Abstract
The association of the caridean shrimps Anchistioides antiguensis (Schmitt, 1924) and Typton gnathophylloides Holthuis, 1951 with the sponges Dysidea janiae (Duchassaing & Michelotti, 1864) and Amphimedon viridis Duchassaing & Michelotti, 1864, respectively, is reported for the first time. The material was collected in coral reefs surrounding Santa Barbara Island, Abrolhos Archipelago, Bahia, Brazil. The shrimps occupied different locations inside the sponges. Previous records of associations between these carideans and other hosts were revised and the possible type of association between the shrimps and their hosts is discussed. The occurrence of the sponge A. viridis in the Abrolhos Archipelago is also reported for the first time.
Key words
Caridea; Anchistioididae; Palaemonidae; Demospongiae; symbiosis
Despite being less numerous than free-living species, symbiotic decapod crustaceans are quite common and this lifestyle has evolved independently in several taxa within the group (Bauer, 2004Bauer, R.T. 2004. Remarkable shrimps: adaptations and natural history of the Carideans. Norman, University of Oklahoma Press, 282p.; Baeza et al., 2011Baeza, J.A.; Bolaños, J.A.; Hernandez, J.E.; Lira, C. and López, R. 2011. Monogamy does not last long in Pontonia mexicana, a symbiotic shrimp of the amber pen-shell Pinna carnea from the southeastern Caribbean Sea. Journal of Experimental Marine Biology and Ecology, 407: 41-47.). Among decapods, caridean shrimps have been commonly reported in association with larger invertebrates and even with fishes (e.g., Castro, 1971Castro, P. 1971. The natantian shrimps (Crustacea, Decapoda) associated with invertebrates in Hawaii. Pacific Science, 25: 395-403.; Bruce, 1976Bruce, A.J. 1976. Coral Reef Caridea and “Commensalism”. Micronesica, 12: 83-98.; Knowlton and Keller, 1983Knowlton, N. and Keller, B.D. 1983. A new, sibling species of snapping shrimp associated with the Caribbean sea anemone Bartholomea annulata. Bulletin of Marine Science, 33: 353-362.; Karplus, 1987Karplus, I. 1987. The association between gobiid fishes and burrowing alpheid shrimp. Oceanography and Marine Biology: an annual Review, 25: 507-562.; Bauer, 2004Bauer, R.T. 2004. Remarkable shrimps: adaptations and natural history of the Carideans. Norman, University of Oklahoma Press, 282p.). However, the true kind of symbiosis between shrimps and their hosts remains unknown in most cases and, for this reason, the term “association” has been used to describe such interactions (Bauer, 2004Bauer, R.T. 2004. Remarkable shrimps: adaptations and natural history of the Carideans. Norman, University of Oklahoma Press, 282p.).
Caridean shrimps generally use cavities, cracks or even the inside of sessile organisms as shelters, breeding sites or as refuge from predators. Sponges are one of the main hosts of caridean shrimps (e.g., Bruce, 1976Bruce, A.J. 1976. Coral Reef Caridea and “Commensalism”. Micronesica, 12: 83-98.; Anker et al., 2008Anker, A.; Hurt, C.; Javier, A.J. and Knowlton, N. 2008. Revision of the Alpheus cylindricus Kingsley, 1878 species complex (Crustacea: Decapoda: Alpheidae), with revalidation of A. vanderbilti Boone, 1930. Zootaxa, 1943: 53-68.; Pachelle et al., 2015Pachelle, P.P.G.; Anker, A. and Tavares, M. 2015. New and additional records of the sponge shrimp genus Typton Costa, 1844 (Decapoda: Palaemonidae) from the Brazilian coast. Papéis Avulsos de Zoologia, 55: 317-322.). The type of the associations varies from facultative to obligatory symbiosis (Bruce, 1976Bruce, A.J. 1976. Coral Reef Caridea and “Commensalism”. Micronesica, 12: 83-98.). Some snapping shrimps of the genus SynalpheusSpence Bate, 1888Spence Bate, C. 1888. Report on the Crustacea Macrura collected by the Challenger during the years 1873-76.- Report on the Scientific Results of the Voyage of H.M.S. ”Challenger” during the years 1873-76 24: i-xc, 1-942, Pl., 1-157., for example, are obligatory sponge symbionts (Duffy, 1992Duffy, J.E. 1992. Host use patterns and demography in a guild of tropical sponge-dwelling shrimps. Marine Ecology Progress Series, 90: 127-138.; Macdonald et al., 2006Macdonald, K.S.; Ríos, R. and Duffy, J.E. 2006. Biodiversity, host specificity, and dominance by eusocial species among sponge-dwelling alpheid shrimp on the Belize Barrier Reef. Diversity and Distributions, 12: 165-178.; Ríos and Duffy, 2007Ríos, R. and Duffy, J.E. 2007. A review of the sponge-dwelling snapping shrimp from Carrie Bow Cay, Belize, with description of Zuzalpheus, new genus, and six new species (Crustacea: Decapoda: Alpheidae). Zootaxa, 1602: 3-89.).
During a survey of caridean shrimps carried out in the Abrolhos Archipelago, Bahia, Brazil, Soledade et al. (2015Soledade, G.O.; Fonseca, M.S. and Almeida, A.O. 2015. Shallow water stenopodidean and caridean shrimps from Abrolhos Archipelago, Brazil: new records and updated checklist. Zootaxa, 3905: 52-68. ) registered 11 new shrimp records from this region, with some species collected in association with sponges; however, the identity of the host sponges was not elucidated at that time. Recently, the sponges were identified and we verified that some of them were never previously registered in association with two caridean shrimps that occur in the area. Thus, the objective of this study is to report these new associations and to provide a new record of one of the sponge hosts in the Abrolhos Archipelago. To infer about the kind of association between shrimps and sponges we reviewed previous records of associations of species of shrimp with different hosts, and also took into consideration the location of the shrimps inside the sponges.
The material analyzed was obtained in coral reefs surrounding Santa Barbara Island (17°57’49”S 38°41’53”W). The sponges were collected between 22th July and 4th August 2013. Once collected, the specimens were placed in plastic bags (in situ) to prevent escape of associated organisms.
In the laboratory, the sponges were carefully inspected, and the associated fauna was removed, anesthetized on ice, and fixed in ethanol 70%. The associated shrimp were identified and deposited in the Crustacean Collection of the Museu de Oceanografia of Universidade Federal de Pernambuco, Recife, Brazil (MOUFPE). The sponges were deposited in the Coleção de Porifera of Universidade Federal de Pernambuco, Recife, Pernambuco, Brazil [Amphimedon viridisDuchassaing & Michelotti, 1864Duchassaing, P. and Michelotti, G. 1864. Spongiaires de la Mer Caraibe. Natuurkundige verhandelingen van de Hollandsche maatschappij der wetenschappen te Haarlem, 21: 1-124., UFPEPOR 1890, Fig. 1A ; Dysidea janiae (Duchassaing & Michelotti, 1864), UFPEPOR 1892, Fig. 1B ].
Family Anchistioididae Borradaile, 1915Borradaile, L.A. 1915. Notes on Carides. The Annals and Magazine of Natural History, 15: 205-213.
Anchistioides antiguensis ( Schmitt, 1924Schmitt, W.L. 1924. Report on the Macrura, Anomura and Stomatopoda collected by the Barbados-Antigua Expedition from the University of Iowa in 1918. University of Iowa Studies in Natural History, 10: 65-99, pls. 1-5. )
External appearance and color pattern of the two species of sponges associated with caridean shrimps from Abrolhos Archipelago, Bahia, northeastern Brazil. (A) Amphimedon viridis Duchassaing & Michelotti, 1864; (B) Dysidea janiae (Duchassaing & Michelotti, 1864). Scale bars = 1 cm.
Material examined. 4 males, 11 females (1 ovigerous); MOUFPE 18102; Santa Barbara Island (17°57’28”S 38°42’19”W); 3 Nov. 2013; 9 m; in the sponge Dysidea janiae; coll. R.M.C. Barbosa and L.M. Fernandes.
Remarks. Specimens of A. antiguensis were found inhabiting the host’s osculae. Only one specimen was found inside each sponge tube and none was observed on the surface. This species occurs from Bermuda to Espírito Santo, Brazil (De Grave and Anker, 2017De Grave, S. and Anker, A. 2017. An annotated checklist of marine caridean and stenopodidean shrimps (Malacostraca: Decapoda) of the Caribbean coast of Panama. Nauplius, 25: e2017015.) from the intertidal to 118 m (Williams, 1984Williams, A.B. 1984. Shrimps, Lobsters, and Crabs of the Atlantic Coast of the Eastern United States, Maine to Florida. Washington, Smithsonian Institution Press, 550p.). Previous reports of this species on the coast of Brazil did not provide information about its ecological relationships (Chace, 1972; Coelho and Ramos, 1972Coelho, P.A. and Ramos, M.A. 1972. A constituição e a distribuição da fauna de decápodos do litoral leste da América do Sul entre as latitudes 5° N e 39° S. Trabalhos Oceanográficos da Universidade Federal de Pernambuco, 13: 133-236.; Cardoso, 2006Cardoso, I. 2006. Caridea (Crustacea, Decapoda) collected on the Brazilian (13º/22º) continental shelf and slope. Zootaxa, 1364: 1-44.; Coelho et al., 2006Coelho, P.A.; Almeida, A.O.; Souza-Filho, J.F.; Bezerra, L.E.A. and Giraldes, B.W. 2006. Diversity and distribution of the marine and estuarine shrimps (Dendobranchiata, Stenopodidea and Caridea) from North and Northeast Brazil. Zootaxa, 1221: 41-62.; Soledade et al., 2015Soledade, G.O.; Fonseca, M.S. and Almeida, A.O. 2015. Shallow water stenopodidean and caridean shrimps from Abrolhos Archipelago, Brazil: new records and updated checklist. Zootaxa, 3905: 52-68. ). Specimens of A. antiguensis have been observed living inside the sponges Mycale (Arenochalina) laxissima (Duchassaing & Michelotti, 1864Duchassaing, P. and Michelotti, G. 1864. Spongiaires de la Mer Caraibe. Natuurkundige verhandelingen van de Hollandsche maatschappij der wetenschappen te Haarlem, 21: 1-124.) and Niphates erecta (Duchassaing & Michelotti, 1864Duchassaing, P. and Michelotti, G. 1864. Spongiaires de la Mer Caraibe. Natuurkundige verhandelingen van de Hollandsche maatschappij der wetenschappen te Haarlem, 21: 1-124.) in Bocas del Toro, Panama, and it has been considered a facultative sponge associated species (De Grave and Anker, 2017De Grave, S. and Anker, A. 2017. An annotated checklist of marine caridean and stenopodidean shrimps (Malacostraca: Decapoda) of the Caribbean coast of Panama. Nauplius, 25: e2017015.). However, considering that the specimens of A. antiguensis were found within the host’s osculae and the fact that each tube contained one organism, A. antiguensis and D. janiae may have a true relationship. Anchistioides antiguensis may use the interior of D. janiae as refuge or even site for reproduction, given the presence of individuals of both sexes, as well as one ovigerous female in the examined single host.
Family Palaemonidae Rafinesque, 1815Rafinesque, C.S. 1815. Analyse de la Natures ou Tableau de l’Univers et dês corps organisés. Palerme, pp. 1-224.
Typton gnathophylloides Holthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchidae and Pontoniinae. Occasional Papers of the Allan Hancock Foundation, 11: 1-332.
Material examined. 1 male, 1 ovigerous female; (MOUFPE 18104); Santa Barbara Island (17°57’49”S 38°41’53”W); 3 Nov. 2013; shallow tide pool, in the sponge Amphimedon viridis; coll. G.O. Soledade.
Remarks. Specimens of T. gnathophylloides inhabited the channels of the aquiferous system of A. viridis. Sponges of the genus AmphimedonDuchassaing & Michelotti, 1864Duchassaing, P. and Michelotti, G. 1864. Spongiaires de la Mer Caraibe. Natuurkundige verhandelingen van de Hollandsche maatschappij der wetenschappen te Haarlem, 21: 1-124. have a considerable level of toxicity, which can limit the presence of associated organisms within (Albrisio et al., 1995Albrizio, S.; Ciminiello, P.; Fattorusso, E.; Magno, S. and Pawlik, J.R. 1995. Amphitoxin, a new high molecular weight antifeedant pyridinium salt from the Caribbean sponge Amphimedon compressa. Journal of Natural Products, 58: 647-652.; Berlink et al., 1996Berlink, R.G.S.; Ogawa, C.A.; Almeida, A.M.P.; Sanchez, M.A.A.; Malpezzi, E.L.A.; Costa, L.V.; Hadju, E. and Freitas, J.C. 1996. Chemical and pharmacological characterization of halitoxin from Amphimedon viridis (Porifera) from the southeastern Brazilian coast. Comparative Biochemistry and Physiology, 115: 155-163.). Evidences of toxicity have been verified in A. viridis (Campos et al., 2012Campos, C.J.A.; Migotto, A.E.; Pinheiro, U. and Marques, A.C. 2012. Sponges as substrata and early life history of the tubulariid Zyzzyzus warreni (Cnidaria: Hydrozoa) in the São Sebastião Channel, Brazil. Marine Biology Research, 8: 573-583.), which may indicate a natural sponge defense against symbionts. The location of the two specimens of T. gnathophylloides inside A. viridis suggests that shrimp can tolerate the chemical defense of the sponge. Species of TyptonCosta, 1844Costa, O.G. 1844. Su due nuovi generi di Crostacei decapodi macrouri. Annali delle Accademia degli Aspiranti Naturalisti, Napoli, 2: 285-292. are commonly recognized as sponge associated (Holthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchidae and Pontoniinae. Occasional Papers of the Allan Hancock Foundation, 11: 1-332.) and evidence of parasitism in these shrimps based on tissue consumption of host sponges by symbiotic shrimp have already been reported in Typton carneus Holthuis, 1951, Typton distinctus Chace, 1972 and Typton spongicola Costa, 1844 (Duris et al., 2011Duris, Z.; Horká, I.; Juracka, P.J.; Petrusek, A. and Sandford, F. 2011. These squatters are not innocent: the evidence of parasitism in sponge-inhabiting shrimps. PLoS ONE, 6: e21987. ); however, little information is known regarding T. gnathophylloides. The species has been reported from the southeastern coast of Brazil (Nalesso et al., 1995Nalesso, R.C.; Duarte, L.F.L.; Pierozzi, I. Jr. and Enumo, E.F. 1995. Tube epifauna of the polychaete Phyllochaetopterus socialis Claparède. Estuarine, Coastal and Shelf Science, 41: 91-100.; Duarte and Nalesso, 1996Duarte, L.F.L. and Nalesso, R.C. 1996. The sponge Zygomycale parishii (Bowerbank) and its endobiotic fauna. Estuarine, Coastal and Shelf Science, 42: 139-151.). However, this material was recently reanalyzed (in part) and attributed to a new species (Typton fapespaeAlmeida, Anker and Mantelatto, 2014Almeida, A.O.; Anker, A. and Mantelatto, F.L. 2014. A new snapping species of the shrimp genus Typton Costa, 1844 (Decapoda: Palaemonidae) from the coast of São Paulo, southeastern Brazil. Zootaxa, 3835: 110-120. ). Typton gnathophylloides has been previously reported for the Canary Islands (Pérez Sánchez and Moreno Batet, 1991Pérez Sánchez, J.M. and Moreno Batet, E. 1991. Invertebrados marinos de Canarias. Ediciones del Abildo Insular de Grand Canaria. Las Palmas de Gran Canaria, 1-335. ISBN 84-86127-62-9.; González Pérez et al., 1995González Pérez, J.A.; Santana, J.I.; Jimenez S. and Pérez-Barroso, F.I. 1995. Primera cita de Nematocarcinus gracilipes y Centroscymus crytacanthus para Canarias. Boletim do Instituto Oceanográfico, 9: 257-259.) but, according to d’Udekem d’Acoz (1999Udekem d’Acoz, C.d’. 1999. Inventaire et distribution des crustacés decápodes de l’Atlantique nord-oriental, de la Méditerranée et des eaux continentales adjacentes au nord de 25ºN. Patrimoines naturels (M.N.H.N./S.P.N.), 40: 383p.) these records need confirmation. Besides the type material, two specimens from Dry Tortugas, Florida (Holthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchidae and Pontoniinae. Occasional Papers of the Allan Hancock Foundation, 11: 1-332.), the two specimens reported here (previously cited in Soledade et al., 2015Soledade, G.O.; Fonseca, M.S. and Almeida, A.O. 2015. Shallow water stenopodidean and caridean shrimps from Abrolhos Archipelago, Brazil: new records and updated checklist. Zootaxa, 3905: 52-68. ) are the only known specimens of T. gnathophylloides. It is important to highlight that A. viridis is the first host of T. gnathophylloides identified to species level. Amphimedon viridis has been commonly reported along the Brazilian coast, but this is the first record of the species in the Abrolhos archipelago (Hajdu et al., 2011Hajdu, E.; Peixinho, S. and Fernandez, J. 2011. Esponjas marinhas da Bahia: Guia de campo e laboratório. Rio de Janeiro, Museu Nacional, 276p. [Série Livros 45].).
In summary, new records of association between carideans and sponges are provided. It is important to emphasize the taxonomic accuracy of the present reports regarding the identifications of both associated organisms. This reinforces the importance of joint work of taxonomists from different zoological groups, which promotes a greater refinement of results related to the documentation of association records.
Acknowledgements
We thank ICMbio (Instituto Chico Mendes de Conservação da Biodiversidade), Conservation International do Brasil and the Brazilian Navy for their support in the field logistics. To Letícia M. Fernandes, Renata M.C. Barbosa, Irlanda S. Matos, Egno S. Barbosa and Edson Alves for their support in the field. GOS thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the provision of a PhD scholarship. The species collection for this study complied with current applicable state and federal laws of Brazil (license for collection of Zoological Material No. 39642-1 MMA/ICMBio/SISBIO for AOA). AOA and USP thank Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq for a Research Scholarship (Process Numbers 305939/2015-7 and 454908/2014-8, respectively).
References
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- Almeida, A.O.; Anker, A. and Mantelatto, F.L. 2014. A new snapping species of the shrimp genus Typton Costa, 1844 (Decapoda: Palaemonidae) from the coast of São Paulo, southeastern Brazil. Zootaxa, 3835: 110-120.
- Anker, A.; Hurt, C.; Javier, A.J. and Knowlton, N. 2008. Revision of the Alpheus cylindricus Kingsley, 1878 species complex (Crustacea: Decapoda: Alpheidae), with revalidation of A. vanderbilti Boone, 1930. Zootaxa, 1943: 53-68.
- Baeza, J.A.; Bolaños, J.A.; Hernandez, J.E.; Lira, C. and López, R. 2011. Monogamy does not last long in Pontonia mexicana, a symbiotic shrimp of the amber pen-shell Pinna carnea from the southeastern Caribbean Sea. Journal of Experimental Marine Biology and Ecology, 407: 41-47.
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- Campos, C.J.A.; Migotto, A.E.; Pinheiro, U. and Marques, A.C. 2012. Sponges as substrata and early life history of the tubulariid Zyzzyzus warreni (Cnidaria: Hydrozoa) in the São Sebastião Channel, Brazil. Marine Biology Research, 8: 573-583.
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Publication Dates
-
Publication in this collection
2017
History
-
Received
05 June 2017 -
Accepted
08 Aug 2017