Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 66-79, March 2021 (Published Mar. 30, 2021)

Feeding habits of Holothuria (Stauropora) fuscocinerea

(Echinodermata: Holothuroidea) in a Mexican Pacific reef

Brenda Maya-Alvarado

1,2

Laura Georgina Calva-Benítez

Rebeca Granja-Fernández

Jessica Pérez-López

Andrés López-Pérez

1. Programa de Maestría en Ciencias en Biosistemática y Manejo de Recursos Naturales y Agrícolas, Centro

Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Av. Ing. Ramón Padilla Sánchez,

Zapopan, Jalisco, México; brenda.maya9471@alumnos.udg.mx

2. Laboratorio de Ecosistemas Costeros. Departamento de Hidrobiología, Universidad Autónoma Metropolitana Unidad

Iztapalapa, Av. San Rafael Atlixco, Col. Vicentina, Iztapalapa, Ciudad de México, México; cblg@xanum.uam.mx,

je_si13@hotmail.com, alopez@xanum.uam.mx (*Correspondence).

3. Laboratorio de Ecología Marina. Centro Universitario de la Costa, Universidad de Guadalajara, Av. Universidad,

Puerto Vallarta, Jalisco, México; beckygranja@gmail.com

Received 01-VI-2020. Corrected 10-IX-2020. Accepted 07-X-2020.

ABSTRACT

Introduction: The importance of holothuroids in marine ecosystems is related to their feeding activities, which

have been little studied in the eastern Pacific. Objective: To describe the feeding habits of the sea cucumber

Holothuria (Stauropora) fuscocinerea and their bioturbation potential in La Entrega reef, México. Methods:

The population size of H. (Stauropora) fuscocinerea was determined by means of four 20 x 4 m (320 m

) band

transects, while the available sediment for the sea cucumbers and their feces were characterized in three stations

(A-C) via granulometry and quantification of organic carbon and organic matter. Excretion rate was determined

every 4 hr over a 24 hr period and the relationship between sea cucumber length and biomass and the excretion

rate evaluated. Results: According to non-parametric permutation, ordination and percentage similarity analy-

ses, sea cucumber feces mostly comprised a large proportion of small grains compared to the available sediment,

indicating that H. (Stauropora) fuscocinerea is selective on grain size. Preliminary bioturbation potential of the

species may reach up to 8.71 ± 0.17 kg day of sediment in the study area. Conclusion: The spatial distribution

of H. (Stauropora) fuscocinerea in the study area is a product of its selective feeding activity, evidencing the

preliminary importance of the species in the trophic dynamics of La Entrega reef.

Key words: selectivity; distribution; food; bioturbation; sea cucumber.

Maya-Alvarado, B., Calva-Benítez, L.G., Granja-

Fernández, R., Pérez-López, J., & López-Pérez, A.

(2021). Feeding habits of Holothuria (Stauropora)

fuscocinerea (Echinodermata: Holothuroidea) in a

Mexican Pacific reef. Revista de Biología Tropical,

69(S1), 66-79. DOI 10.15517/rbt.v69iSuppl.1.46328

Holothuroids, commonly known as sea

cucumbers, are conspicuous and abundant

invertebrates that contribute largely to the bio-

mass of marine ecosystems (Hendler, Miller,

Pawson & Kier, 1995). As a result of their

feeding activity and diet, they can bioturbate

large amounts of sediments every year (i.e.

Crozier, 1918; Bonham & Held, 1963; Bakus,

1973; Uthicke, 1999; Purcell, Conand, Uthicke

& Byrne, 2016), contributing to important

DOI 10.15517/rbt.v69iSuppl.1.46328

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 66-79, March 2021 (Published Mar. 30, 2021)

chemical and physical processes on the sea-

floor, and promoting the continuous mixing

of the sediment particles (Thayer, 1983). Sea

cucumbers actively participate in the recycling

of nutrients and organic matter within marine

ecosystems (Bakus, 1973; Calva-Benítez,

2002), including coral reefs (Goldberg, 2013;

Sheppard, Davy, Pilling & Graham, 2017).

Despite being conspicuous and abundant

in coral reefs around the world (Sheppard et

al., 2017), the study of their feeding habits

and their importance in sediment bioturbation

in tropical reefs has focused mostly on holo-

thuroids from the Indo-Pacific (Yang et al.,

2005; Bucol, Cadivida & Wagey, 2018; Rioja,

Palomar-Abesamis & Juinio-Meñez, 2020).

Those studies have highlighted the selective

nature of the feeding habits of holothuroids,

as well as their capacity to remove large

amounts of sediment and the wide spatial and

temporal variation that exists among species

(Trefz, 1956; Glynn, 1965; Bakus, 1968, 1973;

Uthicke, 1999; Mezali & Soualili, 2013; Bel-

bachir, Mezali & Soualili, 2014).

Holothuria (Stauropora) fuscocinerea is

among the most common and widely dis-

tributed holothuroid in the Indo and eastern

tropical Pacific (Purcell, Samyn & Conand,

2012; Solís-Marín et al., 2013; Cortés et al.,

2017). However, little is known about its

biology, abundance and distribution, feeding

habits and generally, the role that this species

plays in the ecosystem. To date, the only study

of the species in the region is limited to its

annual reproductive periodicity on the coast

of Oaxaca, México (Benítez-Villalobos, Avila-

Poveda, & Gutiérrez-Méndez, 2013). In the

Mexican Pacific and the Gulf of California, sea

cucumbers such as Isostichopus fuscus (Herre-

ro-Pérezrul & Chávez, 2005) and Holothuria

(Halodeima) inornata are regularly exploited

commercially and are currently under the pro-

tection of Mexican laws (SEMARNAT, 2019).

On the other hand, H. (Stauropora) fuscoci-

nerea, is of commercial importance in China,

Malaysia and the Philippines (Purcell et al.,

2012), but lacks protection status in México.

Due to the paucity of information about the

species, its commercial importance and the rel-

evance of holothuroids for bioturbation in reef

ecosystems, this study aims to: a) determine the

feeding habits of H. (Stauropora) fuscocinerea

in a tropical reef in the Mexican Pacific, and b)

address their bioturbation potential. With this

information, inferences can be made in terms

of its small-scale distribution, along with its

feeding selectivity and its contribution to sedi-

ment bioturbation in a typical reef system of

the eastern tropical Pacific.

MATERIALS AND METHODS

Study area: The study was carried out at

La Entrega bay (15°44’34’’ N & 96°07’35’’ W),

located in southwest end of the Gulf of Tehu-

antepec, Oaxaca, México (Fig. 1). La Entrega

is a small (0.1 km

) embayment located on the

west side of Santa Cruz bay. The seafloor of La

Entrega consists of marine carbonate sediment

mixed with siliciclastic material derived from

the basaltic highlands of the Copalita river

basin (Estrada-Vargas, 2008). The center of

La Entrega is largely covered by an approxi-

mately 4.3 ha reef framework that follows a

southwest-northeast direction and reaches 12

m in depth (Glynn & Leyte-Morales, 1997).

The coral community is composed by 11 coral

species, live coral cover comprises 76.58 %

of the reef area, while the framework is built

mainly by Pocillopora spp. species (> 95 %),

followed by Pavona spp. and Porites pana-

mensis (López-Pérez & López-García, 2008;

Cabral-Tena et al., 2020).

The southwestern portion of the reef cor-

responds to the reef flat (2-5 m in depth) and

comprises most of the reef framework, while

the fore reef comprises ~ 30 % of the area.

While the former results of the interlocking of

Pocillopora spp. colonies, the fore reef area

is a transition zone where live coral cover

is severely reduced (~ 70 %) and branch-

ing Pocillopora spp. and the massive corals

Pavona gigantea and Pavona varians coexist

with the emerald coral P. panamensis, along

with sparse patches of sand and dead corals

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 66-79, March 2021 (Published Mar. 30, 2021)

(Glynn & Leyte-Morales, 1997; López-Pérez

& Hernández-Ballesteros, 2004) (Fig. 1).

La Entrega reef is habitat of several marine

invertebrates, including echinoderms (López-

Pérez et al., 2019). Among the echinoderm

species, the sea cucumber H. (Stauropora) fus-

cocinerea is mainly distributed in the fore reef

transition zone between the reef flat and the

sandy area (transition zone A), as well as in the

live coral-coral rubble (zone B) but absent in

the sand area (C) (Fig. 1). Finally, La Entrega

has been subjected to intense touristic activity

and recurrent dredging at least yearly since the

early 1990’s, which has resulted in high quanti-

ties of organic matter, therefore diminishing the

health of the system (López-Pérez & Hernán-

dez-Ballesteros, 2004; Díaz-Díaz, 2017).

Fieldwork: The population density of H.

(Stauropora) fuscocinerea (Fig. 2A) in La

Entrega was determined during SCUBA div-

ing visual censuses, using four 20 x 4 m (320

m²) belt transects. During January 2018, visual

census was conducted at two stations parallel

to the coastline, called A and B, at a depth of

10 m (Fig. 1).

The available sediment was collected in

situ near the mouth and feces near the anus

of 20 specimens of H. (Stauropora) fuscoci-

nerea (Fig. 2A, 2B, 2C), randomly selected in

each of the stations A and B, in which coral

sand (A) and coral debris (B) predominate

(Fig. 1). The samples were collected manu-

ally with a plastic spoon, placed in individual

Fig. 1. Sampling stations (A, B, C [experimental cages]) and zoning of La Entrega reef, Mexican Pacific. See text for

information regarding sampling stations.

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 66-79, March 2021 (Published Mar. 30, 2021)

sealable plastic bags, and stored frozen until

subsequent processing.

Furthermore, individuals of H. (Stauro-

pora) fuscocinerea were placed in individual

enclosures (one individual per enclosure, ten

enclosures) at station C in order to measure the

rate of excretion of the cucumbers over a total

period of 24 h. These enclosures were con-

structed of wire rod and cloth mesh and were 1

m in diameter (Fig. 3); on the upper and lateral

part, each enclosure was covered with the cloth

mesh, while the lower part allowed H. (Stau-

ropora) fuscocinerea to feed on the sediment.

The enclosures were anchored to the bottom to

prevent escape of the organisms. In each con-

finement, the feces of sea cucumbers were col-

lected at 4 h intervals over a 24 h period (T1 =

21:40 hr; T2 = 1:40 hr; T3 = 5:40 hr; T4 = 9:40

hr, T5 = 13:40 hr; T6 = 17:40 hr; T7 = 21:40

hr). In order to characterize the sediments from

which the sea cucumbers were feeding in each

enclosure, three sediment samples from each

enclosure (3 x 10 enclosures, N = 30) were col-

lected at the beginning (T1) of the experiment.

The collected fecal and sediment samples were

placed in individual sealable plastic bags and

stored at low temperature (≈ 4 °C) until subse-

quent analysis in the laboratory.

Finally, the length of the individuals that

remained in the enclosures was measured with

a metric tape (length/width) every 4 h and this

parameter was related to the wet weight, which

was obtained 90 seconds after removing the

animals from the water (Uthicke, 1999) at the

end of the experiment, using an Oahus CR2200

balance (± 1 g precision).

Laboratory work: Samples (sediment

and feces) were thawed, placed on aluminum

trays and dried at room temperature until dry.

Sediment texture analysis was then performed

and the content of organic carbon (O.C.) and

organic matter (O.M.) determined.

Granulometric analysis was performed

using the dry sieving technique. The dry

weights of the following fractions were deter-

mined: granules (2 000 µm), very coarse sand

(1 000 µm), coarse sand (500 µm), medium

sand (250 µm), fine sand (125 µm), very fine

sand (62.5 µm), and silt (28 µm).

The O.C. content was determined using the

technique proposed by Gaudette, Flight, Toner

& Folger (1974), which consists of drying the

sediments at room temperature and then siev-

ing them to remove gravel through a 62.5 µm

mesh (0.500 g of it is treated). The organic mat-

ter is then oxidized, and the excess potassium

dichromate titrated with ferrous sulfate. The

samples were analyzed in duplicates and two

blanks processed in the same way as controls.

With this technique, the presence of carbonates

does not produce interference, has an accuracy

of ± 0.25 %, and yields solid results (Shoham-

Frider et al., 2020). In addition, the technique

has been successfully used to evaluate the abil-

ity of holothuroids to remove organic matter

Fig. 2. A. Holothuria (Stauropora) fuscocinerea. B. Feces of Holothuria (Stauropora) fuscocinerea. C. Close-up feces.

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 66-79, March 2021 (Published Mar. 30, 2021)

in eutrophic and hypereutrophic environments

(Emiroglu & Günay, 2007).

Finally, the organic matter (O.M.) con-

tent was estimated as the product of the O.C.

using the van Bemmelen factor (1.72; Grybos,

Davranche, Gruau & Petitjean, 2007) who

assume that, on average, 58 % of the O.M. is

composed of carbon.

Data analysis: In order to graphically

represent the relationships between sediment

samples and feces from the three stations (A, B,

C), the database (size fractions + O.C. + O.M.)

was analyzed using a principal components

analysis (PCA) from a normalized matrix.

Since PCA is an ordination technique and

does not have an associated statistical hypoth-

esis, statistical differences between sediment

and feces were evaluated using a permutations-

based unbalanced factor analysis of variance

(PERMANOVA). The stations (A, B, C) were

considered as a fixed factor (type I model).

The PERMANOVA was constructed from a

Euclidean distance matrix following the criteria

of Anderson, Gorley & Clarke (2008). Non-

parametric analysis was performed since data

did not meet the assumptions of normality and

homoscedasticity.

In order to explore the degree of selectivity

of the individuals during the feeding process, a

Fig. 3. Experimental cages used in the field study during January 2018. La Entrega reef, Mexican Pacific.

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 66-79, March 2021 (Published Mar. 30, 2021)

percentage similarity test (SIMPER) was car-

ried out with the aim of estimating the similar-

ity/dissimilarity of the available sediment and

feces among the sampling stations, and also to

identify which variables contributed the most

to explaining these compositional differences.

Simple linear regression models were per-

formed to establish a relationship between the

length of the individuals and the biomass, as

well as between the length and dry weight

of the feces. On the other hand, in sampling

station C, it was evaluated if there were dif-

ferences in the excretion rate over time using

a one-way non-parametric analysis of variance

(ANOVA) with fixed effects. Finally, the pre-

liminary bioturbation potential of the species

in the study area was estimated considering

population density, the area inhabited, and the

excretion rate by H. (Stauropora) fuscocinerea

in La Entrega.

PCA, PERMANOVA and SIMPER were

performed using the PRIMER 6 + PER-

MANOVA software (Anderson et al., 2008).

The regression models and the non-parametric

ANOVA were carried out in the STATISTICA

v.7.1 software (Statsoft, 2020). All statistical

tests used α = 0.05.

RESULTS

Density and individual size: Holothu-

ria (Stauropora) fuscocinerea distribute dif-

ferentially across space in La Entrega reef. The

species is absent from the Pocillopora spp.

interlocking patch and the sandy area (0.0 ind/

), but in the transition and live coral/coral

rubble area may reach an average of 0.27 ind/

(± 0.02). Additionally, individuals had an

average length of 24.60 cm (± 5.77) and an

average weight of 142 g (± 41.64).

Sediment and feces composition: Sedi-

ment and feces composition of H. (Stauropora)

fuscocinerea for each sampling station are

presented in Table 1, and PCA ordination sum-

marize the trends among sediment and feces,

but also among stations.

From sampling station A to C, there is

an increase in large size fractions of sediment

(granule-very coarse sand), while the opposite

trend is recorded for coarse sand to fine sand

fractions, including organic carbon and matter;

meanwhile, for very fine sand and silt fractions,

large values were recorded in station B, fol-

lowed by station A and C, respectively (Table

1). The observed trend in sediment composition

(granulometry, C.O., and M.O.) across space

is supported by permutational analysis of vari-

ance (Pseudo-F

(2,26)

= 6, P = 0.0001); according

to the analysis, differences in sediment compo-

sition occurred among station A and C (Pseudo-

t = 2.81, P = 0.0008), and C and B (Pseudo-t

= 3.42, P = 0.0001), while sediment compo-

sition between station A and B is relatively

homogeneous. In station C, the sediments are

characterized by granules, very coarse sands

and coarse sands with O.C. content of 0.33

% and O.M. content of 0.56 % (Table 1). In

stations A and B, in addition to their O.C. and

O.M. characteristics, the sediments are highly

heterogeneous among samples within the same

station which translates in the wide overlap in

the characteristics between stations A and B

(Pseudo-t = 1.52, P = 0.07; Table 1, Fig. 4).

Regarding feces, for granules and silt,

station B had larger values than station A, fol-

lowed by station C; for very coarse sand and

coarse sand, station C showed larger values

than station B, followed by station A; finally,

for medium sand and fine sand fractions, feces

in station A showed larger values than stations

C and B, respectively (Table 1). Feces com-

position show a relative homogeneity among

samples from the same station (Fig. 4), and the

overlap between stations is relatively smaller,

suggesting there is less variation among feces

than among the sediment available to sea

cucumbers in each sampling station. In general,

the feces from station A are characterized by

their content of medium sand, coarse sand, fine

sand and very coarse sand along with moder-

ate values of O.C. (0.70 %) and O.M. (1.21

%) (Table 1). The feces from station B are

characterized by very coarse sand, granules,

coarse sand, medium sand, and relatively high

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 66-79, March 2021 (Published Mar. 30, 2021)

O.C. (1.04 %) and O.M. (1.8 %) values, while

those at station C are dominated by very coarse

sand, coarse sand, medium sand, and relatively

low O.C. (0.51 %) and O.M. (0.87 %) values

(Table 1, Fig. 4).

Size selection of sediment particles: The

PERMANOVA indicated that there were differ-

ences between sediment and feces composition

in stations B (Pseudo-t = 1.90, P = 0.01) and C

(Pseudo-t = 2.74, P = 0.0007), but not between

Fig. 4. Ordination (Principal Components Analysis) of sediment (open figures) and feces (filled figures) composition across

space in La Entrega reef, Mexican Pacific. Sampling stations, A = green, B = blue, C = red. See Figure 1 for spatial location

of sampling stations. Vector longitude = relative importance of the variable in the ordination. OM = Organic matter, OC =

Organic carbon, G = Granule, VCS = Very coarse sand, CS = Coarse sand, MS = Medium sand, S = Sand, FS = Fine sand,

VFS = Very fine sand, S = Silt.

TABLE 1

Percentage of size fractions, organic carbon and organic matter of available sediments and feces

of Holothuria (Stauropora) fuscocinerea in La Entrega reef, Mexican Pacific

Size fraction

Sediment Feces

A B C A B C

Granule 12.81 ± 9.75 23.91 ± 7.82 36.28 ± 7.26 5.84 ± 8.78 26.62 ± 15.44 3.05 ± 1.59

Very coarse sand 17.08 ± 10.39 21.61 ± 6.34 27.65 ± 3.4 10.06 ± 12.27 28.1 ± 8.17 35.03 ± 11.04

Coarse sand 34.66 ± 10.45 29.76 ± 4.21 26.58 ± 6.05 23.45 ± 11.82 23.55 ± 6.94 29.52 ± 3.12

Medium sand 28.52 ± 14.86 18.35 ± 9.43 8.44 ± 3.95 36.55 ± 14.85 12.05 ± 4.03 22.2 ± 8.18

Fine sand 6.2 ± 6.34 4.65 ± 2.23 1 ± 0.5 19.68 ± 12.68 5.2 ± 2.8 6.23 ± 4.28

Very fine sand 0.57 ± 0.6 1.13 ± 0.42 0.01 ± 0.02 3.51 ± 2.7 3.04 ± 1.47 3.97 ± 3.3

Silt 0.16 ± 0.19 0.59 ± 0.47 0.04 ± 0.11 0.91 ± 1.45 1.44 ± 1 0.0 ± 0.0

Organic carbon 0.73 ± 0.71 0.63 ± 0.42 0.33 ± 0.19 0.70 ± 0.37 1.04 ± 0.42 0.51 ± 0.5

Organic matter 1.26 ± 1.22 1.09 ± 0.73 0.56 ± 0.33 1.21 ± 0.65 1.8 ± 0.73 0.87 ± 0.86

Values represents mean ± standard deviation. See Fig. 1 for location of sampling stations (A, B, C).

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 66-79, March 2021 (Published Mar. 30, 2021)

the available sediments and feces from station

A (Pseudo-t = 0.86, P = 0.54). The statistical

differences observed between sediment and

feces at each station are clearly depicted by the

spatial distance between the open and filled

figures in the PCA ordination in stations B and

C (Fig. 4).

The SIMPER analysis between the char-

acteristics of the available sediment and feces

showed that the greatest differences in the

composition occurred in station C, followed by

station A, and finally station B (Table 2). The

difference between the sediment characteristics

of the feces and those of the available sedi-

ment had a relationship presenting the lowest

percentage of large sand grains (granules, very

coarse, coarse and medium sand), the highest

percentage of small grains (fine and very fine

sands, and silts), a higher percentage of O.C.

with respect to the available sediment in sta-

tions A and B, and a lower percentage of O.M.

and O.C. compared to that of the available sedi-

ment in station C (Table 2).

Sediment bioturbation: According to

data, H. (Stauropora) fuscocinerea bioturbated

0.1 g ind

-1

(± 0.15); across time, Kruskal-

Wallis test evidenced differences in bioturba-

tion (H

(5,57)

= 19.73, P = 0.001) between T1

(0.01 g ind

-1

± 0.04) and T2 (0.0 g ind

-1

± 0.0), regarding T4 (0.21 g ind

-1

± 0.21)

(T1 vs T4, H = 3.09, P = 0.03; T2 vs T4, H =

3.29, P = 0.01).

The simple regression model showed no

relationship between the sea cucumber length

and biomass (R² = 0.09, N = 10, P > 0.05), nor

between the length and weight of feces (R² =

0.08, N = 10, P > 0.05); therefore, available

data did not support that the amount of sedi-

ment that H. (Stauropora) fuscocinerea biotur-

bates through feeding activity varies according

to the size of the organism.

Finally, considering the population density

of the species obtained through visual censuses

(0.27 ± 0.02 ind m

-2

), the extension of the sta-

tions A (10 211 m2) and B (4 200 m

), and the

average bioturbation rate per sea cucumber per

TABLE 2

Summary of SIMPER results for feeding habits of Holothuria (Stauropora) fuscocinerea

in La Entrega reef, Mexican Pacific

Variable Av. Sediment Av. Feces Contribution %

Station A

Average squared distance = 2.05 x 10

O.M. 9.8 x 10

-3

1.1 x 10

-4

91.4

Station B

Average squared distance = 1.51 x 10

O.M. 6.42 x 10

-3

1.2 x 10

-4

94.59

Station C

Average squared distance = 8.73 x 10

Medium sand 3.16 x 10

-14

1.12 x 10

-14

18.27

O.C. 2.56 x 10

-14

2.32 x 10

-14

15.93

O.M. 3.02 x 10

-14

2.42 x 10

-14

15.51

Very fine sand 8.15 x 10

-13

1.88 x 10

-14

14.38

Fine sand 1.15 x 10

-14

1.77 x 10

-14

14.30

Granule 1.78 x 10

-14

1.58 x 10

-14

9.23

Very coarse sand 1.77 x 10

-14

7.65 x 10

-13

5.43

Average contribution (Av. %) of discriminating sedimentary characteristics in each sediment availability and feces group,

their contribution (%) to the dissimilarity between groups, and cumulative total (%) of contributions (90 % cut-off). O.C. =

organic carbon; O.M. = organic matter.

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 66-79, March 2021 (Published Mar. 30, 2021)

day (2.24 ± 3.71 gr ind

-1

day), it is estimated

that 8.71 ± 0.17 kg of sediment in a single day

was bioturbated during the feeding activity of

the H. (Stauropora) fuscocinerea population in

the study area.

DISCUSSION

Studies addressing sediment composition

in eastern Pacific reef systems are scarce

(Estrada-Vargas, 2008; Granja-Fernández &

López-Pérez, 2008; Díaz-Díaz, 2017), while

the effect of sediment characteristics in the

distribution of organisms at small spatial scales

has been exclusively studied in asteroids (Luna-

Salguero & Reyes-Bonilla, 2010) and molluscs

(Barrientos-Lujan et al., 2019). In the same

way, the results of the present research indicate

that the spatial distribution of the sea cucumber

H. (Stauropora) fuscocinerea in La Entrega

reef is closely tied to sediment size distribution

and the amount of organic material associated

with very fine sand and silt fractions. Accord-

ing to data, the species selectively feeds on

sand in the transition zone, collecting sediment

and particles from the seabed with its mouth

tentacles. As a result of these feeding habits,

the species is generally found where granules,

very coarse sands or coarse sands represent less

than 30 % of the sediment, and where the pres-

ence of silts and very fine sands range from 0

to 4 %. Moreover, it is generally found where

the average O.C. content ranges 0.707-1.02 %

and O.M. averages 1.22-1.75 %. Consequently,

H. (Stauropora) fuscocinerea is distributed in

the transition area between the reef patch and

the adjacent sand (i.e. stations A and B), while

its presence is null on corals or in sites where

coarse and very coarse sands are the main

components (i.e. station C). This agrees with

the results of Bakus (1973), who states that

detritivores holothuroids predominate in fine

sediments, Yamanouchi (1939) who observed

that the population density of the sea cucumber

Bohadschia vitiens was lower where live corals

were abundant because there was a low pres-

ence of sand, and Massin & Jangoux (1976)

who indicated that Holothuria (Holothuria)

tubulosa lives exclusively in sandy sediments

and in the absence of a hard substrate. In

summary, the results of the present and afore-

mentioned studies indicate a close relationship

between sedimentary characteristics and the

distribution of holothuroids at small spatial

scales. This distribution could not only be

influenced by the proportion and size of the

sediments, but also by their nutritional value.

In detritivores holothuroids, the relation-

ship between sediment characteristics and the

distribution of organisms is closely related to

the selective feeding habits of the sea cucum-

bers (Massin & Jangoux, 1976; Hammond,

1983; Uthicke, 1994). Results related to the

spatial distribution of H. (Stauropora) fusco-

cinerea individuals within the reef, the large

percentage of smaller sediment fractions (fine

sands to silts) found in the feces compared

to the sediment available in the environment

(Table 1, Fig. 4) and the significant statistical

differences between the composition of the

feces and the available sediments, strongly sup-

ports the selective feeding habits of H. (Stauro-

pora) fuscocinerea in the study area. According

to both, the permutation analysis and SIMPER,

the greatest difference between sediment and

feces was found in station C, where there was

a lesser order of magnitude with very coarse

sands, fewer granules and medium sand. A

higher percentage of fine and very fine sand

in the feces of H. (Stauropora) fuscocinerea

(Table 2), suggested selectivity of small size

sediment fractions as observed in the Holothu-

ria (Roweothuria) poli sea cucumber (40-200

µm) (Mezali & Soualili, 2013; Belbachir et al.,

2014), as well as in Astichopus multifidus that

feeds on fine-grained calcareous sediments

(250 μm) (Glynn, 1965). The fine to very fine

fractions found in H. (Stauropora) fuscocinerea

feces, which were common in the sediments of

stations A and B but scarce in the sediments

of station C, possess a high concentration of

organic matter since the sorption capacity

and the surface-volume ratio increases in fine

fractions (Berthois, Crosnier & Le Calvez,

1968; Poppe, Knebel, Mlodzinska, Hastings &

Seekins, 2000). It seems feasible to suggest that

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 66-79, March 2021 (Published Mar. 30, 2021)

H. (Stauropora) fuscocinerea spatial distribu-

tion is related to the ability of the holothuroids

to locate patches enriched with organic matter

and to the efficiency of food assimilation, intes-

tinal transit time, and the cost of rejecting par-

ticles in these organisms, known as “Optimal

Food Theory” (Taghon, Self & Jumars, 1978;

Billet, Llewellyn & Watson, 1988).

Through their activities of ingestion and

excretion, holothuroids are known to be impor-

tant recyclers of nutrients in reef systems by

converting organic nutrients bound to sedi-

ments into inorganic nutrients dissolved in the

water column (Uthicke, 1999), and further into

biomass in upper trophic levels or as nutrients

that increase primary productivity (Purcell et

al., 2016). Although feces may be enrichened

in nutrients through their transit in the sea

cucumber gut (e.g. Massin, 1979; Hammond,

1983; Amon & Herndl, 1991), most of the time

when sediments pass through the intestines of

holothuroids, the defecated sediments can be

lower in nutrients than the ingested sediments,

and thus these organisms act as sediment-clean-

ers (Longbottom, 1970; Mercier, Battaglene &

Hamel, 1999; Uthicke, 1999; Michio et al.,

2003; Yuan et al., 2006; Zhou et al., 2006), and

have been considered as a means of restricting

or reversing the effects of pollution from aqua-

culture (Slater & Carton, 2009). Emiroglu &

Günary (2007), for example, suggested that H.

(Holothuria) tubulosa can eliminate biological

pollution and improve water quality in eutro-

phic and hypereutrophic environments of the

coastal regions. In this regard, heavily tourist

visits to coastal reef areas such as La Entrega

(FONATUR, 2008), where large amounts of

organic matter have been recorded (Díaz-Díaz,

2017) may benefit from H. (Stauropora) fusco-

cinerea presence and feeding activity.

Holothuroids actively ingest sediments,

but present varied feeding rates since they

are capable of feeding either continuously

(Yamanouchi, 1956; Bonham & Held, 1963;

Massin & Jangoux, 1976; Hammond, 1982;

Uthicke, 1994) or discontinuously within a

24 h cycle (Crozier, 1918; Bakus, 1968; Mas-

sin & Jangoux, 1976). The feeding rates of

holothuroids is related to light intensity, varia-

tions in temperature, and other environmental

conditions such as water movement (Massin &

Jangoux, 1976; Uthicke, 1994). According to

Massin and Jangoux (1976), H. (Holothuria)

tubulosa is a continuous feeder that, in sum-

mer, increases its feeding activity at night and

decreases it during the day, while juveniles

of Holothuria (Metriatyla) scabra feed con-

tinuously (Mercier et al., 1999). In the present

study, differences in the excretion rate in a 24 h

cycle were recorded; according to data, larger

excretion rates occurred early in the morning

probably related to intense feeding activity

during the night (Crozier, 1918; Bakus, 1968;

Massin & Jangoux, 1976), but also may have

resulted from changes in feeding activity of the

experimental organisms since they were relo-

cated to experimental cages in areas where H.

(Stauropora) fuscocinerea does not currently

distribute. More data, nevertheless, are needed

to accurately assess daily and seasonal feeding

rates changes in the species.

Concurrently, while some authors (Cro-

zier, 1918, Isostichopus badionotus; Ruiz,

Ibáñez & Cáceres, 2007, Athyonidium chilen-

sis) observed a relationship between the total

length of the holothuroids and the average

weight of the full alimentary tract, such that

the total length of the intestine increased with

the size of this species, results in La Entrega

indicated a lack of length-weight and weight-

excretion rate relationships in H. (Stauropora)

fuscocinerea individuals. Therefore, our results

should be considered with caution since sea

cucumber size is strongly subjected to changes

in response to handling or its resting state

(Ebert, 2021) and sample size may be insuf-

ficient to address meaningful relationships if

any. Preliminary data, nevertheless, may give

us insight on the bioturbation potential of

H. (Stauropora) fuscocinerea in the studied

area. If it is assumed that all H. (Stauropora)

fuscocinerea individuals in La Entrega have

similar sizes and weights, and hence feed-

ing rates are homogeneous among individu-

als, H. (Stauropora) fuscocinerea population

may have had the potential to bioturbate 8.71

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 66-79, March 2021 (Published Mar. 30, 2021)

± 0.17 kg day of sediment over 14 411 m

corresponding to the area where the species

currently occurs in La Entrega reef. Prelimi-

nary bioturbation potential of H. (Stauropora)

fuscocinerea addressed in the studied area is

smaller than that reported for other species.

Coulon and Jangoux (1993) obtained different

values for the lower and upper part of the algal

grasslands of Lacco Ameno (Italy), at 5.9 and

12.9 kg of dry sediment per year, respectively;

while Uthicke (1999) showed that H. (Halo-

deima) atra removes up to 24.5 kg of sediment

per year and Stichopus chloronotus removes

21.5 kg per year at Lizard Island (Great Bar-

rier Reef). In order to establish meaningful

comparison with other studies, strong empirical

information regarding size-related bioturba-

tion changes, size-frequency distribution of

individuals, population size and their variation

across time are mandatory. It should be noted

that this study addressed the preliminary bio-

turbation potential of H. (Stauropora) fuscoci-

nerea, while the importance of other abundant

and widespread species such as Isostichopus

fuscus and Holothuria (Halodeima) inornata

remains unquantified. Addressing the bioturba-

tion potential of sea cucumbers without doubt,

it is of relevance for understanding the impor-

tance of the guild in the functioning of coastal

systems, particularly in reef systems with high

organic load such as those located on the east-

ern tropical Pacific.

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 are thankful to Buceo Huatulco for

logistical support in the field, particularly to

Carlos (Papi) Armería and to Tania (Torcy)

González for addressing reef size. This work

was conceived and carried out by the Reef

and Biodiversity Laboratory (ARBIOLAB)

in collaboration with the Coastal Ecosystem

Laboratory. The work was carried out with

funds from the Universidad Autónoma Met-

ropolitana and CONACYT (236654) granted

to ALP and LGCB. We thank four anonymous

reviewers and editor for commenting and

improving the manuscript.

RESUMEN

Hábitos alimenticios de Holothuria (Stauropora)

fuscocinerea (Echinodermata: Holothuroidea) en

un arrecife del Pacífico Mexicano

Introducción: La relevancia de los holoturoideos en

los ecosistemas marinos está relacionada con sus activida-

des alimenticias, las cuales han sido escasamente estudia-

das en el Pacífico oriental. Objetivo: Describir los hábitos

alimenticios del pepino de mar Holothuria (Stauropora)

fuscocinerea y su potencial de bioturbación en el arrecife

La Entrega, México. Métodos: Se determinó el tamaño

poblacional de H. (Stauropora) fuscocinerea mediante

cuatro transectos de banda de 20 x 4 m (320 m

), mientras

que la caracterización de los sedimentos disponibles y las

heces de los pepinos se realizó en tres estaciones (A-C)

mediante granulometría y cuantificación de carbono orgá-

nico y materia orgánica. Se determinó la tasa de excreción

cada 4 hr durante un periodo de 24 hr y se evaluó la rela-

ción entre la talla y la biomasa con la tasa de excreción.

Resultados: De acuerdo con un análisis no paramétrico

mediante permutaciones, ordenación y similitud, las heces

de los pepinos estuvieron compuestas en su mayoría por

una gran cantidad de granos pequeños en comparación

con el sedimento disponible, lo que sugiere que H. (Stau-

ropora) fuscocinerea es una especie selectiva respecto al

tamaño de grano. El potencial de bioturbación preliminar

de la especie puede alcanzar 8.71 ± 0.17 kg día en el área

de estudio. Conclusiones: La distribución espacial de H.

(Stauropora) fuscocinerea en el área de estudio es producto

de su selectividad alimenticia, evidenciando la importancia

de la especie en la dinámica trófica del arrecife La Entrega.

Palabras clave: selectividad; distribución; alimento; bio-

turbación; pepino de mar.

REFERENCES

Amon, R.M.W., & Herndl, G.J. (1991). Deposit feeding

and sediment: I. Interrelationship between Holothu-

ria tubulosa (Holothurioida, Echinodermata) and

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 66-79, March 2021 (Published Mar. 30, 2021)

the sediment microbial community. Marine Ecology,

12(2), 163-174.

Anderson, M.J., Gorley, R.N., & Clarke, K.R. (2008).

PERMANOVA+ for PRIMER. Guide to software and

statistical methods. Plymouth, UK: PRIMER-E.

Bakus, G.J. (1968). Defensive mechanisms and ecology of

some tropical holothurians. Marine Biology, 2, 23-32.

Bakus, G.J. (1973). The biology and ecology of tropical

holothurians. In O.A. Jones & R. Endean (Eds.),

Biology and Geology of Coral Reefs (Vol. 2, pp. 325-

367). New York, USA: Academic Press.

Barrientos-Lujan, N.A., López-Pérez, A., Ríos-Jara, E.,

Ahumada-Sempoal, M.A., Ortiz, M., & Rodríguez-

Zaragoza, F.A. (2019). Ecological and functional

diversity of gastropods associated with hermatypic

corals of the Mexican tropical Pacific. Marine Biodi-

versity, 49, 193-205.

Belbachir, N., Mezali, K., & Soualili, D.L. (2014). Selecti-

ve feeding behaviour in some aspidochirotid holothu-

rians (Echinodermata: Holothuroidea) at Stidia,

Mostaganem Province, Algeria. SPC Bêche-de-mer

Information Bulletin, 34, 34-37.

Benítez-Villalobos, F., Avila-Poveda, O.H., & Gutié-

rrez-Méndez, I.S. (2013). Reproductive biology of

Holothuria fuscocinerea (Echinodermata: Holothu-

roidea) from Oaxaca, Mexico. Sexuality and Early

Development in Aquatic Organisms, 1, 13-24.

Berthois, L., Crosnier, A., & Le Calvez, Y. (1968). Con-

tribution à l’étude sédimentologique du plateau con-

tinental dans la baie de Biafra. Cahier ORSTOM,

6(3-4), 55-86.

Billett, D.S.M., Llewellyn, C., & Watson, J. (1988). Are

deep-sea holothurians selective feeders? In R.D.

Burke, P.V. Mladenov, P. Lambert & R.L. Parsley

(Eds.), Echinoderm biology (pp. 421-429). Rotter-

dam: A. Balkema Publishers.

Bonham, K., & Held, E.E. (1963). Ecological observations

on the sea Cucumbers Holothuria atra and H. leu-

cospilota at Rongelap Atoll, Marshall Islands. Pacific

Science, 17, 305-314.

Bucol, L.A., Cadivida, A.A., & Wagey, B.T. (2018).

Sediment removal activities of the sea cucumbers

Pearsonothuria graeffei and Actinopyga echinites

in Tambisan, Siquijor Island, Central Philippines.

Jurnal Pesisir dan Laut Tropis, 1(1), 1-7.

Cabral-Tena, R.A., López-Pérez, A., Alvarez-Filip, L.,

González-Barrios, F.J., Calderón-Aguilera, L.E., &

Aparicio-Cid, C. (2020). Functional potential of coral

assemblages along a typical Eastern Tropical Pacific

reef tract. Ecological Indicators, 119, 106795.

Calva-Benítez, L.G. (2002). Hábitos alimenticios de algu-

nos equinodermos. Parte 2. Erizos de mar y pepinos

de Mar. ContactoS 3ª, 47, 54-63.

Cortés, J., Enochs, I.C., Sibaja-Cordero J., Hernández, L.,

Alvarado, J.J., Breedy, O., . . . Zapata, F.A. (2017).

Marine biodiversity of Eastern tropical Pacific coral

reefs. In P. Glynn, D. Manzello & I. Enochs (Eds.),

Coral reefs of the Eastern tropical Pacific (Vol. 8,

pp. 203-250). Dordrecht, The Netherlands: Springer.

Coulon, P., & Jangoux, M. (1993). Feeding rate and sedi-

ment reworking by the holothuroid Holothuria tubu-

losa (Echinodermata) in a Mediterranean seagrass

bed off Ischia Island, Italy. Marine Ecology Progress

Series, 92, 201-204.

Crozier, W.J. (1918). The amount of bottom material

ingested by holothurians (Stichopus). Journal of

Experimental Zoology, 26(2), 379-389.

Díaz-Díaz, A.D. (2017). Sedimentación en arrecifes corali-

nos del corredor Puerto Ángel – Bahías de Huatulco,

Oaxaca, México (Bachelor thesis). Universidad del

Mar, México.

Ebert, T.A. (2021). Problems and puzzles in echinoderm

demography. Revista de Biología Tropical, 69(S1),

1-13. DOI 10.15517/rbt.v69iSuppl.1.46318

Emiroglu, D.I., & Günay, D. (2007). The effect of sea

cucumber Holothuria tubulosa (G., 1788) on nutrient

and sediment of Aegean Sea shores. Pakistan Journal

of Biological Sciences, 10(4), 586-589.

Estrada-Vargas, L. (2008). Determinación de metales

pesados en agua, sedimento y coral (Pocillopora

damicornis) en Bahías de Huatulco, Oaxaca (Master

thesis). Universidad del Mar, México.

FONATUR. (2008). Libro blanco. Relanzamiento del CIP

Huatulco. México: Fondo Nacional de Fomento al

Turismo.

Gaudette, H.E., Flight, W.R., Toner, L., & Folger, D.W.

(1974). An inexpensive titration method for the

determination of organic carbon in recent sediments.

Journal of Sedimentary Research, 44(1), 249-253.

Glynn, P.W. (1965). Active movements and other aspects

of the biology of Astichopus and Leptosynapta

(Holothuroidea). The Biological Bulletin, 129(1),

106-127.

Glynn, P.W. & Leyte-Morales, G.E. (1997). Coral reefs

of Huatulco, west México: Reef development in

upwelling Gulf of Tehuantepec. Revista de Biología

Tropical, 45(3), 1033-1047.

Goldberg, W.M. (2013). The biology of reefs and reef orga-

nisms. Chicago, USA: University of Chicago Press.

Granja-Fernández, M.R., & López-Pérez, R.A. (2008).

Sedimentación en comunidades arrecifales de Bahías

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 66-79, March 2021 (Published Mar. 30, 2021)

de Huatulco, Oaxaca, México. Revista de Biología

Tropical, 56(3), 1179-1187.

Grybos, M., Davranche, M., Gruau, G., & Petitjean, P.

(2007). Is trace metal release in wetland soils contro-

lled by organic matter mobility or Fe-oxyhydroxides

reduction? Journal of Colloid and Interface Science,

314(2), 490-501.

Hammond, L.S. (1982). Patterns of feeding and activity in

deposit-feeding holothurians and echinoids (Echino-

dermata) from a shallow back-reef lagoon, Discovery

Bay, Jamaica. Bulletin of Marine Science, 32(2),

549-571.

Hammond, L.S. (1983). Nutrition of deposit-feeding

holothuroids and echinoids (Echinodermata) from a

shallow reef lagoon, Discovery Bay, Jamaica. Marine

Ecology Progress Series, 10, 297-305.

Hendler, G., Miller, J.E., Pawson, D.L., & Kier, P.M.

(1995). Sea stars, sea urchins, and allies: Echino-

derms of Florida and the Caribbean. Washington,

London: Smithsonian Institute Press.

Herrero-Pérezrul, M.D., & Chávez, E.A. (2005). Optimum

fishing strategies for Isostichopus fuscus (Echinoder-

mata: Holothuroidea) in the Gulf of California, Mexi-

co. Revista de Biología Tropical, 53(3), 357-366.

Longbottom, M.R. (1970). The distribution of Arenicola

marina (L.) with particular reference to the effects

of particle size and organic matter of the sediments.

Journal of Experimental Marine Biology and Ecolo-

gy, 5(2), 138-157.

López-Pérez, R.A., & Hernández-Ballesteros, L.M. (2004).

Coral community structure and dynamics in the

Huatulco area, western Mexico. Bulletin of Marine

Science, 75(3), 453-472.

López-Pérez, R.A., & López-García, A. (2008). Identifi-

cation of priority conservation sites for reef building

corals in Oaxaca state, Mexico. Hidrobiológica,

18(3), 239-249.

López-Pérez, A., Granja-Fernández, R., Valencia-Méndez,

O., Aparicio-Cid, C., Torres-Huerta, A.M., Barrien-

tos-Lujan, N.A., . . . Hernández, L. (2019). Biodiver-

sity associated with southern Mexican Pacific corals.

In A.L. Ibáñez (Ed.), Mexican aquatic environments

(pp. 119-114). Switzerland: Springer.

Luna-Salguero, B.M., & Reyes-Bonilla, H. (2010). Com-

munity and trophic structure of sea stars (Echinoder-

mata: Asteroidea) in rocky reefs of Loreto, Gulf of

California, Mexico. Hidrobiológica, 20(2), 127-34.

Massin, C. (1979). The sediment ingested by Holothuria

tubulosa Gmel (Holothuroidea: Echinodermata). In

M. Jangoux (Ed.), Proceedings of the 2nd European

Colloquium on Echinoderms (pp. 205-208). Rotter-

dam: A. Balkema Publishers.

Massin, C., & Jangoux, M. (1976). Observations écologi-

ques sur Holothuria tubulosa, H. poli et H. forskali

(Echinodermata, Holothuroidea) et comportement

alimentaire de H. tubulosa. Cahiers de Biologie

Marine, 17, 45-59.

Mercier, A., Battaglene, S.C., & Hamel, J.F. (1999). Daily

burrowing cycle and feeding activity of juvenile sea

cucumbers Holothuria scabra in response to envi-

ronmental factors. Journal of Experimental Marine

Biology and Ecology, 239(1), 125-156.

Mezali, K., & Soualili, D.L. (2013). The ability of holothu-

rians to select sediment particles and organic matter.

SPC Beche-de-Mer Information Bulletin, 33, 38-43.

Michio, K., Kengo, K., Yasunori, K., Hitoshi, M., Takayu-

ki, Y., Hideaki, Y., & Hiroshi, S. (2003). Effects of

deposit feeder Stichopus japonicus on algal bloom

and organic matter contents of bottom sediments

of the enclosed sea. Marine Pollution Bulletin, 47,

118-125.

Poppe, J.L., Knebel, H.J., Mlodzinska, Z.J., Hastings,

M.E., & Seekins, B.A. (2000). Distribution of sur-

ficial sediment in Long Island Sound and adjacent

waters: texture and total organic carbon. Journal of

Coastal Research, 16(3), 567-574.

Purcell, S.W., Samyn, Y., & Conand, C. (2012). Commer-

cially important sea cucumbers of the world. Rome,

Italy: FAO Species Catalogue for Fishery Purposes

No. 6.

Purcell, S.W., Conand, C., Uthicke, S., & Byrne, M.

(2016). Ecological roles of exploited sea cucum-

bers. Oceanography and Marine Biology: An Annual

Review, 54, 367-386.

Rioja, R.A., Palomar-Abesamis, N., & Juinio-Meñez,

M.A. (2020). Development of nocturnal feeding and

photosensitivity in early juveniles of the warty sea

cucumber Stichopus cf. horrens. Behavioural Proces-

ses, 178, 104181.

Ruiz, J.F., Ibánez, C.M., & Cáceres, C.W. (2007). Mor-

fometría del tubo digestivo y alimentación del pepi-

no de mar Athyonidium chilensis (Semper, 1868)

(Echinodermata: Holothuroidea). Revista de Biología

Marina y Oceanografía, 42(3), 269-274.

SEMARNAT. (2019). Modificación del Anexo Normativo

III, Lista de especies en riesgo de la Norma Oficial

Mexicana NOM-059-SEMARNAT-2010, Protección

ambiental-Especies nativas de México de flora y

fauna silvestres-Categorías de riesgo y especifica-

ciones para su inclusión, exclusión o cambio-Lista

de especies en riesgo. Ciudad de México, México:

SEGOB.

Sheppard, C.R.C., Davy, S.K., Pilling, G.M., & Graham,

N.A.J. (2017). The biology of coral reefs. Oxford,

UK: Oxford University Press.

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 66-79, March 2021 (Published Mar. 30, 2021)

Shoham-Frider, E., Gertner, Y., Guy-Haim, T., Herut, B.,

Kress, N., Shefer, E., & Silverman, J. (2020). Legacy

groundwater pollution as a source of mercury enrich-

ment in marine food web, Haifa Bay, Israel. Science

of the Total Environment, 714, 1-34.

Slater, M.J., & Carton, A.G. (2009). Effect of sea cucumber

(Australostichopus mollis) grazing on coastal sedi-

ments impacted by mussel farm deposition. Marine

Pollution Bulletin, 58(8), 1123-1129.

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

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

S.M. (2013). Appendix. In J.J. Alvarado-Barrientos

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

diversity in Latin America (pp. 543-658). Berlin:

Springer Heidelberg.

StatSoft, Inc. (2020). STATISTICA (data analysis software

system) (Version 7.1) Retrieved from https://www.

jmp.com/en_us/download-jmp-free-trial.html.

Taghon, G.L., Self, R.F., & Jumars, P.A. (1978). Predicting

particle selection by deposit feeders: A model and its

implications. Limnology and Oceanography, 23(4),

752-759.

Thayer, C.W. (1983). Sediment-mediated biological distur-

bance and the evolution of marine benthos. In M.J.S.

Tevesz & P.L. McCall (Eds.), Biotic interactions

in recent and fossil benthic communities. Topics in

geobiology (Vol. 3, pp. 479-625). Boston, USA:

Springer.

Trefz, S.M. (1956). Observations on the anatomy, both

macroscopical and microscopical, of the intestinal

tract and of accompanying organs and on the phy-

siology of digestion in Holothuria atra (Jager) with

additional observations on the ecology of Holothu-

rians and their possible role in the destruction of

coral reefs. Honolulu, Hawaii: Hawaii University

Honolulu.

Uthicke, S. (1994). Distribution patterns and growth of two

reef flat holothurians, Holothuria atra and Stichopus

chloronotus. In B. David, A. Guille, J.P. Féral & M.

Roux (Eds.), Echinoderms (Dijon), Proceedings of

the 8th International Echinoderm Conference (pp.

569-576). Rotterdam: A. Balkema Publishers.

Uthicke, S. (1999). Sediment bioturbation and impact of

feeding activity of Holothuria (Halodeima) atra

and Stichopus chloronotus, two sediment feeding

holothurians, at Lizard Island, Great Barrier Reef.

Bulletin of Marine Science, 64(1), 129-141.

Yamanouchi, T. (1939). Ecological and physiological

studies on the holothurians in the coral reef of Palao

Islands. Palao Tropical Biological Station Studies,

4, 603-634.

Yamanouchi, T. (1956). The daily activity rhythms of the

holothurians in the coral reef of Palao Islands. Publi-

cations of the Seto Marine Biological Laboratory,

3(5), 347-362.

Yang, H., Yuan, X., Zhou, Y., Mao, Y., Zhang, T., & Liu,

Y. (2005). Effects of body size and water temperature

on food consumption and growth in the sea cucum-

ber Apostichopus japonicus (Selenka) with special

reference to aestivation. Aquaculture Research, 36,

1085-1092.

Yuan, X., Yang, H., Zhou, Y., Mao, Y., Zhang, T., & Liu,

Y. (2006). The influence of diets containing dried

bivalve faeces and/or powdered algae on growth and

energy distribution in sea cucumber Apostichopus

japonicus (Selenka) (Echinodermata: Holothuroi-

dea). Aquaculture, 256(1-4), 457-467.

Zhou, Y., Yang, H., Liu, S., Yuan, X., Mao, Y., Liu, Y., …

Zhang, F. (2006). Feeding and growth on bivalve

biodeposits by the deposit feeder Stichopus japonicus

Selenka (Echinodermata: Holothuroidea) co-cultured

in lantern nets. Aquaculture, 256(1-4), 510-520.