Volume 6, Issue 2, p. 01-08, August 2023
Doi: https://doi.org/10.32435/envsmoke-2023-0001
Environmental Smoke, e-ISSN:
2595-5527
“A leading multidisciplinary
peer-reviewed journal”
Full
Article:
TWO IN ONE: REPORT OF
TWO EPIBIONTS GROUPS ON THE Callinectes bocourti A.
MILNE-EDWARDS, 1879 (DECAPODA: PORTUNIDAE) FROM THE AMAZON PROVINCE
Flavio de Almeida Alves-Júnior1,2* (https://orcid.org/0000-0003-3002-6845); Déborah
Elena Galvão Martins1,2 (https://orcid.org/0000-0002-3829-4388); Barbara
Siqueira Monteiro2 (https://orcid.org/0009-0004-3595-6843); Jonata Arruda Francisco3 (https://orcid.org/0000-0002-7607-6904); Alex
Garcia Cavalleiro de Macedo Klautau4 (https://orcid.org/0000-0002-0029-7639); Israel
Hidenburgo Aniceto Cintra2 (https://orcid.org/0000-0001-5822-454X)
1Universidade Federal do Pará, Núcleo de
Ecologia Aquática e Pesca (NEAP), Rua Augusto Corrêa, S/N Guamá, CEP:
66075-110, Belém, Pará, Brasil. Programa de Pós-Graduação em Ecologia Aquática
e Pesca (PPGEAP) da Universidade Federal do Pará (UFPA), Belém, Pará, Brasil
2Laboratório de Crustáceos (LABCRUS), Instituto
Socioambiental e dos Recursos Hídricos (ISARH), Universidade Federal Rural da
Amazônia (UFRA), Avenida Presidente Tancredo Neves - Terra Firme, nº 2501,
Belém, Pará, Brasil
3Centro Nacional de Pesquisa e Conservação da
Biodiversidade Marinha do Nordeste (CEPENE). Rua Samuel Hardman,
s/n - Tamandaré, CEP: 55578-000, Pernambuco, Brasil
4Centro de Pesquisa e Conservação da Biodiversidade
Marinha do Norte / Instituto Chico Mendes de Conservação da
Biodiversidade-ICMBio, Belém, Pará, Brasil. Rua Tancredo Neves, 2501 -
Mangueirão, CEP: 66635-110, Belém, Pará, Brasil
*Corresponding author: bioflavio@hotmail.com
Submitted on: 27 May 2023
Accepted on: 14 Jul. 2023
Published on: 31 Aug. 2023
License:
https://creativecommons.org/licenses/by/4.0/
Case studies reporting crustaceans acting as basibionts for a wide range of encrusting invertebrates are
widely observed in the literature. For swimming crabs of the genus Callinectes, these commensal
interactions are commonly observed in estuaries and coastal zones worldwide.
Despite the broad distribution of Callinectes
bocourti A. Milne-Edwards, 1879 in Amazon
province, the occurrence of epibiosis for this
species in the area is rarely reported. Herein, we report the double occurrence of epibiont
groups: the mollusks Ostrea puelchana d’Orbigny,
1842 and Sphenia fragilis (H. Adams & A. Adams,
1854) and the barnacles Amphibalanus improvisus (Darwin,
1854) and Chelonibia testudinaria
(Linnaeus, 1758) from the new host C. bocourti, collected from the Amazon province, Brazil.
The specimens of C. bocourti
showing epibionts were collected manually in low tide, with a baited trap
called “puçá”, in the region of Curuçá
River mouth, state of Pará (0°40’3,705”S, 047°54”43,405”W). We observed five specimens of C. bocourti showing double cases of epibiosis, composed by mollusks and crustaceans sharing the
same area. In addition, here, we expand the range extension of the mollusk O. puelchana and we register the presence of the invasive
species barnacle A. improvisus
from the state of Pará, being this last species, reported as parasite adhered
in carapace and branchial chambers of the host.
Keywords:
Mollusk. Barnacle. Commensal interaction. Non-native species. New host
interaction.
1 Introduction
Epibiosis is
the main mechanism used by marine benthic sessile organisms in search of
settlement for their development on hard substrates (ABELLÓ et al., 1990;
NEGREIROS-FRANSOZO et al., 1995; EMPARANZA et al. 2011). For the attachment in
hard bottoms, the individuals present a wide range of morphological and
behavioral adaptations, enabling survival in the aquatic environment (WAHL,
2008; DOLDAN et al., 2012). However, in aquatic habitats, hard substrate is
limited or it exhibits high competition for space, especially in estuarine and
coastal areas, where soft sediments and high levels of sedimentation are common
(WAHL, 2008; LIMA et al., 2017).
As
adaptation to fixation in environments with high hydrodynamics and
sedimentation levels, fouling organisms use the body structures of other groups
for adherence (MCDERMOTT, 2006; RIBEIRO et al., 2016). This is widely observed
for mollusks and crustaceans (barnacles), and also for other invertebrates and
vertebrates (EMPARANZA et al., 2011; GÓNGORA-GÓMEZ et al., 2015). In the
commensal interaction, mollusks and barnacles are broadly reported as epibionts
in several invertebrate groups such as crabs, sponges, echinoderms, corals,
ascidians and in vertebrates adhered in whales, dolphins, manatees and turtles
(LEWIS, 1978; LIMA et al., 2017).
The
commercial swimming crabs of the family Portunidae Rafinesque, 1815 are
commonly found in estuarine and coastal zones around the world, being a source
of food and livelihood for several families at different levels of fishing
activity (MORUF;
LAWAL-ARE, 2017; CORDEIRO et al., 2021). The presence of epibiosis in
species of the genus Callinectes Stimpson,
1860 was reported by Ganon and Wheatl (1992),
Negreiros-Fransozo et al. (1995), Key Jr. et al.
(1999), Santos and Bueno (2002) and Mantelatto et al.
(2003), especially with barnacles adhered on carapace, chelipeds and ambulatory
legs. According to Marin and Belluga (2005), Lima et
al. (2017) and Alves-Júnior et al. (2021), this fixation favors the supply of
food for the epibiont, based on the fact that the basibiont
is vagile, on the other hand, for the host, it can be harmful because of the
extra weight and friction in the water.
According to Farrapeira (2010), one of most
representative epibiont barnacle in literature is Chelonibia testudinaria (Linnaeus, 1758), followed by the
invasive species Amphibalanus improvisus (Darwin,
1854), which is reported along the Brazilian waters fixed in a wide range of
organisms, covering invertebrates and vertebrates.
In addition, the bivalve mollusk Ostrea puelchana d’Orbigny,
1842 was observed as epibiont in some crustaceans such as Callinectes exasperatus (Gerstaecker, 1856) and Eriphia gonagra (Fabricius, 1781) (LIMA et al.
2011; ALVES-JÚNIOR et al., 2021). However, the mollusk species Sphenia fragilis (H. Adams & A. Adams,
1854) is not reported in the literature as epibiont in decapods, being
recorded, in Brazil, from Pará to Paraná, on
mussel and barnacle beds along the intertidal zone. Herein, we report the double
occurrence of epibionts groups; the barnacles C. testudinaria and A.
improvisus and the mollusks O. puelchana and S.
fragilis in the new host Callinectes
bocourti A. Milne-Edwards, 1879, collected from the Amazon
province, Brazil; additionally, extending the range extension of one barnacle
and two mollusk species for the northern Brazil.
2 Material and
Methods
Study Area
The specimens of C. bocourti and their epibionts were
manually collected in low tide, with a baited trap called “puçá”, in Santa Maria River, Iririteua
comunity, located in the municipality of Curuçá, state of Pará (0°40’3,705”S, 047°54”43,405”W) (Figure 1), between January and
May 2023. The region is a fluvial-marine plain, in the region of Curuçá River mouth, influenced by Curuçá,
Mocajuba and Maripanema
Rivers and subjected to sedimentation process and macro-tidal range. The collection was
authorized by the “Sistema de Autorização e Informação em Biodiversidade” (SISBIO
Number 44915-3), “Instituto Chico Mendes
de Conservação da Biodiversidade”
(ICMBio), Ministry of Environment, from the Federative Republic of Brazil.
Figure 1. Map of the study area, A. Northern Brazilian coast. B. Municipality of Curuçá, state of Pará. C. Sampling point (black circle) in Santa Maria River.
Access on: https://docs.google.com/uc?id=1OHQQ86ZU3hCFBuETy0ZdR5GA_qjw51kj
Laboratory Procedures
After collected, the individuals showing epibiosis were sorted out, frozen and carried to the
Carcinology Laboratory of Universidade Federal
Rural da Amazônia (UFRA), where they were photographed, measured in carapace width (CW),
carapace length (CL) and wet weight (W) (swimming crabs), largest and smallest
diameter (∅) (barnacles); and the mollusks the valve
length (VL). The total area of the
carapace and chelipeds was counted as 100%, and the area occupied in
centimeters by each epibiont was evaluated and assigned a percentage of host
occupancy following the methodology of Lima et al. (2017). Species
identification followed Melo
(1996) for the swimming crabs, while the barnacles
identification followed Young (1999); and the mollusk species according to Rios
(2009). The specimens were then fixed in 70% ethanol and deposited at the Carcinological Collection of Carcinology Laboratory of
UFRA.
3 Results and Discussion
We collected five specimens of C. bocourti (CL:
5.81- 6.30 cm; CW 11.5 - 14.12 cm; W 87.2 - 216.76 g) showing epibiosis composed by two barnacles
species: C. testudinaria (∅: 1.34 - 3.16 cm) and A. improvisus (∅: 0.60 - 0.88 cm). We observed 73
individuals of C. testudinaria, covering ~47% of carapace and ~18% of
chelipeds (Figures 2A-B; 3A-B; 4 F-G-H-I-J); 11 individuals of A. improvisus,
covering ~16% of the carapace area, and ~53% of the branchial chambers (Figures
2C - 3C-D; 4 A-B-C-D-E). In addition, we observed 4 specimens of O. puelchana (VL: 1.12 - 2.44 cm) adhered only in
chelipeds, represented by ~28% of the chelipeds region (Figures 2B-D), while 9
specimens of the bivalve S. fragilis
(VL: 0.69 - 0.97 cm) were represented adhered only to the carapace, with ~3% of
total area occupied (Figure 2E).
Figure 2. A-B. The swimming
crab Callinectes bocourti
A. Milne-Edwards, 1879 showing epibiosis by Chelonibia testudinaria (Linnaeus, 1758); B. Ostrea puelchana d’Orbigny,
1842 adhered to the left cheliped of C. bocourti. C. Amphibalanus improvisus (Darwin, 1854) in highlighted
view. D. Ostrea puelchana
in highlighted
view. E. Sphenia fragilis (H. Adams & A. Adams,
1854) in highlighted view. Scale bars= swimming crabs = 20 mm; barnacle = 1 mm;
mollusks = 5 mm.
Access
on: https://drive.google.com/file/d/1HyaM9gSuTjCQBfqtwdRY6p9ueANo0x-1/preview
Figure 3. A.
The
swimming crab Callinectes bocourti A. Milne-Edwards, 1879 showing double epibiosis promoted by the barnacle Amphibalanus improvisus
(Darwin, 1854)
and the mollusk Ostrea puelchana d’Orbigny,
1842. B. High infestation by Chelonibia testudinaria (Linnaeus, 1758) in C. bocourti. C.
Branchial chamber of C. bocourti indicating A. improvisus
as endoparasite. D.
Amphibalanus improvisus as
endoparasite in highlighted view. Scale bars = swimming crabs = 20 mm.
Access
on: https://drive.google.com/file/d/1UfIgLcMw-idzCOL8x2lNMSbAZGdRL3m1/preview
Figure 4. A.
Amphibalanus improvisus (Darwin,
1854) view of the shell, top view. B. Tergum, exterior view. C.
Tergum, internal view. D. Scutum, exterior view. E. Scutum,
internal view. F. Chelonibia testudinaria
(Linnaeus 1758), view of the shell, top view. G. Tergum,
exterior view. H. Tergum,
internal view. I. Scutum, exterior view. J. Scutum, internal view. Scale = 1 mm.
Access on: https://drive.google.com/file/d/1wU3CtyPiiwWivYXkycETGoaa5P5DrrIN/preview
The presence of epibiosis
in swimming crabs may be associated with its free horizontal and vertical
migration through the water column and in non-consolidated substrata, which
turns the epibionts able to spread out in the aquatic environment (KEY Jr. et
al. 2021; ALVES-JÚNIOR et al., 2022).
The occurrence of epibiosis
in other semi terrestrial crustaceans, as Ucides cordatus (Linnaeus, 1763), E. gonagra or
fiddler crabs of the genera Uca Leach,
1814, Minuca Bott, 1953 and Leptuca Bott,
1973 from Brazil are rare or non-existent, due the exposition of epibiont to
air, high temperatures, sun and desiccation, which can lead the epibiont to
death (GILI et al., 1993; ALVES-JÚNIOR et al., 2021).
The occurrence of epibionts in swimming
crabs as C. bocourti
may expand the geographic distribution for these sessile animals. They occupy
different environments, increasing the species' occurrence area and
distribution along estuarine and marine habitats; their larvae have a greater
reach and greater food supply along different habitats (LIMA et al., 2017;
ALVES-JÚNIOR et al., 2021; 2022; KEY Jr. et al. 2021). Another positive feature
of epibiosis is the ability of the sessile epibiont
to escape from predation, for the case of the barnacles and mollusks which are
predated by puffer fish, budion, octopus, sea stars
or other crabs (KEY Jr. et al. 1997; O’CONNOR; NEWMAN, 2001).
As previously observed, the crustacean
carapace acts as a hard substrata in aquatic environments, favoring the
presence and attachment of epibionts, however, the crustacean species have
mechanisms to avoid the adhesion, such as carapace cleaning using oral
appendages and chelipeds or burying in the sediment or galleries (BAUER 1989,
BECKER; WAHL, 1996; COSTA et al., 2010). In studies provided by Abelló et al.
(1990), Lima et al. (2017) and Alves-Júnior et al. (2021; 2022), the crustacean
carapace acts only as a temporary substrata for the fixation of epibionts, due
the process of ecdysis (molting), in which the old carapace is discarded to the
environment carrying the epibionts, which are often destroyed by the action of
waves, currents, sedimentation or predators. In specimens of C. testudinaria
observed herein (Figure 2A), the largest sizes can be related to the high
growth rates promoted by the epibionts, specifically to rapidly reach the
reproductive period and spread of the planktonic larvae to different regions
(due the mobility of swimming crab), before the molting period of the basibiont.
The presence of A. improvisus adhered in branchial
chambers may be considered a parasitism, due to the damage caused by the
fixation of barnacle species and its growth among the gills (Figures 3C-D). The
adhesion in this area may be associated to high level of gasses and the water flux
promoted by the respiration of basibiont, however,
this action damages the gill chamber, reducing the basibiont
breathing rate according to the growth of the barnacle (GANON; WHEATLY, 1992;
POULIN, 2007).
The presence of O. puelchana in the northern region of Brazil (state
of Pará), represents the northernmost record of this species, which has been
reported in Rio Grande do Sul, Paraná, Espírito Santo, Pernambuco and
Paraíba. The bivalve species Sphenia fragilis
was reported in a few localities such as Pará, Rio Grande do Sul, Santa
Catarina and Paraná (RIOS, 2009).
For the barnacle species C. testudinaria
the report from the Amazon province was performed by Farrapeira
(2010) and Alves-Júnior et al. (2022), adhered in a large range of epibionts as
swimming crabs, lobsters, rocks forming barnacle beds, mangroves roots and
piers.
The high risk to native Amazon
biodiversity is the presence in the state of Pará of invasive species A. improvisus,
which was reported as non-native species from Brazilian waters by Farrapeira (2006), in samples performed along the state of
Pernambuco, and in additional reports covering the states of Maranhão to
Pernambuco by Farrapeira (2010), adhered in a wide range of crustacean hosts as prawns and crabs,
especially in the swimming crabs Callinectes
bocourti, C.
danae, C. exasperatus and C.
larvatus (see complete list in Farrapeira, 2010). The species A. improvisus is native to the
Indo-Pacific regions, being transported to Brazil through ship's hulls and/or
ballast water.
The report of the barnacle A. improvisus in
the Amazon province is an alert for the bioinvasion
in the region, being necessary studies for assessing the invasion rate, and the
environmental and trophic damage to the Amazon natural environments.
4 Conclusions
We highlight the
occurrence of new epibionts for the swimming crab C. bocourti, through
adhesion of the barnacles A. improvisus
and C. testudinaria (indicating the occurrence
of A. improvisus in the gill chamber of C. bocourti);
and the mollusks species O. puelchana and S. fragilis.
Additionally, warning about the risk of invasion of the barnacle A. improvisus in the Amazon
province.
CREDIT AUTHORSHIP
CONTRIBUTION STATEMENT
FAAJ, DEGM and BSM conceived the research
ideas and designed the study and writing the manuscript; JAF, AMCK and IHAC
species identification, first draft of this manuscript and revisions along the
main text.
DECLARATION OF INTEREST
The
authors declare that they have no known competing financial interests or
personal relationships that could have appeared to influence this study.
FUNDING SOURCE
No financial contribution was
used for the development of this article.
ACKNOWLEDGEMENTS
The authors would like to thank the Centro Nacional de Pesquisa
e Conservação da Biodiversidade
Marinha do Norte - CEPNOR / ICMBio for the support and laboratory for this study. Also, we
would like to thank the anonymous reviewers for their precious comments in this
manuscript.
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