INTRODUCTION
Symbiotic organisms have abandoned the free-living lifestyle of their ancestors and adapted for living in close association with another, usually larger species, called the host. Different types of symbiosis are defined according to the costs and benefits to the species involved in the relationship (i.e. mutualism, commensalism and parasitism), the degree of interdependence between pairs (obligate versus facultative symbiosis) and the amount of species used by one or both associated organisms (specialists versus generalists). Symbiosis has evolved several times independently among crustaceans (Ross, Reference Ross, Vernberg and Vernberg1983; Bauer, Reference Bauer2004; Baeza et al., Reference Baeza, Bolaños, Hernandez, Lira and López2011).
Caridean shrimps, especially the palaemonids of the subfamily Pontoniinae, and of the families Alpheidae and Hippolytidae, include large amounts of symbiotic species living in association with several invertebrate phyla and with fish species (Bruce, Reference Bruce1976; Bauer, Reference Bauer2004). In most cases, the true nature of the relationship between these shrimp and their hosts is unknown and, consequently, the term ‘association’ has been frequently used instead of symbiosis (Bauer, Reference Bauer2004).
In Brazil, studies focusing on decapod crustaceans in association with cnidarians (e.g. Chace, Reference Chace1969; Johnsson et al., Reference Johnsson, Neves, Franco and Silveira2006; Martinelli Filho et al., Reference Martinelli Filho, Stampar, Morandini and Mossolin2008; Wirtz et al., Reference Wirtz, Melo and Grave2009; Badaro et al., Reference Badaro, Neves, Castro and Johnsson2012) and sponges (e.g. Duarte & Nalesso, Reference Duarte and Nalesso1996; Ribeiro et al., Reference Ribeiro, Omena and Muricy2003; Bezerra & Coelho, Reference Bezerra and Coelho2006; Alves et al., Reference Alves, Carvalho, Barros-Alves and Cobo2012) are very scarce. In the case of an estuarine environment, records of association are even scarcer (e.g. Almeida et al., Reference Almeida, Terossi, Araújo-Silva and Mantelatto2013; Soledade et al., Reference Soledade, Baeza, Boehs, Simões, Santos, Costa and Almeida2013).
The azooxanthellate octocoral Carijoa riisei (Duchassaing & Michelotti, Reference Duchassaing and Michelotti1860) (Cnidaria: Anthozoa: Alcyonacea: Clavulariidae) is commonly found in waters from Florida (USA) to Santa Catarina (Brazil) and throughout the Caribbean region (Bayer, Reference Bayer1961; Silva & Perez, Reference Silva and Perez2002); it has also been recorded in Hawaii (Kahng & Grigg, Reference Kahng and Grigg2005) and has been widely reported in the Indo-West Pacific (Calcinai et al., Reference Calcinai, Bavestrello and Cerrano2004; Concepcion et al., Reference Concepcion, Crepeau, Wagner, Kahng and Toonen2008, Reference Concepcion, Kahng, Crepeau, Franklin, Coles and Toonen2010; Padmakumar et al., Reference Padmakumar, Chandran, Yogesh Kumar and Sornaraj2011). This species is very abundant in north-eastern Brazil, and previous studies have examined their associated fauna, trophic ecology and reproductive biology (see Barbosa et al., Reference Barbosa, Gomes, Bergeron, Santos, Chagas, Freitas and Perez2014 and references therein). It is a colonial species that grows by means of creeping stolons and has a branching structure that provides a suitable habitat for epibionts (Bayer, Reference Bayer1961). It inhabits a wide variety of substrates and water conditions, and is found in turbid and turbulent waters, shaded caves, associated with sponges and hydroids, in estuaries around hard bottoms and on ship hulls (Rees, Reference Rees1972).
The sponge Dragmacidon reticulatum (Ridley & Dendy, Reference Ridley and Dendy1886) (Porifera: Demospongiae: Axinellidae) occurs in the western Atlantic from North Carolina to Brazil (from just off the mouth of the Amazon River to Santa Catarina) (Muricy et al., Reference Muricy, Lopes, Hajdu, Carvalho, Moraes, Klautau, Menegola and Pinheiro2011). Its shape ranges from massive-amorphous to globular or mound-shaped. It occurs exposed or semi-exposed to light, on rock patches, mangrove roots and coral reefs at depths of 0.5–80 m (Alvarez et al., Reference Alvarez, Van Soest and Rützler1998 as Pseudaxinella reticulata; Mothes et al., Reference Mothes, Campos, Lerner and Ferreira-Correia2004; Moraes, Reference Moraes2011).
During the sampling activities of projects aiming to survey caridean shrimp fauna in three estuaries of north-eastern Brazil, portions of colonies of C. riisei and D. reticulatum were collected in two localities along the coast of the state of Bahia (Camamu Bay and Caravelas) and in Ilha de Itamaracá, state of Pernambuco, respectively. The occurrence of caridean shrimps for those hosts has not been previously reported.
MATERIALS AND METHODS
Colonies of Carijoa riisei (Figure 1A, B) were collected on jetties in the shallow subtidal in the estuary of Caravelas River (17°44′39.4″S 39°14′49.7″W), Caravelas, southern Bahia, in August 2007, and from lantern-nets used for farming the oyster Crassostrea mangle Amaral & Simone, Reference Amaral and Simone2014 in Camamu Bay (13°56′04″S 39°01′08″W), central coast of Bahia, between August 2010 and July 2011. The collection of Dragmacidon reticulatum was carried out in the estuary of Paripe River (07°48′38.6″S 34°51′23.0″W), Ilha de Itamaracá, Pernambuco, in September 2008. The sponges (Figures 1C, D) were fouling on hard substrate in the intertidal and shallow subtidal to a depth of approximately 30 cm. In Caravelas and Itamaracá, octocoral colonies and sponges, respectively, were fully wrapped in plastic bags to prevent the escape of possible associated organisms. In Camamu Bay, sampling was conducted onboard of a small boat, during which the permanently submerged lantern-nets were raised and overturned into plastic trays on the boat and carideans were separated. All samplings were carried out in the high-salinity areas of the mixing zone of the estuaries. Salinity was obtained by using an optical refractometer. The collected material was stored in 70% ethanol and later sorted and identified in the laboratory. Voucher shrimp specimens were deposited in the collection of crustaceans at the Universidade Estadual de Santa Cruz (UESC), Ilhéus, Bahia, Brazil.
New invertebrate hosts recorded for some caridean shrimp species. (A, B) Colony of the octocoral Carijoa riisei (Duchassaing & Michelotti, Reference Duchassaing and Michelotti1860) attached to lantern-nets used for farming the oyster Crassostrea mangle Amaral & Simone, Reference Amaral and Simone2014 in Camamu Bay, Bahia, Brazil. (C, D) The demosponge Dragmacidon reticulatum (Ridley & Dendy, Reference Ridley and Dendy1886) attached to a hard surface in the estuary of the Paripe River, Pernambuco, Brazil. Photographs: A, B: Anna Gabrielle La Macchia Pedra; C, D: Alexandre Oliveira Almeida.
RESULTS AND DISCUSSION
On Carijoa riisei, we recorded the alpheids Synalpheus apioceros Coutière, Reference Coutière1909, Synalpheus fritzmuelleri Coutière, Reference Coutière1909, Alpheus formosus Gibbes, Reference Gibbes1850, Alpheus carlae Anker, Reference Anker2012 (Figure 2A, C, F) and the palaemonid Cuapetes americanus (Kingsley, Reference Kingsley1878). The latter two species plus the alpheid Alpheus buckupi Almeida et al., Reference Almeida, Terossi, Araújo-Silva and Mantelatto2013 (Figure 2B, D, E) were recorded in association with Dragmacidon reticulatum.
Alpheid shrimps in association with invertebrate hosts. Alpheus carlae Anker, Reference Anker2012: (A) male and (C) ovigerous female obtained in cavities of the demosponge Dragmacidon reticulatum (Ridley & Dendy, Reference Ridley and Dendy1886); (F) specimen among branches of the octocoral Carijoa riisei (Duchassaing & Michelotti, Reference Duchassaing and Michelotti1860). Alpheus buckupi Almeida et al., Reference Almeida, Terossi, Araújo-Silva and Mantelatto2013: (B) male and (D) ovigerous female obtained in cavities of Dragmacidon reticulatum; (E) specimen in a cavity of D. reticulatum. Photographs: A–E: Alexandre Oliveira Almeida; F: Anna Gabrielle La Macchia Pedra.
Cuapetes americanus was found among the colony branches of Carijoa riisei and there is no information on the precise location on the sponge host (cavities or surface). Cuapetes americanus has been recorded in association with the following invertebrate hosts: the anemones Bartholomea annulata (Le Sueur, Reference Le Sueur1817) (Chace, Reference Chace1972; Mahnken, Reference Mahnken1972; Criales, Reference Criales1984) and Bunodosoma granuliferum (Le Sueur, Reference Le Sueur1817) (Criales, Reference Criales1984) and the crinoid Nemaster grandis Clark, Reference Clark1909 (Criales, Reference Criales1984). Moreover, the species can be found in a wide variety of other types of substrata (e.g. sea grass, dead coral and soft bottoms) (Chace, Reference Chace1972; Carvacho, Reference Carvacho1979; Almeida et al., Reference Almeida, Boehs, Araújo-Silva and Bezerra2012; Santos et al., Reference Santos, Soledade and Almeida2012).
Alpheus buckupi is a scarcely known, recently described coastal species, commonly found in male–female pairs (Almeida et al., Reference Almeida, Terossi, Araújo-Silva and Mantelatto2013). Almeida et al. (Reference Almeida, Terossi, Araújo-Silva and Mantelatto2013) recorded the species in cavities of an unidentified estuarine sponge, in the estuary of the Paripe River, Pernambuco, now recognized as D. reticulatum (Figure 2E). This sponge, although mostly massive, exhibited large cavities near the rock surface, inhabited by male–female pairs or single specimens of Alpheus buckupi. These cavities, however, are rather different from those where eusocial species of Synalpheus Spence Bate, Reference Spence Bate1888 have been recorded, i.e. the aquiferous canals, characterized by sinuous networks of narrow spaces through which the sponge pumps a continuous water current (Duffy, Reference Duffy, Kikuchi, Higashi and Azuma2003). The present record is the first of this species in association with a living organism.
Alpheus carlae is recorded for the first time in association with invertebrate hosts. In Camamu Bay, specimens were found among dense branches of Carijoa riisei, covered with fouling organisms (mostly unidentified algae and sponges) (Figure 2F) and in male–female pairs in cavities like those described for Alpheus buckupi in D. reticulatum. Alpheus carlae is commonly recorded in both marine and estuarine environments in several types of habitats and substrata (including soft and hard bottoms) from the intertidal to shallow subtidal (see Anker, Reference Anker2012; Santos et al., Reference Santos, Soledade and Almeida2012). Alpheus formosus is another species of Alpheus Fabricius, Reference Fabricius1798 commonly found on various types of hard substrata (see Anker et al., Reference Anker, Hurt and Knowlton2008; Santos et al., Reference Santos, Soledade and Almeida2012). However, it has not been recorded in association with Carijoa riisei. Examples of other invertebrate hosts for this species include sponges, bryozoans, living corals and polychaete reefs (see Anker et al., Reference Anker, Hurt and Knowlton2008 and references therein).
Synalpheus apioceros and Synalpheus fritzmuelleri are recorded for the first time in association with Carijoa riisei. The former species was found in large numbers on the portions of the Carijoa riisei colonies sampled in Caravelas, Bahia (N = 62 specimens, including nine ovigerous females). It is considered a monogamous, free-living species, sometimes associated with sponges (see Anker et al., Reference Anker, Pachelle, De Grave and Hultgren2012 and references therein) and several other substrata (see Almeida et al., Reference Almeida, Boehs, Araújo-Silva and Bezerra2012; Anker et al., Reference Anker, Pachelle, De Grave and Hultgren2012). Synalpheus fritzmuelleri is also found in male–female pairs and it lives in various types of substrata (e.g. rock crevices, coral rubble and clumps of Halimeda). The species has also been found in association with several living and non-living substrata (see Anker et al., Reference Anker, Pachelle, De Grave and Hultgren2012 and references therein).
Symbiotic shrimps use their hosts in order to obtain refuge (protection), food (directly or indirectly) and as sites for reproduction (Ross, Reference Ross, Vernberg and Vernberg1983; Bauer, Reference Bauer2004). The very dense branches of Carijoa riisei and the cavities of D. reticulatum described above seem to be a very suitable habitat for shrimp colonization. However, all species recorded in association with those hosts are generalist, i.e. their degree of association is likely to be very low. The collection of dozens of specimens of Synalpheus apioceros on Carijoa riisei branches, including several ovigerous females, may illustrate that this octocoral could provide safe shelter and a reproduction site for the associated shrimp. The only shrimp previously recorded in association with Carijoa riisei in Brazil is the non-indigenous Lysmata vittata (Stimpson, Reference Stimpson1860) (Caridea: Hippolytidae) (Soledade et al., Reference Soledade, Baeza, Boehs, Simões, Santos, Costa and Almeida2013). As far we know, there are no previous records of crustaceans in association with D. reticulatum. Thus, the present records contribute to the knowledge of the ecology and habitat of hosts and the associated shrimp.
ACKNOWLEDGEMENTS
The authors would like to thank the FAPESB (Fundação de Amparo à Pesquisa do Estado da Bahia) (PPP0073/2010) and the Universidade Estadual de Santa Cruz (00220.1100.590) for providing financial support to the project ‘Diversidade de Crustáceos Decápodos Marinhos e Estuarinos do Sul da Bahia, Brasil’. The authors are also indebted to Anna Gabrielle La Macchia Pedra for providing some photographs, to all other colleagues that helped in the field activities and to the anonymous referees for their criticisms that improved the manuscript. The collecting of specimens for the present study complied with the current applicable state and federal laws of Brazil (DIFAP/IBAMA/126/05; permanent license for collection of Zoological Material No. 24408-1 MMA/IBAMA/SISBIO to AOA).
Appendix: List of shrimp material examined in this study
Cuapetes americanus: one male, Pernambuco, Itamaracá, Paripe River near Vila Velha, on Dragmacidon reticulatum, 0–0.3 m water depth, UESC 1441, coll. by A.O. Almeida, R.J.C. Paiva and F.S. Santana, 01 September 2008; five ovigerous females, UESC 1442, same data as lot UESC 1441; seven specimens (not deposited, sex not identified), Bahia, Camamu Bay, Grande Island, on Carijoa riisei from lantern-nets used for farming the oyster Crassostrea mangle, coll. by G.O. Soledade, December 2010.
Alpheus buckupi: eight males, ten females (six ovigerous females), Pernambuco, Itamaracá, Paripe River near Vila Velha, in cavities of Dragmacidon reticulatum, 0–0.3 m water depth, UESC 1367, coll. by A.O. Almeida, R.J.C. Paiva and F.S. Santana, 1 September 2008.
Alpheus carlae: four males, one ovigerous female, one sex not identified, Pernambuco, Itamaracá, Paripe River near Vila Velha, in cavities of Dragmacidon reticulatum, 0–0.3 m water depth, UESC 1450, coll. by A.O. Almeida, R.J.C. Paiva and F.S. Santana, 1 September 2008; four males, one ovigerous female, Bahia, Camamu Bay, Grande Island, on Carijoa riisei from lantern-nets used for farming the oyster Crassostrea mangle, UESC 1539, coll. by G.O. Soledade, 10 April 2010; two males, one female, Bahia, Caravelas, Caravelas River, Station 1, on Carijoa riisei, salinity 36, UESC 1087, coll. by A.O. Almeida and G.B.G. Souza, 28 August 2007.
Alpheus formosus: five males, six ovigerous females, Bahia, Camamu Bay, Grande Island, on Carijoa riisei from lantern-nets used for farming the oyster Crassostrea mangle, UESC 1540, coll. by G.B.G. Souza, G.O. Soledade and T.M. Ourives, 4 August 2010.
Synalpheus apioceros: 53 non-ovigerous specimens, nine ovigerous females, Bahia, Caravelas, Caravelas River, Station 1, on Carijoa riisei, salinity 36, UESC 1088, coll. by A.O. Almeida and G.B.G. Souza, 28 August 2007.
Synalpheus fritzmuelleri: five non-ovigerous specimens, three ovigerous females, Bahia, Camamu Bay, Grande Island, on Carijoa riisei from lantern-nets used for farming the oyster Crassostrea mangle, UESC 1541, coll. by G.O. Soledade, 3 May 2011.
