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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 787–803, e49587, enero-diciembre 2022 (Publicado Nov. 21, 2022)

The role of spine length in crustacean and fish associations

with echinoids at Los Cabos, Baja California Sur, Mexico

Floyd E. Hayes1*; https://orcid.org/0000-0003-3032-8405

Sean T. Richards1, 2; https://orcid.org/0000-0002-4554-5499

Antonio I. Robles1; https://orcid.org/0000-0002-2408-8022

Robert A. Gouveia1; https://orcid.org/0000-0001-8846-8350

Gillund G. Fayard1; https://orcid.org/0000-0002-5656-0790

1. Department of Biology, Pacific Union College, 1 Angwin Ave., Angwin, CA 94508, United States of America;

floyd_hayes@yahoo.com (* Correspondence), serichards@puc.edu, airobles@puc.edu, ragouveia@puc.edu,

ggfayard@puc.edu

2. Department of Earth and Biological Sciences, Loma Linda University, Loma Linda, CA 82350, United States of

America.

Received 14-I-2022. Corrected 18-X-2022. Accepted 16-XI-2022.

ABSTRACT

Introduction: Echinoids (sea urchins) provide shelter for a variety of facultative or obligatory ectosymbionts.

Objective: To evaluate the hypothesis that decapods and fishes prefer to associate with echinoid individuals and

species that have longer spines.

Methods: We visually studied the frequency of decapod crustaceans and fishes associated with echinoids in

shallow water (< 4 m) and deeper water (5-20 m) at Los Cabos, Baja California Sur, Mexico, during 1-6 January

2019.

Results: We inspected 1 058 echinoids of six species. Five decapod species associated with three species of echi-

noids. When compared with other echinoid species, in shallow water, decapods associated 5.1 times more often

with the longest-spined echinoid Diadema mexicanum (7.0 times more decapods per individual D. mexicanum);

in deeper water, association frequency was similar for all echinoid species. Fourteen fish species associated with

four echinoid species. In shallow water, fishes associated 2.6 times more with D. mexicanum (4.5 times more

fishes per individual). There was no preferred echinoid species in deeper water. Longer-spined D. mexicanum

had more decapods and fishes. Associations were more frequent in shallow water. Multiple individuals and spe-

cies of decapods and fish often associated together with a single D. mexicanum. The decapod that presumably is

Tuleariocaris holthuisi showed a possible obligatory association with one of the equinoids (D. mexicanum); the

other decapods and all fish species are facultative associates.

Conclusion: Our results support the hypothesis that decapods and fishes associate most frequently with echi-

noids with the longest spines, presumably to reduce the risk of predation.

Key words: coastal ecology; ectosymbionts; facultative association; Gulf of California; rocky subtidal.

RESUMEN

El papel de la longitud de la espina en la asociación de crustáceos y peces con equinoideos

en Los Cabos, Baja California Sur, México

Introducción: Los equinoideos (erizos de mar) brindan refugio a una variedad de ectosimbiontes facultativos

u obligatorios.

https://doi.org/10.15517/rev.biol.trop..v70i1.49587

AQUATIC ECOLOGY

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INTRODUCTION

Sea urchins (hereafter referred to as echi-

noids) comprise an integral component of many

shallow benthic marine ecosystems, modifying

habitats by grazing algae and seagrasses, creat-

ing new habitats through bioerosion of hard

substrates, and providing prey for predators

(Steneck, 2013). In addition, the pointed spines

of echinoids and the burrows echinoids create

provide shelter for a variety of invertebrate and

vertebrates ectosymbionts, including many spe-

cies of crustaceans (e.g., Bruce, 1976; Hayes et

al., 2016; Ross, 1983) and fishes (e.g., Giglio

et al., 2017; Hayes et al., 2019; Karplus, 2014).

Previous studies have demonstrated that

several species of crustaceans (Castro, 1978;

Hayes et al., 2016; Joseph et al., 1998) and

fishes (Giglio et al., 2017; Gould et al., 2014;

Hartney & Grorud, 2002; Hayes et al., 2019;

Magnus, 1967; Tamura, 1982) prefer to associ-

ate with models, live individuals, or species

of echinoids with longer or denser spines,

presumably to gain protection from predators.

Some species of crustaceans (Bruce, 1976;

Bruce, 1982; Chace, 1969; Fricke & Hentschel,

1971; Lewis, 1956; Patton et al., 1985) and

fishes (Eibl-Eibesfeldt, 1961; Fricke, 1970;

Gould et al., 2014; Hartney & Grorud, 2002;

Lachner, 1955; Magnus, 1967; Strasburg,

1966; Tamura, 1982) are nearly always associ-

ated with long-spined echinoid species; these

obligate ectosymbionts often exhibit morpho-

logical adaptations such as matching the color

of echinoid hosts, possessing dark horizontal

lines that are aligned with echinoid spines, or

changing color when departing from echinoid

hosts. However, many species of crustaceans

(e.g., Hayes, 2007; Hayes et al., 2006, Hayes et

al., 2016) and fishes (e.g., Giglio et al., 2017;

Hayes et al., 2019; Karplus, 2014) associate

facultatively with echinoids, sometimes only

during the juvenile stage of their life cycle, and

lack specialized morphological adaptations for

associating with echinoids.

The frequency of ectosymbionts associ-

ated with echinoids in the eastern Pacific

Ocean has been studied for only two species

of echinoids: Centrostephanus coronatus in

California (Hartney & Grorud, 2002) and Echi-

nometra vanbrunti in Colombia (Schoppe &

Werding, 1996; Vallejo, 2007). In this study we

provide data on the frequency of five species

of decapod crustaceans (hereafter referred to

Objetivo: Evaluar la hipótesis de que los decápodos y los peces prefieren asociarse con individuos y especies de

equinoideos con espinas más largas.

Métodos: Estudiamos visualmente la frecuencia de crustáceos decápodos y peces asociados con equinoideos en

aguas poco profundas (< 4 m) y aguas más profundas (5-20 m) en Los Cabos, Baja California Sur, México, del

1-6 de enero 2019.

Resultados: Examinamos 1 058 equinoideos de seis especies. Cinco especies de decápodos se asociaron con

tres especies de equinoideos. Al comparar con otras especies de equinoideos, en aguas poco profundas, los decá-

podos se asociaron 5.1 veces más frecuentemente con la especie de equinoideo de espinas más largas, Diadema

mexicanum (7.0 veces más decápodos por individuo en D. mexicanum); en aguas más profundas, la frecuencia

fue similar para todas las especies de equinoideos. Catorce especies de peces se asociaron con 4 especies de

equinoideos. En aguas poco profundas, los peces se asociaron 2.6 veces más con D. mexicanum (4.5 veces más

peces por individuo). No hubo preferencia por una especie de equinoideo en aguas más profundas. Individuos

de D. mexicanum con espinas largas tuvieron más asociación con decápodos y peces. Las asociaciones se dieron

con mayor frecuencia en aguas poco profundas. Múltiples individuos y especies de decápodos y peces a menudo

se asociaron con un solo D. mexicanum. Un decápodo que presumiblemente es Tuleariocaris holthuisi mostró

una posible asociación obligatoria con uno de los equinoideos (D. mexicanum); las otras especies de decápodos

y todas las especies de peces presentaron asociaciones facultativas.

Conclusión: Nuestros resultados apoyan la hipótesis de que los decápodos y los peces se asociaron con mayor

frecuencia con los equinoideos con las espinas más largas, presumiblemente para reducir el riesgo de depredación.

Palabras clave: ecología costera; ectosimbiontes; asociación facultativa; Golfo de California; submareal rocoso.

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as decapods) and 14 species of fishes associ-

ated with six species of echinoids in shallow

water (< 4 m) and deeper water (5-20 m) at

Los Cabos, Baja California Sur, Mexico. We

evaluate the hypothesis that decapods and

fishes associate most frequently with echinoid

individuals and species with the longest spines,

presumably to reduce the risk of predation.

MATERIALS AND METHODS

Study area: Our study sites were located

along the coast between Cabo San Lucas

(22°52’36” N & 109°53’46” W) and Playa

Palmilla (23°00’34” N & 109°42’55” W),

within the Municipality of Los Cabos in Baja

California Sur, Mexico, at the southern tip of

the Baja California Peninsula. The study area

occurs within the Del Cabo biogeographical

province (Comisión Nacional para el Cono-

cimiento y Uso de la Biodiversidad, 1997) and

represents the southwestern border of the Gulf

of California. The coastal habitats comprise a

mixture of sandy beaches and rocky shores.

Scattered patches of stony corals and algae

cover subtidal rocks. The marine ecosystems

of the area are strongly influenced by seasonal

movements of the Inter-Tropical Convergence

Zone, which determines the southern limit of

the southward-flowing California Current and

the northern limit of the northward-flowing

Costa Rica Current (Lavín & Marinone, 2003).

The marine ecology of the Southern Gulf of

California region, which is rich in macrofaunal

diversity, is described by Brusca et al. (2005),

Brusca (2010), Ganster et al. (2012), Lluch-

Cota et al. (2007), and Thomson et al. (2000).

Sampling methods: During 1-6 January

2019 we visually surveyed the decapod crus-

taceans and fishes associated with echinoids

in rocky subtidal areas of the study area. No

specimens were collected. Snorkeling equip-

ment was used to survey echinoids in water

< 4 m deep at five localities: Playa del Amor

(22°52’36” N & 109°53’46” W), Playa las

Viudas (22°55’21” N & 109°49’24” W), Playa

Santa María (22°55’46” N & 109°48’56” W),

Playa el Chileno (22°56’49” N & 109°48’23”

W), and Playa Palmilla (23°00’34” N &

109°42’55” W). Scuba equipment was used

to survey echinoids in water 5-20 m deep at

two localities: Pared Norte (22°52’44” N &

109°53’57” W) and Roca Pelícano (22°52’44”

N & 109°53’54” W). To avoid sampling the

same echinoids twice, each species was sur-

veyed by a different observer. We surveyed an

area of approximately 6.94 ha (measured by the

dimensions of areas surveyed, which we plotted

on Google Earth; www.google.com/earth). Sur-

veys were conducted only during periods of fair

weather when the skies were clear or cloudy

and the sea surface was relatively calm.

To obtain data on the densities of shallow-

water echinoids, at Playa el Chileno only we

counted the number of echinoids of each spe-

cies in three circular 100 m2 plots for a total

of 300 m2. At each study site we carefully

inspected each echinoid observed for decapods

and fishes. An association was considered to

occur whenever a decapod or fish sought shel-

ter within 5 cm of the spines of an echinoid

and remained within 5 cm of the spines for

at least 10 s when we approached. Decapods

and fishes observed > 5 cm from an urchin

were not considered to be associated with an

urchin. We did not inspect echinoids that were

partially hidden within a crevice so that the

base of the echinoids could not be adequately

observed. We counted the number of individu-

als of each decapod and fish species associated

with each individual echinoid. For the diadema-

tid echinoids Centrostephanus coronatus and

Diadema mexicanum, which are the longest

spined echinoid species and varied the most in

spine length, we used cm markings on the edge

of an underwater writing slate held near each

echinoid to estimate spine length based on one

of three categories: 0-5 cm, 5-10 cm, and > 10

cm. We did not attempt to precisely measure

the spines because inserting a ruler within the

spines would have disturbed the echinoids and

broken off some spines. All data were written

on underwater writing slates.

The echinoids, decapods, and fishes were

identified directly in the field or photographed

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and subsequently identified based on field

guides (Allen & Robertson, 1994; Bertsch &

Aguilar Rosas, 2016; Hickman, 1998; Kerstitch

& Bertsch, 2007; Robertson & Allen, 2015) and

technical literature (Alvarado et al., 2015). The

long-spined diadematid echinoids C. coronatus

and D. mexicanum are difficult to distinguish in

the field. Centrostephanus coronatus has band-

ed spines in contrast with the uniformly dark

spines of D. mexicanum (Bertsch & Aguilar

Rosas, 2016; Hickman, 1998), but the spines

of juvenile D. mexicanum are often banded

(Alvarado et al., 2015) and the spines of some

large C. coronatus are nearly black (Pawson &

Miller, 1983). Centrostephanus coronatus is

best diagnosed by small, purple-tipped, club-

shaped spines on the aboral surface, which are

difficult to observe while inspecting echinoids

in the water, and small spines surrounding the

peristome on the oral surface, which requires

picking up an individual and turning it over for

examination (Alvarado et al., 2015; Bertsch &

Aguilar Rosas, 2016; Pawson & Miller, 1983).

None of the echinoids, decapods, or fishes were

handled or collected. Our taxonomy is based on

Solís-Marín et al. (2005) for species and Kroh

& Smith (2010) for the sequence of echinoids,

De Grave et al. (2009) for decapod crustaceans,

and Froese and Pauly (2021) for fishes.

Statistical analysis: The percent frequen-

cy of echinoids occupied by decapods and

fishes and the mean number of decapods and

fishes per echinoid were calculated separately

for each echinoid species in shallow water (< 4

m) and deeper water (5-20 m). Because of the

difficulty of identification, we combined the

data for the diadematids D. mexicanum and C.

coronatus in deeper water, where both species

were recorded (only one species was recorded

in shallow water). A Mann-Whitney U test (z

statistic; Zar, 2010) was used to compare spine

length of the diadematids between shallow and

deeper water. Chi-square analyses of contin-

gency tables (X2 statistic; Zar, 2010) or Fisher

exact tests (with exact P value) were calculated

to compare the proportions of decapods, fishes,

and all ectosymbionts combined associated

with different species of echinoids and in dif-

ferent water depth categories. When sample

sizes were too small to avoid an expected fre-

quency of < 1, no chi-square analyses were

used. Kruskal-Wallis tests (H statistic; Zar,

2010) or Mann-Whitney U tests were used to

compare the number of decapods, fishes, and

all ectosymbionts combined per echinoid of

different water depths in different water depth

categories. Spearman rank correlation coef-

ficients (rs statistic; Zar, 2010) were calculated

to compare the number of decapods, fishes, and

all ectosymbionts combined with spine length

categories of the diadematids in different water

depth categories and for all data combined.

RESULTS

Echinoid diversity, morphology, and

abundance: We visually inspected 1,058 echi-

noids of six species. The longest-spined were

the diadematids D. mexicanum and C. coro-

natus, with very thin spines up to about 15 cm

and 12.5 cm long, respectively. Two species had

medium-length spines: the echinometrid Echi-

nometra vanbrunti with thin spines up to about

6 cm long and the cidarid Eucidaris thouarsii

with thick spines up to about 5 cm long. Two

species had short spines: the toxopneustids Tri-

pneustes depressus with thin spines up to about

2 cm long and Toxopneustes roseus with thin

spines up to about 1 cm long.

In shallow water (< 4 m) at Playa el Chile-

no, E. vanbrunti was the most common species

(0.16 ind./m2), followed by D. mexicanum (0.14

ind./m2), T. depressus (0.12 ind./m2), T. roseus

(0.02 ind./m2), and E. thouarsii (0.02 ind./m2).

No individuals of C. coronatus were observed

in shallow water. In deeper water (5-20 m) at

Pared Norte and Roca Pelícano, the most com-

mon species was D. mexicanum followed by E.

thouarsii and C. coronatus. Large individuals

of the latter species were distinguished from

D. mexicanum by their banded spines, but

some unbanded individuals may have been

C. coronatus; small individuals of both D.

mexicanum and C. coronatus were banded and

unidentified. We estimated that 85 % of the

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larger diadematids in deeper water were D.

mexicanum and 15 % were C. coronatus. Spine

length of the diadematids averaged shorter in

deeper water (mean size class = 1.96, SD =

0.41, N = 95) than in shallow water (mean size

class = 2.61, SD = 0.51, N = 370; z = 10.05,

P < 0.001). No individuals of T. roseus, T.

depressus, or E. vanbrunti were observed in

deeper water.

Decapod-echinoid associations: Five spe-

cies of decapods associated with three spe-

cies of echinoids (Table 1). The frequency of

echinoids hosting decapods in shallow water

(< 4 m) differed significantly among the five

species of echinoids (X2 = 87.2, d.f. = 4, P

< 0.001) and was 5.1 times higher for the

longest-spined species, D. mexicanum, than

that of any other echinoid species (16.2 % vs

3.2 % for E. thouarsii; Table 1). No decapods

were observed associated with the two species

of echinoids with the shortest spines, T. roseus

and T. depressus (Table 1). The mean number

of decapods per echinoid in shallow water was

7.0 times higher for the longest-spined species,

D. mexicanum, than that of any other echinoid

species (0.21 vs 0.03 for E. thouarsii; H =

271.7, P < 0.001; Table 1). The frequency of

echinoids hosting decapods in deeper water did

not differ significantly between the diadematids

and E. thouarsii (2.1 % vs 3.0 %; Fisher exact

P = 1.0; Table 1) and the mean number of deca-

pods per echinoid in deeper water did not differ

significantly between the diadematids and E.

thouarsii (0.02 vs 0.03; z = 0.29, P = 0.77).

Five species of decapods associated with

D. mexicanum; of these, five species associ-

ated with 16.2 % of D. mexicanum in shallow

water and one species associated with 2.1 %

of the diadematids (none confirmed with C.

coronatus) in deeper water (Table 1). Decapods

associated more frequently with D. mexicanum

in shallow water than with the diadematids in

deeper water (X2 = 13.0, d.f. = 1, P < 0.001),

with significantly more decapods per echinoid

in shallow water than in deeper water (0.21 vs

0.02; z = 3.62, P < 0.001; Table 1). The num-

ber of decapods per echinoid was positively

correlated with spine length of D. mexicanum

in shallow water (rs = 0.13, P = 0.01) but not

with spine length of the diadematids in deeper

water (rs = 0.19, P = 0.06), and was positively

correlated with spine length of the diadematids

when all data were combined (rs = 0.19, P <

0.001; Fig. 1).

Fig. 1. Mean number of decapod and fish individuals associated with Diadema mexicanum and Centrostephanus coronatus

hosts of different size categories (data combined for shallow and deeper water) at Los Cabos, Mexico.

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TABLE 1

Percentage (mean number of individuals) of echinoids occupied by decapods, fishes, and ectosymbionts at Los Cabos, Baja California Sur, Mexico

Associates

Echinoids

Eucidaris thouarsii

< 4 m (n = 31)

Eucidaris thouarsii

5-20 m (n = 33)

Diadema

mexicanum

< 4 m (n = 370)

Diadema mexicanum

& Centro-stephanus

coronatus 5–20 m

(n = 95)

Toxopneustes roseus

< 4 m (n = 46)

Tripneustes

depressus

< 4 m (n = 116)

Echinometra

vanbrunti

< 4 m (n = 367)

Decapods (combined) 3.2 (0.03) 3.0 (0.03) 16.2 (0.21) 2.1 (0.02) — — 0.5 (0.005)

Tuleariocaris holthuisi — — 0.3 (0.003) — — — —

Petrolisthes sanfelipensis 3.2 (0.03) 3.0 (0.03) 9.5 (0.11) 2.1 (0.02) — — —

Calcinus californiensis — — 3.2 (0.04) — — — —

Percnon gibbesi — — 3.0 (0.04) ———0.3 (0.003)

Plagusia sp. — — 0.3 (0.003) ———0.3 (0.003)

Fishes (combined) 16.1 (0.19) 24.2 (0.24) 42.4 (0.86) 24.2 (0.51) 2.2 (0.02) —2.2 (0.02)

Arcos erythrops — — 0.3 (0.008)* ** — — —

Gobiesox adustus — — 0.5 (0.005)* ** — — —

Tomicodon myersi — — 0.8 (0.008)* ** — — —

Doryrhamphus excisus ———3.2 (0.05) — — —

Apogon retrosella —3.0 (0.03) 1.1 (0.01) 3.2 (0.05) — — —

Microspathodon dorsalis — — 0.5 (0.005) — — — —

Stegastes flavilatus — — 0.3 (0.003) — — — —

Thalassoma lucasanum 3.2 (0.03) —7.3 (0.11) 4.2 (0.06) — — 0.3 (0.003)

Axoclinus storeyae — — 1.6 (0.03)* ** — — 0.3 (0.003)

Cirriemblemaria lucasana — — 0.5 (0.005) — — — —

Tigrigobius limbaughi ———4.2 (0.08) — — —

Tigrigobius puncticulatus 9.7 (0.13) 15.2 (0.15) 37.3 (0.56) 7.4 (0.15) 2.2 (0.02) —1.6 (0.02)

Bathygobius ramosus — — 0.3 (0.003) — — — —

Canthigaster punctatissima 3.2 (0.03) —1.1 (0.01) 6.3 (0.06) — — —

Unidentified fishes —3.0 (0.03) 8.4 (0.11) 5.3 (0.05) — — —

Ectosymbionts (decapods and

fishes combined)

19.4 (0.23) 27.3 (0.27) 51.9 (1.07) 26.3 (0.53) 2.2 (0.02) —2.7 (0.02)

* Additional individuals possibly observed but unidentified. ** Possibly observed but unidentified.

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One species of decapod associated with

3.2 % of E. thouarsii in shallow water and

with 3.0 % in deeper water, with an average

of 0.03 decapods per echinoid in both shal-

low and deeper water (Table 1). Two species

of decapods associated with 0.5 % of E. van-

brunti, with a mean of 0.005 decapods per

echinoid (Table 1).

We observed 76 individuals of five deca-

pod species associated with echinoids in shal-

low water and two decapods of one species in

deeper water. The porcellanid crab Petrolisthes

sanfelipensis was the most common decapod

associate of echinoids, comprising 56.6 % of

the decapods observed in shallow water and

all of the decapods observed in deeper water

(Table 1). It associated with two species of

echinoids, E. thouarsii and D. mexicanum, but

did not differ between the two species in its fre-

quency of association in shallow water (Fisher

exact P = 0.34; insufficient data for deeper

water; Table 1). It usually occurred alone (83.8

%), but sometimes as a duo (13.5 %) and rarely

as a trio (2.7 %). All individuals were under-

neath the spines of echinoids (Fig. 2A); none

were observed apart from echinoids.

The diogenid hermit crab Calcinus cali-

forniensis accounted for 21.1 % of the deca-

pods associated with echinoids in shallow

water; it was not encountered in deeper water.

It associated only with the longest-spined echi-

noid, D. mexicanum (Table 1), occurring either

alone (66.7 %) or with a second individual

(33.3 %). It was usually underneath or beside

the spines of echinoids (Fig. 2B) and quick-

ly retreated deeper under the spines when

Fig. 2. Decapod crustaceans associated with the echinoid Diadema mexicanum at Los Cabos, Mexico: A. Petrolisthes

sanfelipensis; B. Calcinus californiensis; C. Percnon gibbesi; D. Plagusia immaculata or P. squamosa. Photographs by F.

E. Hayes.

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threatened. We occasionally saw individuals

apart from echinoids.

The plagusiid crab Percnon gibbesi com-

prised 18.4 % of the decapods associated with

echinoids in shallow water; it was not encoun-

tered in deeper water. It associated only with

the longest-spined echinoid, D. mexicanum

(Table 1), occurring either alone (81.8 %) or

with a second individual (18.2 %). It was usu-

ally beside the spines of echinoids and quickly

retreated under the spines when threatened

(Fig. 2C). We occasionally saw individuals

apart from echinoids.

We observed two unidentified individuals

of the plagusiid crab Plagusia immaculata or

Plagusia squamosa (Hendrickx, 1996; Schu-

bart & Ng, 2000; Schubart et al., 2001), which

accounted for 2.6 % of the decapods associated

with echinoids in shallow water; none were

encountered in deeper water. It associated

with two species of echinoids (Table 1), D.

mexicanum and E. vanbrunti, occurring alone

on both occasions under the spines of the

echinoid (Fig. 2D). We did not observe it apart

from echinoids.

A small and dark palaemonid shrimp,

presumably Tuleariocaris holthuisi (which had

been previously collected within the study area;

Wicksten & Hernández, 2000), was briefly

observed on a spine of a D. mexicanum (Table

1) at Playa el Chileno, accounting for 1.3 % of

the decapods observed associated with echi-

noids. It was not observed apart from echinoids.

Fish-echinoid associations: Fourteen spe-

cies of fishes associated with echinoids (Table

1). The frequency of echinoids hosting fishes

in shallow water (< 4 m) differed significantly

among the five species of echinoids (X2 =

283.3, d.f. = 4, P < 0.001) and was greatest

for the longest-spined species, D. mexicanum,

which was 2.6 times higher than that of any

other echinoid species (42.4 % vs 16.1 % for

E. thouarsii; Table 1). The mean number of

fishes per echinoid in shallow water was 4.5

times higher for the longest-spined species,

D. mexicanum, than that of any other echinoid

species (0.86 vs 0.19 for E. thouarsii; H =

381.6, P < 0.001; Table 1). The frequency of

echinoids hosting fishes in deeper water (5-20

m) did not differ significantly between the

diadematids and E. thousarsii (24.2 % vs 24.2

%; X2 = 0.0, d.f. = 4, P = 1.0; Table 1) and the

mean number of fishes per echinoid in deeper

water did not differ significantly between the

diadematids and E. thouarsii (0.52 vs 0.24; z =

0.25, P = 0.80).

All fourteen species of fishes associated

with D. mexicanum; of these, 12 species associ-

ated with 42.4 % of D. mexicanum in shallow

water and six species associated with 24.2 % of

the diadematids (none confirmed with C. coro-

natus) in deeper water, averaging 0.86 fishes

per echinoid in shallow water and 0.51 fishes

per echinoid in deeper water (Table 1). Fishes

associated significantly more frequently with

D. mexicanum in shallow water than with the

diadematids in deeper water (X2 = 9.8, d.f. = 1,

P = 0.001), with significantly more fishes per

echinoid in shallow water than in deeper water

(0.86 vs 0.51; z = 3.30, P = 0.001; Table 1).

The number of fishes per echinoid was not cor-

related with spine length of D. mexicanum in

shallow water (rs = 0.08, P = 0.12) or with spine

length of the diadematids in deeper water (rs =

-0.03, P = 0.76), but was positively correlated

with spine length when all data were combined

(rs = 0.13, P = 0.005).

Five species of fishes associated with E.

thouarsii; of these, three species associated

with 16.1 % of the echinoids in shallow water

and three species associated with 24.2 % of

the echinoids in deeper water (Table 1). The

frequency of fishes associated with E. thouar-

sii did not differ between shallow and deeper

water (X2 = 0.25, d.f. = 1, P = 0.62) and the

mean number of fishes per echinoid did not

differ between shallow and deeper water (0.2

vs 0.2; z = 0.71, P = 0.48; Table 1).

Three species of fishes associated with

2.2 % of E. vanbrunti, with an average of 0.02

fishes per echinoid (Table 1). Only one species

of fish associated with 2.2 % of T. roseus, with

an average of 0.02 fishes per echinoid (Table

1). No fish was observed associated with

T. depressus.

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We observed 335 individuals of 12 fish

species associated with echinoids in shallow

water and 55 fishes of six species in deeper

water. Three species of gobiesocid clingfishes

associated with echinoids: Arcos erythrops,

Gobiesox adustus, and Tomicodon myersi.

All three species associated exclusively with

the longest-spined echinoid, D. mexicanum,

together comprising 2.4 % of the fishes associ-

ated with echinoids in shallow water (Table 1).

Additional individuals were possibly observed

in both shallow and deeper water but were

not identified to species. Only adults were

observed. All were beside or underneath the

spines of echinoids (Fig. 3A). None were

observed apart from echinoids, but these cryp-

tically colored species are easily overlooked.

The syngnathid pipefish Doryrhamphus

excisus did not associate with echinoids in

shallow water but it comprised 9.1 % of the

fishes associated with echinoids in deep water,

only with the longest-spined species of echi-

noid, D. mexicanum (Table 1). Only adults

were observed, occurring alone (33.3 %) or

in pairs (66.7 %). None were observed apart

from echinoids.

The apogonid cardinalfish Apogon retro-

sella comprised 1.2 % of the fishes associated

with echinoids in shallow water and 10.9 %

in deeper water (Table 1). In both shallow and

deeper water, it associated almost exclusively

with the longest-spined species of echinoid,

D. mexicanum, but it did not associate more

frequently with the diadematids in either shal-

low or deeper water (Fisher exact P = 0.15;

Table 1). One individual associated with an E.

thouarsii in deep water (Table 1). It was usu-

ally alone (87.5 % for all echinoids combined)

but one D. mexicanum hosted three individu-

als. Both adults and juveniles associated with

Fig. 3. Fishes associated with the echinoid Diadema mexicanum at Los Cabos, Mexico: A. Tomicodon myersi; B. Apogon

retrosella; C. juvenile Microspathodon dorsalis; D. juvenile Thalassoma lucasanum. Photographs by F. E. Hayes.

796 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 787–803, e49587, enero-diciembre 2022 (Publicado Nov. 21, 2022)

echinoids, sheltering beside or under the spines

(Fig. 3B). We often observed individuals in

crevices apart from echinoids.

Two species of pomacentrid damselfishes,

Microspathodon dorsalis and Stegastes fla-

vilatus, associated exclusively with the longest-

spined species of echinoid, D. mexicanum,

accounting for 0.6 % and 0.3 %, respectively, of

the fishes associated with echinoids in shallow

water (Table 1). Most individuals, including all

adults, did not associate with echinoids. Only a

few juveniles < 6 cm long associated with echi-

noids, sheltering among the spines (M. dorsalis

in Fig. 3C).

The labrid wrasse Thalassoma lucasanum

was the second most common fish associ-

ated with echinoids, comprising 12.5 % of the

fishes associated with echinoids in shallow

water and 10.9 % in deeper water (Table 1). In

shallow water it associated with three species

of echinoids but it associated most frequently

with the longest-spined species, D. mexicanum

(X2 = 25.1, d.f. = 2, P < 0.001), at a rate 2.3

times higher than any other echinoid species

(7.3 % vs 3.2 % for E. thouarsii; Table 1). It

usually occurred alone (77.8 % for all echinoid

species combined), with up to five individuals

associated with D. mexicanum. In deeper water

it associated only with D. mexicanum (and

possibly C. coronatus), either alone (50 %) or

in pairs (50 %). Its frequency of association

with the diadematids did not differ between

shallow water and deeper water (X2 = 0.71, d.f.

= 1, P = 0.40). The number of individuals per

echinoid was not correlated with spine length

of the diadematids in either shallow water (rs

= 0.10, P = 0.07) or deeper water (rs = 0.02,

P = 0.82), but the correlation was significant

for both depth categories combined (rs = 0.10,

P = 0.04; Fig. 1). Most individuals, including

all adults, did not associate with echinoids. We

only observed juveniles < 6 cm long associ-

ated with echinoids, seeking shelter among the

spines (Fig. 3D).

The tripterygiid triplefin Axoclinus sto-

reyae comprised 3.3 % of the fishes associated

with echinoids in shallow water. Additional

individuals may have been observed but were

not identified. Up to three associated only with

the longest-spined species of echinoid, D. mexi-

canum (Table 1). All were adults and were shel-

tering beside or beneath the spines of echinoids.

Some were observed apart from echinoids.

The chaenopsid blenny Cirriemblemaria

lucasana accounted for 0.6 % of the fishes

associated with echinoids in shallow water,

exclusively with the longest spined-species of

echinoid, D. mexicanum (Table 1). Both were

solitary adults, sheltering beneath the spines of

echinoids (Fig. 4A). None was observed apart

from echinoids.

The gobiid goby Tigrigobius puncticulatus

was the most common fish associated with

echinoids, comprising 65.4 % of the fishes

associated with echinoids in shallow water and

33.9 % of the fishes in deeper water (Table

1). In shallow water it associated with four

species of echinoids, most frequently with the

longest-spined species, D. mexicanum (X2 =

167.9, d.f. = 3, P < 0.001), at a rate 3.8 times

higher than any other echinoid species (37.3 %

vs 9.7 % for E. thouarsii; Table 1). It usually

occurred alone (66.2 % for all echinoid species

combined), with up to six individuals with D.

mexicanum and up to two with E. thouarsii and

E. vanbrunti. In deeper water it associated with

two species of echinoids, E. thouarsii and D.

mexicanum (none confirmed with C. corona-

tus), with similar frequencies (X2 = 0.95, d.f.

= 1, P = 0.33), usually alone (83.3 % for both

echinoid species combined) but with up to six

individuals with D. mexicanum. It associated

more frequently with the diadematids in shal-

low water than in deeper water (X2 = 30.2,

d.f. = 1, P < 0.001), but it did not differ in

its frequency of association with E. thouarsii

between shallow water and deeper water (X2

= 0.08, d.f. = 1, P = 0.78; Table 1). The mean

number of individuals per diadematid was sig-

nificantly higher in shallow water than in deep-

er water (0.56 vs 0.15; z = 5.51, P < 0.001).

The number of individuals per echinoid was not

correlated with spine length of the diadematids

in either shallow water (rs = 0.02, P = 0.64)

or deeper water (rs = 0.03, P = 0.75), but was

significantly correlated with spine length when

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all data were combined (rs = 0.14, P = 0.002).

Individuals of all ages usually occurred around

the perimeter of echinoids and most quickly

sought refuge under the spines when disturbed

(Fig. 4A, Fig. 4B). Although we often observed

individuals apart from echinoids, most were

within 10 cm of echinoids. The only individual

associated with the short-spined echinoid T.

roseus retreated repeatedly underneath it.

Two other gobiid gobies associated much

less frequently with echinoids. Tigrigobius

limbaughi did not associate with echinoids in

shallow water but it comprised 14.3 % of the

fishes associated with the diadematids, under

the spines, in deeper water (Table 1, Fig. 4B).

Up to three individuals, all adults, associated

with an echinoid. A single juvenile Bathygobi-

us ramosus rested on top of an unidentified

sponge under the spines of a D. mexicanum

(Fig. 4C), representing only 0.3 % of the fishes

associated with echinoids in shallow water

(Table 1).

The tetraodontid puffer Canthigaster

punctatissima accounted for 1.5 % of the fishes

associated with echinoids in shallow water

and 12.3 % in deeper water (Table 1). In both

shallow and deeper water it associated almost

exclusively with the longest-spined species

of echinoid, D. mexicanum (none confirmed

with C. coronatus), but one individual in shal-

low water shuttled back and forth between a

D. mexicanum and an E. thouarsii (Table 1).

It associated more frequently with the diade-

matids in deeper water than in shallow water

(Fisher exact P = 0.007; Table 1). Most indi-

viduals, including all adults, did not associate

Fig. 4. Fishes associating with the echinoid Diadema mexicanum at Los Cabos, Mexico: A. Cirriemblemaria lucasana

(above) and two Tigrigobius puncticulatus (below); B. two Tigrigobius puncticulatus (left) and Tigrigobius limbaughi

(center); C. Bathygobius ramosus; D. juvenile Canthigaster punctatissima. Photographs by F. E. Hayes.

798 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 787–803, e49587, enero-diciembre 2022 (Publicado Nov. 21, 2022)

with echinoids. We only observed juveniles <

6 cm long, always alone, seeking shelter within

the spines of echinoids (Fig. 4D).

Ectosymbiont-echinoid associations:

Multiple individuals and species of decapods

and fishes often associated together with a

single D. mexicanum host in shallow water (<

4 m), with maximum counts of three decapod

individuals, two decapod species, eight fish

individuals, four fish species, and two deca-

pod species together with two fish species.

In deeper water (5-20 m) we never observed

more than one decapod or a decapod and fish

together with an echinoid host, but we observed

up to nine fish individuals and four fish species

with a host.

The frequency of echinoids hosting ecto-

symbionts (decapods and fishes combined) in

shallow water (< 4 m) differed significantly

among the five species of echinoids (X2 =

310.6, d.f. = 4, P < 0.001) and was greatest

for the longest-spined species of echinoid, D.

mexicanum, which was 2.7 times higher than

for any other echinoid species (51.9 % vs 19.4

% for E. thouarsii; Table 1). The mean number

of ectosymbionts per echinoid in shallow water

was 4.7 times higher for the longest-spined

species, D. mexicanum, than that of any other

echinoid species (1.07 vs 0.23 for E. thouarsii;

H = 426.9; P < 0.001; Table 1). The frequency

of echinoids hosting ectosymbionts in deeper

water (5-20 m) did not differ significantly

between the diadematids and E. thousarii (26.3

% vs 27.3 %; X2 = 0.0, d.f. = 1, P = 1.0;

Table 1). The mean number of ectosymbionts

per echinoid in deeper water did not differ

significantly between the diadematids and E.

thouarsii (0.53 vs 0.27; z = 0.18, P = 0.86). The

number of ectosymbionts per echinoid was cor-

related with spine length of D. mexicanum in

shallow water (rs = 0.13, P = 0.01) but not with

spine length of the diadematids in deeper water

(rs = 0.03, P = 0.80), and was correlated with

spine length of the diadematids when all data

were combined (rs = 0.20, P < 0.001).

DISCUSSION

Decapod-echinoid associations: We

recorded seven new records of association

between decapods and echinoids. No species

of decapod had been reported associating with

the echinoid E. thouarsii; thus, our study adds

P. sanfelipensis as an associate of E. thouarsii.

Only three species of decapods, Clastotoe-

chus gorgonensis, Stenorhynchus debilis, and

T. holthuisi, had been reported associating

with the echinoid D. mexicanum (Marin &

Anker, 2009; Salas-Moya et al., 2021; Schoppe

& Werding, 1996; Wicksten & Hernández,

2000). Our study adds P. sanfelipensis, C.

californiensis, P. gibbesi, and Plagusia sp. as

associates of D. mexicanum. No species of

decapod had been reported associating with

the echinoids C. coronatus or T. roseus, and

one decapod, Gnathophylloides mineri, had

been reported associating with the echinoid T.

depressus (Salas-Moya et al., 2021; Wicksten

& Hernández, 2000). We did not confirm any

decapods associating with these three echinoid

species. At least ten taxa of decapods had

been reported associating with the echinoid E.

vanbrunti (Vallejo, 2007), including Palaemon

sp., Gnathophyllidae sp., Alpheus sp., C. gorgo-

nensis, Petrolisthes armatus, Pachycheles sp.,

Megalobrachium sp., Mithraculus denticulatus,

Xanthidae sp., and Pachygrapsus transversus.

Our study adds P. gibbesi and Plagusia sp. as

associates of E. vanbrunti.

Only one of the five species of decapods

observed during this study, T. holthuisi, appears

to associate exclusively with echinoids (Marin

& Anker, 2009). However, Percnon gibbesi usu-

ally associates with echinoids of four species,

especially Diadema antillarum, in the Caribbe-

an Sea (Hayes et al., 2016), but it has not been

reported associating with any echinoids in the

Pacific Ocean or where it has been introduced

in the Mediterranean Sea (Félix-Hackradt et

al., 2018). Our observations confirm that P.

gibbesi also associates with echinoids in the

eastern Pacific Ocean. Our observations also

reveal that P. sanfelipensis and C. californiensis

frequently associate with echinoids. Although

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four of the five species of decapods in our

study appeared to associate facultatively with

echinoids, some associations may have been

incidental rather than intentional.

Decapods in shallow water (< 4 m) associ-

ated with the longest-spined species of echi-

noid, D. mexicanum, more frequently and with

a higher number of individuals per echinoid

than for any other echinoid species. These

results are consistent with controlled experi-

ments demonstrating that the palaemonid

shrimp Tuleoariocaris neglecta and the inachid

crab Stenorhynchus seticornis, when given a

choice of several echinoid species, preferred

to associate with the longest-spined species, D.

antillarum (Castro, 1978; Joseph et al., 1998).

Our results are also consistent with an obser-

vational study demonstrating that decapods in

Honduras preferred to associate with the lon-

gest-spined species of echinoid, D. antillarum,

more frequently and with a higher number of

individuals per echinoid than that of any other

echinoid species (Hayes et al., 2019). In deeper

water (5-20 m), the frequency of association

and the number of decapods per echinoid inex-

plicably were not significantly greater for the

longest-spined diadematids. However, the num-

ber of decapods per echinoid was positively

correlated with spine length of the diadematids

when all data were combined. These results

contrast with a previous study in which the

decapods P. gibbesi and S. seticornis did not

prefer to associate with the longest-spined indi-

viduals of D. antillarum (Hayes et al., 1998).

Fish-echinoid associations: Of the 14 fish

species that we observed associated with echi-

noids, only two had been reported associating

with echinoids: Tigrigobius puncticulatus asso-

ciated with the echinoid E. thouarsii (Thom-

son et al., 2000), which we also documented,

and G. adustus associated with the echinoid

E. vanbrunti (Vallejo, 2007), which we did

not document. An additional species of fish,

Arcos decoris, has been reported associating

with E. vanbrunti (Schoppe & Werding, 1996).

We recorded 21 new records of association

between fishes and echinoids, including: the

fishes A. retrosella, T. lucasanum and A. hispi-

dus associated with the echinoid E. thouarsii;

the fishes A. erythrops, G. adustus, T. myersi,

D. excisus, A. retrosella, M. dorsalis, S. flavila-

tus, T. lucasanum, A. storeyae, C. lucasana, T.

limbaughi, T. puncticulatus, B. ramosus, and

A. hispidus associated with the echinoid D.

mexicanum; the fish T. puncticulatus associ-

ated with the echinoid T. roseus; and the fishes

T. lucasanum, A. storeyae, and T. puncticulatus

associated with the echinoid E. vanbrunti.

None of the 14 species of fishes are known

to associate exclusively with echinoids, indicat-

ing that the associations are facultative rather

than obligatory. All fishes associated with echi-

noids were small, < 6 cm in body length. Only

small fishes are capable of retreating under-

neath or among the spines of echinoids, poten-

tially benefitting from the protective spines

of echinoids (Karplus, 2014). In five of the

14 fish species only juveniles associated with

echinoids. Many larger fish species are known

to associate facultatively with echinoids only as

juveniles (e.g., Giglio et al., 2017; Hayes et al.,

2019; Karplus, 2014).

Fishes in shallow water (< 4 m) associated

with the longest-spined species of echinoid, D.

mexicanum, more frequently and with a higher

number of individuals per echinoid than for any

other echinoid species. These results are consis-

tent with an observational study demonstrating

that fishes in Honduras preferred to associate

with the longest-spined species of echinoid, D.

antillarum, more frequently and with a higher

number of individuals per echinoid than that of

any other echinoid species (Hayes et al., 2019).

In deeper water (5-20 m), the frequency of

association and the number of fishes per echi-

noid inexplicably were not significantly greater

for the longest-spined species, D. mexicanum

(and C. coronatus). However, the number of

fishes per echinoid was positively correlated

with spine length of the diadematids when all

data were combined.

Echinoids are preyed upon by a variety of

fish species, with at least seven fish species

known to prey on D. mexicanum (Alvarado et

al., 2015). Small fishes seeking shelter under or

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among the spines of echinoids do not constitute

an existential threat to the echinoids (Karplus,

2014), but some fishes prey upon the podia

and pedicillaria of echinoid hosts (Briggs,

1955; Dix, 1969; Pfaff, 1942; Russell, 1983;

Sakashita, 1992; Teytaud, 1971). Although we

did not observe any predation on echinoids

by fishes, predation on podia and pedicillaria

may provide an alternative explanation for why

fishes associate with echinoids.

Ectosymbiont-echinoid associations:

Our data indicate that multiple individuals and

species of decapods and fishes often associ-

ate together with a single echinoid host, all

presumably seeking shelter to reduce the risk

of predation. Although we did not observe

any interspecific behavior interactions among

decapods, fishes, and their echinoid hosts, we

cannot exclude the possibility of competitive or

predatory interactions. Such potential interspe-

cific behavioral interactions merit further study.

Decapods, fishes, and both groups com-

bined associated more frequently with echi-

noids in shallow water (< 4 m) than in deeper

water (5-20 m). A previous study found no

difference between the association of decapods

with echinoids in shallow water and deeper

water in Honduras (Hayes et al., 2016), but

P. gibbesi associated more frequently with D.

antillarum in shallow water and S. seticornis

associated more frequently with D. antillarum

in deeper water. Our results suggest that pre-

dation on decapods and fishes may be more

intense in shallow water than in deeper water,

but more investigation is needed before any

conclusions are warranted.

Our results support the hypothesis that

decapods and fishes associate most frequently

with echinoid individuals and species with the

longest spines, presumably to reduce the risk of

predation. Other factors may also affect the fre-

quency and abundance of ectosymbionts asso-

ciated with echinoids, such as the availability of

nutrients (which influences size of echinoids),

type of substrate, shape of substrate (cracks and

cavities may attract more ectosymbionts), and

water currents.

Ethical statement: The authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict 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

Our field work was funded by the Her-

bert Family Faculty Development Fund and

Margaret Hughes Biology Faculty Research

Fund of Pacific Union College. We thank

Michel Hendrickx for assistance with identify-

ing crustaceans, Ross Robertson for assistance

with identifying fishes, and two anonymous

reviewers for suggestions that improved the

manuscript.

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