Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58623, marzo 2024 (Publicado Mar. 01, 2024)

Population survey of Holothuria (Halodeima) grisea

(Aspidochirotida: Holothuriidae) at its limit of geographic distribution

in the Western South Atlantic

Guilherme Sabino Rupp1*; https://orcid.org/0000-0002-5476-9689

Adriano Weidner Cacciatori Marenzi2; https://orcid.org/0000-0002-8154-5867

Robson Ventura de Souza1; https://orcid.org/0000-0003-0588-0038

Rafael Schroeder2,3; https://orcid.org/0000-0001-7340-0214

1. Empresa de Pesquisa Agropecuária e Extensão Rural de Santa Catarina (EPAGRI), Centro de Desenvolvimento em

Aquicultura e Pesca, Florianópolis, SC, Brazil; rupp@epagri.sc.gov.br (*Correspondence),

robsonsouza@epagri.sc.gov.br

2. Universidade do Vale do Itajaí (UNIVALI), Escola Politécnica, Rua Uruguai 458, Centro 88302-901, Itajaí, Brazil;

marenzi@univali.br, schroederichthys@gmail.com

3. Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR/CIMAR), Terminal de Cruzeiros do Porto de

Leixões, Avenida General Norton de Matos S/N, 4550-208 Matosinhos, Portugal.

Received 23-I-2023. Corrected 14-IX-2023. Accepted 27-IX-2023.

ABSTRACT

Introduction: The sea cucumber Holothuria (Halodeima) grisea Selenka, 1867 is a common echinoderm in inter-

tidal regions along the Brazilian coast, which recently became the focus of unreported and unregulated fisheries.

This study was carried out in sandy-rocky substrates at Armação do Itapocoroy, Penha, Santa Catarina (26o47’ S;

48o36’ W), near its southern limit of geographic distribution.

Objective: To determine the densities (individuals*m-2) of Holothuria (H.) grisea within a spatial-temporal per-

spective as well as to determine biometric and growth characteristics of the population.

Methods: Two-meter wide transects perpendicular to the coastline were carried out in winter and spring 2019

and in summer and spring 2020, in periods of spring low-tides. In each sampling occasion the total number of

specimens of H. grisea were determined, and a group of 90 organisms was submitted to in situ biometrics (weight,

length and width), and immediately returned alive to their habitat.

Results: The densities of H. (H.) grisea were significantly higher in the subtidal sector and lower in the upper

intertidal sector with no indication of significant differences among sampling campaigns. Depth was the primary

factor explaining the observed density patterns and rugosity of the substrate was secondary but also important.

The body length ranged from 5.2 to 22.5 cm, whereas the weight varied from 6.0 to 230 g. The mean and modal

lengths were 12.54 and 13 cm, respectively. Approximately 75 % of the population sampled was between 10 and

14 cm and the average weight was 60 g. Estimates from von Bertalanffy growth function indicate that the young-

est sea cucumber was one year-old, and the oldest had approximately two and a half years.

Conclusions: This is the first study to determine biometric parameters for H. (H.) grisea in southern Brazil and

the first one to estimate growth and age estimates for a wild population of this species. The densities recorded

in the present study were lower than those previously reported for this region, suggesting anthropic influence.

Key words: Holothuria (Halodeima) grisea; Santa Catarina; densities; spatial distribution; population.

https://doi.org/10.15517/rev.biol.trop..v72iS1.58623

SUPPLEMENT

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58623, marzo 2024 (Publicado Mar. 01, 2024)

INTRODUCTION

Sea cucumbers play an important role in

marine ecosystems (Purcell et al., 2016), and

present outstanding commercial value through-

out the world (Purcell et al., 2018), however

little is known about their populations in Brazil

(Mendes et al., 2006; Ponte & Feitosa, 2019;

Souza Jr. et al., 2017; Ventura et al., 2013). The

greed for these high priced-organisms has led

to intense capture in more than 70 Countries,

threatening the populations of various species

around the planet (Purcell et al., 2013; Purcell

et al., 2023), including Latin America (Conand,

2018; Sonnenholzner, 2021).

Although a wide diversity of sea cucumbers

is described for shallow waters of the Brazilian

coast (Martins, 2012; Martins & Souto, 2020;

Martins & Tavares, 2021; Martins et al., 2022),

only three species are described for south-

ern Brazil (Rupp et al., 2023). Among them,

Holothuria Halodeima grisea Selenka, 1867 is

considered the most common, being recorded

in the intertidal region at the base of the rocks,

usually in contact with the bottom sand (Bueno

et al., 2015; Martins, 2012; Mendes et al., 2006;

Tiago & Ditadi, 2001; Tommasi, 1969). Nev-

ertheless this species is already threatened by

unreported and unregulated capture in Brazil

(Ponte & Feitosa, 2019; Rupp & Marenzi, 2021;

Souza Jr. et al., 2017). The geographic distribu-

tion of H. (H.) grisea is predominantly tropical,

and includes the west coast of Africa, Florida,

Gulf of Mexico, Panamá, Caribbean islands,

Colombia, Venezuela, and Brazil up to Santa

Catarina (Martins, 2012; Pawson et al., 2010).

In latter location Rupp et al. (2023) recorded

the occurrence of H. (H.) grisea in nine out of

the eleven intertidal sampled sites, with higher

densities (> 1.7 ind.m-2) recorded in the central

portion of the state, and none found further

south than the locality of Garopaba.

The objective of the present study was

to evaluate the abundance and densities

RESUMEN

Estudio poblacional de Holothuria (Halodeima) grisea (Aspidochirotida: Holothuriidae)

en su límite de distribución geográfica en el Atlántico Sur Occidental

Introducción: El pepino de mar Holothuria (Halodeima) grisea Selenka, 1867 es un equinodermo común en

las regiones intermareales a lo largo de la costa brasileña, que recientemente se convirtió en foco de pesquerías

no declaradas y no reguladas. Este estudio se realizó en sustratos arenosos-rocosos en Armação do Itapocoroy,

Penha, Santa Catarina (26o47’ S; 48o36’ W), cerca del límite sur de su distribución geográfica.

Objetivo: Determinar las densidades (individuos*m-2) de Holothuria (H.) grisea dentro de una perspectiva

espacio-temporal así como determinar las características biométricas y de crecimiento de la población.

Métodos: Se realizaron transectos de dos metros de ancho perpendiculares a la línea de costa en invierno y pri-

mavera de 2019 y en verano y primavera de 2020, en periodos de bajamar sicigia. En cada ocasión de muestreo se

determinó el número total de especímenes de H. (H.) grisea, y se sometió un grupo de 90 organismos a biometría

in situ (peso, longitud y ancho), e inmediatamente se los devolvieron vivos a su hábitat.

Resultados: Las densidades de H. (H.) grisea fueron significativamente más altas en el sector submareal y más

bajas en el sector intermareal superior sin indicios de diferencias significativas entre las campañas de muestreo.

La profundidad fue el factor principal que explica los patrones de densidad observados y la rugosidad del sustrato

fue secundaria pero también importante. La longitud del cuerpo varió de 5.2 a 22.5 cm, mientras que el peso varió

de 6.0 a 230 g. Las longitudes media y modal fueron 12.54 y 13 cm, respectivamente. Aproximadamente el 75 %

de la población muestreada midió entre 10 y 14 cm y el peso promedio fue de 60 g. Estimados de la función de

crecimiento de von Bertalanffy indican que el ejemplar más joven presentaba un año de edad, mientras el más

viejo presentaba cerca de dos años y medio.

Conclusiones: Este es el primer estudio que determina parámetros biométricos para una población de H. (H.)

grisea en el sur de Brasil y el primero en estimar el crecimiento y edades para una población salvaje de esta especie.

Las densidades registradas en el presente estudio fueron inferiores a las reportadas previamente para esta región

sugiriendo la ocurrencia de influencia antrópica.

Palabras clave: Holothuria (Halodeima) grisea; Santa Catarina; densidades; distribución espacial; población.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58623, marzo 2024 (Publicado Mar. 01, 2024)

(individuals.m-2) of H. (H.) grisea within a

spatial-temporal perspective, at a locality where

a previous study has been conducted (Mendes

et al., 2006) nearly 16 years earlier. Addition-

ally, biometric parameters of the population

as such length and weight distributions were

determined, as well as growth parameters. Such

basic information could be useful for future

conservation practices as well as for fishery

management and aquaculture of this species.

MATERIALS AND METHODS

Field methods: The study site is in the lit-

toral zone of Armação Itapocoroy cove, Penha,

Santa Catarina (26º 47’S; 48º36’W) (Fig. 1),

which is a low-energy wave action area. The

site has a slight slope and rocky-sandy sub-

strate consisting of coarse grain-sized sedi-

ments (Mendes et al., 2006). This site is located

approximately 150 km from the southernmost

point where the Holothuria (H.) grisea have

been recorded (Rupp et al., 2023). Four Holo-

thuria (H.) grisea sampling campaigns were

carried out between August 2019 and Octo-

ber 2020 during low spring tides. Restrictions

imposed by the Covid-19 pandemic prevented

sampling from being carried out from autumn

to winter 2020. On each occasion, three two-

meter wide transects (T1, T2 and T3) distant

15 m from each other (Fig. 2) were deployed

perpendicularly to the shore, with lengths rang-

ing from 33 to 50 m (Table 1), depending on the

tidal level. The transect areas were surveyed by

visual and tactile inspections and the numbers

of H. (H.) grisea in each one-meter division

of the transects were recorded. The samplings

always started at T2, then proceeding to T3 and

finally to T1. In three opportunities it was not

possible to finalize the sampling at T1 and T3

due to tidal surge. The rocks at the sampling

area were not revolved in order to avoid habitat

disturbance. The length of the transects was

divided in three sectors based on tidal expo-

sure: A – upper intertidal (length 0 to 16 m),

B – lower intertidal (length 17 to 33 m) and C –

subtidal (length 34 to 50 m). Their depths were

determined in the middle of each sector. To do

that, tidal tables from the Brazil’s Navy Hydrog-

raphy and Navigation Center (Centro de Hidro-

grafia e Navegação [CHN], n.d.) and from a

nearby tide gauge from the Santa Catarina State

Institution for Agricultural Research and Rural

Extension (Empresa de Pesquisa Agropecuária

e Extensão Rural de Santa Catarina, n.d.) were

used as references. The rugosity of each sector

was estimated using the chain method (Luck-

hurst & Luckhurst, 1978). A metal chain with

small links was laid along the central portion of

the transects, so that it followed the contours of

Fig. 1. Location of the study site at Armação do Itapocoroy, Penha (SC).

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58623, marzo 2024 (Publicado Mar. 01, 2024)

the substratum as closely as possible. The ratio

between the contour length of the chain and

the sector actual length (Rg) was used to infer

rugosity index:

Ri = 1-(1/Rg)

Where Ri is the rugosity index and Rg is the

ratio between the chain length and the actual

length of the sector of the transect (Mendes et

al., 2006).

A group of 90 animals was randomly sam-

pled, on each campaign, for in loco biometry.

The following parameters were registered: total

length and width with contracted body, and

total weight after light pressure to expel the

liquid from the internal cavity. Linear measure-

ments were carried out with a precise ruler

(± 0.5 mm) and a field DC digital scale was

used to determine weights (± 0.1 g). Samplings

were non-destructive and the animals were

immediately returned to their habitat after

biometry. The moon phase and the following

environmental parameters were recorded in

each sampling occasion: air temperature, sky

coverage (clouds), water temperature and salin-

ity. Tidal information was obtained at CHN

tables (CHN, n.d.). This study was carried out

under license for collection of native fauna of

the Brazilian Ministry of Environment MMA/

SISBIO No. 68215.

Statistic approach: Normality and

homoscedasticity of the datasets were veri-

fied respectively with Shapiro-Wilk and Lev-

ene’s tests using StatisticaR, version 12 (Statsoft

Inc. USA), and density data was square root

transformed in order to meet those premises

(Zar, 1999). Two-Way ANOVA was used to

compare densities on spatial-temporal scale

(among transects, sectors and season) (Sokal

& Rohlf, 2000). Significant differences were

considered when P < 0.05 and Tuckey’s test

was used as post-hoc analysis. The comparison

Fig. 2. Plots of the transects at Armação do Itapocoroy, Penha (SC) (A - Google Earth); (B) aerial photo of the sampling area.

(Arrows indicate North).

Table 1

Surveyed months and respective seasons, transects lengths and the comparable sectors used for statistical analysis.

Month Season Transect distance (m) Comparable sectors

T1 T2 T3 T1 T2 T3

August/2019 Winter-19 33 50 50 A-BA-B-C A-B-C

October/2019 Spring-19 33 50 33 A-BA-B-C A-B

March/2020 Summer-20 50 50 50 A-B-C A-B-C A-B-C

October/2020 Spring-20 45 50 50 A-BA-B-C A-B-C

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58623, marzo 2024 (Publicado Mar. 01, 2024)

of mean length and weight of Holothuria (H.)

grisea among the sampling campaigns was

explored using One-Way ANOVA, however the

assumption for this analysis were not met, even

after data transformation, therefore the non-

parametric Kruskal-Wallis test was used in lieu

of ANOVA (Sokal & Rohlf, 2000).

Considering that it was not possible to

complete Sector C on T1 in 3 opportunities

and on T3 in one opportunity, only the sectors

fully sampled were included in the statisti-

cal analyses (Table 1). The comparison of the

mean densities on temporal scale was carried

out considering T2 (sectors A, B and C) for all

sampling occasions, as well as for all transects

using sector B only. The comparison among all

sectors and transects was carried out within the

summer-20 campaign and the comparison of

the densities among sectors B was carried out

considering all transects and seasons.

Aiming to explain the density of sea-

cucumbers based on both the mean depth of

the sectors and their rugosity indexes, linear

regression analyses were carried out. The den-

sity of animals was the response variable, while

the depth and rugosity were tested as explana-

tory variables, both separately and combined as

a multiple regression model, using the software

“R”, version 4.3.0 (R Core Team, 2023). The

relation between size and weight of the stud-

ied population was explored using the power

model regression:

Y = aXb

Where Y = weight, X = length, b = allometric

coefficient, a = intercept (Gould, 1966).

Considering that body measurements in

holothuroids is often imprecise due to body

wall elasticity, the compound index which com-

bines body length and width (SLW = square

root of the length-width product) was used

to further analyze its relationship with body

weight, as indicated for several species of sea-

cucumbers (see Poot-Salazar et al., 2014 for

details). To increase growth parameter accu-

racy, lengths were recalculated using a power

regression between length and SLW (a = 1.0731,

b = 0.6855).

Growth analyses of different SLW cor-

rected length classes (Le) were conducted by

Electronic Length Frequency Analysis (ELE-

FAN) in R 4.3.0 (R Core Team, 2023) using

the TropFishR package (Mildenberger et al.,

2017). The von Bertalanffy growth function

was applied as follows:

Where Let is the predicted corrected size at

age t; Le∞ is the asymptotic size; k is curvature

parameter per year, expressing the rate at which

Le∞ is approached; and to is the theoretical ‘‘age’’

if the organism were to have a size equal to zero.

Relative ages at certain lengths and weights

were generated by replacing the growth para-

meters with their respective values as follows:

RESULTS

Environmental variables: The environ-

mental variables recorded during the surveys

carried out from August 2019 to October 2020

are shown in Table 2. The sectors’ surveyed

areas, and the respective depths and rugosity

indexes are presented in Table 3.

Densities and spatial-temporal distribu-

tion: The total number of Holothuria (H.)

grisea counted during the study was 566 indi-

viduals out of which 360 were used for bio-

metrics. The highest density of H. (H.) grisea

recorded per unit area of the transects was 22.5

individuals*m-2 (T3-winter-09). The densities

varied along the transects for all sampling cam-

paigns (Fig. 3).

The mean densities of Holothuria (H.) gri-

sea within the different sectors of each transect

for all sampling campaigns are presented in

Fig. 4. It clearly shows that transect A (upper

intertidal) had lower densities than sectors

B (lower intertidal) and C (subtidal) in all