniquil

Rocky and Pocillopora

spp. Reef

10º55’49” 85º43’16”

Cas Las Cástula, muelle de Cuajiniquil Rocky intertidal zone 10º56’56” 85º42’47”

Far Farallones, Santa Elena Peninsula Boulders, sand and

gravel bottom

10º53’14” 85º56’50”

ICa Isla Los Cabros, Bahía Santa Elena Rocky reef 10º56’29” 85º48’47”

IDa Isla David, Santa Elena Peninsula

Pocillopora spp. Reef

10º57’21” 85º43’30”

IPi Isla Pitahaya; Santa Elena Peninsula Boulders 10º56’08” 85º48’06”

Isl Islita, Cuajiniquil, Santa Elena Peninsula Rocky bottom 10º57’47” 85º41’49”

Mat Matapalito, Santa Elena Peninsula

Pocillopora spp. Reef

10º55’57” 85º47’45”

Mog Mogotes, Isla Negritos, Playa Blanca, Santa

Elena Peninsula

Boulders and sand 10º55’08” 85º53’56”

PBl Punta Blanca, Santa Elena Peninsula Sandy bottom 10º56’44” 85º55’09”

PRo Punta Roja, Santa Elena Peninsula Boulders, sand and

gravel bottom

10º52’30” 86º52’46”

Vit La Vita, Santa Elena Peninsula Boulders 10º53’18” 85º55’08”

491

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 000-000, March 2021 (Published Mar. 10, 2021)

following the taxonomic classification proposed

by WoRMS (http://www.marinespecies.org/).

The samples were tagged by site and mor-

pho-species, with an alphanumeric code. One

specimen of each morpho-species was photo-

graphed and used as a voucher for bar-coding

tissue sample extraction. Samples from all

vouchered specimens were sent to the Center

for Biodiversity Genomics, at the University

of Guelph, for DNA sequencing and barcoding

(Cortés & Joyce, 2020). That could lead us

to build a barcode library (Hebert, Cywinska,

Ball & de Waard, 2003; Janzen & Hallwachs,

2019), and will serve as a reference inventory

and as the start point for many kinds of ecolo-

gical, phylogeographic, systematic, genomic,

and evolutive studies. The samples were cata-

loged and deposited in the Museo de Zoología

(MZ-UCR) of the Centro de Investigación en

Biodiversidad y Ecología Tropical (CIBET),

Universidad de Costa Rica.

Taxonomic and spatial analysis: The

lowest taxonomic hierarchy at which all sam-

ples were identified was to family level. So,

the taxonomic affinity between sites was com-

pared at this level. The family-site similitude

was performed by cluster analysis. And the

sites affinity was compared by a Non-metric

Multidimensional Scaling Analysis (nMDS),

using the geographical area (peninsula or archi-

pelago) as groups, in addition to the family

richness, depth, and substrate type as variables

for the bidimensional model. The variance

of groups and sites was tested with a simple

one-way PERMANOVA, that compares the

spread among groups, using the average values

from the distances of individual observations

to the centroids of their own group, in a cho-

sen measure of dissimilarity (using Jaccard

distances for richness comparison). Assuming

exchangeability, where p-values are calculated

by permutation, avoiding the assumption of

normality, as well as being robust to the hete-

rogeneity of unbalanced designs, and is not

sensitive to differences in correlation structure

among groups (Anderson, 2017). These analy-

zes were performed using Past 3 software.

RESULTS

A total of 497 samples were collected,

distributed in 62 morpho-species, seven for

Asteroidea, 13 for Ophiuroidea, 31 for Holothu-

roidea and 11 for Echinoidea (Table 2). Of

these, three sea cucumber did not correspond to

any species described for the Eastern Tropical

Pacific before. We found a total 43 echinoderm

species that are new records for ACG. Inclu-

ding seven that had not been previously repor-

ted for the Central American Pacific coasts

(Isla del Coco not included) (Table 2, Table 3).

With these new records, the total number of

echinoderm species present on the Pacific coast

of Costa Rica reaches 233, and the total number

of species recorded for the country is now 306

(see Alvarado et al., 2017; Borrero-Pérez &

Vanegas-González, 2019; Cambronero-Solano,

Benavides, Solís-Marín & Alvarado, 2019;

Granja-Fernández, Pineda-Enríquez, Solís-

Marín & Laguarda-Figueras, 2020).

We found 27 echinoderm families, five

of Asteroidea, eight of Ophiuroidea, six of

Holothuroidea and eight of Echinoidea (Table

TABLE 2

Echinoderm records by Class, collected in the BioMar-ACG Project. NR-ACG = new records for the ACG;

NR-CAP = new records for the Central American Pacific (not including Isla del Coco)

Taxa

Number of

individuals

Orders Families Morpho-species

Possible

new species

NR- ACG NR-CAP

Echinodermata 497 12 27 62 3 43 7

Asteroidea 56 1 5 7 0 6 1

Ophiuroidea 159 2 8 13 0 12 1

Holothuroidea 192 4 6 31 3 15 4

Echinoidea 90 5 8 11 0 10 1

492

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 000-000, March 2021 (Published Mar. 10, 2021)

TABLE 3

Echinoderm species by site at ACG, with indication of new records. Bold = new record for the ACG; * = new record

for Costa Rica (without including Isla del Coco); ** = new record for Central America; + = First record outside the

archipelago of the Galápagos Islands; ++ = First record outside Panamá. Sampling sites are presented in Table 1

Taxa Sample site

Class Asteroidea (7 species)

Order Valvatida

Family Acanthasteridae

Acanthaster planci (Linnaeus, 1758) BPo

Family Asteropseidae

Asteropsis carinifera (Lamarck, 1816) Ace; IPy; Ica

Family Mithrodiidae

Mithrodia bradleyi Verrill, 1867* Ace; Arc; ICc; Cha; Ida

Family Oreasteridae

Nidorellia armata (Gray, 1840) Ace; Cas; CBP; Cha. ICa; IPi, ISJ

Pentaceraster cumingi (Gray, 1840)

Ace; Ica

Family Ophidiasteridae

Phataria unifascialis (Gray, 1840) Ace; BTh; CBP; Cha; ICa; ICc; ICo; IGo; IPe;

ISJ; Isl; Mog; PRo; Vit

Pharia pyramidata (Gray, 1840) Ace; BNe; BTh; CBP; ICa; ICc; IGo; IPe; IPi;

Isl; Mog; PBl; Vit

Class Ophiuroidea (13 taxa)

Order Amphilepidida

Family Amphiuridae IPi; ISJ; Mog

Family Ophiactidae

Ophiactis savignyi (Müller & Troschel, 1842) BNe; BPo; BTh; Cha; IGo; IPe; IPi; ISJ

Ophiactis simplex (LeConte, 1851) BNe; IPe; IPi; Isl

Family Ophiolepididae

Ophiolepis pacifica Lütken, 1856 ICa; IPe; Mog; PRo; SPe

Family Ophionereididae

Ophionereis annulata (Le Conte, 1851) 4x4; Ace; Arc; BNe; BPo; ICc; ICo; Cha; IGo;

IPe; IPi; ISJ; Mog; PBl; Vit

Family Hemieuryalidae

Ophioplocus hancocki Ziesenhenne, 1935**+ Cha

Family Ophiotricidae

Ophiothela mirabilis Verrill, 1867 BNe; Cha; Far; ICo; IPe; ISJ; Vit

Ophiothrix (Ophiothrix) spiculata Le Conte, 1851 4x4; Ace; BNe; BPo; BTh; Cas; CBP; Cha;

Far; ICa; ICc; IGo; IPi; Isl; Mat; Mog; PBl;

SPe; Vit

Order Ophiacanthida

Family Ophiocomidae

Ophiocoma aethiops Lütken, 1859 BTh; Cas; CBP; Cha; ICc; IPe; Isl; Mat; Mog;

Vit

Ophiocomella alexandri (Lyman, 1860) 4x4; Arc; BPo; BTh; Cas; Cha; CBP; Far; ICa;

ICc; ICo; IGo; IPe; ISJ; Isl; Mog; PBl; Vit

Family Ophiodermatidae

Ophioderma hendleri Granja-Fernández, Pineda-Enríquez, Solís-Marín &

Laguarda-Figueras, 2020

Arc; ICa; ICc; ICo; Far; IPe; IPi; Vit

Ophioderma panamense Lütken, 1859 BNe; Cas; Cha; ICa; ICc; ICo; IPe; IPi; Isl;

PRo; SPe

493

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 000-000, March 2021 (Published Mar. 10, 2021)

TABLE 3 (Continued)

Taxa Sample site

Ophioderma teres (Lyman, 1860) Ace; BTh; Cha; CBP; Far; ICa; ICc; ICo; IDa;

IPe; IPi; ISJ; PR; SPe

Class Holothuroidea (28 taxa)

Order Apodida

Family Chiridotidae

Chiridota aponocrita Clark, 1920* Ace; BNe; BPo; BTh; ICa; IGo; IPe; IPi;

ISJ; Isl; Mat; Mog; PBl

Family Synaptidae

Epitomapta tabogae Heding, 1928**++ IGo

Euapta godeffroyi (Semper, 1868) IPi; ISJ; Mat

Order Dendrochirotida

Family Cucumariidae

Cucumaria flamma Solís-Marín & Laguarda-Figueras, 1999

Cha; IDa; ICa; IPi; Cas; Arc

Neocucumis veleronis (Deichmann, 1941)

4x4; BTh; Cas; ICa; ICo; IPi; ISJ; Isl; Mat;

Mog; PBl

Pseudocnus californicus (Semper, 1868)

Cas; ICc; ICo; Far; Cha; IPi; ISJ; Isl; Mog;

PBl

Trachythyone peruana (Semper, 1868)* Ica

Family Phyllophoridae

Pentamera chierchiae (Ludwig, 1886)

Ida

Thyone bidentata Deichmann, 1941** Cas

Family Sclerodactylidae

Afrocucumis ovulum (Selenka, 1867)

IPi

Neothyone gibber (Selenka, 1867)

4x4; Ace; BPo; BTh; Cas; Cha; ICa; ICc; ICo;

IDa; IPi; ISJ; Isl;

Mog; PBl; Vit

Order Holothuriida

Family Holothuriidae

Holothuria (Cystipus) rigida (Selenka, 1867)

Ace; BPo; Cha; IPe; IPi

Holothuria (Halodeima) inornata Semper, 1868 4x4; BNe; BTh; Isl; Cas; Mog

Holothuria (Halodeima) kefersteinii (Selenka, 1867)

ICc; ICo; IGo; Isl; Vit

Holothuria (Lessonothuria) pardalis Selenka, 1867 4x4; BTh; BPo; Cas; Cha; ICa; ICo; IGo; IPi;

Isl; Mog; PBl; Pro

Holothuria (Mertensiothuria) hilla Lesson, 1830 BNe; BPo; CBP;

Holothuria (Mertensiothuria) viridiaurantia Borrero-Pérez &

Vanegas-González, 2019**

Ace; IPi; Mog

Holothuria (Platyperona) difficilis Semper, 1868 ICa; Ida

Holothuria (Selenkothuria) lubrica Selenka, 1867

4x4; Cas

Holothuria (Selenkothuria) portovallartensis Caso, 1954 4x4; Cas; Isl

Holothuria (Semperothuria) languens Selenka, 1867

IPi; Isl; PBl

Holothuria (Stauropora) pluricuriosa Deichmann, 1937 BPo; CBP; Ica

Holothuria (Thymiosycia) arenicola Semper, 1868

Ace; BNe; BPo; Cas; IGo; IPe; ISJ; Mog;

PRo; SPe

Holothuria (Thymiosycia) impatiens (Forsskål, 1775)

BNe; ICc; ICo; IPe; IPi; ISJ; Isl; Mat; PBl; Vit

Labidodemas americanum Deichmann, 1938 ICa; ICo

Labidodemas maccullochi (Deichmann, 1958) BNe; IGo; ISJ

Order Synallactida

Family Stichopodidae** CBP

Isostichopus fuscus (Ludwig, 1875) Cha; ICa; IDa; IGo; IPi; ISJ

494

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 000-000, March 2021 (Published Mar. 10, 2021)

2). Although there are some associations bet-

ween peninsular or archipelago influence sites

(R = 0.82), the taxonomic affinity at the family

level was not determined by the geographical

area. The clusters are heterogeneous, com-

paring the family richness among sites by

sector (Fig. 2). The spatial distribution of the

localities according to their taxonomic affinity

and environmental heterogeneity, also did not

reflect discrete clusters regarding the influen-

ce of the geographical area (PERMANOVA

p > 0.05, Fig. 3).

Isla David and Punta Roja showed less simi-

larity to other sample sites (Fig. 2). They pre-

sent seven and six families respectively, some

of them are rare for other localities (Mithrodii-

dae, Phyllophoridae, Stichopodidae and Cucu-

mariidae on Isla David; Ophiolepididae and

Loveniidae at Punta Roja), in combination with

widely distributed families (Ophiodermatidae,

Ophidiasteridae, Holothuriidae, Sclerodac-

tylidae) (Table 3). Another locality separated

from the rest is Farallones (Fig. 2), presenting

a particular family composition, some com-

mon in the peninsula sector and others in the

archipelago (Ophiotrichidae, Ophiodermatidae,

Ophiocomidae, Arbaciidae, and Brissidae).

Localities with greater similarity by pairs in the

peninsular sector (Pitahaya Island-Los Cabros

Island; Punta Blanca-Mogotes) have a large

number of families, some rare (Asteropseidae,

Amphiuridae, Cucumariidae, Stichopodidae,

Synaptidae, Prenasteridae and Oreasteridae in

the first peninsular pair; Amphiuridae, Ophio-

lepididae, and Cucumariidae; in the second

peninsular pair) in combination with other ones

TABLE 3 (Continued)

Taxa Sample site

Class Echinoidea (11 species)

Order Arbacioida

Family Arbaciidae

Arbacia stellata (Blainville, 1825; ?Gmelin, 1791) 4x4; Ace; BTh; Far; ICa; ICo; IPi; Mat

Order Camarodonta

Family Echinometridae

Echinometra vanbrunti A. Agassiz, 1863

4x4; BTh; Cas; ICc

Family Toxopneustidae

Toxopneustes roseus (A. Agassiz, 1863) Ace; BTh; Cas; CBP; Cha; ICa; ICc; IGo; IPi;

ISJ; Mog; PBl; Vit

Tripneustes depressus A. Agassiz, 1863 Ace; Cas; Cha

Order Cidaroida

Family Cidaridae

Eucidaris thouarsii (L. Agassiz & Desor, 1846) 4X4; Ace; BNe; BPo; BTh; Cas; CBP; Cha;

ICo; IGo; IPe; ISJ; Isl; Mat; Mog; PBl; Vit;

Order Diadematoida

Family Diadematidae

Astropyga pulvinata (Lamarck, 1816) Ace; CBP; Cha

Diadema mexicanum A. Agassiz, 1863 Ace; BTh; CBP; Cha; IPe; Mat; Mog

Order Spatangoida

Family Prenasteridae

Agassizia scrobiculata Valenciennes, 1846 BPo; IPi; Vit

Family Brissidae

Brissus obesus Verrill, 1867 BPo; CBP; ICa; ICc; IPe; IPi; ISJ; Mog; SPe;

Vit

Meoma ventricosa (Lamarck, 1816) Cha; CBP; Far; IGo; SPe

Family Loveniidae

Lovenia cordiformis A. Agassiz, 1872* Ace; CBP; IGo; Pro

495

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 000-000, March 2021 (Published Mar. 10, 2021)

Fig. 3. Non-metric Multidimensional Scaling Analysis for echinoderm family richness and habitat heterogeneity

at ACG. Based on Jaccard’s distance. Stress level of 0.18. Blue dots represent peninsular sample sites, whereas the red ones

represent archipelago sample sites.

Fig. 2. Echinoderm family richness at ACG cluster. Based on Jaccard’s index. R = 0.82. Blue codes represent peninsular

sample sites, whereas the red ones represent archipelago sample sites.

496

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 000-000, March 2021 (Published Mar. 10, 2021)

common (Table 3). The most similar sites in

the archipelago (Isla Pelada-Bajo Negro) pre-

sent a widely-distributed families in the ACG

(Table 1, Fig. 2).

DISCUSSION

The 15 echinoderm species previously

reported for the ACG (Cortés, 2017), represent

only 6% of the 226 known species for the Paci-

fic of Costa Rica (Alvarado et al., 2017). Two

of those, were not collected in our research,

the holothuroids Pseudocnus dubiosus and

Neothyone gibbosa. The presence of crinoids

in the region is still unknown, and possibly

they could be found in deeper waters near to

the continental slope that is very close to the

coast, in the area of the Mesoamerican trench

(Cortés, 2017). We found species in ACG that

have not been registered for any other coastal

locality in Costa Rica, as the sea star Mithrodia

bradleyi, and the irregular sea urchin Love-

nia cordiformis, that are also present at Isla

del Coco (Cortés, 2012). The sea cucumber

Trachythyone peruana is a new record for the

Costa Rican Pacific waters, while Chiridota

aponocrita, Thyone bidentata, and Epitomap-

ta tabogae (until now considered endemic to

Panama) are first recorded for the Central Ame-

rican mainland Pacific coasts. We also confirm

the presence of the recently described species

Holothuria (Mertensiothuria) viridiaurantia,

and Ophioderma hendleri for the ACG (Borre-

ro-Pérez & Vanegas-González, 2019; Granja-

Fernández, Pineda-Enríquez, Solís-Marín &

Laguarda-Figueras, 2020).

There is a specimen belonging to the

family Stichopodidae that does not correspond

to any known species in the region (Solís-

Marín et al., 2009). Externally, the orange

bivium is spotted whit irregular (small and

large) dark areas of pointed papillae and white

little spots on the tegument surface, in the tri-

vium the texture is smooth and the coloration

is pale cream, whit dark pelted oral tentacles

oriented to the substrate. The skin is thick and

soft, the body length is up to 30 cm, and the

maximum diameter is near to 10 cm in the

mid-posterior body region. The ossicles of the

dermic wall are mainly tables and bars, whit

some “C” and “S” bodies widely disperse. This

specimen had ten pearlfish (Carapidae) inside

its cloaca, which got out when their host died.

We speculate that when the water O

concen-

tration of its container dropped to hypoxia, the

stressed fish got outside.

Two other morpho-species of the family

Holothuriidae, have a combination of tables,

buttons, and perforated plaques that do not

match whit the ossicles for reported species.

One of them has a homogeneous white color

whit disperse minute yellow dots over the

bivium, as well on the tip of their podia, at

trivium. The top of the pelted oral tentacles

was yellow too. The skin is rugose, nor thin or

thick, and has neither kind of distinguishable

ossicle on dermic tissue samples. The total

length of this animal was 2 cm approx. Other

holothurid morpho-species have a combination

of characters, including light or dark green-

brown tegument surface, whit yellowish pelted

oral tentacles and projected podia on the tri-

vium, at bivium surface the skin has a rugose

appearance, the length is up to 5 cm and close

to 2 cm wide, by ossicle comparison we were

not able to distinguish between them and other

Holothuria spp.

Finally, the discovery of Ophioplocus han-

cocki in ACG extents the distribution range to

this species. Collected during the Allan Han-

cock expeditions (1933 and 1934) and thought

to be endemic for the Galápagos Islands (Zies-

enhenne, 1940; Maluf, 1991). Currently, there

are three specimens in the Smithsonian’s Natio-

nal Museum of Natural History, a holotype, and

two vouchers (https://collections.nmnh.si.edu/

search/iz/?q=qn+Ophioplocus+hancocki). In

addition to a paratype and seven vouchers

at the Museum of Comparative Zoology at

Harvard University (https://mczbase.mcz.har-

vard.edu/SpecimenResults.cfm?taxon_name_

id=446882). So, the specimen collected during

the expeditions of the BioMar-ACG Project

constitutes the twelfth specimen recorded in

scientific collections for this species.

497

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 000-000, March 2021 (Published Mar. 10, 2021)

As found for other groups of marine orga-

nisms studied in the BioMar-ACG Project,

echinoderms richness has been underestimated

(Vargas-Castillo & Cortés, 2019; Cortés &

Joyce, 2020). When compared to other marine

areas of Costa Rica, like the Osa Peninsula and

Isla del Coco, the ACG Marine Sector registe-

red a low echinoderm mean diversity (Alvara-

do et al., 2017). The research efforts carried out

by the BioMar-ACG project release an update

of 1. 479 marine species, a richness compa-

rable to other highly rich, but more extensive

regions of the Eastern Tropical Pacific (Cortés

& Joyce, 2020). That could be explained by

the high environmental heterogeneity on the

rugged littoral structure and the seasonal upwe-

lling in the region, which increases primary

productivity and together may increase the

chance to support a higher species richness and

densities (Cortés, 2014; Cortés & Joyce, 2020).

This work demonstrates that the effort and

sampling techniques employed determine the

knowledge and the interpretations made on the

echinoderm diversity of ACG. The taxonomic

echinoderm richness of ACG, increased by 20

%. So, we want to highlight the importance

of taxonomic baseline studies, as well as the

importance to support and publish their results.

Which combined with the appropriate tools

and technologies, could help us to understand

the true diversity of our oceans, the opportuni-

ties to legislate them, and the risks of do not.

Now, we know that this area presents at least

26 % of the echinoderm species listed for the

Costa Rican Pacific (Solís-Marín et al., 2013

Alvarado et al., 2017). And several species that

have not been found in any other location in

the Central American Pacific. Defining itself

as a site of great importance for echinoderm

and other marine taxa conservation (Cortés,

2017; Vargas-Castillo & Cortés, 2019; Cortés

& Joyce, 2020).

Despite some families were exclusively

present in one or few sites of the peninsular

or the archipelago sectors, the sampled sites

were not discretely distributed in the cluster

ordination or in the Non-metric Multidimen-

sional Scaling Analysis. Possibly, due to the

taxonomic hierarchy used for the construc-

tion of the model, as well as the quantity and

variability of the environmental factors used.

Since many of the substrates were redundant,

and the depths between sites were similar,

as reflected in the PERMANOVA test. Some

research shows that the geographic and tem-

poral scale, as well as the number of varia-

bles, and taxonomic resolution are usually

decisive in solving the distribution patterns

affinities (de Entrambasaguas, 2008; Iken et

al., 2010; Alvarado, Guzmán & Breedy, 2012;

Ramírez-Ortiz et al., 2017).

There are echinoderm families with wide

distribution, throughout the Eastern Tropical

Pacific (Pérez-Ruzafa et al., 2013; Solís-Marín

et al., 2013; Lessios & Baums, 2017). Similar

observations of distribution patterns on echi-

noderms as in other taxonomic groups, have

been documented even at larger spatial scales

(Glynn & Ault, 2000; Lessios & Robertson,

2006; Hellberg, 2009; Duda & Lessios, 2009;

Lessios & Baums, 2017). For example, when

latitude decreases, the richness decreases and

the abundance of observed species increase

(decrease in alpha diversity and increase in beta

diversity), a generalized biogeographic phe-

nomenon in tropical regions, which is usually

associated with climatic stability and habitat

heterogeneity, that tends to homogenize rich-

ness (Iken et al., 2010; González-Gándara et

al., 2015; Mutschke, Gerdes & Ríos, 2017).

Although most of the observed echino-

derm families may have planktotrophic larvae,

that are able to cross long distances by marine

currents and drift (Smith, 1997; Raff & Byrne,

2006), some species may possibly be restricted

by their reproductive strategy and/or its dis-

persal ability (i.e., O. hancocki, H. lubrica, H.

portovallartensis) (Maluf, 1991; Solís-Marín et

al., 2013). So, increasing the resolution of taxo-

nomic hierarchies at the species level, as well

as the inclusion of functional traits, and genetic

analysis could perform our understanding of the

echinoderm patterns distribution, habitat use,

and dispersal limitation. These data, combined

with those from other taxa (corals, mollusks,

crustacean, fishes, etc.) adequately interpreted

498

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 000-000, March 2021 (Published Mar. 10, 2021)

and truly used, could lead us to establish cri-

teria in decision-making for the management,

conservation, and use of natural resources in

the Marine Sector of Área de Conservación

Guanacaste, in order to maintain the health

of the marine ecosystems, and their resilience

to global change and anthropogenic impacts

in the area (Janzen, 2000; Cortés & Joyce,

2020; Janzen & Hallwachs, 2020). We strongly

recommend continuing the research effort on

echinoderms in ACG, especially towards new

sample sites and deeper waters.

Ethical statement: authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we

followed all pertinent ethical and legal proce-

dures and requirements. All financial sources

are fully and clearly stated in the acknowled-

gements section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We thank Frank Joyce, Yelba Vega, Gilber-

th Ampié, Minor Lara, Anibal Lara, Carolina

Sheridan-Rodríguez, Cristian Mora-Barboza,

and Génesis Coto for their support during sam-

pling. We are thankful to Juan Ignacio Abarca-

Odio for his advice on statistical analysis. We

are grateful to Rebeca Granja-Fernández and

Francisco Solís-Marín for their comments on

our results. We thank the park rangers of the

Isla San José station at Murciélago Islands for

their support in the expeditions. This study was

possible due to the support of the Center for

Research in Marine Sciences and Limnology

(CIMAR), Museo de Zoología (MZ-UCR),

and Escuela de Biología of the Universidad

de Costa Rica. The BioMar-ACG project was

funded by the Guanacaste Dry Forest Conser-

vation Fund (GDFCF). Sampling permits were

granted by the National System of Conserva-

tion Areas (SINAC). We are very thankful to

the Iberoamerican Network of Echinoderms

and the organizing team of the 4th Latin Ame-

rican Congress on Echinoderms. Finally, we

thank three anonymous scientific revisors of

our manuscript and to the scientific editors of

the supplement.

RESUMEN

Equinodermos del Área de Conservación Guanacaste,

Pacífico Norte de Costa Rica

Introducción: El estudio de la diversidad marina

del Pacífico Norte de Costa Rica inició con expediciones

extranjeras aisladas en la década de 1930, y fue desarro-

llado sistemáticamente a mediados de la década de 1990

por el Centro de Investigaciones en Ciencias del Mar y

Limnología de la Universidad de Costa Rica, como con-

secuencia ahora se reporta un total de 1 479 especies en

esta región. Objetivo: Presentar una actualización de la

riqueza de equinodermos del Área de Conservación Guana-

caste. Métodos: Realizamos muestreos exhaustivos en 25

localidades y estimamos la similitud entre sitios con base

en la riqueaza de familias y la heterogeneidad ambiental.

Resultados: Encontramos 61 taxa, que representan el 26%

de las especies reportadas para la costa pacífica del país.

De estas, 43 especies son nuevos registros para el Área de

Conservación Guanacaste y siete para las costas de Costa

Rica y el Pacífico centroamericano. Tres morfoespecies no

coinciden con las descripciones disponibles para las espe-

cies del Pacífico Tropical Oriental. Por último, hallamos un

ejemplar del holoturoideo Epitomapta tabogae y otro del

ofiuroideo Ophioplocus hancocki, considerados endémicos

para Panamá y las Islas Galápagos respectivamente. La

proximidad entre los sitios muestreados y la redundancia

de ciertas familias pueden explicar por qué no se encon-

traron diferencias entre las localidades. Conclusiones:

La riqueza de equinodermos de esta área de conservación

es al menos 20% mayor que la reportada anteriormente,

alcanzando niveles similares a los de otros sitios de alta

diversidad del Pacífico Tropical Oriental.

Palabras clave: Islas Murciélago; Santa Elena; aflo-

ramiento costero; colecciones científicas; taxonomía;

Echinodermata.

REFERENCES

Alfaro, E.J. & Cortés, J. (2012). Atmospheric forcing of

cold subsurface water events in Bahía Culebra, Costa

Rica. Revista de Biología Tropical, 60(Suppl. 2),

173-186.

Alvarado, J.J., Guzmán. H. & Breedy, O. (2012). Distri-

bution and diversity of echinoderms (Asteroidea,

Echinoidea, Holothuroidea) in the islands of the Gulf

of Chiriqui, Panama. Revista de Biología Marina y

Oceanografía, 47(1), 13-22.

499

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 000-000, March 2021 (Published Mar. 10, 2021)

Alvarado, J.J., Chacón-Monge, J.L., Solís-Marín, F.A.,

Pineda-Enríquez, T., Caballero-Ochoa, A.A., Solano

Rivera, S., & Romero Chaves, R. (2017). Equino-

dermos del Museo de Zoología de la Universidad de

Costa Rica. Revista de Biología Tropical, 65(Supl.

1), 272-287.

Alvarado, J.J., Cortés, J., Esquivel, M.F. & Salas, E.

(2012). Costa Rica’s Marine Protected Areas: status

and perspectives. Revista de Biología Tropical, 60

(1), 129-142.

Anderson, M. (2017). Permutational Multivariate Analysis

of Variance (PERMANOVA). In: Balakrishnan, N.,

Colton, T., Everitt, B., Piegorsch, W., Ruggeri, F. &

Teugels, J. (Eds.), Wiley StatsRef: Statistics Reference

Online, 1-15.

Borrero-Pérez, G.H. & Vanegas-González, M.J. (2019).

Holothuria (Mertensiothuria) viridiaurantia sp. nov.

(Holothuriida, Holothuriidae), a new sea cucumber

from the Eastern Pacific Ocean revealed by morpho-

logy and DNA barcoding. ZooKeys, 893, 1-19.

Cambronero-Solano, S., Benavides, R., Solís-Marín. F.A.

& Alvarado, J.J. (2019). New reports of echinoderms

on the Caribbean continental slope of Central Ameri-

ca. Zoosymposia, 15, 5–12.

Cortés, J. (2012). Marine biodiversity of an Eastern Tropi-

cal Pacific oceanic island, Isla del Coco, Costa Rica.

Revista de Biología Tropical, 60(Suppl. 3), 131-185.

Cortés, J. (2016). The Pacific coastal and marine ecosys-

tems. In M. Kappelle (Ed.), Costa Rican Ecosystems

(pp. 97-138). Chicago and London: University of

Chicago Press.

Cortés, J. (2017). Marine biodiversity baseline for Área

de Conservación Guanacaste, Costa Rica: published

records. ZooKeys, 652, 129-179.

Cortés,

J. & Joyce, F. (2020). BioMar-ACG: A successful

partnership to inventory and promulgate marine bio-

diversity. Biotropica, 52, 1104-1107. DOI: 10.1111/

btp.12841.

Cortés, J., Samper-Villarreal, J. & Bernecker, A. (2014).

Seasonal phenology of Sargassum liebmannii J.

Agardh (Fucales, Heterokontophyta) in an upwelling

area of the Eastern Tropical Pacific. Aquatic Botany,

119, 105-110.

Costello, M.J., Michener, W. K., Gahegan, M., Zhang, Z.Q.

& Bourne, P.E. (2013). Biodiversity data should be

published, cited, and peer reviewed. Trends in Ecolo-

gy & Evolution, 28, 454-461.

de Entrambasaguas, M.L. (2008). Estudio faunístico y

ecológico de los equinodermos del archipiélago de

Cabo Verde (Doctoral dissertation). Universidad de

Murcia, Spain.

Duda, T.F. & Lessios, H.A. (2009). Connectivity of popu-

lations within and between major biogeographic

regions of the tropical Pacific in Conus ebraeus,

a widespread marine gastropod. Coral Reefs, 28,

651-659.

González-Gándara, C., Solís-Marín, F.A. de la Cruz-

Francisco V., Granados-Barba, A., Salas-Pérez, J.J.,

Argüelles-Jiménez J. & Escárcega-Quiroga, P. A.

(2015). Riqueza y distribución de equinodermos en

los arrecifes del norte de Veracruz, México. Revista

de Biología Tropical, 63(2), 183-193.

Granja-Fernández, R., Herrero-Pérezrul, M., López-Pérez,

R., Hernández, L., Rodríguez-Zaragoza, F., Wallace

Jones, R. & Pineda-López, R. (2014). Ophiuroidea

(Echinodermata) from coral reefs in the Mexican

Pacific. ZooKeys, 406, 101-145.

Granja-Fernández, R., Pineda-Enríquez, T., Solís-Marín,

F.A. & Laguarda-Figueras, A. (2020). Ophioder-

ma hendleri sp. nov. (Echinodermata: Ophiuroidea:

Ophiodermatidae) and its congeners from the Eastern

Pacific. European Journal of Taxonomy 729: 11–41.

Glynn, P.W. & Ault, J.S. (2000). A biogeographic analysis

and review of the far eastern Pacific coral reef region.

Coral Reefs, 19, 1-23.

Hebert, P.D.N., Cywinska, A., Ball, S. L. & deWaard, J. R.

(2003). Biological identifications through DNA bar-

codes. Proceedings of the Royal Society of London.

Series B: Biological Sciences, 270, 313–321.

Hellberg, M.E. (2009). Gene flow and isolation among

populations of marine animals. Annual Review of

Ecology, Evolution, and Systematics, 40, 291-310.

Iken, K., Konar, B., Benedetti-Cecchi, L., Cruz-Motta, J.J.,

Knowlton, A., Pohle, G., . . . Silva, A. (2010). Large-

scale spatial distribution patterns of echinoderms in

nearshore rocky habitats. PLoS ONE, 5(11), e13845.

Janzen, D.H. (2000). Costa Rica’s Area de Conservación

Guanacaste: a long march to survival through non-

damaging biodevelopment. Biodiversity, 1(2):7-20.

Janzen, D.H. & Hallwachs, W. (2016). Biodiversity con-

servation history and future in Costa Rica: The

case of area de Conservación Guanacaste (ACG).

Chapter 10. In C. R. Ecosystems & M. Kappelle

(Eds.), Biodiversity conservation history and future

in Costa Rica (pp. 290–341). Chicago, IL: University

of Chicago Press.

Janzen, D.H. & Hallwachs, W. (2019). How a tropical cou-

ntry can DNA barcode itself. iBOL Barcode Bulletin,

9(1), 1-6.

Janzen, D.H. & Hallwachs, W. (2020). Área de Conser-

vación Guanacaste, northwestern Costa Rica: Con-

verting a tropical national park to conservation via

biodevelopment. Biotropica, 52, 1017-1029.

Lessios, H.A. (2005). Echinoids of the Pacific waters

of Panama: Status of knowledge and new records.

Revista de Biología Tropical, 53(3), 147-170.

500

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 000-000, March 2021 (Published Mar. 10, 2021)

Lessios, H.A. & Baums, I.B. (2017). Gene flow in coral

reef organisms of the Tropical Eastern Pacific. In

Glynn, P., Mazello, D. & Enochs, I. (Eds.), Coral

Reefs of the Eastern Tropical Pacific: Persistence

and Loss in a Dynamic Environment (pp. 477-499).

Netherlands: Springer-Verlag.

Lessios, H.A. & Robertson, D.R. (2006). Crossing the

impassable: genetic connections in 20 reef fishes

across the eastern Pacific barrier. Proceedings of

the Royal Society B: Biological Sciences, 273,

2201-2208.

Lizano, O. G. & Alfaro, E. J. (2014). Características de la

dinámica atmosférica y oceánica en algunas regio-

nes del Área de Conservación Guanacaste (ACG),

Costa Rica. Revista de Biología Tropical, 62(Supl.

4), 17-31.

Maluf, L.Y. (1991). Echinoderm fauna of the Galápagos

Islands. In M. James (Ed.), Galápagos Marine Inver-

tebrates (pp. 345-367). New York, USA: Springer

Science, Business Media.

MCZbase. (2020). The Database of the Zoological Collec-

tions Museum of Comparative Zoology - Harvard

University. Available from https://mczbase.mcz.

harvard.edu/SpecimenResults.cfm?taxon_name_

id=446882. Accessed 2020-07-13.

Mutschke, E., Gerdes, D. & Ríos, C. (2017). Distribution

and abundance patterns of echinoderms in the fjord

and channel complex from a subantarctic north

Patagonian Ice field, Magellan region. Revista de

Biología Tropical, 65(1), 60-72.

Pérez-Ruzafa, A., Alvarado, J.J., Solís-Marín, F.A., Her-

nández, J.C., Morata, A., Marcos, C., . . . Williams,

S.M. (2013). Latin America echinoderm biodiversity

and biogeography: Patterns and affinities. In J.J.

Alvarado & F.A. Solís-Marín (Eds.), Echinoderm

Research and Diversity in Latin America (pp. 511

-542). Berlin: Springer Heidelberg.

Raff, R. & Byrne, M. (2006). The active evolutionary lives

of echinoderm larvae. Heredity, 97, 244-252.

Ramírez-Ortiz, G., Calderón-Aguilera, L.E., Reyes-Boni-

lla, H., Ayala-Bocos, A., Hernández, L., Rivera-Melo,

F.F., . . . Dominici-Arosamena, A. (2017). Functional

diversity of fish and invertebrates in coral and rocky

reefs of the Eastern Tropical Pacific. Marine Ecology,

38, e12447.

SINAC (Sistema Nacional de Áreas de Conservación).

2013. Plan de Manejo Área de Conservación Guana-

caste 2014-2024. ACG. Guanacaste. 149 p.

Smith, A. (1997). Echinoderm larvae and phylogeny.

Annual Review of Ecology, Evolution, and Systema-

tics, 2, 219-241.

Smithsonian Institution. (2020). Smithsonian Natio-

nal Museum of Natural History. Available

from https://collections.nmnh.si.edu/search/

iz/?q=qn+Ophioplocus+hancocki. Accessed

2020-07-13.

Solís-Marín, F.A., Alvarado, J.J., Abreu-Pérez, M., Aguile-

ra, O., Alió, J., Bacallado-Aránega, J.J., . . . Williams,

S.M. (2013). Appendix. In J.J. Alvarado & F.A.

Solís-Marín (Eds.), Echinoderm Research and Diver-

sity in Latin America (pp. 543-654). Berlin: Springer

Heidelberg.

Solís-Marín, F.A., Arriaga-Ochoa, J.A., Laguarda-Figue-

ras, A., Frontana-Uribe, S.C. & Durán-González, A.

(2009). Holothuroideos (Echinodermata: Holothu-

roidea) del Golfo de California, México. México:

Comisión Nacional para el Conocimiento y Uso de

la Biodiversidad e Instituto de Ciencias del Mar y

Limnología, UNAM.

Solís-Marín, F.A., Laguarda-Figueras, A., Estrada-Rodrí-

guez, P., Honey-Escandón, M., Cao-Romero, C. &

Durán-Gonzáles, A. (2014). Los asteroideos (Echi-

nodermata: Asteroidea) del Golfo de California,

México. México: UNAM), Instituto de Ciencias del

Mar y Limnología, Secretaría de Medio Ambiente y

Recursos Naturales e Instituto Nacional de Ecología

y Cambio Climático.

Toral-Granda, V. (2008). Population status, fisheries and

trade of sea cucumbers in Latin America and the

Caribbean In: Toral-Granda, V., Lovatelli, A. &

Vasconcellos, M. (Eds.). Sea Cucumbers. A Global

Review of Fisheries and Trade (pp. 213-229). Roma:

FAO Fisheries and Aquaculture Technical Paper

No. 516.

Vargas-Castillo, R. & Cortés, J. (2019). New records of

marine decapods and stomatopods in Área de Conser-

vación Guanacaste (ACG): four years of marine bio-

diversity inventorying. Marine Biodiversity Records,

12(1), 1-8.

Villalobos-Rojas, F., Herrera-Correa, J. Garita-Alvarado,

C., Clarke, T. & Beita-Jiménez, A. (2014). Activi-

dades pesqueras dependientes de la ictiofauna en el

Pacífico Norte de Costa Rica. Revista de Biología

Tropical, 62 (Supl. 4), 119-138.

World Heritage Committee. (2013). Thirty seventh session.

WHC-13/37.COM/8E: Adoption of retrospective Sta-

tements of Outstanding Universal Value, UNESCO.

302 p.

Worm, B., Barbier, E.B., Beaumont, N., Duffy, J.E., Folke,

C., Halpern, B.S., Jackson, J.B.C., . . . Watson, R.

(2006). Impacts of biodiversity loss on ocean ecosys-

tem services. Science 314: 787–790.

WoRMS Editorial Board (2020). World Register of Marine

Species. Available from http://www.marinespecies.

org at VLIZ. Accessed 2020-07-13.

Ziesenhenne, F.C. (1940). New ophiurans of the Allan

Hancock Pacific Expeditions. Allan Hancock Pacific

Expeditions, 8(2), 9-59.