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New hosts and morphological data for the Star pearlfish

Carapus mourlani (Ophidiiformes: Carapidae) from collections

made in the North Pacific coast of Costa Rica

José Leonardo Chacón-Monge

1,2

; https://orcid.org/0000-0002-9754-1254

Arturo Angulo

1,2

; https://orcid.org/0000-0002-4587-1446

Jorge Cortés

1,2

; https://orcid.org/0000-0001-7004-8649

1. Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Universidad de Costa Rica, 11501-2060, San

José, Costa Rica; jose.chaconmonge@ucr.ac.cr, arturo.angs@gmail.com, jorge.cortes@ucr.ac.cr

2. Museo de Zoología, Centro de Investigación en Biodiversidad y Ecología Tropical (CIBET), Universidad de Costa

Rica, 11501-2060, San José, Costa Rica.

Recibido 30-I-2021. Revisado 19-III-2021. Aceptado 30-V-2021.

ABSTRACT

Introduction: The family Carapidae includes about 40 species of marine fishes distributed in coastal habitats

worldwide. The family includes some free-living species, however, most of them are found as commensal inqui-

lines or parasites of marine invertebrates, including several echinoderm species. In the Eastern Tropical Pacific,

the biology and host use of the representatives of the Carapidae is relatively poorly known.

Objective: The present study reports the occurrence of the Star pearlfish Carapus mourlani within three previ-

ously unknown hosts in the region: the sea stars Nidorellia armata, Phataria unifascialis, and the sea cucumber

Stichopus horrens. Some ecological implications and considerations regarding such symbiotic relationships

are raised and discussed. Additional morphometric and meristic data for the fish and the echinoderms are also

provided and discussed.

Methods: Echinoderms were collected, from 25 localities along the North Pacific coast of Costa Rica, and

were carefully examined searching for commensal/parasitic fishes. Echinoderms and fishes were identified and

characterized in accordance with the specialized literature.

Results: A total of 497 echinoderms, including about 60 species, were collected and examined. Commensal/

parasitic fish (a single species represented by 13 specimens) were found in three echinoderm specimens/species.

Conclusions: The list of echinoderm hosts for this carapid fish, through its whole distribution range, rises to 12

species (six sea stars and six sea cucumbers) and that could be a consequence of its wide geographic distribution,

its generalist feeding habits and opportunistic commensal behavior.

Key words: Eastern Tropical Pacific; Central America; Área de Conservación Guanacaste; symbioses;

Nidorellia armata; Phataria unifascialis; Stichopus horrens.

Chacón-Monge, J. L., Angulo, A., & Cortés, J. (2021). New hosts

and morphological data for the Star pearlfish Carapus

mourlani (Ophidiiformes: Carapidae) from collections

made in the North Pacific coast of Costa Rica. Revista de

Biología Tropical, 69(Suppl. 2), S219-S233. https://doi.

org/10.15517/rbt.v69iS2.48319

https://doi.org/10.15517/rbt.v69iS2.48319

The family Carapidae (Ophidiiformes;

Pearlfishes or Asshfishes) includes eight gen-

era and 36 species (Fricke, Eschmeyer, & Van

der Laan, 2021) of marine fishes widely distrib-

uted in coastal habitats worldwide (Machida,

1989; Meyer-Rochow, 1979; Nelson, Grande,

& Wilson, 2016). Members of the family

are diagnosed by the following combination

of characters: body elongated, tapering to a

slender and pointed tail; supramaxilla absent;

origin of the anal fin on the anterior portion

of the body, usually under vertebra 1-13 and

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closer to the pectoral fin origin (when pres-

ent); pelvic fins absent (in neotropical genera);

dorsal and anal fins without spines, confluent

around the caudal fin; and anal fin rays longer

than opposite dorsal fin rays (Nelson et al.,

2016; Robertson & Allen, 2015). Even though

there are some free-living species, most carapid

fishes are found as commensal inquilines (i.e.,

with no metabolic dependency) or parasites

of bivalve mollusks, sea slugs, sea hares, sea

stars, sea cucumbers, and ascidians (Glynn,

Enochs, McCosker, & Graefe, 2008; Parmenti-

er, Lanterbecq, & Eeckhaut, 2016; Parmentier,

Mercier, & Hamel, 2006). These remarkable

associations, as well as a unique early life his-

tory (i.e, planktonic vexillifer larvae, whit a lat-

ter tenuis stage that usually requires a host for

metamorphosis), account for the notoriety of

the group (Markle & Olney, 1990; Parmentier

& Vandewalle, 2005; Trott, 1981).

While the biology of several carapid fishes

has received some degree of attention in recent

years, especially in the Indo-West Pacific and

Atlantic Oceans, the (taxonomic and mor-

phological) diversity and ecology (including

information about feeding, habitat use or pref-

erences, behavior, and distribution, among

others) of the East Pacific species remain

relatively poorly known (Castro-Aguirre, Gar-

cía-Domínguez, & Balart, 1996; Glynn et

al., 2008; Paredes-Ríos & Balart, 1999; Par-

mentier, Mercier, & Hamel, 2006). Currently,

four species (in three genera) of carapids are

known to occur in the Eastern Tropical Pacific

region (ETP) (Robertson & Allen, 2015); these

are: the Nocturnal pearlfish Echiodon exsilium

Rosenblatt, 1961; the Worm pearlfish Enche-

liophis vermicularis Müller, 1842; the Pacific

pearlfish Carapus dubius (Putnam, 1874); and

the Star pearlfish Carapus mourlani (Petit,

1934). Regarding their ecology, E. exsilium is

a free-living species; whereas E. vermicularis

inhabits the guts of sea cucumbers, including

Isostichopus fuscus (Ludwig, 1875) and Holo-

thuria impatiens (Forskål, 1775); C. dubius has

been found inhabiting the body cavity of pearl

shells (Pinctada spp. Röding, 1798), pen shells

(Pinna spp. Linnaeus, 1758), spiny oyster shells

(Spondylus crassisquama Lamarck, 1819),

clams (Megapitaria spp. Grant & Gale, 1931),

cockles (Laevicardium spp. Swainson, 1840)

and the sea cucumbers Apostichopus californi-

cus (Stimpson, 1857), Holothuria sp., I. fuscus

and Neothyone gibbosa Deichmann, 1941;

finally, C. mourlani has been found inside

I. fuscus and in the gill chamber of the sea

hare Dolabella auricularia (Lightfoot, 1786)

(Castro-Aguirre et al., 1996; Glynn et al., 2008;

González & Borrero-Pérez, 2020; Paredes-Ríos

& Balart, 1999; Parmentier, Mercier, & Hamel,

2006; Robertson & Allen, 2015).

Most carapids are known to have species-

specific host associations (Gustato, Villari, &

Villani; 1979; Parmentier, Mercier, & Hamel,

2006; Smith, Tyler, & Feinberg, 1981; Trott

& Trott, 1972). Although, several ex-situ stud-

ies have demonstrated that some species can

associate with hosts in which they had never

been found before in the wild (Parmentier,

Mercier, & Hamel, 2006; Trott, 1970; Trott,

1981). Given this, different fish species can use

the same hosts; however, it seems that different

fish species usually do not co-occur in the same

individual host (Parmentier & Vandewalle,

2005). In some areas, it has been observed a

certain degree of segregation and specialization

between co-occurring fish species regarding the

use of some specific hosts; for example, in the

Indo-West Pacific, C. mourlani restricts their

occurrence to starfishes and other invertebrate

species that are not used by other sympatric

fishes (Parmentier & Vandewalle, 2005). Mul-

tiple con-specific infestation events also have

been observed, mainly in Indo-West Pacific

sea stars and sea cucumbers (Meyer-Rochow,

1977; Parmentier & Vandewalle, 2005), even

in the ETP (Castro-Aguirre et al., 1996); and

the affected individuals appear to be randomly

distributed to other inhabited or uninhabited

conspecific hosts (Meyer-Rochow, 1977; Par-

mentier & Vandewalle, 2005). Such aggrega-

tions may have a reproductive connotation,

considering that carapid fishes have a highly

derived communication system that should

allow a species-specific recognition (Parmenti-

er & Vandewalle, 2005). Therefore, the use and

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suitability of a specific host depend, in addi-

tion to its occurrence and relative abundance

within the distributional range of the fish, to

the degree of protection (shelter) that the host

provides (or can provide), the availability of

food resources (directly provided or not by the

host), as weel as some colonization impedi-

ments (i.e., host size relative to fish size and/or

other mechanical and/or chemical limitations

imposed by the host). Moreover, it may be

affected by the occurrence of other sympatric

fish species, the availability of possible hosts,

seasonal events (such as reproductive aggrega-

tions) and the occurrence and availability of

carapid planktonic eggs and vexillifer larvae

(Parmentier & Vandewalle, 2005; Parmentier,

Mercier, & Hamel, 2006).

In this study we report the occurrence of

the Star pearlfish Carapus mourlani within

three previously unknown hosts in the ETP:

the sea stars Nidorellia armata (Gray, 1840),

Valvatida, Oreasteridae, Phataria unifascialis

(Gray, 1840), Valvatida, Ophidiasteridae, and

the sea cucumber Stichopus horrens Selenka,

1867, Synallactida, Stichopodidae; supported

by material collected from the North Pacific

coast of Costa Rica. At the same time, some

ecological implications and considerations

regarding such symbiotic relationships are

raised and discussed. Additional morphometric

and meristic data for the fish and the echino-

derms are also provided and discussed. The

information herein provided not only increase

our knowledge about the ecology of these spe-

cies, both fish and echinoderm, reporting new

symbiotic associations but also help us to better

know the diversity of such groups by provid-

ing additional morphological information and

updated data on distribution that allows a better

determination at the regional level.

MATERIALS AND METHODS

Echinoderms were manually collected by

SCUBA diving or snorkeling at depths between

0 and 20 m in a total of 25 localities distributed

along the coastline and the marine sector of

the Área de Conservación Guanacaste (ACG),

Costa Rica (Fig. 1) (details in Chacón-Monge,

Azofeifa-Solano, Alvarado, & Cortés, 2021).

Fieldwork was carried out from July 2018 to

August 2019 as part of a multi-institutional

inventorying and monitoring program on the

ACG developed and driven by the Sistema

Nacional de Áreas de Conservación (SINAC),

the Universidad de Costa Rica (UCR), and

Fig. 1. Echinoderms sample sites at the North Pacific of Costa Rica, explored during five field surveys of the BioMar-ACG

project. Modified from Chacón-Monge et al., (2021). Published with permission.

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the Guanacaste Dry Forest Conservation Fund

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

permits (R-SINAC-PNI-SE-002-2018 and

R-SINAC-ACG-PI-004-2019-BIOMAR) were

provided by the SINAC.

Specimens collected were labeled and

placed in plastic bags separated into groups

by locality and taxonomic affinity (i.e, spe-

cies or morpho-species). Then, samples were

transferred into seawater-filled buckets/trays to

the laboratory and anesthetized with different

seawater-menthol, -magnesium chloride, and/

or -alcohol (ethanol) solutions (Chacón-Monge

et al., 2021). These different solutions were

employed considering their availability, the

relative size of the specimen and their taxo-

nomic group, as well as previous observations

regarding the effectiveness of each solution

for each particular case (Chacón-Monge et al.,

2021; Solís-Marín et al., 2014). For example,

to warrant the adequate relaxation, fixation,

and preservation of the samples, undesirable

reactions as a natural response to alien-harsh

solutions must be avoided (i.e. body-, organ-,

appendage-retraction, autotomy, evisceration,

etc.). In this regard, echinoderms belong to

a relatively ancient phyllum, highly special-

ized in the marine life. That is reflected in

the extended absence of complex osmoregu-

latory organs (Diehl, 1986; Pawson, 2007).

Furthermore, whit the exception of the internal

madreporite(s) plate(s) of the water vascular

system of Holothuroidea, all of the extant

echinoderm classes experiment an active

interchange and direct communication to the

surrounding seawater. The time to reach the

specimen relaxation varies from sample to

sample, and depends on the species/individual-

specific tolerance and response through the

narcotization process, as well as on the chemi-

cal quality, among others. At a larger ratio of

soft-sensitive tissue and exposed area, there

is more interaction with the surrounding solu-

tion, thus, small and thin body-layer specimens

(relative to species) must not need too much

time (i.e. 3-5 hours) or high concentrations of

those solutions in their trays to get relaxed. In

general medium- (>6 cm) as large-size (>15

cm) holothuroids requires the injection of

alcohol through their anus to the fixation of

the internal tissues and organs after relaxation,

which could be delated by their apnea abil-

ity. Most sea cucumber, and large samples of

almost all species were lead for a half-day (12

h) in darkness until their death, after progres-

sive incorporation of those narcotic solutions.

Once the specimens were completely anes-

thetized, they were checked for the presence of

commensal/parasitic fishes (while they were

in the buckets/trays, the fishes occupying the

internal cavities of the echinoderms tend to

seek the exterior due to the effect of the

anesthetic, and by the decrease in the oxygen

concentration in the water; this made it easy to

detect them after a quick visual sample inspec-

tion). Echinoderm samples hosting fishes were

photographed and measured (Table 1) with an

analog caliper. All samples were fixed and pre-

served in ethanol 70 %. In the laboratory, some

large specimens, and those for which the pres-

ence of commensal/parasitic fishes was detect-

ed, were dissected to looking for additional

fishes. Echinoderms were identified based

on specialized taxonomic literature for the

region (Borrero-Pérez & Vanegas-González,

2020; Massin, Zulfigar, Tan, & Rizzal, 2002;

Solís-Marín, Arriaga-Ochoa, Laguarda-Figuer-

as, Fontana-Uribe, & Durán-González, 2009;

Solís-Marín et al., 2014; Martín-Cao-Romero,

Solís-Marín, Laguarda-Figueras, & Buitrón-

Sánchez, 2017; Woo, 2013; Woo, 2018; Woo,

Zulfigar, Tan, Kajihara, & Fujita, 2015); the

morphological data and terminology employed

follow Solís-Marín et al. (2014), Woo (2013),

and Woo et al. (2015). Fishes were identified

following Nielsen, Cohen, Markle, and Robins

(1999), and Robertson and Allen (2015); the

morphological data and terminology employed

follow Markle and Olney (1990), and Nielsen

et al. (1999). Morphometric measurements

(Table 2) from all fishes were taken with a digi-

tal caliper, after fixation in formalin 10 %, and

preserved in ethanol 70 %. Counts were taken

following Markle and Olney (1990), on three

specimens that were cleared and stained fol-

lowing Taylor and Dyke (1985). Species valid

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names, authorities, and year of description

follows the WoRMS Editorial Board (2021),

for invertebrates, and Fricke, Eschmeyer, and

Fong (2021), for fishes. Infested echinoderms,

as well as two fish specimens from different

hosts, were photographed and used as vouch-

ers for tissue samples (preserved in ethanol

96 %). Samples from all vouchered speci-

mens were sent to the Center for Biodiversity

Genomics, at the University of Guelph, for

DNA sequencing and barcoding (Cortés &

Joyce, 2020). Both echinoderm (ECH) and fish

(FIS) voucher specimens were deposited at

the Museum of Zoology of the Universidad de

Costa Rica (MZUCR; see details below, “Mate-

rial examined”).

RESULTS

A total of 497 echinoderms, representing

60 species [including seven sea star species rep-

resented by 56 individuals, and 30 sea cucum-

ber species represented by 192 individuals

(see Chacón-Monge et al., 2021, for details)],

were collected. Of these, only three specimens,

including two sea stars and one sea cucumber

were found to host carapid fishes. The two sea

stars were identified as Nidorellia armata (one

host specimen, Fig. 2B, from a total of seven

conspecific samples) and Phataria unifascialis

(one host specimen, Fig. 2C and Fig. 2D, from

a total of 15 conspecific samples), respectively,

whereas the sea cucumber was identified as

Stichopus horrens (one host specimen, Fig.

2E, Fig. 3, Fig. 4, Fig. 5, Fig. 6, Fig. 7, from

a total of two conspecific samples). The sea

stars were found to host one carapid fish each,

whereas the sea cucumber was found to host

a multiple infestation (Table 1, Fig. 2E). Most

fishes (12) were detected in the field; dissec-

tions on the laboratory allowed the detection of

an additional fish in the infested specimen of S.

horrens (Fig. 3), totalizing 13 individuals. All

fishes were identified as C. mourlani and were

considered as commensal, see details below.

TABLE 1

Morphologic and ecological data of three new echinoderm hosts of Carapus mourlani in the ETP, from samples collected in the North Pacific

of Costa Rica. Lat.=latitude, Long.=longitude; L=length, W= width, R= mayor radius length, r=minor radius length

Voucher Species Sample site Sector Lat. (N) Long.(W) Depth (m) Substrate Size (cm)

Total

fishes

Fish size

(mm)

Fish sex

MZUCR-

ECH1878

Stichopus

horrens

Cerca de Bajo

Pochote (CBP),

San José Island

Archipelago 10º51’22” 85º55’24” 11-15 debris, sand

and gravel

L= 37.7 W=10.5 11 88.03- 105.12 8 ovigerous

females and 3

mature males

MZUCR-

ECH1834

Phataria

unifascialis

Mogotes (Mog),

Isla Negritos,

Playa Blanca

Peninsula 10°55’08” 85º53’56” 9 rocky reef,

covered by

algae and sand

R= 6.1 r= 1 1 64.9 Undetermined

MZUCR-

ECH1629

Nidorellia

armata

Isla Pitahaya (IPi) Peninsula 10º56’08” 85º48’06” 8 rocky reef,

covered by

algae and sand

R= 5.4 r= 3.5 1 65.21 undetermined

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Hosts identification

The specimen of N. armata (MZUCR-

ECH 1629; Fig. 2B) was identified based on

the following combination of observed external

characters: disc pentagonal, relatively large,

wide and robust, with five wide and short

arms; abactinal surface convex with a wide

papular area, surrounded by a reticulate pat-

tern composed of polygonal plates, some with

large, conical, and well developed black-purple

spines, which contrast with the cream or light-

brown background surface; abactinal spines

pentagonal-like arranged on the center of the

disc and radially aligned on the arms; madre-

porite relatively large and irregular; marginal

plates well developed. Actinal surface flat,

covered by small granules and slightly rounded

spines; actinal spines regularly distributed and

slightly separated from each other, most of the

same size, except those nearest to the mouth,

whose are comparatively more elongated;

inferomarginal plates with tiny spines, similar

to those over the abactinal surface. Ambulacral

and adambulacral plates similar to each other,

bearing round and short spines; valvated pedi-

cellariae present on the actinal surface, near

to the mouth; centrally linked to the oblong

ambulacral rows, over which runs biseriate

ambulacral podia with sucker terminal discs.

The specimen of P. unifascialis (MZUCR-

ECH 1834; Fig. 2C, Fig. 2D) was identi-

fied based on the following combination of

observed external characters: disc pentagonal,

relatively short, and reduced, with five trigonal

and tapered arms. Papular area restricted to the

TABLE 2

Morphometric (M) and meristic (C) data from examined specimens of Carapus mourlani from ACG, Costa Rica,

and comparative data from material from the Indo-West Pacific (Markle & Olney, 1990). Measurements expressed as

proportions of the head length; head length expressed as proportion of the total length; total length in mm. ND=No Data.

Measurements/Counts

Markle & Olney (1990) This study

n=17(M)/41(C) n=11(M)/3(C)

Min. Max. Min. Max.

Total length 65.00 170.00 64.9 105.12

Body depth 0.49 0.69 0.39 0.67

Head length* ND ND 0.14 0.17

Head depth 0.45 0.55 0.50 0.59

Head width 0.30 0.50 0.34 0.49

Snout length 0.16 0.19 0.17 0.21

Upper jaw lenght 0.43 0.62 0.43 0.58

Lower jaw length 0.44 0.58 0.41 0.57

Eye diameter 0.15 0.22 0.17 0.26

Postocular lenght ND ND 0.55 0.66

Interobital distance 0.14 0.18 0.13 0.19

Prepectoral length ND ND 0.98 1.09

Pectoral fin lenght 0.33 0.47 0.34 0.52

Predorsal length 1.57 1.92 1.62 1.91

Preanal length 0.86 1.00 0.82 0.98

Pectoral-fin rays 17 21 18 20

Anal-fin rays anterior to the origin of the dorsal fin 18 25 19 23

Anal-fin rays to 31st vertebra 54 61 55 59

Dorsal-fin rays to 31st vertebra 35 41 35 39

Vertebrae to the origin of the dorsal fin 11 14 12 13

Vertebrae to the origin of the anal fin 2 4 2 3

Precaudal vertebra 15 17 15 16

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abactinal surface; as a single main papular line

along the upper arm surface, and two small

secondary rows at both sides of the main row.

Anus located centrally on the disc; a single

rounded madreporite with radial striations;

three longitudinal rows of carinal plates along

each arm. Both, the actinal and abactinal sur-

face covered by granulation; granules are large

and dense in the abactinal plates, while being

small and spread in the papular area, granules

of the actinal surface are rounded and spaced.

The ambulacral rows have a single row of

tapering ambulacral spines.

The specimen of S. horrens (MZUCR-

ECH 1878; Fig. 2E, Fig. 3, Fig. 4, Fig. 5, Fig.

6, Fig. 7) was identified based on the following

combination of observed external and internal

characters: body elongated, vermiform, sub-

quadrangular in the cross-section, and robust;

integument thick, with a firm and rough sur-

face, and a slight mid-dorsal wrinkle. Back-

ground orange, dark brown, and yellowish,

with tiny scattered white patches; dorsal- and

ventrolateral papillae conspicuous, with dark

purple-brown bases and white apex. Mouth ori-

ented ventrally, with a crown of 20 peltate oral

tentacles; oral opening surrounded by a ring

of small papillae. Ventral sole (trivium) pale-

cream and flat, with three ambulacral areas, the

median row wider. Cuvierian tubules absent;

anal teeth or papillae around the terminal clo-

aca absent; gonads into two tufts, attached to

the dorsal mesentery. Ossicles in the bivium

and trivium surface as tables, branched rods,

and C-shaped bodies mainly, while those of

the dorsal papillae being as high-spired tables

Fig. 2. Symbiosis between Carapus mourlani and their echinoderms hosts from samples collected in the North Pacific of

Costa Rica during BioMar-ACG project. A): C. mourlani detail; B): Nidorellia armata and its unique carapid inquiline; C)

Phataria unifascialis and its unique carapid inquiline; D): close-up of the tip of P. unifascialis arm, showing a C. mourlani

going out from its ambulacral host. E): multiple infestation of C. mourlani in Stichopus horrens. All scales are 1cm.

Fig. 3. Stichopus horrens dissection showing an additional

Carapus mourlani. Scales 1cm. A): longitudinal slice from

the anus to the mouth of S. horrens; B): protrusion of the C.

mourlani head through cloaca epithelium; C): C. mourlani

view after remove the epithelium cloaca at the side of

the sphincter.

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(tack-liked tables) (Fig. 4, Fig. 5); and fusiform

(spindle-like) ossicles in the tentacles (Fig. 6).

Pearl fish identification

The fishes (MZUCR-FIS 3313-3315)

were identified based on the following com-

bination of observed external characters: body

elongate, short and compressed; translucent,

silvery to coppery on cheek and abdomen,

with many star-shaped dark blotches on the

head and the dorsal portion of the body; the

tip of snout without fleshy flaps. Upper jaw

extending beyond the posterior edge of the

eye, free from head (i.e., not bound to the side

of the head by skin), with one or two large,

conical and curved teeth and an outer row

of small, sharp, and slender teeth; lower jaw

with a patch of small teeth at the front, before

an external row of large, curved and conical

Fig. 4. Ossicles from Stichopus horrens bivium tissue sample. A): tables, C and S body shape;

B): tables; C) and D): tack-liked tables.

Fig. 5. Ossicles from Stichopus horrens trivium tissue

sample. A): tables, rods and perforate plates; B) and C):

approach to tables and perforate plates.

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teeth, and three to five rows of small coni-

cal teeth inside those; roof of the mouth with

two or three large canines at the front, and a

band of short conical teeth on each side. Gill

opening extending above the mid-side; gill

membranes not united below; gill rakers well

developed. Swim bladder constricted, forming

two chambers, without a thin terminal mem-

brane or bulb; pectoral fin well developed, two

to three times the head length, with 17-21 rays;

anus and origin of the anal fin located before

the base of the pectoral fin; dorsal fin origin

located well behind the origin of the anal fin;

dorsal and anal fins confluent with caudal fin;

and tail long and slender. Additional morpho-

metric and meristic data for fish specimens are

provided in Table 2.

Material examined: MZUCR-ECH 1629/

MZUCR-FIS 3313: Isla Pitahaya, Bahía Santa

Elena, Guanacaste, Costa Rica, 10º56’08” N,

85º48’06” W, 8 m depth (rocky reef), collected

by J. L. Chacón-Monge, C. Mora-Barboza, Y.

Vega & G. Ampié on 8-August-2018. MZUCR-

ECH 1834/MZUCR-FIS 3314: Mogotes, Isla

Negritos, Playa Blanca, Península de Santa

Elena, 10°55’08” N, 85º53’56” W, 9 m depth

(rocky reef), collected by J. L. Chacón-Monge,

C. Mora-Barboza, Y. Vega & G. Ampié on

30-July-2019. MZUCR-ECH 1878/MZU-

CR-FIS 3315: Bajo Pochote, Isla San José,

Islas Murciélago, Guanacaste, Costa Rica,

10º51’22” N, 85º55’24” W, 11-15 m depth

Fig. 7. S. horrens: A) and B): on their natural habitat, and C) and D): preserved specimen, scales are 1 cm.

Fig. 6. Ossicles from S. horrens tentacle tissue sample. A):

rods, C and S body shape, fusiform (spindle-like); B) rods

and perforate plates magnification; C): fusiform ossicle

(spindle-like ossicle) magnification.

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(compound reef), collected by J. L. Chacón-

Monge, C. Mora-Barboza, Y. Vega & G. Ampié

on 31-July-2019.

DISCUSSION

Carapus mourlani is widely distributed

in the tropical Indo-Pacific Ocean, from East

Africa, through Oceania and Hawaii, to south-

ern Central America and Ecuador (Glynn et

al., 2008; Markle & Olney, 1990; Robertson &

Allen, 2015) and this distribution is thought to

be related, among other factors (e.g., currents

patterns, water temperature, food availability,

etc.), to the co-occurrence of its preferred hosts

(i.e., sea stars and sea cucumbers in general)

(Machida, 1989). In the central and western

Indo-Pacific Ocean, C. mourlani is known to

inhabit the sea stars Acanthaster planci (Lin-

naeus, 1758), Choriaster granulatus Lütken,

1869, Culcita novaeguineae Müller & Tros-

chel, 1842 and Pentaceraster cumingi (Gray,

1840), the sea cucumbers Actinopyga mauri-

tiana (Quoy & Gaimard, 1834), Holothuria

(Metriatyla) scabra Jaeger, 1833, Bohadschia

argus Jaeger, 1833, Stichopus chloronotus

Brandt, 1835, and Stichopus variegatus Sem-

per, 1868 (Glynn et al., 2008; Markle & Olney,

1990; Meyer-Rochow, 1979). Records of the

species in the ETP are restricted to the sea hare

D. auricularia and the sea cucumber I. fuscus

(Glynn et al., 2008). The identification of two

new sea stars and one new sea cucumber as

hosts for C. mourlani in the ETP support the

observation that the Star pearlfish prefer spe-

cies of echinoderms as hosts and that they can

found shelter in species that are not hosting

other fishes, since none of these species have

been reported as hosts for the other sympatric

commensal or parasitic carapids (Markle &

Olney, 1990; Parmentier, Mercier, & Hamel,

2006; Robertson & Allen, 2015). Moreover,

the record within N. armata, P. unifascialis,

and S. horrens broadens the list of echinoderm

hosts for this carapid fish, considering the

whole distribution range of the species, to 13

different taxa, including six sea stars and six

sea cucumbers.

Nidorellia armata and P. unifascialis are

widely distributed in the ETP, from the Gulf

of California to Perú (Borrero-Pérez & Vane-

gas-González, 2020; Martín-Cao-Romero et

al., 2017; Solís-Marín et al., 2014), however,

they had not been confirmed yet as hosts of

C. mourlani. This could be partly due to the

lack of studies examining in detail such asso-

ciations, the omission of such information in

studies inventorying the echinoderm fauna

at different local and regional scales, and the

little or no interaction and exchange of infor-

mation between specialists working with both

taxonomic groups (Parmentier, Lanterbecq,

& Eeckhaut, 2016; Parmentier, Mercier, &

Hamel, 2006). We also find interesting the

fact that some confirmed hosts of C. mourlani,

such as the sea stars A. planci and P. cumingi

(Glynn et al., 2008; Markle & Olney, 1990),

which occur in the North Pacific of Costa Rica

have not been reported as hosts for this species

in the ETP. In this regard, we could think that

(possible or potential) host species with large

and flexible body cavities [as those cited above,

as well as other sea stars and sea cucumbers

used as hosts by C. mourlani in other latitudes,

some of which are also present in the study

area (Chacón-Monge et al., 2021)] could be

more suitable than -and even preferred- over

other small and rigid species, which have com-

paratively smaller body cavities. However,

as could be derived from our research, this

is not the case. The reasons for this could be

the same as those mentioned before, and/or

correspond to intrinsic biological/ecological

(e.g., physiological, mechanical, ethological,

ontogenetic, among others) and environmental

differences, including different or additional

selective pressures and/or adaptive advantages/

disadvantages, between the different popula-

tions and species involved through their respec-

tive distributional ranges (Machida, 1989;

Parmentier, Lanterbecq, & Eeckhaut, 2016;

Parmentier, Mercier, & Hamel, 2006; Parmen-

tier & Vandewalle, 2005).

As C. mourlani, the distribution of S. hor-

rens encompasses the tropical Indo-Pacific

Ocean, from East Africa, through Oceania

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and Hawaii, to part of the ETP (Cortés, 2012;

Glynn et al., 2008; Massin et al., 2002; Woo,

2013; Woo, 2018; Woo, Zulfigar, Tan, Kaji-

hara, & Fujita, 2015); however, as in the pre-

vious cases, this is the first published record

suggesting a specific association between both

species. On the other hand, despite S. horrens

had already been reported from Isla del Coco,

this is the first confirmed record of occur-

rence of the species within Costa Rican coastal

waters (Alvarado, 2010; Alvarado et al., 2017;

Chacón-Monge et al., 2021; Cortés, 2012).

In other latitudes, there are records of asso-

ciations between Stichopus and C. mourlani

(Glynn et al., 2008), however, such records

refer to S. variegatus sensu lato. This name,

however, is not currently accepted as valid

(see the WoRMS Editorial Board, 2021) and,

as cited by Glynn et al., (2008), it may cor-

respond to one of the following two species:

Stichopus herrmanni Semper, 1868, Stichopus

naso Semper, 1868, or even to S. horrens, with

which was synonymized, in part (WoRMS Edi-

torial Board, 2021). Given this, it is necessary

to confirm the taxonomic identity of the hosts

reported by Glynn et al. (2008) to know if the

association described here correspond, in fact,

to the first report of a specimen of S. horrens

hosting specimens of C. mourlani. Addition-

ally, we herein report for the first time, the pres-

ence of fusiform (spindle-like) ossicles in the

tentacles of S. horrens, as previously reported

for other congeneric species (Woo, 2013; Woo,

2018; Woo et al., 2015).

The morphological identification of the

C. mourlani’s hosts, was tried to be corrobo-

rated by molecular analysis (unpublished data).

Unfortunately, for N. armata and P. unifascia-

lis, there is no nucleotide information available

to compare our vouchers, and the best molecu-

lar identity matches (i.e., have similar/compati-

ble COI sequences) were Iconaster longimanus

from Singapore (81.61%) and Linckia laeviga-

ta from Indonesia (86.47%), respectively (from

sequences available for comparison in BLAST,

https://blast.ncbi.nlm.nih.gov). The sequencing

of the S. horrens host voucher was no success-

ful. Nevertheless, we can confirm indirectly its

identification from the other con-specific speci-

men (not found as C. mourlani host), which is

98.16% similar/compatible (COI sequences) to

S. horrens vouchers from China (from samples

available for comparison in BLAST https://

blast.ncbi.nlm.nih.gov).

We can also confirm our hosts’ identifica-

tion by discarding. First, both sea star species

belongs to the Valvatida Order, which means

that dermo-skeletal formations as granules,

spines, plates, and the valvate pedicellariae

have diagnostic significance (Solís-Marín et

al., 2014). Comparatively, there is no other

sea star that could be confused with N. armata

within the Oreasteridae family (those valvatids

with large, robust, or projected marginal plates;

whose actinal and abactinal plates could be

rounded or polygonal, but never paxilliform) in

the ETP (Solís-Marín et al., 2013; Solís-Marín

et al., 2014). Concerning its distribution, in

Costa Rica, P. unifascialis could be confused

with Pharia pyramidata (Gray, 1840); this

genus also belongs to the Ophidiasteridae

family (those valvatids with no prominent

marginal plates, body densely covered by gran-

ules, small disc and a wide abactinal popular

area; Solís-Marín et al., 2014), but it has been

pointed out that P. unifascialis differs from

other ophidiasterids by the following combina-

tion of characters: 1) popular area restricted

in one longitudinal row along the radius, and

two small papular rows that can reach to half

or less the longitude of the main row, at both

sides of the main popular area, 2) three carinal

plates rows along the radius, and 3) only one

row of ambulacral spines, wider in the base

and tapering (Martín-Cao-Romero et al., 2017).

Finally, there is only two Stichopodidae species

registered for the ETP: I. fuscus, and S. hor-

rens (Solís-Marín et al., 2013), both share the

presence of ossicles like tables, rosettes, rods,

or even “C” and “S” -shaped bodies, and large

gonads in two tufts (Deichmann, 1958; Solís-

Marín et al., 2009; Woo, 2018) as observed

in the dissected host. However, the tack-liked

tables from papillae and fusiform ossicles in

tentacles have never been found in I. fuscus and

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should be considered to be part of the diagnosis

of S. horrens.

On the other hand, fish’s morphomet-

ric and meristic data match well with those

reported from specimens collected in the Indo-

Pacific region, sensu Markle and Olney (1990)

and Nielsen et al. (1999), as well as from

comparative data provided by Robertson and

Allen (2015), based on collections and mate-

rial from other localities within the ETP. These

results suggest that there is no morphological

differentiation (at least in terms of the charac-

ters herein examined) between the populations

of the Indo-West Pacific and the ETP. A pre-

liminary molecular analysis (data not provided/

discussed here) revealed that the samples/data

obtained/generated in this study (i.e., COI

sequences for two C. mourlani individuals) are

98-100 % similar/compatible with sequences

available in GeneBank (https://www.ncbi.nlm.

nih.gov/genbank/) from con-specific specimens

collected in Micronesia. Such results suggest a

low genetic structuring (i.e., high homogeneity

and gene flow between populations), potential-

ly explained by the high dispersal capacity of

the rafting eggs and larval stages of these fishes

(Markle & Olney, 1990; Parmentier & Vande-

walle, 2005). These observations make sense,

considering that most species of the family also

present wide distributions, at a global scale,

with fairly conserved populations in terms of

most of their morphological (external and inter-

nal) features (Markle & Olney, 1990; Nielsen

et al., 1999). This can be reinforced, even,

by some intraspecific ethological patterns, as

the preference of phylogenetically close or

ecologically similar hosts, with relatively well-

known interspecific differences (Markle &

Olney, 1990; Parmentier, Mercier, & Hamel,

2006; Parmentier & Vandewalle, 2005).

Despite the overall low frequency of infes-

tation found in this study, which is compa-

rable with the results of previous inventories

in nearby areas for other species, e.g., the Gulf

of California, Mexico (Castro-Aguirre et al.,

1996) and the mainland of Ecuador (Parmen-

tier, Mercier, & Hamel, 2006), 50 % of the

collected specimens of S. horrens were found

to shelter carapid fish. Moreover, since eleven

fish were found inside this sea cucumber, it

should be considered as a multiple infestation

event. To the authors’ best knowledge, multiple

infestation events in the ETP are relatively rare

and have been recorded only for the species

C. dubius inside specimens of Megapitaria

squalida (G. B. Sowerby I, 1835), for which up

to 5 fishes have been reported in a single host

(Castro-Aguirre et al., 1996). Multiple infesta-

tions have been reported before in other regions

of the world, in other echinoderm hosts, e.g.,

within the sea star C. novaeguineae, and the sea

cucumber B. argus (Parmentier, Lanterbecq,

& Eeckhaut, 2016; Parmentier & Vandewalle,

2005); moreover, such behavior also has been

observed and induced in specimens kept in cap-

tivity (Meyer-Rochow, 1977; Meyer-Rochow,

1979; Parmentier & Vandewalle, 2005). Pre-

vious authors (e.g., Trott, 1970; Parmentier,

Colleye, & Lecchini, 20l6; Parmentier, Fine,

Vandewalle, Ducamp, & Lagardère, 2006; Par-

mentier & Vandewalle, 2005) have suggested

that these multiple infestation events have

reproductive implications, however, this has

not been fully demonstrated. In this study, all

the eleven fish found inside S. horrens were

adults, of these eight were ovigerous females,

and three were mature males. The presence

of these reproductive specimens inside this

host could offer support in favor of a possible

hypothesis of reproductive aggregations; how-

ever, detailed studies are required (both at the

physiological and ethological levels) in order

to corroborate this. On the other hand, the non-

random occurrence of multiple con-specific

infestations, the aggrupation of reproductive

specimens and observations on sex ratio, and

the restricted use of some hosts but no others

of some species in the presence of other car-

apid fish, could support the hypothesis of the

evolution of acoustic signals in these fishes

for the interspecific differentiation, which can

help to avoid interspecific conflicts (Parmen-

tier, Colleye, & Lecchini, 2016; Parmentier &

Vandewalle, 2005). The generalistic pattern of

host selection by C. mourlani could be inferred,

in part, given its feeding behavior (described

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as a generalist carnivorous that feeds outside

its hosts; Parmentier, Mercier, & Hamel 2006;

Robertson & Allen, 2015), as well as the appar-

ently wide “host adaptive landscape” (Zaman

et al., 2014) explored by this species through

its equally wide geographical distribution range

(Parmentier, Lanterbecq, & Eeckhaut, 2016).

Ethical statement: authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We thank Frank Joyce and Cristian Mora-

Barboza for their support before and during

field sampling. We also thank the administra-

tive staff of the CIMAR, the School of Biology

and the Museum of Zoology, CIBET, of the

UCR, for the support and materials, equipment

and workspace provided during the execution

of this work. To the Sistema Nacional de Áreas

de Conservación (SINAC) and the Ministerio

de Ambiente y Energía (MINAE) for facilitat-

ing the research and collection permits. To the

ACG, the Guanacaste Dry Forest Conservation

Fund and the University of Costa Rica for the

financing granted under the BioMar-ACG proj-

ect (808-B9-508). We also thank to the scientif-

ic editors of this volume for their invitation to

colaborate and finally, thanks to the anonymous

reviewers whose comments and suggestions

help to improve and clarify this manuscript.

RESUMEN

Nuevos hospederos y datos morfológicos para

el Pez perla estrella Carapus mourlani

(Ophidiiformes: Carapidae) a partir de recolectas

realizadas al norte de la costa Pacífico de Costa Rica

Introducción: La familia Carapidae está compuesta por

alrededor de 40 especies de peces marinos, presentes en

hábitats costeros alrededor de todo el mundo. Se incluyen

dentro de esta familia algunas especies de vida libre, no

obstante, la mayoría de carápidos son inquilinos oportunis-

tas o parásitos de algunos grupos de invertebrados marinos,

incluyendo varias especies de equinodermos. En el Pacífico

Tropical Oriental (PTO), se sabe relativamente poco sobre

la biología de estos peces, así como de las diversas asocia-

ciones existentes y de los hospederos utilizados.

Objetivo: En este trabajo reportamos la ocurrencia del Pez

perla estrella Carapus mourlani en tres nuevos hospederos:

las estrellas de mar Nidorellia armata y Phataria unifascia-

lis, y el pepino de mar Stichopus horrens. También se dis-

cuten algunas implicaciones y consideraciones ecológicas

relacionadas a estas asociaciones simbióticas. Además, se

proveen y discuten datos morfométricos y merísticos de los

peces y sus hospederos.

Métodos: Se realizaron recolectas de equinodermos, entre

2018 y 2019, en un total de 25 localidades distribuidas al

norte de la costa Pacífico de Costa Rica, los cuales fueron

cuidadosamente revisados en búsqueda de peces comen-

sales/parásitos. Los equinodermos y los peces fueron

identificados y caracterizados de acuerdo con la literatura

especializada.

Resultados: Se recolectaron y examinaron un total de 497

equinodermos, incluyendo alrededor de 60 especies, de los

cuales solo tres individuos-especies estuvieron ocupados

por peces comensales/parásitos.

Conclusiones: La lista de hospederos equinodermos de C.

mourlani a lo largo de su ámbito de distribución geográfico

llega a 12 especies (seis estrellas de mar y seis pepinos de

mar), lo cual podría ser un reflejo de su amplia distribución

geográfica, de sus hábitos de alimentación generalistas

y de su comportamiento oportunista en lo relativo al uso

de hospederos.

Palabras clave: Pacífico Tropical Oriental; América Cen-

tral; Área de Conservación Guanacaste; simbiosis; Nidore-

llia armata; Phataria unifascialis; Stichopus horrens.

REFERENCES

Alvarado, J. J. (2010). Isla del Coco (Costa Rica) Echi-

noderms: State of knowledge. In L.G. Harris, S.A.

Böttger, C.W. Walker, & M.P. Lesser (Eds.), Echi-

noderms: Durham. Proceedings 12th International

Echinoderm Conference (pp. 103–113). Leiden,

Netherlands: CRC Press, Taylor & Francis Group,

Balkema.

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(Supple-

ment 1), S272–S287.

Borrero-Pérez, H., & Vanegas-González, M. J. (2020).

Riqueza, composición y distribución de los

S232

Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(Suppl. 2): S219-S233, October 2021 (Published Oct. 30, 2021)

equinodermos de los Riscales y Morros del norte

del Cocó, Pacífico Colombiano. In L. Chasqui (Ed.),

Biodiversidad de los arrecifes rocosos (riscales y

morros) del Pacífico Norte Chocoano (No. 116, pp.

232–282). Santa Marta, Colombia: Serie Publicacio-

nes Generales de INVEMAR.

Castro-Aguirre, J. L., García-Domínguez, F., & Balart, E.

F. (1996). Nuevos hospederos y datos morfométricos

de Encheliophis dubius (Ophidiiformes: Carapidae)

en el Golfo de California, México. Revista de Biolo-

gia Tropical, 44(2), 753–756.

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(Supplement

1), S487-S500.

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

pical Pacific oceanic island, Isla del Coco, Costa

Rica. Revista de Biología Tropical, 60(Supplement

3), S131–S185.

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.

Deichmann, E. (1958). The Holothurioidea collected by

the Velero III and IV during the years 1932 to 1954.

Part II. Aspidochirota. Allan Hancock Pacif. Expedi-

tions,11, 249–349.

Diehl, W. J. (1986). Osmoregulation in echinoderms.

Comparative Biochemistry and Physiology, 84(2),

199–205.

Fricke, R., Eschmeyer, W. N., & Fong, J. D. (2021). Gene-

ra/Species by Family/Subfamily. Eschmeyer’s Cata-

log of Fishes. http://researcharchive.calacademy.org/

research/ichthyology/catalog/SpeciesByFamily.asp

Fricke, R., Eschmeyer, W. N., & Van der Laan, R. (2021).

Genera, Species, References. Eschmeyer´s Catalog

of Fishes. http://researcharchive.calacademy.org/

research/ichthyology/catalog/fishcatmain.asp).

Glynn, P. W., Enochs, I. C., McCosker, J. E., & Graefe, A.

N. (2008). First record of a Pearlfish, Carapus mou-

rlani, inhabiting the Aplysiid opisthobranch mollusc

Dolabella auricularia. Pacific Science, 62, 593-601.

González, M. J. V., & Borrero-Pérez, G. H. (2020). First

records and new information on the associations of

echinoderms with other phyla in the rocky reefs of

northern Chocó, Colombian Pacific. ZooKeys, 921,

1–22.

Gustato, G., Villari, A., & Villani, G. (1979). Ulteriori dati

sul comportamento di Carapus acus (Gadiformes,

Ophidiodei). Bollettino della Società dei naturalisti

in Napoli, 88, 535-547.

Machida, Y. (1989). New distribution records of the Pearl-

fish, Carapus mourlani, with notes on its Morphome-

try. Japanese Journal of Ichthyology, 36, 363–368.

Markle, D., & Olney., J. (1990). Systematics of the pearl-

fish (Pisces: Carapidae). Bulletin of Marine Science,

47, 269–410.

Martín-Cao-Romero, C., Solís-Marín, F. A., Laguarda-

Figueras, A., & Buitrón-Sánchez. B. E. (2017). Pha-

taria unifascialis (Valvatida: Ophidiasteridae) from

the Eastern Pacific: Redescription and skeletal mor-

phology. Revista de Biologia Tropical, 65(Supple-

ment 1), S258–S271.

Massin, C., Zulfigar, Y., Tan Shau Hwai, A., & Rizzal,

S. (2002). The genus Stichopus (Echinodermata:

Holothuroidea) from the Johore Marine Park (Malay-

sia) with the description of two new species. Biologie,

72, 73–99.

Meyer-Rochow, V. (1977). Comparison between 15 Cara-

pus mourlani in a single Holothurian and 19 C. mou-

rlani from Starfish. Copeia, 3, 582–584.

Meyer-Rochow, V. B. (1979). Stomach and gut contents of

Carapus mourlani from starfish and a holothurian.

Annales Zoologici Fennici, 16, 287–289.

Nelson, J. S., Grande, T. C., & Wilson, M. V. (2016). Fis-

hes of the World. Hoboken, New Jersey: John Wiley

& Sons.

Nielsen, J. G., Cohen, D. M., Markle, D. F., & Robins, C.

R. (1999). Ophidiiform Fishes of the World (Order

Ophidiiformes). An annotated and illustrated cata-

logue of pearlfishes, cusk-eels, brotulas and other

ophidiiform fishes known to date. FAO Fisheries

Synopsis, 18 (125). Rome, Italy: FAO.

Paredes-Ríos, G. A., & Balart, E. F. (1999). Corroboration

of the Bivalve, Pinna rugosa, as a host of the Pacific

Pearlfish, Encheliophis dubius (Ophidiiformes: Cara-

pidae), in the Gulf of California, Mexico. Copeia, 2,

521–522.

Parmentier, E., Colleye, O., & Lecchini, D. (2016). New

insights into sound production in Carapus mourlani

(Carapidae). Bulletin of Marine Science, 92, 1–8.

Parmentier, E., Fine, M., Vandewalle, P., Ducamp, J., &

Lagardère. J. (2006). Sound production in two Cara-

pids (Carapus acus and C. mourlani) and through

the sea cucumber tegument. Acta Zoologica, 87,

113–119.

Parmentier, E., Lanterbecq, D., & Eeckhaut, I. (2016).

From commensalism to parasitism in Carapidae

(Ophidiiformes): heterochronic modes of develop-

ment? PeerJ, 4, (e1786), 1–23.

S233

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(Suppl. 2): S219-S233, October 2021 (Published Oct. 30, 2021)

Parmentier, E., Mercier, A., & Hamel, J. F. (2006). New

host and geographical distribution for the pearlfish

Carapus mourlani (Carapidae) with a discussion on

its biology. Copeia, 1, 122–128.

Parmentier, E., & Vandewalle, P. (2005). Further insight on

Carapid-holothuroid relationships. Marine Biology,

146, 455–465.

Pawson, D. (2007). Phylum Echinodermata. In Z. Q.

Zhang, & W. A. Shear (Eds.), Linnaeus Tercentenary:

Progress in Invertebrate Taxonomy. Zootaxa, 1668,

749–764.

Robertson, D. R., & Allen, G. R. (2015). Shorefishes of the

Tropical Eastern Pacific: online information system.

Version 2.0. Smithsonian Tropical Research Institute,

Balboa, Panamá. http://biogeodb.stri.si.edu/sftep/en/

pages.

Smith, L., Tyler, J., & Feinberg, M. N. (1981). Popula-

tion ecology and biology of the Pearlfish (Carapus

bermudensis) in the Lagoon at Bimini, Bahamas.

Bulletin of Marine Science, 31, 876–902.

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., Alvarado, J. J., Abreu-Pérez, M.,

Aguilera, O., Alió, J., Bacallado-Aránega, J. J., … &

Williams, S. M. (2013). Appendix. In J. J. Alvarado,

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

and Diversity in Latin America (pp. 543-654). Berlin

and Heidelberg: Springer.

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 DF: Universidad Nacional Autóno-

ma de México (UNAM), Instituto de Ciencias del

Mar y Limnología, Secretaría de Medio Ambiente y

Recursos Naturales (Semarnat) e Instituto Nacional

de Ecología y Cambio Climático (INECC).

Taylor, W. R., & Dyke, G. C. (1985). Revised procedu-

res for staining and clearing small fishes and other

vertebrates for bone and cartilage study. Cybium, 9,

107–119.

Trott, L. B. (1970). Contributions to the biology of carapid

fishes (Paracanthopterygii: Gadiformes). University

of California Publications in Zoology, 89, 1–60.

Trott, L. B. (1981). A general review of the pearlfishes

(Pisces, Carapidae). Bulletin of Marine Science, 31,

623–629.

Trott, L. B., & Trott, E. E. (1972). Pearlfishes (Carapidae:

Gadiformes) collected from Puerto Galera, Mindoro,

Philippines. Copeia, 1972, 839–843.

Woo, S. P. (2013). The Diversity, Distribution, and Mor-

phological Descriptions of Stichopodidae (Echino-

dermata: Holothuroidea) in the Vicinity of Malaysian

Waters. (Master of Science dissertation). Universiti

Sains Malaysia, Malaysia.

Woo, S. P. (2018). Systematic Studies on Sea Cucum-

bers of the Family Stichopodidae (Echinodermata:

Holothuroidea). (Doctoral dissertation). Hokkaido

University, Japan.

Woo, S. P., Zulfigar, Y., Tan, S. H., Kajihara, H., & Fujita,

T. (2015). Sea cucumbers of the genus Sticho-

pus Brandt, 1835 (Holothuroidea, Stichopodidae) in

Straits of Malacca with description of a new species.

ZooKeys, 545, 1–26.

WoRMS Editorial Board (2021). World Register of Marine

Species. http://www.marinespecies.org/

Zaman, L., Meyer, J. R., Devangam, S., Bryson, D. M.,

Lenski, R. E., & Ofria, C. (2014). Coevolution drives

the emergence of complex traits and promotes evol-

vability. PLoS Biol, 12(12), e1002023.