The first finding of Ostrea cf. puelchana (Bivalvia) living as epibiont on Callinectes exasperates (Decapoda)/Primeiro registro de Ostrea cf. puelchana (Bivalvia) vivendo como epibionte sobre Callinectes exasperates (Decapoda).
Epibiosis is a spatially close, facultative association between two living organisms in which the epibiont lives attached to the surface of a basibiont used as a substrate for support during the sessile period of the life cycle (Harder, 2009; Fernandez-Leborans, 2010; Romero, Brezina, Hernandez, Casadio, & Bremec, 2013; Azevedo, Brandao, Abdallah, & Silva, 2014). This non-symbiotic relationship can provide a variety of potential benefits or negative impacts for the epibiont and/or basibiont (Wahl, 1989; Wahl & Mark, 1999; Fernandez-Leborans, 2010; Machado, Sanches, Fortuna, & Costa, 2013). Unlike what occurs with symbiosis, species-specific, obligate epibionts are rare and the majority of epibiotic associations are therefore classified as facultative (Wahl & Mark, 1999).
Many groups of marine invertebrates (e.g., annelids, bryozoans, cnidarians, crustaceans, mollusks, polychaetes, poriferans etc.) are recognized as epizoans on a wide variety of other mobile and sessile invertebrates, mainly crustaceans, xiphosurans and mollusks (see Mori & Manconi, 1990; Gili, Abello, & Villanueva, 1993; Key, Jeffries, Voris, & Yang, 1996; Villegas, Stotz, & Laudien, 2005; Fernandez-Leborans, 2010; Farrapeira & Calado, 2010; Lima, Queiroz, Bravo de Laguna, & Mioso, 2014; Lima, Queiroz, Oliveira, Christoffersen, & Guimaraes, 2016; Machado et al., 2013; Romero et al., 2013).
Bivalves are known to have a multitude of lifestyles: free-living (Morton, 1973; Lutzen & Nielsen, 2005), commensal (Goto, Hamamura, & Kato, 2007), mutualist (Mokady, Loya, & Lazar, 1998), epizoic (Villegas et al., 2005) or parasitic (Malard, 1903). Members of the family Ostreidae Rafinesque, 1815 are among the sessile marine invertebrates that live on a variety of abiogenic and biogenic substrates (Slack-Smith, 1998; Fernandez-Leborans, 2010). These bivalves have been reported specifically as epizoans on mangrove roots, gorgonians, corals (Slack-Smith, 1998), decapod crustaceans (Fernandez-Leborans, 2010) and other mollusks (Cope, 1968; Eschweile & Buschbaum, 2011; Zell, Beckmann, & Stinnesbeck, 2014).
In February 2016, a specimen of Ostrea cf puelchana (in vivo) was found cemented to the carapace of a crab of the species Callinectes exasperatus (Gerstaecker, 1856). The brachyuran was captured during a study on molluscan and crustacean fauna in the estuary of the Paraiba River, in the state of Parafba (northeastern Brazil). Ostrea cf. puelchana inhabits subtidal waters attached to a variety of hard substrates (Rios, 2009). Callinectes exasperatus is a euryhaline crab that inhabits intertidal and shallow subtidal zones to dephts of about 8 m, including estuaries near river mouths and mangroves (Melo, 1996; Carvalho & Couto, 2011), as a deposit feeder or preying on other invertebrates (Carvalho & Couto, 2011). Both have widespread distribution throughout the Atlantic coast of South America. However, there is no previous mention of epibiosis between the two species in the literature. Thus, the epibiosis of the oyster Ostrea cf. puelchana on the crab C. exasperates is recorded for the first time herein and the probable consequences of this relationship are discussed.
Material and methods
This study was conducted in February 16th to 18th, 2016 on a beach located on the property denominated Treze de Maio and Costinha de Santo Antonio (06[degrees]58'17.59"S, 34[degrees]51'47.19"W), which is within the area of influence of the estuary of the Parafba River in the municipality of Lucena, state of Parafba, northeastern Brazil. The surrounding coastal environment is characterized by the presence of mangrove forests (Sassi, 1991) in non-urbanized areas and a large sand bank, which is exposed at low tide. The area is under the influence of the Atlantic Ocean (Medeiros, Hepp, Patricio, & Molozzi, 2016) and main tributaries on the right (Sanhaua, Tambia and Mandacaru Rivers) and left (Paroeira, Tiririm, Ribeira and Guia Rivers) margins of the estuary, which transport sediment and nutrients as well as domestic and industrial sewage (Sassi, 1991; Marcelino, Sassi, Cordeiro, & Costa, 2005). The area is not under the direct influence of the impact of the waves and has a beach with flat to slightly steep areas, with predominantly sandy-muddy and detritic bottoms (Sassi, 1991) (Figure 1).
Sampling and treatment of samples
A total of 21 crabs were captured using traps known locally as "manzua" [see Carvalho and Couto (2011)]. Five traps were linearly installed on the bed of a small affluent at a depth of approximately 2 m in the mangrove area at low tide. Each trap contained 100 g of bait consisting of a mixture of beef (90%) and fish (10%). The traps were examined every 24 hours for three days and captured specimens were removed. An oyster found cemented to the carapace of a crab was photographed immediately after collection (Figure 2). All specimens, including the basibiont were placed in plastic recipients with sea water, stored in a cold container and then fixed in 70% ethanol for subsequent identification. In the laboratory, the oyster was removed from the crab carapace. Crab is housed in the Paulo Young Invertebrate Collection, Department of Systematics and Ecology of the Universidade Federal da Paraiba (UFPB CRUSTACEA 6165 $), Joao Pessoa, Parafba, Brazil and oyster is deposited in the mollusc collection, Museu de Zoologia, Universidade de Sao Paulo (MZSP 131977), Sao Paulo, Brazil.
The caparace of Callinectes exasperates served as a favorable, sufficiently large, firm substrate for the opportunistic occupation of Ostrea cf. puelchana. The carapace is heavily armored, dorsoventrally flattened and relatively rough, composed of numerous small tubercles that offer favorable conditions as a biogenic surface for the settlement and growth of the oyster. The specimen of O. cf. puelchana had a wet weight of 0.81 g and a shell length of 27 mm, with the shell occupying an area of 4.3 [mm.sup.2]. The specimen of C. exasperates had a wet weight of 53.5 g and a carapace width of 104 mm. The epibiont covered about 20% of the dorsal surface of the carapace (Figure 2). The oyster was closely attached to the left side, covering 60 to 70% of the epibranchial surface and about 90% of the mesobranchial and metabranchial regions. The antero-ventral and postero-ventral parts of the left valve of the oyster were completely cemented to the carapace of the crab, while the antero-dorsal and postero-dorsal parts of the valve (except part of the submedian margins) were not cemented, and only loosely covered the carapace.
Information on oysters as epibionts on recent mobile marine invertebrates is scarce (Winter & Masunari, 2006; Eschweile & Buschbaum, 2011). However, fossil records seem not to be uncommon (Cope, 1968; Bishop, 1981; Tshudy & Feldmann, 1988; Fernandez-Leborans, 2010; Paul & Simms, 2012; Zell et al., 2014). Such records include Liostrea roemeri (Quenstedt, 1843) attached to the shells of ammonites in the Jurassic to Cretaceous periods in northeastern Mexico (Zell et al., 2014) and Pycnodonta vesiculosa (Sowerby, 1823) living on the lobster Hoploparia stokesi (Weller, 1903) in the Cretaceous period in Antarctica (Tshudy & Feldmann, 1988). This is the first record of epibiosis between bivalves of the genus Ostrea Linnaeus, 1758 and crabs of the genus Callinectes Stimpson, 1860.
The case of epibiosis found here in the current stage of the species is obviously favorable to the epibiont and also seems to be advantageous to the basibiont. The considerable capacity for movement of the basibiont may be advantageous to the epibiont with regard to the avoidance of predators and the obtainment of nutrients. Oysters are predated by a number of marine invertebrates, such as platyhelminthes (Littlewood & Marsbe, 1990; O'connor & Newman, 2001), crustaceans (Elner & Lavoie, 1983; Eggleston, 1990), polychaetes (Sabry & Magalhaes, 2005; Radashevsky, Lana, & Nalesso, 2006) and other mollusks (Carriker, 1955; Herbert, Dietl, Fortunato, Simone, & Sliko, 2009). Studies suggest that an epizoitic lifestyle is beneficial by hindering the approach of sedentary predators due to the movements or defensive shield of certain basibionts (Wahl, 1989; Abello, Villanueva, & Gili, 1990). Epibiont invertebrates (e.g., hydroids, polychaetes and barnacles) on decapods may also benefit from resuspended debris (Williams & Moyse, 1988) or the diet of the host (Bowers, 1968; Abello et al., 1990).
Conversely, settling on a crustacean could be a poor option. The carapace of Callinectes exasperates is an available hard substrate for the attachment of Ostrea cf. puelchana mainly in a predominantly soft sediment environment. However, some aspects of the biology of crustaceans and the ecology of C. exasperates may negatively affect an epibiont. Ecdisys (molting) makes the carapace of crustaceans only a semi-permanent substrate for epizoans (Ross, 1983; Wahl, 1989; Gili et al., 1993). As a result, there are few reports of epibiosis between bivalves and crustaceans (Gili et al., 1993; Villegas et al., 2005). Ostrea cf. puelchana may also be negatively affected by stressful environmental conditions due to the burrowing activity of C. exasperates (Abello et al., 1990; Fernandez-Leborans, 2010).
According to Wahl and Mark (1999), epibiosis may negatively affect basibionts by increasing weight and friction, decreasing flexibility, shading basibionts from light and access to dissolved nutrients or inflicting 'shared doom'. On the other hand, basibionts may benefit from the presence of epibionts due to effects such as optical and chemical camouflage, reduced friction, protection against desiccation and harmful irradiation or associational defense. The continued growth of an epibiont oyster to adulthood on the carapace of Callinectes exasperates could adversely affect the buoyancy and locomotion of the latter, making the crab more vulnerable to predation. A similar harmful pattern has been seen involving the oyster Crassostrea gigas (Thunberg, 1793), which impaired the mobility of the gastropod Littorina littorea (Linnaeus, 1758). Villegas et al. (2005) report that the epibiont mussel Semimytilus algosus (Gould, 1850) is apparently unfavorable to the basibiont Emerita analoga (Stimpson, 1857) by increasing its mass and damaging the surface of the carapace as well as reducing the growth and buoyancy of this sand crab. However, the specimen of Ostrea cf. puelchana in the juvenile stage described in the present study likely did not have a negative effect on the basibiont C. exasperates as the oyster (weight: 0.81 g) was attached to only about 20% of the dorsal carapace and did not overlap any appendage or other articulated structure on the carapace and therefore probably did not impair movement, flexibility or the function of organs in the basibiont. The same pattern has been reported in other cases of epibiosis among marine invertebrates (Overstreet, 1983; Wahl, 1989; Cadee, 1991; Wahl & Mark, 1999; Fernandez-Leborans, 2010). Furthermore, no injuries were found on the carapace of the crab after the removal of the oyster. Another important point is that the shell of this ostreid may offer additional protection from potential predators of the crab. There are many examples of epibionts that may discourage predation on basibionts (Feifarek, 1987; Laudien & Wahl, 1999; Marin & Belluga, 2005).
The specimen of Ostrea cf. puelchana was able to grow on the carapace of Callinectes exasperates enough to reach about half its adult size (27 mm in shell length) without being affected by the process of ecdysis. Thus, the oyster may has been between three and four months of age (based on growth rate of other ostreids, such as Crassostrea gigas) (Acosta Ruiz & Gutierrez Wing, 1996) and the basibiont was an adult crab in terminal an ecdysis, thereby providing a rather stable substrate for the epibiont. The carapace width of the crab studied herein was within the estimated size (61 to 160 mm) for first gonadal maturation, based on data from congeners (Tagatz, 1968; Branco & Masunari, 1992; Branco & Lunardon-Branco, 1993; Severino-Rodrigues, Musiello-Fernandes, Moura, Branco, & Caneo, 2013; Sumer, Teksam, Karatas, Beyhan, & Aydin, 2013), which live between 2.3 and 4 years (Tagatz, 1968; Williams, 1974; Ferreira & D'incao, 2008; Keunecke, D'Incao, Moreira, Silva, & Verani, 2008). However, biological data on C. exasperates are practically non existent, likely due to low abundance of the species. Furthermore, oysters are filter feeding bivalves adapted to a sessile epifaunal lifestyle in marine or brackish waters and are dependent on hard substrates (Amaral & Simone, 2014).
This study expands knowledge on the diversity of epibiosis among marine invertebrates through the record of the bivalve Ostrea cf. puelchana attached to the crab Callinectes exasperates on the coast of Brazil. The case epibiosis found apparently not adversely affected both epibiont and basibiont. However, future studies on the biology and life cycle of the crab and oyster will be decisive to the determination of factors that are either favorable or unfavorable.
The authors would like to thank MSc. Karlla Morgana (Real Consultoria e Solugoes LTDA) for logistical support and carrying out the fieldwork in the estuary of the Parafba River; Mr. Genilson C. Silva for assisting with the fieldwork and photographing the case of epibiosis; Dr. Douglas F. R. Alves (Crustacean Laboratory, Universidade Federal do Sergipe, Brazil) for assistance with the literature and the anonymous reviewers for critically reviewing the manuscript; Vinicius Queiroz thanks FAPESP (Proc. 2015/21460-5) for financial support.
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Received on September 28, 2016.
Accepted on February 3, 2017.
Silvio Felipe Barbosa Lima (1) *, Ruda Amorim Lucena (2), Vinicius Queiroz (3), Carmen Regina Parisotto Guimaraes (4) and Andre Breves (5)
(1) Universidade Federal de Campina Grande, Centro de Formacao de Professores, Unidade Academica de Ciencias Exatas e da Natureza, Rua Sergio Moreira de Figueiredo, s/n, Bairro Casas Populares, 58900-000, Cajazeiras, Paralba, Brazil. (2) Laboratorio de Invertebrados Paulo Young, Departamento de Sistematica e Ecologia, Universidade Federal da Paralba, Joao Pessoa, Paralba, Brazil. (3) Departamento de Fisiologia Geral, Instituto de Biociencias, Universidade de Sao Paulo, Sao Paulo, Sao Paulo, Brazil. (4) Laboratorio de Bentos Costeiro, Departamento de Biologia, Centro de Ciencias Biologicas e da Saude, Universidade Federal de Sergipe, Sao Cristovao, Sergipe, Brazil. (5) Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Rio de Janeiro, Brazil. * Author for correspondence. E-mail: email@example.com
Caption: Figure 1. (A) Map of coast of Brazil and state of Paraiba (red); (B) Photo of estuary of Paraiba River indicating sampling location (upper region of property denominated Treze de Maio and Costinha de Santo Antonio) (Google Earth); (C) Photo of stretch of beach showing affluent in which traps were installed (yellow lozenge) (Google Earth).
Caption: Figure 2. (A) Specimen of Ostrea cf puelchana cemented to carapace of Callinectes exasperates; (B) Detail of right valve of O. cf. puelchana; (C) Internal view of right valve of O. cf. puelchana showing denticles on hinge. Scale bars: A. 2 cm, B. 1 cm, C. 5 mm.
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|Title Annotation:||texto en ingles|
|Author:||Lima, Silvio Felipe Barbosa; Lucena, Ruda Amorim; Queiroz, Vinicius; Guimaraes, Carmen Regina Pariso|
|Publication:||Acta Scientiarum. Biological Sciences (UEM)|
|Date:||Jan 1, 2017|
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