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On two species of Periclimenaeus Borradaile, 1915 (Caridea: Palaemonidae) from colonial tunicates in the southwestern Atlantic

Abstract

Two species of the palaemonid genus Periclimenaeus Borradaile, 1915, P. ascidiarum Holthuis, 1951 and P. maxillulidens (Schmitt, 1936), are reported from the offshore Escalvada Island, Espírito Santo, Brazil. The location represents a new southernmost record for these species in the western Atlantic. Both species were found inside an undescribed tunicate species of Diplosoma, dwelling inside the circulatory channels, among the zooid clusters. Although P. ascidiarum is known to occur in tunicates, the finding of the rare P. maxillulidens inside an ascidian host represents the first record of this association. Illustrations for both species and a taxonomic key for the southwestern Atlantic Periclimenaeus are provided based on the present material and literature records.

Keywords
Ascidiacea; biodiversity; caridean shrimps; ecology; South Atlantic

INTRODUCTION

Currently composed of 83 species worldwide, PericlimenaeusBorradaile, 1915Borradaile, L.A. 1915. Notes on Carides. The Annals and Magazine of Natural History , Series 8, 15: 205-213. is a specious genus within the Palaemonidae (Bruce, 2011Bruce, A.J. 2011. Periclimenaeus pulitzerfinali sp. nov. (Crustacea: Decapoda: Palaemonidae), a new pontoniine shrimp from East Africa. The Beagle, Records of the Museums and Art Galleries of the Northern Territory, 27: 113-121.; 2012aBruce, A.J. 2012a. Periclimenaeus parkeri sp. nov. (Crustacea: Decapoda: Pontoniinae) from the Kimberley, Western Australia. Cahiers de Biologie Marine, 53: 289-298.; 2012bBruce, A.J. 2012b. Notes on some Indo-Pacific Pontoniinae, 51. Periclimenaeus quadridentatus (Rathbun, 1906) and P. crassipes (Calman, 1939) (Decapoda, Pontoniinae), with the designation of P. calmani and P. serenei spp. nov. Crustaceana, 85: 513-531.; 2012cBruce, A.J. 2012c. Periclimenaeus dactylodon sp. nov. (Decapoda: Pontoniinae), from Heron Island, Queensland, Australia. Zootaxa, 3436: 51-60.; 2013Bruce, A.J. 2013. Notes on some Indo-Pacific Pontoniinae, LIII. Periclimenaeus species from the Hawaiian region. Crustaceana, 86: 1605-1622.; 2014aBruce, A.J. 2014a. Periclimenaeus species (Crustacea: Decapoda: Pontoniinae) from Hawaii. Zootaxa, 3754: 461-472.; 2014bBruce, A.J. 2014b. Periclimenaeus colemani sp. nov. (Crustacea; Palaemonidae; Pontoniinae) from Heron island, Queensland.Zootaxa , 3774: 258-264.; 2014cBruce, A.J. 2014c. Periclimenaeus denticulodigitus sp. nov. (Crustacea: Decapoda: Palaemonidae: Pontoniinae), from Heron Island, Queensland, Australia. Zootaxa , 3753: 71-78.; 2014dBruce, A.J. 2014d. Notes on some Indo-Pacific Pontoniinae, LIV. New Periclimenaeus species (Decapoda, Pontoniinae), from Cartier Island Reef, Western Australia. Crustaceana, 87: 64-82.; De Grave and Fransen, 2011De Grave, S. and Fransen, C.H.J.M. 2011. Carideorum catalogus: the recent species of the dendrobranchiate, stenopodidean, procarididean and caridean shrimps (Crustacea: Decapoda). Zoologische Mededelingen, 89: 195-589.; Ďuriš et al., 2011Ďuriš, Z.; Horká, I. and Al-Horani, F. 2011. Periclimenaeus echinimanus sp. nov. (Crustacea: Decapoda: Pontoniinae), a new species from the Gulf of Aqaba, Red Sea. Zootaxa , 2983: 57-68.; Ramos-Tafur and Lemaitre, 2017Ramos-Tafur, G.E and Lemaitre, R. 2017. A new species of shrimp of the genus Periclimenaeus Borradaile, 1915 (Decapoda: Caridea: Palaemonidae) from the southeastern Gulf of Mexico, including a key to the western Atlantic species of the genus. Zootaxa , 4303: 491-508.). Among the Atlantic palaemonids, the genus is readily recognized by the well-developed, highly asymmetrical second pereopods with snapping mechanism on the major chela (molar process on the dactylus and opposing fossa on the fixed finger), presence of an antennal tooth, absence of both hepatic and epigastric teeth, supraorbital tooth usually absent (when present, small), and a well-developed scaphocerite (Bruce, 1995Bruce, A.J. 1995. A synopsis of the Indo-West Pacific genera of the Pontoniinae (Crustacea: Decapoda: Pontoniinae). Theses Zoologicae, 25: 1-172.).

Periclimenaeus species are typically found in cryptic habitats, dwelling inside sponge and ascidian hosts, and are most abundant in shallow tropical waters (Bruce, 2013Bruce, A.J. 2013. Notes on some Indo-Pacific Pontoniinae, LIII. Periclimenaeus species from the Hawaiian region. Crustaceana, 86: 1605-1622.). Out of the 14 species known from the western Atlantic, eight are reported as sponge-associated, one as ascidian-associated and the remaining five species have no host records (see Tab. 1).

Table 1.
List of hosts for the western Atlantic PericlimenaeusBorradaile, 1915Borradaile, L.A. 1915. Notes on Carides. The Annals and Magazine of Natural History , Series 8, 15: 205-213. based on literature records. (?) - Host unknown; * - Species previously reported from Brazil

In Brazil, the genus was hitherto represented by only seven species: Periclimenaeus ascidiarumHolthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332., Periclimenaeus atlanticus (Rathbun, 1901Rathbun, M.J. 1901. Investigations of the Aquatic Resources and Fisheries of Porto Rico by the United States Fish Commission Steamer Fish Hawk in 1899. The Brachyura and Macrura of Porto Rico. Bulletin of the United States Fish Commission, 20: 1-127.), Periclimenaeus bruceiCardoso and Young, 2007Cardoso, I.A. and Young, P.S. 2007. Caridea (Crustacea, Decapoda: Disciadidae, Palaemonidae, Processidae, Rhynchocinetidae) from Rocas Atoll including two new species of Periclimenaeus Borradaile, 1951. Arquivos do Museu Nacional, Rio de Janeiro, 65: 277-337., Periclimenaeus caraibicusHolthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332., Periclimenaeus crosnieriCardoso and Young, 2007Cardoso, I.A. and Young, P.S. 2007. Caridea (Crustacea, Decapoda: Disciadidae, Palaemonidae, Processidae, Rhynchocinetidae) from Rocas Atoll including two new species of Periclimenaeus Borradaile, 1951. Arquivos do Museu Nacional, Rio de Janeiro, 65: 277-337., Periclimenaeus pearsei (Schmitt, 1932Schmitt, W.L. 1932. Appendix in Pearse, Inhabitants of certain sponges at Dry Tortugas. Carnegie Institute of Washington Publication, 435: 123-124.), and Periclimenaeus perlatus (Boone, 1930Boone, P.L. 1930. New decapod and isopod crustaceans from Gonave Bay, Haiti. Zoologica, New York, 12: 41-53.), all restricted to the northernmost coast of the country (Cardoso and Young, 2007Cardoso, I.A. and Young, P.S. 2007. Caridea (Crustacea, Decapoda: Disciadidae, Palaemonidae, Processidae, Rhynchocinetidae) from Rocas Atoll including two new species of Periclimenaeus Borradaile, 1951. Arquivos do Museu Nacional, Rio de Janeiro, 65: 277-337.; Souza et al., 2011Souza, J.A.F.; Schwamborn, R.; Barreto, A.V.; Farias, I.D.; Fernandes, L.M.G. and Coelho, P.A. 2011. Marine and estuarine shrimps (Dendrobranchiata, Stenopodidea, and Caridea), of Pernambuco State (Brazil) and northeastern Brazilian oceanic islands. Atlântica, Rio Grande, 33: 33-63.; Vieira et al., 2012Vieira, R.R.R.; Ferreira, R.S. and D’Incao, F. 2012. Pontoniinae (Crustacea: Decapoda: Caridea) from Brazil with taxonomic key. Zootaxa , 3149: 1-38.). Interestingly, P. atlanticus, originally reported from Paraíba by Young (1986Young, P.S. 1986. Análise quantitativa e qualitativa da fauna associada a corais hermatípicos (Coelenterata, Scleractinia) nos recifes de João Pessoa, PB. Revista Brasileira de Biologia, 46: 99-126.), was missing in subsequent major checklists (e.g., Ramos-Porto and Coelho, 1998Ramos-Porto, M. and Coelho, P.A. 1998. Malacostraca. Eucarida. Caridea (Alpheoidea excluded). p. 325-350. In: Young, P.S. (ed), Catalogue of Crustacea of Brazil. Rio de Janeiro, Museu Nacional. (Série Livros 6); 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 (Dendrobranchiata, Stenopodidea and Caridea) from north and northeast Brazil. Zootaxa , 1221: 41-62.; Vieira et al., 2012Vieira, R.R.R.; Ferreira, R.S. and D’Incao, F. 2012. Pontoniinae (Crustacea: Decapoda: Caridea) from Brazil with taxonomic key. Zootaxa , 3149: 1-38.), and only briefly mentioned by Cardoso and Young (2007Cardoso, I.A. and Young, P.S. 2007. Caridea (Crustacea, Decapoda: Disciadidae, Palaemonidae, Processidae, Rhynchocinetidae) from Rocas Atoll including two new species of Periclimenaeus Borradaile, 1951. Arquivos do Museu Nacional, Rio de Janeiro, 65: 277-337.: 296). Although Young (1986Young, P.S. 1986. Análise quantitativa e qualitativa da fauna associada a corais hermatípicos (Coelenterata, Scleractinia) nos recifes de João Pessoa, PB. Revista Brasileira de Biologia, 46: 99-126.) did not provide illustrations or a proper taxonomic treatment for his material, the identity of his specimens was confirmed by D. Grangeiro and M.L. Christoffersen (pers. comm.) through the examination of some of Young’s (1986Young, P.S. 1986. Análise quantitativa e qualitativa da fauna associada a corais hermatípicos (Coelenterata, Scleractinia) nos recifes de João Pessoa, PB. Revista Brasileira de Biologia, 46: 99-126.) vouchers deposited in the carcinological collection of the Universidade Federal da Paraíba, Paraíba, Brazil.

During ascidian samplings in Escalvada Island (Espírito Santo, Brazil), specimens of P. ascidiarum and P. maxillulidens (Schmitt, 1936Schmitt, W.L. 1936. Zoologische Ergebnisse einer Reise nach Bonaire, Curaçao und Aruba im Jahre 1930. No. 16. Macruran and anomuran Crustacea from Bonaire, Curaçao and Aruba. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere, 67: 363-378.) were retrieved from two colonies of an undescribed species of Diplosoma Macdonald (Ascidiacea: Didemnidae) (S. Vieira, pers. comm.). The material represents the southernmost record of both shrimp species in the southwestern Atlantic Ocean and the first host record for P. maxillulidens in the literature.

MATERIAL AND METHODS

The shrimps were extracted from two colonies of the ascidian Diplosoma sp. associated with coral rubble obtained by scuba diving at approximately 15 m depth on the northernmost part of the Escalvada Island, Espírito Santo, Brazil. The tunicate hosts were preserved in 10% formaldehyde in sea water and deposited in the Ascidiacea collection of the Zoology Department at Universidade Federal do Paraná, Paraná, Brazil (DZUP).

The shrimps were extracted from the ascidian’s circulatory channels and preserved in 70% ethanol; subsequently, they were studied and deposited in the carcinological collection of the Museu de Zoologia, Universidade de São Paulo (MZUSP). The shrimps were drawn under a stereomicroscope equipped with a camera lucida to illustrate the most important taxonomic characters. Carapace length (CL, in mm) was used as standard measurement for the shrimps, measured from the level of the posterior orbital margin to the posterior margin in the midline of the carapace.

SYSTEMATICS

Palaemonidae Rafinesque, 1815Rafinesque, C.S. 1815. Analyse de la nature ou tableau de l'univers et des corps organisés. Palermo (self-published), 223p.

Periclimenaeus Borradaile, 1915Borradaile, L.A. 1915. Notes on Carides. The Annals and Magazine of Natural History , Series 8, 15: 205-213.

Periclimenaeus ascidiarum Holthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.

(Figs. 1-3)

Figure 1.
Periclimenaeus ascidiarumHolthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332., ovigerous female, 2.7 mm CL, MZUSP 39106: (A) rostrum, lateral view; (B) frontal margin and cephalic appendages, lateral view; (C) right antennule, first article of peduncle, dorsal view; (D) right scaphocerite, dorsal view; (E) left first pereopod, lateral view; (F) telson, dorsal view; (G) right uropod, diaeresis, dorsal view.

Figure 2.
Periclimenaeus ascidiarumHolthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332., ovigerous female, 2.7 mm CL, MZUSP 39106: (A) major (left) second pereopod, lateral view; (B) same, fingers, dorsal view; (C) same, cutting edges, mesial view; (D) minor (right) second pereopod, lateral view; (E) same, fingers, dorsal view; (F) same, cutting edges, lateral view.

Figure 3.
Periclimenaeus ascidiarumHolthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332., ovigerous female, 2.7 mm CL, MZUSP 39106: (A) left third pereopod, lateral view; (B) same, dactylus, lateral view; (C) left fourth pereopod, lateral view; (D) same, dactylus, lateral view; (E) left fifth pereopod, lateral view; (F) same, dactylus, lateral view.

Periclimenaeus ascidiarumHolthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.: 80, pl. 22, figs. g-l, pl. 23, figs. a-i.- Chace, 1972Chace, F.A. 1972. The shrimps of the Smithsonian-Bredin Caribbean Expeditions with a summary of the West Indian shallow-water species (Crustacea: Decapoda: Natantia). Smithsonian Contribution to Zoology, 98: 1-179.: 25, 26.- 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 de 5ºN e 39ºS. Trabalhos Oceanográficos da Universidade Federal de Pernambuco, 13: 133-236.: 146.- Ramos-Porto, 1980Ramos-Porto, M. 1980. Estudo ecológico da região de Itamaracá, Pernambuco, Brasil. VII. Crustáceos Decápodos Natantes. Trabalhos Oceanográficos da Universidade Federal de Pernambuco, 15: 277-309.: 297.- Abele and Kim, 1986Abele, L.G. and Kim, W. 1986. An illustrated guide to the marine decapod crustaceans of Florida. Tallahassee, State of Florida Department of Environmental Regulation (Technical Series, 8), 760p.: 11, 89.- Ramos-Porto and Coelho, 1990Ramos-Porto, M. and Coelho, P.A. 1990. Sinopse dos crustáceos decápodos brasileiros (Família Palaemonidae). Anais da Sociedade Nordestina de Zoologia, 3: 93-111.: 105.- Ramos-Porto and Coelho, 1998Ramos-Porto, M. and Coelho, P.A. 1998. Malacostraca. Eucarida. Caridea (Alpheoidea excluded). p. 325-350. In: Young, P.S. (ed), Catalogue of Crustacea of Brazil. Rio de Janeiro, Museu Nacional. (Série Livros 6): 337.- 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 (Dendrobranchiata, Stenopodidea and Caridea) from north and northeast Brazil. Zootaxa , 1221: 41-62.: 50, tab. 3.- Souza et al., 2011Souza, J.A.F.; Schwamborn, R.; Barreto, A.V.; Farias, I.D.; Fernandes, L.M.G. and Coelho, P.A. 2011. Marine and estuarine shrimps (Dendrobranchiata, Stenopodidea, and Caridea), of Pernambuco State (Brazil) and northeastern Brazilian oceanic islands. Atlântica, Rio Grande, 33: 33-63.: 44.- Vieira et al., 2012Vieira, R.R.R.; Ferreira, R.S. and D’Incao, F. 2012. Pontoniinae (Crustacea: Decapoda: Caridea) from Brazil with taxonomic key. Zootaxa , 3149: 1-38.: 13, fig. 7 (map).- Ramos-Tafur and Lemaitre, 2017Ramos-Tafur, G.E and Lemaitre, R. 2017. A new species of shrimp of the genus Periclimenaeus Borradaile, 1915 (Decapoda: Caridea: Palaemonidae) from the southeastern Gulf of Mexico, including a key to the western Atlantic species of the genus. Zootaxa , 4303: 491-508.: 505 (key).- Pachelle et al., 2018Pachelle, P.P.G.; Leray, M.; Anker, A. and Lasley, R. 2018. Five new records of marine shrimps (Decapoda: Caridea, Stenopodidea) from the Caribbean coast of Panama. Zootaxa , 4438: 128-136.: 130, fig. 2.

Material examined. Brazil, Espírito Santo, off Vitória, Escalvada Island, 20º41’55.3”S 40º24’20.8”W, scuba dive, 15 m depth, coral rubble, inside Diplosoma sp. (Fig. 4), coll. Sandra Vieira Paiva, 29 March 2017: 1 ovigerous female, 2.7 mm CL, MZUSP 39106; 1 ovigerous female, 2.7 mm CL, MZUSP 39107.

Figure 4.
The ascidian host, Diplosoma sp. (Didemnidae), at Ilha Escalvada, Espírito Santo (Brazil), photographed in situ. Note the spaces between the zooid clusters where the shrimps were dwelling.

Distribution. Western Atlantic: USA (Florida), Colombia (Cape de La Vela), Dominica, Cuba (Batabanó Gulf), Panama (Bocas del Toro) and Brazil (Maranhão, Ceará, Pernambuco, Espírito Santo) (Holthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.; Chace, 1972Chace, F.A. 1972. The shrimps of the Smithsonian-Bredin Caribbean Expeditions with a summary of the West Indian shallow-water species (Crustacea: Decapoda: Natantia). Smithsonian Contribution to Zoology, 98: 1-179.; Vieira et al., 2012Vieira, R.R.R.; Ferreira, R.S. and D’Incao, F. 2012. Pontoniinae (Crustacea: Decapoda: Caridea) from Brazil with taxonomic key. Zootaxa , 3149: 1-38.; Pachelle et al., 2018Pachelle, P.P.G.; Leray, M.; Anker, A. and Lasley, R. 2018. Five new records of marine shrimps (Decapoda: Caridea, Stenopodidea) from the Caribbean coast of Panama. Zootaxa , 4438: 128-136.; present study).

Remarks. The morphological characters in our specimens agree well with those described by Holthuis (1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.), including (i) shape and armature of the rostrum (Fig. 1A), (ii) first article of antennular peduncle with distolateral angle produced into small tooth (Fig. 1C), (iii) scaphocerite twice as long as broad, with a distinct lateral tooth (Fig. 1D), (iv) proportions of the first pereopod (Fig. 1E); (v) overall shape and armature of the second pereopods (Fig. 2), and (vi) pereopods 3-5 with dactyli distally biunguiculate and bearing an additional proximoventral tooth (Fig. 3B, D, F).

Holthuis (1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.) described P. ascidiarum based on specimens associated with unidentified ascidians from Florida (USA) and Cape la Vela (Colombia). Since then, the species has been reported from several localities in the Caribbean and Brazil, but with no mention of an ascidian host (Vieira et al., 2012Vieira, R.R.R.; Ferreira, R.S. and D’Incao, F. 2012. Pontoniinae (Crustacea: Decapoda: Caridea) from Brazil with taxonomic key. Zootaxa , 3149: 1-38.). The new material suggests that P. ascidiarum occurs in colonial ascidians of the genus Diplosoma; however, the range of host species remains to be investigated. The present material also represents the first record of P. ascidiarum in Espírito Santo, extending considerably its known southern distribution in the Atlantic Ocean from Pernambuco (8-9ºS) to Escalvada Island (20ºS).

Periclimenaeus maxillulidens ( Schmitt, 1936Schmitt, W.L. 1936. Zoologische Ergebnisse einer Reise nach Bonaire, Curaçao und Aruba im Jahre 1930. No. 16. Macruran and anomuran Crustacea from Bonaire, Curaçao and Aruba. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere, 67: 363-378. )

(Figs. 5-7)

Figure 5.
Periclimenaeus maxillulidens (Schmitt, 1936Schmitt, W.L. 1936. Zoologische Ergebnisse einer Reise nach Bonaire, Curaçao und Aruba im Jahre 1930. No. 16. Macruran and anomuran Crustacea from Bonaire, Curaçao and Aruba. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere, 67: 363-378.), ovigerous female, 3.7 mm CL, MZUSP 39108: (A) rostrum, lateral view; (B) frontal margin and cephalic appendages, lateral view; (C) right antennule, first article of peduncle, dorsal view; (D) right scaphocerite, dorsal view; (E) right first pereopod, lateral view; (F) telson, dorsal view; (G, H) right and left uropods, respectively, diaeresis, dorsal view.

Figure 6.
Periclimenaeus maxillulidens (Schmitt, 1936Schmitt, W.L. 1936. Zoologische Ergebnisse einer Reise nach Bonaire, Curaçao und Aruba im Jahre 1930. No. 16. Macruran and anomuran Crustacea from Bonaire, Curaçao and Aruba. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere, 67: 363-378.), ovigerous female, 3.7 mm CL, MZUSP 39108: (A) major (right) second pereopod, lateral view; (B) same, fingers, dorsal view; (C) same, mesial view; (D) minor (left) second pereopod, lateral view; (E) same, fingers, dorsal view; (F) same, mesial view.

Figure 7.
Periclimenaeus maxillulidens (Schmitt, 1936Schmitt, W.L. 1936. Zoologische Ergebnisse einer Reise nach Bonaire, Curaçao und Aruba im Jahre 1930. No. 16. Macruran and anomuran Crustacea from Bonaire, Curaçao and Aruba. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere, 67: 363-378.), ovigerous female, 3.7 mm CL, MZUSP 39108: (A) left third pereopod, lateral view; (B) same, dactylus, lateral view; (C) left fourth pereopod, lateral view; (D) same, dactylus, lateral view; (E) left fifth pereopod, lateral view; (F) same, dactylus, lateral view.

Periclimenes maxillulidensSchmitt, 1936Schmitt, W.L. 1936. Zoologische Ergebnisse einer Reise nach Bonaire, Curaçao und Aruba im Jahre 1930. No. 16. Macruran and anomuran Crustacea from Bonaire, Curaçao and Aruba. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere, 67: 363-378.: 371, pl. 13, fig. 3a-o.

Periclimenaeus maxillulidens.- Holthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.: 87, pl. 26.- Abele and Kim, 1986Abele, L.G. and Kim, W. 1986. An illustrated guide to the marine decapod crustaceans of Florida. Tallahassee, State of Florida Department of Environmental Regulation (Technical Series, 8), 760p.: 11, 90.- Chace, 1972Chace, F.A. 1972. The shrimps of the Smithsonian-Bredin Caribbean Expeditions with a summary of the West Indian shallow-water species (Crustacea: Decapoda: Natantia). Smithsonian Contribution to Zoology, 98: 1-179.: 28.- Cardoso and Young, 2007Cardoso, I.A. and Young, P.S. 2007. Caridea (Crustacea, Decapoda: Disciadidae, Palaemonidae, Processidae, Rhynchocinetidae) from Rocas Atoll including two new species of Periclimenaeus Borradaile, 1951. Arquivos do Museu Nacional, Rio de Janeiro, 65: 277-337.: 295 (key), 296.- Santana-Moreno et al., 2013Santana-Moreno, L.D.; De Grave, S. and Simões, N. 2013. New records of caridean shrimps (Decapoda: Caridea) from shallow water along the northern Yucatan peninsula coasts of México. Nauplius, 21: 225-238.: 231, fig. 2G.- Ramos-Tafur and Lemaitre, 2017Ramos-Tafur, G.E and Lemaitre, R. 2017. A new species of shrimp of the genus Periclimenaeus Borradaile, 1915 (Decapoda: Caridea: Palaemonidae) from the southeastern Gulf of Mexico, including a key to the western Atlantic species of the genus. Zootaxa , 4303: 491-508.: 505 (key) .- Pachelle et al., 2018Pachelle, P.P.G.; Leray, M.; Anker, A. and Lasley, R. 2018. Five new records of marine shrimps (Decapoda: Caridea, Stenopodidea) from the Caribbean coast of Panama. Zootaxa , 4438: 128-136.: 132.

Material examined. Brazil, Espírito Santo, off Vitória, Escalvada Island, 20º41’55.3”S 40º24’20.8”W, scuba dive, 15 m depth, coral rubble, inside Diplosoma sp. (Fig. 4), coll. Sandra Vieira Paiva, 29 March 2017: 1 ovigerous female, 3.7 mm CL, MZUSP 39108.

Distribution. Western Atlantic: USA (Florida), Mexico (Yucatan), Bonaire, Panama (Bocas del Toro) and Brazil (Espírito Santo) (Schmitt, 1936Schmitt, W.L. 1936. Zoologische Ergebnisse einer Reise nach Bonaire, Curaçao und Aruba im Jahre 1930. No. 16. Macruran and anomuran Crustacea from Bonaire, Curaçao and Aruba. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere, 67: 363-378.; Holthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.; Santana-Moreno et al., 2013Santana-Moreno, L.D.; De Grave, S. and Simões, N. 2013. New records of caridean shrimps (Decapoda: Caridea) from shallow water along the northern Yucatan peninsula coasts of México. Nauplius, 21: 225-238.; Pachelle et al., 2018Pachelle, P.P.G.; Leray, M.; Anker, A. and Lasley, R. 2018. Five new records of marine shrimps (Decapoda: Caridea, Stenopodidea) from the Caribbean coast of Panama. Zootaxa , 4438: 128-136.; present study).

Remarks.Schmitt (1936Schmitt, W.L. 1936. Zoologische Ergebnisse einer Reise nach Bonaire, Curaçao und Aruba im Jahre 1930. No. 16. Macruran and anomuran Crustacea from Bonaire, Curaçao and Aruba. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere, 67: 363-378.) described P. maxillulidens (as Periclimenes maxillulidens) based on one male collected in Bonaire. Afterwards, the species was only reported from USA (Florida), Mexico (Yucatan) and Panama (Bocas del Toro) (Holthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.; Santana-Moreno et al., 2013Santana-Moreno, L.D.; De Grave, S. and Simões, N. 2013. New records of caridean shrimps (Decapoda: Caridea) from shallow water along the northern Yucatan peninsula coasts of México. Nauplius, 21: 225-238.; Pachelle et al., 2018Pachelle, P.P.G.; Leray, M.; Anker, A. and Lasley, R. 2018. Five new records of marine shrimps (Decapoda: Caridea, Stenopodidea) from the Caribbean coast of Panama. Zootaxa , 4438: 128-136.). The present female from Escalvada Island represents the fourth record of this rare species and its first record in Brazil and the southwestern Atlantic Ocean.

Our specimen agrees well with the specimens described and illustrated in Schmitt (1936Schmitt, W.L. 1936. Zoologische Ergebnisse einer Reise nach Bonaire, Curaçao und Aruba im Jahre 1930. No. 16. Macruran and anomuran Crustacea from Bonaire, Curaçao and Aruba. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere, 67: 363-378.: pl. 13) and Holthuis (1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.: pl. 26), including (i) shape and armature of the rostrum (Fig. 5A), (ii) first article of antennular peduncle with distolateral angle blunt, lacking a tooth (Fig. 5C), (iii) scaphocerite wider distally, with a small lateral tooth (Fig. 5D), (iv) proportions of the first pereopod (Fig. 5E), (v) overall shape and armature of the major second pereopod (Fig. 6A-C), and (vi) pereopods 3-5 with dactyli simple, lacking both subdistal and proximoventral teeth (Fig. 7B, D, F). The minor second pereopod, herein illustrated for the first time for the species (Fig. 6D-F), lacks granules on its surface, but is furnished with setae, which are more abundant on the chela fingers. The fingers are slightly curved inwards; the cutting edge of the fixed finger has a small triangular tooth on its proximal half and a series of tiny teeth on the distal half; the dactylus has a wide, laterally excavated process proximally, separated from the rest of the cutting edge by a sinus; cutting edge distally serrated (Fig. 6F).

According to Holthuis (1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.), P. maxillulidens is morphologically very similar to two other Atlantic species, P. atlanticus and P. schmittiHolthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.. Periclimenaeus maxillulidens, however, can be readily separated from both species by the combination of three morphological characters: (i) shape and armature of rostrum (1-2 dorsal teeth in P. maxillulidens and P. schmitti, 4 teeth in P. atlanticus; cf. Holthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.: pl. 24, fig. b; Fig. 5A), (ii) armature of the scaphocerite (blunt in P. schmitti, with small tooth in P. maxillulidens, with distinct tooth in P. atlanticus; cf. Holthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.: pl. 24, fig. e; pl. 27, fig. c; Fig. 5D), and (iii) the shape of pereopods 3-5 dactyli (simple in P. maxillulidens and P. atlanticus, biunguiculate in P. schmitti; cf. Holthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.: pl. 24, fig. o; pl. 27, fig. m; Fig. 7B, D, F).

Although most species of Periclimenaeus are known to associate with sponges and ascidians, the hosts for several species are either unknown or reported as unidentified sponges or ascidians (Holthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.; Bruce, 2006Bruce, A.J. 2006. Periclimenaeus nielbrucei sp. nov. (Crustacea: Decapoda: Pontoniinae), a new sponge associate from the Capricorn Islands, Queensland, with notes on related Periclimenaeus species. Zootaxa, 1224: 1-22.; Fransen, 2006Fransen, C.H.J.M. 2006. On Pontoniinae (Crustacea, Decapoda, Palaemonidae) collected from ascidians. Zoosystema, 28: 713-746.; Dobson et al., 2016Dobson, N.C.; Johnson, M.L. and De Grave, S. 2016. Insights into the morphology of symbiotic shrimp eyes (Crustacea, Decapoda, Palaemonidae); the effects of habitat demands. PeerJ, 4: e1926.). Periclimenaeus maxillulidens has been reported from sandy debris (Schmitt, 1936Schmitt, W.L. 1936. Zoologische Ergebnisse einer Reise nach Bonaire, Curaçao und Aruba im Jahre 1930. No. 16. Macruran and anomuran Crustacea from Bonaire, Curaçao and Aruba. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere, 67: 363-378.), broken shells, gravel, sand and coral (Holthuis, 1951Holthuis, L.B. 1951. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. I. The subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Foundation Publications, Occasional Papers, Los Angeles, 11: 1-332.; Santana-Moreno et al., 2013Santana-Moreno, L.D.; De Grave, S. and Simões, N. 2013. New records of caridean shrimps (Decapoda: Caridea) from shallow water along the northern Yucatan peninsula coasts of México. Nauplius, 21: 225-238.). Pachelle et al. (2018Pachelle, P.P.G.; Leray, M.; Anker, A. and Lasley, R. 2018. Five new records of marine shrimps (Decapoda: Caridea, Stenopodidea) from the Caribbean coast of Panama. Zootaxa , 4438: 128-136.) reported a single ovigerous female of P. maxillulidens in epibiotic growth on mangrove roots, but without specifying whether the specimen was collected inside sponges or ascidians. Therefore, the present study confirms that the species is, at least, associated with colonial ascidians of the genus Diplosoma (Fig. 1).

Identification key for the species of Periclimenaeus from the southwestern Atlantic

1a. Pereopods 3-5 with dactyli simple ............................................................................ 2

1b. Pereopods 3-5 with dactyli biunguiculate ................................................................. 3

2a. Rostrum straight, dorsal margin with 4 teeth; scaphocerite with lateral tooth distinct, strong ............................................................................................................. P. atlanticus

[Brazil: Paraíba]

2b. Rostrum sinuous, dorsal margin with 2-3 teeth; scaphocerite with lateral tooth subtle, weak ............................................................................................. P. maxillulidens

[Brazil: Espírito Santo (Escalvada Island)]

3a. Rostrum with a ventral tooth; carapace with small supraorbital tooth or acute tubercle; scaphocerite with lateral tooth distinct, clearly overreaching blade; dactyli of pereopods 3-5 with unguis ventrally serrulate …………………………… P. caraibicus

[Brazil: Rio Grande do Norte (Atol das Rocas)]

3b. Rostrum with ventral margin unarmed; orbital region of carapace smooth; scaphocerite with lateral tooth not as distinct, at most reaching the distal margin of the blade; dactyli of pereopods 3-5 with unguis ventrally smooth ...................................... 4

4a. Telson with both pairs of dorsal spines inserted in the anterior half of telson; outer pair of distal spines of telson removed from the distal margin, inserted more proximally than the remaining two distal pairs of spines .................................................................. 5

4b. Telson with posterior pair of dorsal spines inserted in the posterior half of telson; outer pair of distal spines of telson placed in the distal margin, in line with the remaining two distal pairs of spines ……………………………………………............ 7

5a. Rostrum very high, dorsal teeth large; pereopod 1 carpus long, almost twice as long as chela ............................................................................................................. P. perlatus

[Brazil: Ceará, Paraíba, Pernambuco]

5b. Rostrum not very high, dorsal teeth medium-sized; pereopod 1 carpus short, slightly longer than chela .............................................................................................................. 6

6a. Carapace not inflated; second pereopods with palm furnished with numerous granules ............................................................................................................... P. brucei

[Brazil: Rio Grande do Norte (Atol das Rocas)]

6b. Carapace inflated; second pereopods chelae smooth, without granules ......................................................................................................................... P. crosnieri

[Brazil: Rio Grande do Norte (Atol das Rocas)]

7a. Rostrum long, distinctly overreaching the corneas; stylocerite slender, tip acute; dactylus of both second pereopods with cutting edge serrated near apex; minor second pereopod fingers serrated near apex; propodus of pereopod 3 with ventral spines restricted to the distoventral angle …………………………...................... P. ascidiarum

[Brazil: Maranhão, Ceará, Pernambuco, Espírito Santo (Escalvada Island)]

7b. Rostrum short, not reaching the distal margin of the corneas; stylocerite broad, tip triangular; dactylus of both second pereopods with cutting edge smooth near apex; minor second pereopod fingers smooth near apex; propodus of pereopod 3 with ventral spines distributed along the margin .................................................................. P. pearsei

[Brazil: Maranhão]

ACKNOWLEDGEMENTS

We are grateful to Dr. Roberto Gomes de Freitas Berlinck (USP) for providing the ascidian specimens included in the present study. The material was collected during the project “Componentes da biodiversidade e seus caracteres metabólicos de ilhas do Brasil - uma abordagem integrada” funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) under the number BIOTA/BIOprospecTA grant 2013/50228-8. Special thanks go to Dr. Rosana Moreira da Rocha (UFPR) for providing a color photo of the ascidian used in this study, to Dr. Martin L. Christoffersen and MSc. Daniela Grangeiro (UFPB) for examining specimens of P. atlanticus deposited in the UFPB collection, to Dr. Marcos Tavares (MZUSP) for providing work space and access to the collection under his care. We also thank Dr. Zdenek Ďuriš and an anonymous reviewer for providing valuable comments that greatly improved the originally submitted manuscript.

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Publication Dates

  • Publication in this collection
    03 July 2020
  • Date of issue
    2020

History

  • Received
    08 Oct 2019
  • Accepted
    05 May 2020
Sociedade Brasileira de Carcinologia Instituto de Biociências, UNESP, Campus Botucatu, Rua Professor Doutor Antônio Celso Wagner Zanin, 250 , Botucatu, SP, 18618-689 - Botucatu - SP - Brazil
E-mail: editor.nauplius@gmail.com