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NOTES ON GEOGRAPHIC DISTRIBUTION Check List 14 (2): 453-459

https://doi.org/10.15560/14.2.453

Occurrence of the non-indigenous brittle star Ophiothela cf.
mirabilis Verrill, 1867 (Echinodermata, Ophiuroidea) in natural and
anthropogenic habitats off Santa Catarina, Brazil

Jonathan W. Lawley,' Adriana Carvalhal Fonseca,? Edson Faria Junior,’ Alberto Lindner*

1 Universidade de Sao Paulo, Instituto de Biociéncias, Departamento de Zoologia, Rua do Matao, travessa 14, 101, 05508-090, Sao Paulo, SP,
Brazil. 2 Instituto Chico Mendes de Conserva¢ao da Biodiversidade, Reserva Biol6gica Marinha do Arvoredo, Rodovia Mauricio Sirotsky
Sobrinho, km 02, 88053-700, Floriandpolis, SC, Brazil. 3 Instituto Brasileiro de Biodiversidade, Rua Senador Dantas, 20, 20031-205, Rio de
Janeiro, RJ, Brazil. 4 Universidade Federal de Santa Catarina, Centro de Ciéncias Biologicas, Departamento de Ecologia e Zoologia, Rua Joao Pio
Duarte Silva, 241, Edificio Fritz Miller, 88040-970, Florianopolis, SC, Brazil.

Corresponding author: Jonathan W. Lawley, jwlawley@ib.usp.br

Abstract

The brittle star Ophiothela cf. mirabilis, an ophiuroid introduced in the Atlantic, has expanded its range north to Trini-
dad and Tobago and south to Parana, Brazil. By monitoring the coast of Santa Catarina, Brazil, with both recruitment
plates in harbors and scuba diving, we were able to observe specimens of O. cf. mirabilis in both natural and anthro-
pogenic habitats. This confirms its reported range extension of roughly 80 km south and emphasizes the importance of
anthropogenic means for their spread and establishment.

Key words
Ophiuroid; introduction; exotic species; invasive species; Atlantic Ocean.

Academic editor: Sergio N. Stampar | Received 28 November 2017 | Accepted 18 March 2018 | Published 13 April 2018

Citation: Lawley JW, Fonseca AC, Faria Junior E, Lindner A (2018) Occurrence of the non-indigenous brittle star Ophiothela cf. mirabilis Verrill,
1867 (Echinodermata, Ophiuroidea) in natural and anthropogenic habitats off Santa Catarina, Brazil. Check List 14 (2): 453-459. https://doi.
org/10.15560/14.2.453

Introduction In 2000, Ophiothela cf. mirabilis Verrill, 1867 was
first observed in the Atlantic, off the southeastern coast of
Brazil, in Ilha do Pai, Rio de Janeiro (Hendler et al. 2012).
In 2004 it was seen off Bahia, northeastern Brazil, and in
2009 on the Parana coast, in southern Brazil, as well as in

intermediate locations in Sao Paulo and Espirito Santo; its

The Ophiuroidea or brittle stars, as they are commonly
called, are the largest group of living echinoderms and
occur in all oceans from the intertidal to great depths
(Stohr et al. 2012). Most of them are 5-armed, while
Ophiothela Verrill, 1867, a genus of epizoic ophiuroids,

belongs to a guild that exhibits 6 arms, as well as fis-
siparity, a mode of asexual reproduction that, by dividing
across the disk, produces clones with regenerating arms
(Hendler and Brugneaux 2013). Ophiuroids within this
genus were thought to be confined to Pacific waters
(Clark 1976).

range was extended to encompass approximately 1,800
km of coastline (Hendler et al. 2012). Later from 2011 to
2014, new observations were made not only further north
in Brazil (Pernambuco; Mantellato et al. 2016), but also
in French Guinea and in the Caribbean, including Tobago
(Hendler and Brugneaux 2013) and St Vincent (Hendler

Copyright Lawley et al. This isan open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and source are credited.

A54

Check List 14 (2)

Parana

Santa
Catarina

Atlantic
Ocean

Figure 1. Occurrence of Ophiothela cf. mirabilis in the Western Atlantic. Black circles represent sites where Ophiotela cf. mirabilis was already
recorded; red circles represent the records presented in this study, which are detailed on the inset map.

et al. 2012), the northernmost record in the Atlantic so far
(Fig. 1, Table 1).

Although Pacific specimens of O. cf. mirabilis vary
in color, the Atlantic representatives are nearly all yel-
low-orange, which indicates the prevalence of a single
lineage, as well as a single introduction (Hendler et al.
2012). Nevertheless, the little that is known of its biol-
ogy agrees with the pattern of dispersal and colonization
seen in the Atlantic. Their hooked arm spines help them
attach to a multitude of hosts, which can include macro-
invertebrates that foul ships’ hulls; the fissiparous asexual
reproduction can aid the establishment in new localities;
and sexual reproduction could lead to larval dispersal
through oceanic currents or even in ballast water (Hen-
dler and Brugneaux 2013). The fact that O. cf. mirabilis
is observed near harbors that are far apart from each
other, indicates the potential for anthropogenic dispersal
in the Atlantic (Hendler et al. 2012).

The multitude of hosts in which they are found includes
sponges, cnidarians, ascidians, other echinoderms, algae,
bryozoans, and even seahorses, which emphasizes a lack
of host specificity and a lack of color association between
the ophiuroid and its host in Atlantic waters (Mantellato
et al. 2016). Nevertheless, in Mexican Pacific specimens
of O. mirabilis, in which there is greater color variability,

a significant association was identified between the color
of the brittle star and the host, which differs from what
occurs in the Atlantic (Granja-Fernandez et al. 2014).
This suggests a lack of predators or even the presence
of a predator deterrent, such as chemical defense, in the
Atlantic representatives (Mantellato et al. 2016). Also,
the very high prevalence of O. cf. mirabilis suggests a
potential negative effect for their Atlantic hosts (Mantel-
lato et al. 2016). Nevertheless, these hypotheses are yet
to be tested.

We provide the full details of our records of O. cf.
mirabilis in the state of Santa Catarina, Brazil (as briefly
reported in Mantellato et al. 2016, although without
details, description or correct reference). These Santa
Catarina records are presently the southernmost known
occurrence in the Atlantic.

Methods

Our collections began in December 2012, as part of
the Marine Bioinvaders Project (Projeto Bioinvasores
Marinhos, Programa Costa Atlantica V/2012, SISBIO
collection permit 33662), through which recruitment
granite plates were installed in 3 harbors along the Santa
Catarina coast and monitored monthly until December

Lawley et al. | Ophiothela cf. mirabilis in Santa Catarina, southern Brazil

455

Table 1. Updated geographic distribution of Ophiothela cf. mirabilis in the Atlantic. Coordinates in italic type are approximations based on

the source’s accounts.

Locality (as mentioned in

Country State/ region sources)
Saint Vincent and the Several more Vincentian sites
Grenadines
Saint Andrew Campden Park Bay
Trinidad and Tobago Tobago Goat Island
Little Tobago
Store Bay
French Guiana Les Battures
Brazil Pernambuco
Bahia Farol da Barra

Espirito Santo
Ilha do Pai
Ilha Grande, Lagoa Azul

Rio de Janeiro

Ilha Grande, Barretos

Ilha Grande, Morcegos

Ilha Grande, Abradaozinho right
Ilha Grande, Abradozinho left

Sao Paulo Araca Bay

From Sao Paulo to Espirito Santo
Parana Baleia Rock

Techint Pier

Ilha do Mel

Galheta Island
Currais Archipelago

Santa Catarina Sao Francisco do Sul harbor

Tamboretes Archipelago

2013. There were 5 metal sets per locality, each with
three 25 x 30 cm square granite plates attached, hung
directly into the water by steel ropes so that during low
tide they would still be at a minimum of 2 m underwater.
During each monitoring event, the metal sets were lifted
and placed in a container with seawater from the site, as
photoquadrats were taken and further observations were
made, with few collections and minimal alterations to the
biota on the plates. Plates were returned to the water until
the next monitoring event.

The study sites were the piers of S40 Francisco do Sul
harbor (26°14'00" S, 048°38'15" W), Centro Nacional de
Pesquisa e Conservacao da Biodiversidade Marinha do
Sudeste e Sul (CEPSUL), Itajai (26°54'31" S, 048°39'04"
W), and Imbituba harbor (28°13'49" S, 048°39'06" W).
All of the sites are in harbors or very near them, which
commonly characterizes anthropized areas. Furthermore,
the Sao Francisco do Sul and Imbituba harbors are on or
very near the coast, while CEPSUL is almost 2 km from
the shore, in the Itajai-Acu river.

Scuba dives were also made along the state’s rocky
shores as part of the Marine Bioinvaders Project and
another project, the Marine Biodiversity of Santa Cata-
rina Project (UFSC/FAPESC 4302/2010-8). These dives
were performed regularly, often more than once a month,
from 2010 to 2014, and included not only the assessment
of exotic and invasive species, but also the study of the
benthic community and environmental variables moni-
tored by data loggers.

From Sao Paulo to Espirito Santo

Perea Latitude Longitude Source
2012 13.1783 -061.2661 Hendler et al. 2012
2011 13.1703 -061.2496 Hendler et al. 2012
2013 11.3007 -060.5186 Hendler & Brugneaux 2013
2013 11.2957 -060.5017 Hendler & Brugneaux 2013
2013 11.1553 -060.8411 Hendler & Brugneaux 2013
2012 04.9268 -051.9586 Hendler & Brugneaux 2013
2014 -08.0803 -034.8349 Mantellato et al. 2016
2004 -13.0093 -038.5329 Hendler et al. 2012
-19.8422 -039.7895 Hendler et al. 2012
2000 -22.9856 -043.0854 Hendler et al. 2012
2014 -23.0841 -044.2356 Mantellato et al. 2016
2014 -23.1040 -044.1925 Mantellato et al. 2016
2014 -23.1303 -044.1491 Mantellato et al. 2016
2014 -23.1336 -044.1509 Mantellato et al. 2016
2014 -23.1344 -044.1542 Mantellato et al. 2016
2012 -23.8167 -045.4000 Alitto etal. 2016
-24,3931 -046.5757 Hendler et al. 2012
2013 -25.4138 -048.4063 Bumbeer & Rocha 2016
2012 -25.5536 -048.3648 Bumbeer & Rocha 2016
2009 -25.5748 -048.3161 Hendler et al. 2012
2013 -25.5830 -048.3206 Bumbeer & Rocha 2016
2012 -25.7334 -048.3680 Bumbeer & Rocha 2016
Bumbeer et al. 2016
2013 -26.2334 -048.6376 This study
2014 -26.3838 -048.5227 This study

Five specimens from the Sao Francisco do Sul harbor
were collected and identified under a stereomicroscope.
These specimens were later fixed in 100% ethanol and
donated to the echinoderm collection of the Museu
Nacional in Rio de Janeiro (EQMN) for more detailed
molecular and morphological studies that are currently
ongoing for O. cf. mirabilis in the Atlantic (Tavares and
Ventura unpublished).

Results

Records. Brazil: Santa Catarina. Sao Francisco do Sul
harbor, recruitment granite plates, depth 2 m (26°14'00" S,
048°38'15" W), Jonathan W. Lawley and Adriana Carval-
hal Fonseca, January—December 2013, many individuals
throughout the year (EQMN 4425, 5 specimens); Acarai
State Park: Tamboretes Archipelago, depth 7 m (26°23'2”
S, 048°31'22" W), Jonathan W. Lawley and Edson Faria
Junior, January 2014, dive survey, many individuals.

During monitoring of the recruitment granite plates, the
non-indigenous O. cf. mirabilis was observed exclusively
in the S40 Francisco do Sul harbor (Fig. 2A—C). In this
locality, the alien ophiuroid was observed every month,
although density was much higher from January to April
(up to 60 individuals per plate) than from May to Decem-
ber (occasionally only a couple of individuals per plate)
(Fig. 2B, C). The ophiuroids were observed associated
with encrusting macroinvertebrates, such as ascidians,

456 Check List 14 (2)

Figure 2. Records of Ophiotela cf. mirabilis in artificial and natural environments in Santa Catarina state, southern Brazil. A. Detail of some
specimens found in recruitment granite plates at Sao Francisco do Sul harbor (ca 1.7 mm disc diameter for both specimens). B. A quarter
of a recruitment plate in March 2013, with more than 30 individuals of Ophiotela cf. mirabilis. C. A quarter of the same recruitment plate
in July 2013, with only 1 ophiuroid found; black arrows point to the ophiuroid individuals. D. Individuals of Ophiotela cf. mirabilis found in
natural environment covering the gorgonian Leptogorgia punicea in Tamboretes Archipelago. E. Detail of ophiuroids wrapped around the
same gorgonian.

Lawley et al. | Ophiothela cf. mirabilis in Santa Catarina, southern Brazil 457

Figure 3. Morphological characteristics of Ophiotela cf. mirabilis collected in Santa Catarina state, southern Brazil. A. Dorsal view of a live
specimen, with detail on disc and 1 complete arm. Scale bar = 1.5 mm. B. Details of the lobulated disc and dorsal arm plates, both covered
with round grains. C. Ventral view of the specimen after fixation, with detail on the jaw and its rounded dental papillae, as well as on the
spines of the lateral arm plate; the white arrow points to a hook at the tip of a spine.

bryozoans, cnidarians, and sponges (Fig. 2B, C). Also,
throughout the study period, most of the specimens had 3
arms much shorter than the others (Fig. 2A), or in some
cases only 3 arms in total (Fig. 2C, arrow points to speci-
men).

While performing scuba dive surveys in the Tambo-
retes Archipelago (26°23'2" S, 048°31'22" W), a natural
habitat in the Acarai State Park off the northern coast of
Santa Catarina, in January 2014, O. cf. mirabilis was
recorded in high densities exclusively associated with
the gorgonian Leptogorgia punicea (Milne Edwards &
Haime, 1877) (Fig. 2D, E).

Identification. Ophiuroids collected and photographed in
the field were identified as Ophiothela cf. mirabilis based
on the key and description present in Granja-Fernandez
et al. (2014), as well as on the original description by
Verrill (1867). The specimens have a lobulated disk (disk
diameter = 1.5—2.0 mm) with scattered round unequal
grains, and with 6 arms (Fig. 3A, B). Each lateral arm
plate has 5—6 thorny arm spines with hooks at the tip,
the middle spine usually the longest (Fig. 3C). The dorsal

arm plates are also covered with rounded unequal grains,
with intervals between these plates indicated by naked
spaces (Fig. 3A, B). On the ventral (oral) side, tentacle
scales are absent and ventral arm plates have rounded
edges (Fig. 3C). Oral papillae are absent, while rounded
dental papillae form a cluster in the apex of the jaw
(Fig. 3C). Also, specimens are similar in size, color, and
overall morphology to other specimens in the Atlantic
(Hendler et al. 2012, Hendler and Brugneaux 2013). Nev-
ertheless, even though the aforementioned morphological
features are present in the species’ description and used
in an identification key (Verrill 1867, Granja-Fernandez
et al. 2014), proper identification of Atlantic specimens
remains provisional, due to morphological similarity and
lack of taxonomic resolution in the genus Ophiothela
(Clark 1976, Hendler and Brugneaux 2013).

Discussion

In the recruitment granite plates monitored in the Sao
Francisco do Sul harbor, the ophiuroid density decrease

458

from May to December might be related to the lower
density of encrusting macroinvertebrates present. These
invertebrates, such as ascidians, bryozoans, cnidarians,
and sponges, serve as host species for the establishment
of O. cf. mirabilis (Mantellato et al. 2016), which only
started regaining its previous density later in December
when the density of the hosts increased. Furthermore,
there seemed to be no host preference, as these brittle
stars were not concentrated in any portion of the recruit-
ment plates (Fig. 2B, C). This characterizes the described
opportunistic and generalist behavior of O. cf. mirabilis in
relation to its host species (Mantellato et al. 2016). Addi-
tionally, the observation on most specimens of 3 much
shorter arms, or only 3, of the usual total of 6, indicates
they were regenerating body structures after undergoing
fission, which likely contributes for their establishment in
new localities (Hendler and Brugneaux 2013).

In Tamboretes Archipelago, the ophiuroids were
only observed associated with gorgonians, which is not
unprecedented (Hendler and Brugneaux 2013, Mantellato
et al. 2016). Moreover, this archipelago is near Sao Fran-
cisco do Sul Island (ca 5 km), and approximately 40 km
away from the Sao Francisco do Sul harbor, located in the
Baia da Babitonga estuary (nearest waterway distances).
This record in a nearby natural habitat emphasizes the
potential spread of non-indigenous species from man-
made focal points, such as harbors, in which they seem
to establish. This has also been recorded for O. cf. mira-
bilis in the coast of Parana (Bumbeer and Rocha 2016).
These records confirm the range extension, as reported
in Mantellato et al. (2016), of almost 80 km south into
a new State in the Brazilian coast, which highlights the
continuous spread of O. cf. mirabilis along the Western
Atlantic and the importance of anthropogenic means for
their establishment and, potentially, for their spread, such
as the hulls of ships and ballast water. Dispersal by natu-
ral means could also occur, such as a planktonic larval
stage spread by oceanic currents.

The absence of the ophiuroid in the CEPSUL can pos-
sibly be explained by the lower average salinity in the
area (8 PSU; Schettini 2008) if compared to the other har-
bors monitored that are closer to shore (30.3—32.6 PSU;
Cunha and Costa 2002, Schettini et al. 2005), which are
more likely to have a greater richness of marine inver-
tebrates. However, O. cf. mirabilis is also absent from
Imbituba harbor, which might be explained by the higher
frequency of temperatures below 16 °C characteristic of
waters south of the Island of Santa Catarina (Faria Junior
2014); these brittle stars originate from tropical waters
of the Eastern Pacific. The state of Santa Catarina is the
southern limit of distribution for many species of cor-
als, fish, and other invertebrates (e.g. Floeter et al. 2008,
Capel et al. 2012). In that sense, the absence of the ophiu-
roids in the monitored localities mentioned above as well
as other southernmost localities surveyed by scuba div-
ing can be due to biological limitations, although it could
also have yet to expand its distribution.

Check List 14 (2)

Acknowledgements

We thank the Instituto COMAR for transportation to
Tamboretes Archipelago and Johnatas Adelir Alves and
Paulo Eduardo Pereira Faria for their assistance with the
scuba diving surveys. We also thank Diana Carla Floriani,
Leandro Zago da Silva and other ICMBaio staff for all the
assistance during monitoring of recruitment plates, and to
Instituto Ekko Brasil for support in other project logistics.
This research was funded by FAPESC (4302/2010-8) and
by the Programa Costa Atlantica (V/2012, Projeto Bioin-
vasores Marinhos).

Authors’ Contributions

JWL, ACF, and AL conceived the experiment and JWL,
ACF, and EFJ collected the data. JWL wrote the text,
and all authors reviewed, finalized, and approved the
manuscript.

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