Synalpheus brooksi Coutière, 1909

Anker, Arthur, Pachelle, Paulo P. G., Grave, Sammy De & Hultgren, Kristin M., 2012, 3598, Zootaxa 3598 (1), pp. 1-96 : 26-31

Synalpheus brooksi Coutière, 1909

( Figs 15–18 )

Synalpheus brooksi Coutière 1909: 69 , fig. 41; Coutière 1910: 487; McClendon 1911: 57, pl. 1, fig. 1; Pearse 1932: 119; Pearse

1950: 150; (?) Holthuis 1959: 104; Dobkin 1965: 450, figs 1-5; Chace 1972: 92 (partim); (?) Coelho & Ramos 1972: 151;

Christoffersen 1979: 335, figs 20-22 (partim); (?) Westinga & Hoetjes 1981: 142; Dardeau 1984: 26, figs 11–14 (partim);

Lemaitre 1984: 426; Abele & Kim 1986: 202, 220–221, figs f, g; Erdman & Blake 1987: 328; Duffy 1992: 130; Duffy

1993: 459; Duffy 1996a: 360; (?) Martínez-Iglesias et al. 1996: 35; (?) Hernández Aguilera et al. 1996: 36; Christoffersen

1998: 362 (partim); McClure 2005: 171, figs 35-37; Macdonald & Duffy 2006: 18, fig. 16; Macdonald et al. 2009: 13. Synalpheus brooksi strepsiceros Coutière 1909: 72–73 , fig. 42. Synalpheus brooksi eleutherae Coutière 1909: 73 , fig. 43. Synalpheus ? brooksi — Fausto Filho & Sampaio Neto 1976: 67. Zuzalpheus brooksi — Ríos & Duffy 2007: 14, pl. 1.? Synalpheus longicarpus — Corrêa 1972: 3 [not S. longicarpus ( Herrick, 1891) ]. For more exhaustive synonymy see Dardeau (1984).

Material examined. Panama: 1 male-looking individual, RMNH D54847, Bocas del Toro , Isla Colón, Punta Caracol, in Lissodendoryx colombiensis , 1–2 m, coll. A. Anker et al. (shrimp taxonomy class), 08.08.2008 [fcn 08- 233D]; 1 ov. female, OUMNH. ZC.2012-07-120, Bocas del Toro , Isla Colón, Punta Caracol, 2–3 m, in sponge ( L. colombiensis or another sponge), coll. A. Anker, J.A. Baeza, 28.04.2007 [fcn 07-143B*]; 1 ov. female, USNM 1187896 , Bocas del Toro , Isla San Cristobal, in Calyx podatypa , 1–3 m, coll. K. Hultgren, 30.10.2007 [fcn P07- 902-3] . USA: 3 ov. females, 4 male-looking individuals, 7 juveniles, MNHN-IU-2010-4164, Florida Keys, Marathon Key, ocean side, in large black sponge ( Spheciospongia vesparium ?), 0.5 m, coll. A. Anker, A.L. Rhyne, 19.04.2004 [fcn 04-001*]; 7 ov. females, 6 male-looking individuals, 14 juveniles, OUMNH. ZC.2012-07-047, Florida Keys, Bahia Honda , ocean side, in unidentified sponge, 0.5 m, coll. A. Anker, A.L. Rhyne, 18.04.2004 [fcn 04-004]; 1 male-looking individual, RMNH D54846, Florida Keys, Bahia Honda , ocean side, in unidentified sponge, 0.5–1 m, coll. A. Anker, A.L. Rhyne, 19.04.2004 [fcn 04-008]; 1 ov. female, RMNH D54850, same collection data [fcn 04-007]; 1 post-ov. female, OUMNH. ZC.2012-07-046, Florida Keys, Seven Mile Bridge, Missouri-Ohio channel, in Spheciospongia vesparium , 0.5 m, coll. A. Anker et al., 06.09.2008 [fcn 08-261*]; 1 male-looking individual, OUMNH. ZC.2012-07-045, same collection data [fcn 08-263*]; 1 ov. female, OUMNH. ZC.2012-07-048, same collection data [fcn 08-260*]; 1 ov. female, MNHN-IU-2010-4112, same collection data [fcn 08-266]; 1 ov. female, MNHN-IU-2010-4113, same collection data [fcn 08-265]; 10 specimens, RMNH D54845 , same collection data [fcn 08-273]; 1 male, RMNH D54849 , same collection data [fcn 08-264]; 1 ov. female, MNHN-IU-2010-4114, same collection data [fcn 08-259*]; 2 male-looking individuals, MNHN-IU-2010-4115, same collection data [fcn 08-262*] . Mexico: 1 ov. female, OUMNH. ZC.2012-07-126, Quintana Roo , Isla Cozumel, 5 km north of Cozumel town, mixed soft-hard bottom flat with rubble, in S. vesparium , 1–2 m, coll. A. Anker, J. Duarte-Gutiérrez, 08.07.2010 [fcn COZ1-002 ]; 1 male-looking individual, OUMNH. ZC.2012-07-122, same collection data [fcn COZ1-007 ]; 1 female, MNHN-IU-2010-4117, same collection data [fcn COZ1-008 ]; 1 male, RMNH D54848, same collection data [fcn COZ1-009 ]; 1 male-looking individual, UNAM-CNCR, same collection data [fcn COZ1-016 ]; 1 ov. female, UNAM-CNCR, Gulf of Mexico north of Yucatan , Arrecife Alacranes off Yucatan Peninsula, in orange sponge “with many cavities”, 10 m, coll. J. Duarte-Gutiérrez, 08.08.2009 [fcn JD-029A];> 30 specimens, UNAM-CNCR, same collection data [fcn JD-029B] . Belize: 1 ov. female, MNHN-IU-2010-4116, Carrie Bow Cay, in L. colombiensis , coll. E. Tóth, 18.07.2005 [fcn 05- 191]; 2 male-looking individuals, 4 juveniles, RMNH D54851, same collection data [fcn 05-193] . Honduras: 2 male-looking individuals, NHM, “British Honduras”, locality unknown, in velvet sponge, J.O. Borley Esq. , no further data . Guyana: 3 male-looking individuals, NHM 1958: 11-12-8-9, 07°47’ N, 57°32’W, 33–35 fathoms

(60–64 m), in unknown sponge, coll. McCormick 24.04.1938. Brazil: 1 male-looking individual, MZUSP 27616 , Ceará, Icapuí, mud bank with seagrass (mainly Halodule sp ) and algae, in unidentified sponge, coll. UFC class, 02.06.2012 [fcn 12-051*]; 1 ov. female, OUMNH. ZC.2012-07-049, Ceará, Pecém , harbour jetty, in Ircinia sp. , 0.5–1 m, coll. L.E.A. Bezerra, 10.09.2011 [fcn 11-110]; 8 male-looking individuals (4 with eggs), OUMNH. ZC.2012-07-051, same collection data [fcn 11-111]; 1 female, 17 male-looking individuals (7 with eggs), MZUSP 25253 , same collection data [fcn 11-107]; 6 male-looking individuals with eggs, MNHN-IU-2010-4118 , same collection data [fcn 11-109]; 16 male-looking individuals (3 with eggs), RMNH D54844 , same collection data [fcn 11-108]; 5 specimens (not sexed), UFC 456 , Ceará, near-shore area (“litoral”), locality not specified (“litoral do estado do Ceará ”), 35–40 m, coll. “Barco SWJ”, 24.11.1972 ; 2 specimens (not sexed), UFC 465 , Ceará, Fortaleza , Mucuripe, coll. M. Erones, 08.05.1968 .

Material tentatively identified as Synalpheus brooksi (?): Panama: 1 ov. female, OUMNH. ZC.2012-07-050, Isla Grande , between village and Playa de la Punta, coral rocks in cryptic sponge, 1–1.5 m, coll. A. Anker , 04.09.2006 [fcn 06-444*]. Brazil: 2 males (1 dissected), 1 ov. female, 4 immature specimens (unsexed), MNRJ 23338 , Atol das Rocas, Canal do Barretão , in unidentified sponge, ~ 5 m, coll. F.B. Pitombo , R. Barroso , 26.12.2000; 1 male, OUMNH. ZC.2012-07-142 Atol das Rocas, sta. R10 , in Ircinia sp. , coll. P.S. Young, P.C. Paiva, A.A. Aguiar , 11.10.2000; 1 immature male, MZUSP 25350 , Ceará, Banco Canopus , in sponge, depth unknown, coll. J. Coltro , 11.2005.

Description. For description and illustrations see Coutière (1909), Christoffersen (1979), Dardeau (1984), Macdonald & Duffy (2006), and Ríos & Duffy (2007); for illustrations of S. brooksi (?) from Atol das Rocas see Fig. 18 (also see remarks below).

Size range. Males or male-looking individuals, 3.2–5.6 mm cl; females, 3.8–4.9 mm cl.

Colour in life. Semitransparent whitish, with pinkish tinge on distal portion of major chela; ovaries or freshly laid eggs usually pale reddish pink, sometimes dull green ( Figs 15 , 16 ; see under Remarks below); see also colour photograph in Ríos & Duffy (2007).

Type locality. Sugar Loaf Key , Florida .

Distribution. Western Atlantic: Florida; Bahamas; throughout Caribbean Sea (e.g., Lesser Antilles, Virgin Islands, Panama, Yucatan etc.); Gulf of Mexico; Suriname; Brazil: Amapá to Bahia ( Coutière 1909; Dardeau 1984; Chace 1972; Christoffersen 1998; Ríos & Duffy 2007; present study; see map in Fig. 51 ).

Ecology. Shallow subtidal near coral reefs and shallow flats with abundance of sponges, rubble and seagrass; depth range 0.5–73 m ( Dardeau 1984), usually less than 10 m; obligate symbiont of demosponges, typically the loggerhead sponge, Spheciospongia vesparium , for instance in Florida, Yucatan, Belize, Panama, Curaçao, Bonaire and the Bahamas ( Coutière 1910; McClendon 1911; Pearse 1932; Dobkin 1965; Westinga & Hoetjes 1981; Dardeau 1984; Duffy 1992; Ríos & Duffy 2007; present study); also in Lissodendoryx colombiensis , e.g., in Belize ( Ríos & Duffy 2007; present study); Agelas dispar , e.g., in the Florida Middle Ground ( Dardeau 1984) and in Panama (K. Hultgren, pers. obs.); Agelas clathrodes , Hymeniacidon caerulea , and Calyx podatypa , for instance in Panama (K. Hultgren, pers. obs.); record of association of S. brooksi with Ircinia spp. in Florida’s Dry Tortugas ( Pearse 1932) possibly refers to another, closely related species; the record of S. brooksi from Agelas clathrodes in San Blas, Panama ( Duffy 1992) may refer to the closely related S. carpenteri , according to Macdonald & Duffy (2006). Typically found in “subsocial” groups ranging from 10 to over 1000 individuals, with only a few ovigerous females ( Ríos & Duffy 2007; A. Anker, pers. obs.; also see below); however, S. brooksi associated with Hymeniacidon caerulea in Panama, were found in heterosexual pairs (K. Hultgren, pers obs.).

Remarks. Two “subspecies” of S. brooksi were described by Coutière (1909): S. brooksi strepciceros Coutière, 1909 from St. Thomas, and S. brooksi eleutherae Coutière, 1909 from Eleuthera, the Bahamas. These subspecies were based on the proportions of the carpus of the minor cheliped and the proportions of the carpocerite. Dardeau (1984) placed both of them in the synonymy of S. brooksi . Macdonald & Duffy (2006), describing two species from the S. brooksi species complex, did not comment on their taxonomic status, presumably thus simply following Dardeau (1984).

One ovigerous female from Panama (OUMNH.ZC.2012-07-047) has four instead of the typical five articles of the carpus of the second pereiopod. In all other characters, including colour pattern ( Fig. 15h ), this female matches S. brooksi and has also been confirmed as S. brooksi in a DNA analysis (K. Hultgren, pers. obs.). These aberrant specimens can easily be confused with S. agelas or some other species with four articles in the carpus of the second pereiopod.

Several specimens are here tentatively assigned to S. brooksi (?), awaiting collection of more fresh material followed by DNA analyses. These include an ovigerous female from Panama ( Isla Grande: OUMNH.ZC.2012-07- 050) and several specimens from northeastern Brazil (Ceará: MZUSP 25350; Atol das Rocas: MNRJ 23338, OUMNH.ZC.2012-07-142). In all these specimens, the distal tooth of the major chela is projecting directly forward (i.e. more like in S. idios ) and not obliquely upwards, as is typical for S. brooksi ( Fig. 18d ). In males of S. brooksi (?), the first pleuron has a small pointed tooth, whilst the third to fifth pleura each are produced ventrally into a small point, which is typical for S. brooksi and not found in S. idios ( Fig. 18m ). In most other characters, these specimens agree well with S. brooksi ( Fig. 18 ). The female from Isla Grande was carrying dull greenish eggs ( Fig. 15e, f ), which contrasts with dull pinkish or pink-greyish eggs in most S. brooksi ( Fig. 15c ) or dark reddish eggs in S. idios ( Fig. 38 ); the egg colour of the ovigerous female from Atol das Rocas remains unknown. In summary, the identity of all specimens of S. brooksi with a directly forward pointing distal tooth on the major chela and/or greenish eggs (another example illustrated in Fig. 15d ) remain to be clarified genetically.

Synalpheus brooksi usually lives in “subsocial” groups with “male”-biased sex ratio ( Ríos & Duffy 2007). This social structure was also observed in the material from Ircinia sp. collected in Ceará, Brazil. Only two ovigerous females were found among 40 or so specimens extracted from three sponges. All other specimens look externally like males, i.e. they have a relatively slender abdomen with sharp ventral angles on the pleurae and a massive major cheliped. Curiously, many of these “males” (or externally male-looking colony members known as “helpers”) carry eggs under the abdomen, and some of them have a small cluster of oviferous setae on the protopods of some pleopods. The number of eggs carried by the “males” varies from one to several dozen. Some eggs are small and whitish and are probably infertile, but others are larger, more yellow, and may be fertile, although none was close to hatching. The presence of infertile eggs in individuals with male secondary characters in S. brooksi , which was also observed by Coutière (1909), Chace (1972) and Dardeau (1984), remains incompletely explained (see Dardeau 1984 for discussion). In addition, there is a possibility that the “males” of S. brooksi may actually be intersex helper individuals, as reported in some populations of S. duffyi Anker & Tóth, 2008 ( Tóth & Bauer 2008, as S. paraneptunus ); this, however, remains to be confirmed by a SEM study of the gonopores (see Tóth & Bauer 2007). In the Ceará material of S. brooksi , several “male”-looking colony members also have a very peculiarly shaped major chela, with an almost disproportionally swollen palm and very short fingers ( Fig. 17b ). In all other features, these specimens appear to be typical S. brooksi . Presently, we have no explanation for this unusual inflation of the major chela and the reduction of the fingers in these specimens, but similar observations were made by Banner (1957) for some individuals of S. charon ( Heller, 1861) and interpreted as growth anomalies. These observations raise serious doubts about the validity of S. macromanus Edmondson, 1925 known from a single specimen from Hawaii with a greatly inflated major chela, but otherwise presenting all features of S. paraneomeris Coutière, 1905 ( Edmondson 1925; Banner 1953).

Figures

FIGURE 15. Synalpheus brooksi Coutière, 1909: a, b, male from Cozumel, Mexico (RMNH D54848), in dorsal (a) and lateral (b) views; c, female from the same locality (MNHN-IU-2010-4117); d, ovigerous female from Panama (not deposited); e, f, ovigerous female from Isla Grande, Panama [identification tentative] (OUMNH.ZC.2012-07-050), in dorsal (e) and lateral (f) views; g, ovigerous female from Bocas del Toro, Panama (OUMNH.ZC.2012-07-120); h, ovigerous female from the same locality, with four articles in the carpus of the second pereiopod (OUMNH.ZC.2012-07-047). Photographs: a, b, c, e, f, g, h, by A. Anker; d, by E. Tóth.

FIGURE 16. Synalpheus brooksi Coutière, 1909: male-looking individual from Ceará, Brazil (MZUS 27616), dorsal view. Photograph by A. Anker.

FIGURE 17. Synalpheus brooksi Coutière, 1909: major chelae of two “male”-looking individuals from Ceará, Brazil; a, normal chela (RMNH D54844); b, greatly swollen chela with diminutive fingers (OUMNH.ZC.2012-07-051). Scale bar = 1 mm.

FIGURE 18. Synalpheus brooksi Coutière, 1909 (?): male from Atol das Rocas, Brazil (MNRJ 23338); a, frontal region, dorsal; b, same, lateral; c, third maxilliped, lateral; d, major cheliped, lateral; e, major chela, mesial; f, major cheliped, ischium to carpus, mesial; g, minor cheliped, mesial; h, same, lateral; i, fingertips of minor chela, mesial; j, second pereiopod, lateral; k, third pereiopod, lateral; l, same, propodus and dactylus, lateral; m, abdomen, lateral; n, uropod, dorsal; o, telson, dorsal; p,

FIGURE 38. Synalpheus idios (Ríos & Duffy, 2007): a, ovigerous female from Bocas del Toro, Panama (OUMNH.ZC.2012-07- 040); b, male from the same locality (OUMNH.ZC.2012-07-040); c, four individuals (breeding female largest) from a subsocial

FIGURE 51. Presently known geographic ranges of Synalpheus africanus Crosnier & Forest, 1965; S. cf. africanus (eastern and western Atlantic); S. agelas Pequegnat & Heard, 1979; S. anasimus Chace, 1972; S. antillensis Coutière, 1909; S. apioceros Coutière, 1909; S. bocas Anker & Tóth, 2008; S. bousfieldi Chace, 1972; S. brooksi Coutière, 1909; S. carpenteri Macdonald & Duffy, 2006; S. chacei Duffy, 1998; S. congoensis Crosnier & Forest, 1965; S. dardeaui (Ríos & Duffy, 2007); S. dominicensis Armstrong, 1949; S. elizabethae (Ríos & Duffy, 2007); S. filidigitus Armstrong, 1949; S. fritzmuelleri Coutière, 1909; S. goodei