Volume 7, Manuscript ID
es20240011, p. 01-06, 2024
Doi: https://doi.org/10.32435/envsmoke-2024-0011
Environmental
Smoke, e-ISSN: 2595-5527
“A leading multidisciplinary
peer-reviewed journal”
Full
Article:
REVIEWING THE DISTRIBUTION
OF THE SEA SLUG Bursatella leachii BLAINVILLE, 1817 (APLYSIIDAE, MOLLUSCA) IN
BRAZIL, WITH ITS FIRST RECORD IN THE STATE OF SERGIPE, NORTHEASTERN REGION
Caio Correia
Régis-Silva1,2* (https://orcid.org/0009-0007-2776-1765); Leonardo Cruz da Rosa1,2 (https://orcid.org/0000-0002-4263-332X)
1Universidade Federal
de Sergipe (UFS), Centro de Ciências Agrárias Aplicadas (CCAA), Departamento de
Engenharia de Pesca e Aquicultura (DEPAq),
Laboratório de Ecologia Bentônica (LEB). Avenida Marcelo Déda Chagas, s/n,
Bairro Rosa Elze, CEP 49107-230, São Cristóvão, Sergipe, Brasil.
2Universidade Federal
de Sergipe. Programa de Pós-Graduação em Ecologia e Conservação (PPEC), São
Cristóvão, Sergipe, Brasil.
*Corresponding author: regis_silva_br@outlook.com
Submitted
on: 11 Dec. 2024
Accepted
on: 18 Dec. 2024
Published
on: 21 Dec. 2024
License:
https://creativecommons.org/licenses/by/4.0/
Abstract
This study
expands and establishes the known distribution of Bursatella leachii in
Brazil through a review of the literature on the species' distribution in the
country and the first records of the species in the state of Sergipe,
Northeastern region. The literature review involved a search in the Google
Scholar database, as well as data from preserved specimens in biological
collections Available from GBIF. Specimens of B. leachii were examined
and photographed in the field, during the dry season (summer) on sandy-muddy
bottoms within estuaries with distinctives disturbance levels in the State of
Sergipe, Northeastern Brazil. Egg masses were also recorded at one locality.
These records correspond to the first records of the species for the state. The
review of B. leachii records in Brazil, together with the first records
for Sergipe, allowed us to establish that B. leachii occurs along the
Brazilian coast from Rio Grande do Sul to Ceará.
Keywords: Estuary.
Gastropoda. Heterobranchia. Mollusca. Southwest
Atlantic.
1
Introduction
Heterobranch
gastropods, commonly known as sea slugs, are a mollusk subclass characterized
by evolutionary changes resulting in reduced, internalized, or absent shells,
particularly in their more recent lineages (FERREIRA JUNIOR et al., 2015;
DELGADO et al., 2022). These group are not easily observed or studied due to their
rarity, appearing infrequently in both space and time (LARKIN et al., 2018;
SCHUBERT; SMITH, 2020). Of the 6000 described species, approximately 250 sea
slugs are reported in Brazil, with 124 for the Northeastern region (RIOS, 2009;
DELGADO et al., 2022).
Commonly known as the shaggy sea hare,
ragged sea hare, hairy sea hare, and blue-spotted sea hare, Bursatella leachii
Blainville, 1817 is a sea slug belonging to the family Aplysiidae (PERISSINOTTO
et al., 2014; ALENCAR et al., 2024). This species has a pantropical
distribution, occurring in warm temperate to tropical marine waters, with no
occurrences reported only along the Eastern Pacific and European Atlantic
coasts (BAZZICALUPO et al., 2018; 2020). Nowadays, it is considered an invasive
species in the Eastern Mediterranean (ZENETOS et al., 2005).
The first record of Bursatella leachii
in Brazil is attributed to Couthouy in Gould (1852),
based on a specimen from Rio de Janeiro, initially identified as Bursatella
lacinulata (BAZZICALUPO et al., 2020).
However, the first research focused on the distribution of B. leachii in
Brazil dates back to the 20th century, with research
by Marcus (1955) aimed at inventorying Opisthobranchia
in the state of São Paulo. Later, García-García; Álvarez; Troncoso (2008), in
their book about opistobranchs from Brazil, recorded this species only to São
Paulo coast, while Rios (2009) in his compendium of seashells from Brazil cite
the species to states of Pernambuco, Rio de Janeiro, São Paulo and Rio Grande
do Sul. Recently, Alencar et al. (2024) increased a distribution extension of B.
leachii on Rio Grande do Norte, northeastern Brazil and stated the states
of Paraná, São Paulo, Rio de Janeiro, Ceará and Alagoas as distributional area
of the species.
Overall, a few studies have addressed the
occurrence of Bursatella leachii with its presence typically recorded
within broader local and regional malacological surveys (e.g. FERREIRA JUNIOR
et al., 2015; DELGADO et al., 2022; ALENCAR et al., 2024). This knowledge gap
regarding the known range of the species in Brazil has been exacerbated by the
scattered nature of existing information, with newer studies lacking a review
of the species' records, leading to uncertainties about the actual distribution
of the species in the country.
In this study, we recorded by the first
time the occurrence of Bursatella leachii in the Sergipe coast,
northeastern Brazil. Additionally, we are gathering all information about the
occurrence of this species along Brazilian coast from a bibliographic survey
and its updated distribution is provided.
2 Material
and Methods
On December 31, 2021, one individual with
approximately 91 mm long (Figure 1D) was recorded during the low tide period in
a shallow water (10 cm of depth) sandy-muddy bottom of the Parapuca
Channel (10°34.491' S 36°35.827' W), at the municipality of the Pacatuba,
northern coast of Sergipe state (Figures 1A-1B). The individual was examined,
photographed and released back to the environment. Three years later and 62 km
southward, at the Aracaju city, capital of Sergipe state (10°55.810' S
37°2.569' W; Figures 1A; 1C), six other individuals with lengths ranging from
45 to 74 mm were recorded in a sandy-muddy tidal flat near to mouth of the
Sergipe Estuary, during a field class carried out on January 27, 2024 (Figure
1E). In this occasion, it was also possible record egg mass deposited on rock
fragments (Figure 2).
Considering
the distribution range of Bursatella leachii along the Brazilian
coast, we conducted a bibliographic research in the Google Scholar database
using the terms “(Bursatella OR leachi OR leachii)
AND (Brazil OR Brasil)” and “(Bursatella OR leachi OR leachii) AND (the name of each one coastal state
of Brazil individually)”. Additionally, we consulted the Global Biodiversity
Information Facility (GBIF) database (www.gbif.org) to verify possible records of preserved
specimens of B. leachii in biological collections not documented in
scientific publications.
3 Results
Taxonomy:
Phylum Mollusca
Cuvier, 1795
Class Gastropoda
Cuvier, 1795
Order
Aplysiida (Fischer, 1883)
Family
Aplysiidae Lamarck, 1809
Genus Bursatella
Blainville, 1817
Bursatella
leachii Blainville, 1817
Examined
material: BRAZIL – State of Sergipe, Pacatuba, Parapuca
Channel, (10°34.491' S 36°35.827' W; Figures 1A-1B), 31.X.2021; one specimen,
91 mm long (Figure 1D). Sergipe, Aracaju (10°55.810' S 37°2.569' W; Figures 1A;
1C), 27.I.2024, six specimens, ranging from 45 to 74 mm (Figure 1E) and an egg
mass (Figure 2).
Figure
1. Study Area: A. Map of the State of Sergipe. B. Sampling
site of Bursatella leachii Blainville, 1817 in the Parapuca
Channel (red dot). C. Sampling site of B. leachii at the mouth of the
Sergipe River (green dot). D. Specimen of B. leachii recorded at the Parapuca Channel. E. One of the specimens of B. leachii
recorded at the mouth of the Sergipe River. Access on: https://drive.google.com/file/d/17Q7CyvtFrMv3mILIDINILRi_HZW3MI5-/preview
Figure
2. Egg masses of B.
leachii recorded at the mouth of the Sergipe River on a rocky substrate.
Access on: https://drive.google.com/file/d/1xDLbU-njCppKuE9OxiYSK6ujUyXRQrJN/preview
Diagnosis: Absence of a shell and a long oval-shaped soft body that
tapers at the anterior part and is wider at the posterior part. The dorsal
region of the head features two rhinophores and several tentacles around the
mouth.
The dorsal region is covered with ramified
papillae, varying in size, with the primary papillae being larger than their
branches. There are two small fused parapodial flaps covering the gills in the
posterior region. All specimens were greenish with papillae of orange/copper
color. The egg mass was a resilient, gelatinous tube-shaped cord.
Remarks: All these external morphological characteristics
corroborate with the descriptions proposed by Meirelles, Galvão Filho and
Matthews-Cascon (2011), Bazzicalupo et al. (2020) and
Delgado et al. (2022) to the Bursatella leachii. Thus, the present
record represents the first occurrence of this species in the coastal zone of
the Sergipe state.
Global
distribution: Pantropical distribution,
inhabiting warm temperate and tropical marine waters worldwide, except along
the eastern Pacific and European Atlantic coasts. Western Atlantic from USA
to Brazil, Eastern Atlantic from Canary Islands to South Africa. Mediterranean
and Red Seas. Indian and Pacific Oceans, ranging from Japan to Australia,
including New Zealand and French Polynesia, but absent from the Hawaiian Islands
(ZENETOS et al., 2005; PERISSINOTTO et al., 2014; GUTIÉRREZ et al., 2015; BAZZICALUPO
et al., 2018; 2020).
Distribution in the Brazilian states: Ceará (BARROSO;
MATTHEWS-CASCON, 2009), Rio Grande do Norte (DELGADO et
al., 2022; ALENCAR et al., 2024), Paraíba (DUARTE;
MOTA; DIAS, 2014), Pernambuco (MARCUS, 1972; RIOS, 2009), Alagoas (PADULA et al., 2012), Sergipe (this
study), Rio de Janeiro (GOULD, 1852; RIOS, 2009;
BAZZICALUPO et al., 2020), São Paulo (MARCUS, 1955;
RIOS, 2009), Paraná (FERREIRA JUNIOR et al., 2015),
Santa Catarina (LINDNER, 2014), Rio Grande do Sul (RIOS, 2009).
Additional
information from the reports in Brazil: Our bibliographic
survey identified the occurrence of Bursatella leachii in ten of
the 17 Brazilian coastal states. According with GBIF database, there are
records of preserved specimens of the B. leachii for the states of
Espirito Santo, material deposited in the Mollusk Collection of the Museu Nacional do Rio de Janeiro (MNRJ) on ID
“Br:MNRJ:Mollusca:10644” (PIMENTA, 2024 - https://www.gbif.org/occurrence/1435843043), and
Bahia, material deposited in the Gastropoda Collection of the Museu de Zoologia da UNICAMP
(ZUEC-GAS) on ID “BRA:UNICAMP:ZUEC-GAS:6696” (DIAS PASSOS, 2024 - https://www.gbif.org/occurrence/2973759884).
4 Discussion
The
species Bursatella leachii is a benthic herbivorous and
detritivores organism (MARCUS, 1955; CLARKE, 2006; GUTIÉRREZ et al., 2015),
inhabiting shallow waters, from intertidal to less than 10 m (GUTIÉRREZ et al.,
2015; ALENCAR et al., 2024).
This
species has been found in various habitats, including sandy beaches (MARCUS,
1972; CLARKE, 2006; DELGADO et al., 2022; ALENCAR et al., 2024), tide pools
(PERISSINOTTO et al., 2014), intertidal sand-mud flats (MEIRELLES; GALVÃO
FILHO; MATTHEWS-CASCON, 2011; FERREIRA JUNIOR et al., 2015), patch reefs
(DUARTE; MOTA; DIAS, 2014), shell mound zones, rocky coastal areas (CLARKE,
2006; ALENCAR et al., 2024), saline mangroves (BARROSO; MATTHEWS-CASCON, 2009;
ALENCAR et al., 2024), estuaries and rivers (BARROSO; MATTHEWS-CASCON, 2009;
PERISSINOTTO et al., 2014).
B. leachii also has
been associated with seagrass beds (CLARKE, 2006; GUTIÉRREZ et al., 2015) and
algae mats, including Gracilaria cervicornis (Turner, 1808) (MARCUS, 1955) and others
(see CLARKE, 2006).
In Sergipe
coast, both records occurred in estuarine tidal flats during low tide periods.
The Parapuca Channel is part of the delta of the São
Francisco River, extending approximately 25 km southward of the river mouth.
This channel is situated inside the Santa Isabel Biological Reserve; the region
is relatively undisturbed with low urbanization level.
Therefore,
this area might be considered as a pristine environment, despite the increasing
presence of nearby shrimp farms (SANTOS et al., 2016).
In other
hand, the Sergipe estuarine area is a very disturbed and polluted area affected
by whole metropolitan region of Aracaju (ALVES; PASSOS;
GARCIA, 2007; ROSA, 2023).
The
presence of individuals as well as their egg mass in this highly polluted area
suggests a great plasticity of this species to explore areas with different
levels of disturbance.
Thus,
considering the first record of this species on Sergipe coast documented here
and the results of our bibliographic surveys, the distribution range of Bursatella
leachii along the Brazilian coast extends from Rio Grande do Sul to
Ceará.
5 Conclusions
In this
study, we describe the first records of Bursatella leachii for the coast of
Sergipe, in different localities and years.
We address
the distribution gap of B. leachii in Sergipe, increases the recorded
marine invertebrates for the state, and updates the species' known range in
Brazil.
CREDIT AUTHORSHIP CONTRIBUTION STATEMENT
All the authors contributed with the conceptualization,
study design, species identification, and manuscript writing.
DECLARATION
OF INTEREST
The authors disclose that they have no known
competing financial interests or personal relationships that could have
appeared to influence the study reported in this manuscript.
FUNDING
SOURCE
The authors declare that no funding is
applicable for this research.
AI-BASED
WRITING STATEMENT
The authors who carried out this research
declare the use of AI-based tools, specifically OpenAI's ChatGPT (https://chatgpt.com/) and Google Gemini (https://gemini.google.com/), to assist in the language revision of this
manuscript.
REFERENCES
ALENCAR, C.E.R.D.; SILVA, T.A.; RODRIGUES,
L.S.; MELO, M.D.; PERETTI, D. Distribution extension of the sea slug Bursatella
leachii Blainville, 1817 (Gastropoda, Heterobranchia)
on Rio Grande do Norte, Northeast Brazil. Oecologia
Australis, v. 28, n. 2, p. 134–140, 2024. Available from: https://doi.org/10.4257/oeco.2024.2802.05
ALVES, J.P.H.; PASSOS, E.A.; GARCIA, C.A.B.
Metals and Acid Volatile Sulfide in Sediment Cores from the Sergipe River
Estuary, Northeast, Brazil. Journal of the Brazilian Chemical Society,
v. 18, n. 4, p. 748–758, 2007. Available from: https://doi.org/10.1590/S0103-50532007000400013
BARROSO, C.X.;
MATTHEWS-CASCON, H. Distribuição espacial e temporal da malacofauna
no estuário do rio Ceará, Ceará, Brasil. Pan-American Journal of Aquatic Sciences, v. 4, n. 1, p. 79–86, 2009. Available
from: https://panamjas.org/artigos.php?id_publi=166. Accessed on: 11 Aug. 2024.
BAZZICALUPO, E.; CROCETTA, F.;
ESTORES-PACHECO, K.; GOLESTANI, H.; BAZAIRI, H.; GIACOBBE, S.; JAKLIN, A.;
POURSANIDIS, D.; SNEHA CHANDRAN, B.K.; CERVERA, J.L.; VALDÉS, Á. Population
genetics of Bursatella leachii (De Blainville, 1817) and implications
for the origin of the Mediterranean population. Helgoland Marine Research,
v. 72, n. 1, 2018. Available from: https://doi.org/10.1186/s10152-018-0521-7
BAZZICALUPO, E.; CROCETTA, F.; GOSLINER,
T.M.; BERTEAUX-LECELLIER, V.; CAMACHO-GARCÍA, Y.E.; SNEHA CHANDRAN, B.K.;
VALDÉS, Á. Molecular and morphological systematics of Bursatella leachii
de Blainville, 1817 and Stylocheilus
striatus Quoy & Gaimard,
1832 reveal cryptic diversity in pantropically distributed taxa (Mollusca:
Gastropoda: Heterobranchia). Invertebrate
Systematics, v. 34, n. 5, p. 535–568, 2020. Available from: https://doi.org/10.1071/IS19056
CLARKE, C.L. The population dynamics and
feeding preferences of Bursatella leachii (Opisthobranchia:
Anaspidea) in northeast Queensland, Australia. Records
of the Western Australian Museum, Supplement, v. 69, n. 1, p. 11, 2006.
Available from: https://doi.org/10.18195/issn.0313-122x.69.2006.011-021
DELGADO, M.; FREIRE, F.A.M.; MEIRELLES,
C.A.O.; D’OLIVEIRA, R.G.; PADULA, V.; BAHIA, J.; BRANDÃO, S.N. Sea slugs
(Gastropoda: Heterobranchia) from Rio Grande do
Norte, Northeastern Brazil. Papeis Avulsos de Zoologia, v. 62, 2022. Available from: https://doi.org/10.11606/1807-0205/2022.62.063
DIAS
PASSOS, F. ZUEC-GAS - Coleção de Gastropoda
do Museu de Zoologia da UNICAMP. Version
1.93. Universidade Estadual de Campinas - Instituto de Biologia. Occurrence dataset accessed via GBIF.org. Available from: https://doi.org/10.15468/73mksc
DUARTE, R.C.S.; MOTA,
L.S.; DIAS, T.L.P. Mollusk fauna from
shallow-water back reef habitats of Paraíba coast, northeastern Brazil. Strombus, v. 21, n. 2, p. 15–29, 2014. Available from: https://strombusjournal.org/archives/405-2/. Accessed on: 11 Aug. 2024.
FERREIRA JUNIOR, A.; CARVALHO, I.; CHRISTO,
S.; ABSHER, T. New records of marine “sea slugs” (Mollusca: Gastropoda: Heterobranchia) in the outlets of the estuary systems in
Paraná, southern Brazil. Check List, v. 11, n. 1, 2015. Available from: https://doi.org/10.15560/11.1.1548
GARCÍA-GARCÍA,
F.J.; ÁLVAREZ, M.D.; TRONCOSO, J.S. Opistobranquios de
Brasil: Descripción y distribución de opistobranquios del
litoral de Brasil y del Archipiélago Fernando de Noronha. Vigo: Feito, 2008. Available
from: https://dialnet.unirioja.es/servlet/libro?codigo=720285. Accessed on: 11
Aug. 2024.
GOULD, A.A. Mollusca
and shells in United States Exploring Expedition. During the years 1838, 1839,
1840, 1841, 1842. Under the Command of Charles Wilkes, U.S.N. Gould &
Lincoln: 1852. Available from: https://www.biodiversitylibrary.org/page/10991152#page/12/mode/1up. Accessed on: 11
Aug. 2024.
GUTIÉRREZ, M.C.; ORTEA, J.; RIVERO, N.;
TUCKER, G.C.; MALAQUIAS, M.A.E.; NARCISO, S. The opisthobranch gastropods
(Mollusca: Heterobranchia) from Venezuela: An
annotated and illustrated inventory of species. Zootaxa,
v. 4034, n. 2, p. 201–256, 2015. Available from: https://doi.org/10.11646/zootaxa.4034.2.1
LARKIN, M.F.; SMITH, S.D.A.; WILLAN, R.C.;
DAVIS, T.R. Diel and seasonal variation in heterobranch
sea slug assemblages within an embayment in temperate eastern Australia. Marine
Biodiversity, v. 48, n. 3, p. 1541–1550, 2018. Available from: https://doi.org/10.1007/s12526-017-0700-9
LINDNER,
A. (ed.). Vida marinha de Santa Catarina.
Florianópolis:
Editora da UFSC, 2014. Available from: https://livraria.ufsc.br/. Accessed on: 11 Aug. 2024.
MARCUS,
E. Opisthobranchia from
Brazil. Boletim da Faculdade de Filosofia, Ciências e Letras, Universidade de
São Paulo. Zoologia, v. 20, n. 20, p. 89-261,
1955. Available from: https://doi.org/10.11606/issn.2526-3382.bffclzoologia.1955.120213
MARCUS, E. On the
Anaspidea (Gastropoda: Opisthobranchia)
of the warm waters of the western Atlantic. Bulletin of Marine Science v. 22, n. 4, p.
841–874, 1972. Available from:
https://www.ingentaconnect.com/content/umrsmas/bullmar/1972/00000022/00000004/art00005. Accessed on: 11
Aug. 2024.
MEIRELLES,
C.A.O.; GALVÃO FILHO, H.; MATTHEWS-CASCON, H. Bursatella leachii de
Blainville, 1817. In: MATTHEWS-CASCON, H.; ROCHA-BARREIRA, C.A.; MEIRELLES,
C.A.O. (eds.) Egg masses of some Brazilian mollusks [Desovas de alguns moluscos Brasileiros]. Fortaleza:
Expressão Gráfica e Editora, 2011. p. 91-93. Available
from: https://www.researchgate.net/publication/216719335_Egg_Masses_of_some_Brazilian_Mollusks_-_Desovas_de_alguns_Moluscos_Brasileiros.
Accessed on: 11 Aug. 2024.
PADULA,
V.; BAHIA, J.; CORREIA, M.D.; SOVIERZOSKI, H. H. New records of opisthobranchs (Mollusca: Gastropoda) from
Alagoas, Northeastern Brazil. Marine Biodiversity Records, v. 5, n. 3, p.
1–11, 2012. Available from: https://doi.org/10.1017/S1755267212000346
PERISSINOTTO, R.; MIRANDA, N.A.F.; RAW,
J.L.; PEER, N. Biodiversity census of lake St Lucia, iSimangaliso
Wetland Park (South Africa): Gastropod molluscs. ZooKeys, n. 440, p. 1–43, 2014. Available from: https://doi.org/10.3897/zookeys.440.7803
PIMENTA, A.
(2024). Mollusca Collection
- Museu Nacional/UFRJ. Version
1.10. Museu Nacional / UFRJ. Occurrence
dataset accessed via GBIF.org. Available from: https://doi.org/10.15468/g5ykee
RIOS, E.C. Compendium
of Brazilian sea shells. Rio
Grande: Editora Evangraf. 2009. Available
from: https://books.google.com.br/books/about/Compendium_of_Brazilian_Sea_Shells.html?id=_ETYZwEACAAJ&redir_esc=y.
Accessed
on: 11 Aug. 2024.
ROSA, L.C. Plastic debris usage by
tube-building polychaete Diopatra cuprea complex. Arquivos de Ciências do
Mar, v.
56, n. 2, 2023. Available from:
https://doi.org/10.32360/acmar.v56i2.82806
SANTOS, L.C.M.; ROLLO
JUNIOR, M.M.; COSTA, T.M.; PINHEIRO, M.A.A.; DAHDOUH-GUEBAS, F.; BITENCOURT,
M.D. Spatial analysis of a coastal area for conservation and fishery of mangrove edible crab (Ucides
cordatus). Journal of Coastal Research, v. 1, n. 75, p. 685–689, 2016. Available
from: https://doi.org/10.2112/SI75-137.1
SCHUBERT, J.; SMITH, S.D.A. Sea slugs—“rare in space and time”—but not always. Diversity,
v. 12, n. 11, p. 1–14, 2020. Available from: https://doi.org/10.3390/d12110423
ZENETOS, A.; ÇINAR, M.E.; PANCUCCI-PAPADOPOULOU, M.A.; HARMELIN, J.G.; FURNARI, G.; ANDALORO, F.; BELLOU, N.; STREFTARIS, N.; ROWIUS, H.Z. Annotated list of marine alien species in the Mediterranean with records of the worst invasive species. Mediterranean Marine Science, v. 6, n. 2, p. 63–118, 2005. Available from: https://doi.org/10.12681/mms.186