Leptalpheus axianassae Dworschak & Coelho, 1999

Scioli, Justin A., Robles, Rafael & Felder, Darryl L., 2024, New species and records of the symbiotic shrimp genus Leptalpheus Williams, 1965, with notes on Fenneralpheus Felder & Manning, 1986, and preliminary molecular analysis of phylogenetic relationships (Crustacea: Decapoda: Alpheidae), Zootaxa 5466 (1), pp. 1-72 : 30-33

Leptalpheus axianassae Dworschak & Coelho, 1999

( Figs. 17–19 , 20d–h )

Leptalpheus axianassae Dworschak & Coelho, 1999: 477 , figs. 1–30.— Schmidt de Melo et al.,

2003: 425.— Almeida et al., 2012: 15, fig. 4.— Almeida et al., 2013: 1399.— Anker & Lazarus, 2015: fig. 8.— Pachelle et al., 2016: 10, figs. 6A, B.— Almeida et al., 2018: 345, fig. 2C.— Vera Caripe et al., 2021: 182.

Leptalpheus petronii Ramos-Porto & Souza, 1994: 22 ; De Grave & Fransen, 2011: 475 (listed as nomen dubium).

“ Leptalpheus ” axianassae . — Felder et al., 2003: table 3.— Robles, 2005: chapter 3, table 1.

“ Leptalpheus ” sp. 5.— Robles, 2005: chapter 3, table 1.

Material examined. Brazil: 1 male (cl 5.7 mm), ULLZ 18186 [ USNM 1706456 ], São Paulo, São Sebastião, Araçá mangroves, coll. F.L. Mantelatto, 10.12.2000 ; 1 female (cl 7.0 mm), ULLZ 5913 [ USNM 1541191 ], São Paulo, São Sebastião, Praia do Araçá , with Axianassa australis (host catalog no. ULLZ 5912 [ USNM 1541190 ]), coll. R. Robles et al., 09.10.2000 ; 1 male (cl 5.1 mm), ULLZ 5923 [ USNM 1541201 ], same locality as previous, coll. R. Robles et al., 09.10.2000 ; 1 male (cl 5.9 mm), 1 ovigerous female (cl 6.9 mm), ULLZ 5925 [ USNM 1541203 ], same locality as previous, with A. australis (host catalog no. ULLZ 5924 [ USNM 1541202 ]), coll. R. Robles et al., 10.10.2000 . Colombia: 1 male (cl 6.8 mm), ULLZ 18181 [ USNM 1706451 ], Bahía de Cispatá , Punta Calixto, coll. D.L. Felder et al., 05.03.1997 ; 2 males (cl 3.0, 5.3 mm), 1 ovigerous female (cl 6.8 mm), ULLZ 18184 [ USNM 1706454 ], Punta Calixto, Río Sinú estuary, coll. R. Lemaitre, D.L. Felder, et al., 06.03.1997 ; 1 male (cl 6.7 mm), ULLZ 18185 [ USNM 1706455 ], Bahía de Cispatá, Ciénaga de Soledad , coll. D.L. Felder, R. Lemaitre & S. Nates, 08.01.1995 . Panama: 1 male (cl 7.1 mm), UF 51713 , Bocas del Toro , Isla Colón, near Smithsonian Tropical Research Institute docks, between mangrove and seagrass meadow, coll. P.P.G. Pachelle, 04.04.2019 . Mexico: 1 male (cl 6.9 mm) , 1 female (cl 5.4 mm), ULLZ 18182 [ USNM 1706452 ], Tabasco, Puerto Ceiba , coll. D.L. Felder & R. Robles, 05.07.2002 ; 1 ovigerous female (cl 5.9 mm), ULLZ 5909 [ USNM 1541187 ], same locality as previous, with Axianassa sp. (host catalog no. ULLZ 5908 [ USNM 1541186 ]), coll. D.L. Felder & R. Robles, 05.07.2002 ; 1 male (cl 5.7 mm), ULLZ 5911 [ USNM 1541189 ], same locality as previous, with Axianassa sp. (host catalog no. ULLZ 5910 [ USNM 1541188 ]), coll. D.L. Felder & R. Robles, 05.07.2002 ; 1 male (cl 6.8 mm), ULLZ 18112 [ USNM 1706391 ], same locality as previous, with A. australis (host catalog no. ULLZ 15118 [ USNM 1548144 ]), coll. D.L. Felder & R. Robles, 05.07.2002 ; 1 male (cl 7.0 mm), 2 females (cl 6.2, 7.6 mm), ULLZ 18183 [ USNM 1706453 ], Tabasco, tidal lagoon on highway 187, coll. D.L. Felder, J. Staton, et al., 27.03.1991 ; 1 male (cl 4.3 mm), 1 female (cl 4.4 mm), ULLZ 18054 [ USNM 1706386 ], Veracruz, Laguna la Mancha , with A. australis (host catalog no. ULLZ 18056 [ USNM 1706387 ]), coll. D.L. Felder & R. Robles, 03.07.2002 ; 2 males (cl 5.4, 5.6 mm), 2 females (cl 5.8, 7.0 mm), ULLZ 18058 [ USNM 1706389 ], same locality as previous, coll. D.L. Felder & R. Robles, 02.07.2002 ; 2 females (cl 5.2, 5.8 mm), ULLZ 18111 [ USNM 1706390 ], same locality as previous, with Axianassa sp. (host catalog no. ULLZ 14736 [ USNM 1548489 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 female (cl 5.2 mm), ULLZ 18116 [ USNM 1706393 ], same locality as previous, with A. australis (host catalog no. ULLZ 18115 [ USNM 1706392 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 male (cl 5.9 mm), ULLZ 18117 [ USNM 1706394 ], same locality as previous, with A. australis (host catalog no. ULLZ 18118 [ USNM 1706395 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 male (cl 6.2 mm), ULLZ 18122 [ USNM 1706397 ], same locality as previous, with A. australis (host catalog no. ULLZ 15110 [ USNM 1548131 ]), coll. D.L. Felder & R. Robles, 03.07.2002 ; 1 male (cl 6.7 mm), 1 female (cl 6.0 mm), ULLZ 18124 [ USNM 1706399 ], same locality as previous, coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 male (cl 4.8 mm), 1 ovigerous female (cl 4.8 mm), ULLZ 18129 [ USNM 1706402 ], same locality as previous, with A. australis (host catalog no. ULLZ 18130 [ USNM 1706403 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 male (cl 4.6 mm), ULLZ 18131 [ USNM 1706404 ], same locality as previous, with A. australis (host catalog no. ULLZ 18132 [ USNM 1706405 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 male (cl 6.1 mm), ULLZ 18133 [ USNM 1706406 ], same locality as previous, with A. australis (host catalog no. ULLZ 14739 [ USNM 1548493 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 2 males (cl 5.0, 6.9 mm), 1 female (cl 6.5 mm), ULLZ 18134 [ USNM 1706407 ], same locality as previous, with A. australis (host catalog no. ULLZ 18135 [ USNM 1706408 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 male (cl 4.7 mm), 1 female (cl 4.6 mm), ULLZ 18136 [ USNM 1706409 ], same locality as previous, with A. australis (host catalog no. ULLZ 14732 [ USNM 1548091 ]), coll. D.L. Felder & R. Robles, 03.07.2002 ; 1 male (cl 5.5 mm), 1 ovigerous female (cl 5.2 mm), ULLZ 18146 [ USNM 1706418 ], same locality as previous, with A. australis (host catalog no. ULLZ 18145 [ USNM 1706417 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 female (cl 6.6 mm), ULLZ 18148 [ USNM 1706420 ], same locality as previous, with A. australis (host catalog no. ULLZ 18147 [ USNM 1706419 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 male (cl 6.7 mm), ULLZ 18150 [ USNM 1706422 ], same locality as previous, with A. australis (host catalog no. ULLZ 18149 [ USNM 1706421 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 2 males (cl 6.2, 7.2 mm), 1 female (cl 6.3 mm), ULLZ 18152 [ USNM 1706424 ], same locality as previous, with A. australis (host catalog no. ULLZ 18151 [ USNM 1706423 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 female (cl 6.4 mm), ULLZ 18154 [ USNM 1706426 ], same locality as previous, with A. australis (host catalog no. ULLZ 18153 [ USNM 1706425 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 male (cl 7.2 m), ULLZ 18155 [ USNM 1706427 ], same locality as previous, with A. australis (host catalog no. ULLZ 14731 [ USNM 1548089 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 male (cl 6.5 mm), 1 female (cl 6.0 mm), ULLZ 18156 [ USNM 1706428 ], with A. australis (host catalog no. ULLZ 15114 [ USNM 1548138 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 female (cl 4.1 mm), ULLZ 18158 [ USNM 1706430 ], same locality as previous, with A. australis (host catalog no. ULLZ 18157 [ USNM 1706429 ]), coll. D.L. Felder & R. Robles, 03.07.2002 ; 1 male (cl 6.2 mm), ULLZ 18160 [ USNM 1706432 ], same locality as previous, with A. australis (host catalog no. ULLZ 18159 [ USNM 1706431 ]), coll. D.L. Felder & R. Robles, 03.07.2002 ; 1 male (cl 3.7 mm), ULLZ 18162 [ USNM 1706434 ], same locality as previous, with A. australis (host catalog no. ULLZ 18161 [ USNM 1706433 ]), coll. D.L. Felder & R. Robles, 03.07.2002 ; 1 male (cl 4.1 mm), ULLZ 18163 [ USNM 1706435 ], same locality as previous, with A. australis (host catalog no. ULLZ 14794 [ USNM 1706378 ]), coll. D.L. Felder & R. Robles, 03.07.2002 ; 1 male (cl 5.3 mm), 1 female (cl 4.8 mm), ULLZ 18165 [ USNM 1706437 ], same locality as previous, with A. australis (host catalog no. ULLZ 18164 [ USNM 1706436 ]), coll. D.L. Felder & R. Robles, 03.07.2002 ; 1 female (cl 5.0 mm), ULLZ 18167 [ USNM 1706439 ], same locality as previous, with A. australis (host catalog no. ULLZ 18166 [ USNM 1706438 ]), coll. D.L. Felder & R. Robles, 03.07.2002 ; 1 male (cl 6.2 mm), ULLZ 5927 [ USNM 1541205 ], same locality as previous, with A. australis (host catalog no. ULLZ 5926 [ USNM 1541204 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 male (cl 7.3 mm), 1 female (cl 8.4 mm), ULLZ 5929 [ USNM 1541207 ], same locality as previous, with A. australis (host catalog no. ULLZ 5928 [ USNM 1541206 ]), coll. D.L. Felder & R. Robles, 02.07.2002 ; 1 female (cl 6.2 mm), ULLZ 15018 [ USNM 1548158 ], Tamaulipas, Barra del Tordo , coll. D.L. Felder, 20.04.1998 . USA: 2 females (cl 3.5, 9.9 mm), ULLZ 18121 [ USNM 1706396 ], Texas, Port Isabel , mud flats near Tarpon Hole, coll. D.L. Felder et al., 11.10.2002 ; 1 male (cl 3.8 mm), 1 female (cl 4.6 mm), ULLZ 18140 [ USNM 1706412 ], same locality as previous, with A. australis (host catalog no. ULLZ 18139 [ USNM 1706411 ]), coll. D.L. Felder et al., 11.10.2002 ; 1 male (cl 3.1 mm), ULLZ 18142 [ USNM 1706414 ], same locality as previous, with A. australis (host catalog no. ULLZ 18141 [ USNM 1706413 ]), coll. D.L. Felder et al., 11.10.2002 ; 1 female (cl 3.6 mm), ULLZ 18144 [ USNM 1706416 ], same locality as previous, with A. australis (host catalog no. ULLZ 18143 [ USNM 1706415 ]), coll. D.L. Felder et al., 11.10.2002 ; 1 male (cl 6.8 mm), 1 female (cl 6.4 mm), ULLZ 18180 [ USNM 1706450 ], Texas, Cameron county, Boca Chica , black mangrove channel, with A. australis (host catalog no. ULLZ 18179 [ USNM 1706449 ]), coll. D.L. Felder & L. Bilodeau, 29.02.2000 ; 2 males (cl 4.4, 5.5 mm), ULLZ 11839 [ USNM 1545922 ], Florida, Ft. Pierce, Indian River Lagoon , Little Jim Island , coll. D.L. Felder & R. Robles, 27.07.2001 ; 1 male (cl 7.8 mm), ULLZ 18125 [ USNM 1706400 ], same locality as previous, collected from resin cast of host burrow, coll. D.L. Felder, 03.07.1997 ; 1 male (cl 7.0 mm), 1 female (cl 7.9 mm), ULLZ 18126 [ USNM 1706401 ], same locality as previous, with Axianassa sp. (host catalog no. ULLZ 10396 [ USNM 1545016 ]), coll. D.L. Felder, 31.07.1996 ; 2 males (cl 6.9, 7.7 mm), 1 female (cl 8.9 mm), ULLZ 18137 [ USNM 1706410 ], same locality as previous, coll. D.L. Felder, 23.07.2004 ; 3 males (cl 5.0– 8.2 mm), 2 ovigerous females (cl 5.2, 8.0 mm), ULLZ 18170 [ USNM 1706440 ], same locality as previous, from burrow of Axianassa sp. , coll. D.L. Felder, 27.07.1999 ; 1 male (cl 6.7 mm), ULLZ 18171 [ USNM 1706441 ], same locality as previous, coll. D.L. Felder, 23.07.2004 ; 1 male (cl 6.2 mm), 2 females (cl 8.2, 8.9 mm), ULLZ 18172 [ USNM 1706442 ], same locality as previous, coll. D.L. Felder, 23.07.2004 ; 1 male (cl 7.3 mm), 1 ovigerous female (cl 8.4 mm), ULLZ 18173 [ USNM 1706443 ], same locality as previous, from burrow of Axianassa sp. , coll. D.L. Felder, 31.07.1996 ; 2 males (cl 7.8, 10.0 mm), 1 female (cl 8.0 mm), ULLZ 18174 [ USNM 1706444 ], same locality as previous, coll. D.L. Felder, 27.07.1995 ; 2 males (cl 5.0, 9.4 mm), 2 ovigerous females (cl 5.7, 7.6 mm), ULLZ 18175 [ USNM 1706445 ], same locality as previous, with Axianassa sp. (host catalog no. ULLZ 18705 [ USNM 1706531 ]), coll. D.L. Felder & W. Lee, 24.07.1995 ; 1 ovigerous female (cl 9.2 mm), ULLZ 18176 [ USNM 1706446 ], same locality as previous, with Axianassa sp. , coll. D.L. Felder, 27.07.1995 ; 1 ovigerous female (cl 7.5 mm), ULLZ 18178 [ USNM 1706448 ], same locality as previous, with A. australis (host catalog no. ULLZ 18177 [ USNM 1706447 ]), coll. D.L. Felder & W. Lee, 24.07.1995 ; 3 males (cl 7.0– 7.4 mm), 1 female (cl 8.4 mm), ULLZ 5919 [ USNM 1541197 ], same locality as previous, from burrow of Axianassa sp. , coll. D.L. Felder, collection date not recorded ; 3 males (cl 5.8–7.5 mm), 2 non-ovigerous females (cl 8.0, 8.1 mm), 1 ovigerous female (cl 5.7 mm), ULLZ 5920 [ USNM 1541198 ], same locality as previous, from burrow of Axianassa sp. , coll. D.L. Felder, 28.07.1997 ; 2 males (cl 6.4, 6.6 mm), 1 female (cl 8.1 mm), ULLZ 5921 [ USNM 1541199 ], same locality as previous, from burrow of Axianassa sp. , coll. D.L. Felder, 27.07.1999 ; 1 male (cl 7.6 mm), 3 non-ovigerous females (cl 5.0– 8.3 mm), 2 ovigerous females (cl 6.8, 8.1 mm), ULLZ 18123 [ USNM 1706398 ], Florida, Ft. Pierce, Indian River Lagoon, near Little Jim Island , north of inlet, coll. D.L. Felder, H. Bracken & R. Robles, 26.07.2005 ; 1 male (cl 5.0 mm), ULLZ 5907 [ USNM 1541185 ], Florida, Ft. Pierce, Indian River Lagoon , Coon Island , mangrove, from burrow of Axianassa sp. , coll. D.L. Felder, 30.07.2002 .

Description. See Dworschak & Coelho (1999).

Color in life. Body largely semitransparent, speckled throughout with red chromatophores; chromatophores densest on anterior margins of abdominal somites, dorsal surface of carapace, antennal and antennular peduncles, chelipeds, and telson; major chela hyaline-white; walking legs semitransparent, without chromatophores; ovaries and eggs yellow-green ( Figs. 20d–h ; also see Pachelle et al., 2016: fig. 6A, B; Almeida et al., 2018: fig. 2C). Specimens with expanded chromatophores appear generally reddish except for distal portions of pereopods ( Figs. 20f–h ).

Type locality. Praia do Araçá , São Sebastião, São Paulo, Brazil .

Distribution. Throughout the western Atlantic region, including the Gulf of Mexico and Caribbean Sea: Brazil ( Dworschak & Coelho 1999; Almeida et al. 2012; 2013; 2018; Anker & Lazarus 2015; Botter-Carvalho et al. 2015; Pachelle et al. 2016; present study); Caribbean coasts of Venezuela ( Vera Caripe et al. 2021), Colombia (present study), and Panama (present study); Atlantic coast of Florida, USA ( Felder et al. 2003; present study); Gulf coasts of Texas, USA (present study), and Tabasco, Veracruz, and Tamaulipas, Mexico (present study).

Ecology. Obligate burrow cohabitant of the laomediid mudshrimp Axianassa australis Rodrigues & Shimizu, 1992 ( Dworschak & Coelho 1999; Felder et al. 2003; Botter-Carvalho et al. 2015; present study).

Remarks. The numerous records of L. axianassae in association with Axianassa australis listed and cited above strongly suggest that this species is an ecological specialist that is only associated with one host species. A. australis has a very broad geographic range that extends from Brazil to Florida, as well as south Texas and the southwestern Gulf of Mexico ( Felder 2001). With the extension of the range of L. axianassae to the Gulf of Mexico, this species has now been reported from all the major biogeographic regions in which A. australis occurs. It appears to have the broadest geographic range of any described species in the LGC, which is unsurprising given that its host has an unusually broad range for a mudshrimp species ( Felder 2001). Our genetic results supported the hypothesis that L. axianassae is a single, broadly distributed species, as genetic distances between specimens collected in Brazil, Panama, and the Atlantic coast of Florida were consistent with intraspecific distances in other species of Leptalpheus (16S pairwise distances = 0.2–1.1%). We also found no major morphological distinction between specimens of L. axianassae from the Atlantic coast of Florida, Gulf of Mexico, or Caribbean Sea with those from Brazil (compare L. axianassae from Florida, Figs. 17–19 vs. L. axianassae from Brazil, Dworschak & Coelho 1999: figs. 1–30).

The species Leptalpheus petronii Ramos-Porto & Souza, 1994 is herein listed as a junior synonym of L. axianassae , following the rationale of Anker et al. (2006b). The description of this species, which was published as a conference abstract without illustrations or diagnoses, is not in accordance with the criteria for legitimate descriptions outlined by the International Code of Zoological Nomenclature (ICZN), and therefore nominal priority is given to L. axianassae despite its description being published later.

Figures

FIGURE 17. Leptalpheus axianassae Dworschak & Coelho, 1999, male (cl 10.0 mm), ULLZ 18174 [USNM 1706444], from Ft. Pierce, Florida, USA: a, habitus, lateral; b, frontal margin, dorsal; c, same, lateral; d, antennular peduncle, ventral; e, antennal peduncle, ventral; f, mandible, mesial.

FIGURE 18. Leptalpheus axianassae Dworschak & Coelho, 1999, male (cl 10.0 mm), ULLZ 18174 [USNM 1706444], from Ft. Pierce, Florida, USA: a, second pereopod, lateral; b, third pereopod, lateral; c, fourth pereopod, lateral; d, fifth pereopod, lateral; e, first pleopod, mesial; f, second pleopod with appendix masculina and appendix interna, mesial; g, telson and uropods, lateral; h, same, dorsal.

FIGURE 19. Leptalpheus axianassae Dworschak & Coelho, 1999, male (cl 10.0 mm) (a–f, h, i) and female (cl 8.0 mm) (g), ULLZ 18174 [USNM 1706444], from Ft. Pierce, Florida, USA: a, maxillule, lateral; b, maxilla, lateral; c, first maxilliped, lateral; d, second maxilliped, lateral; e, third maxilliped, lateral; f, major cheliped, lateral; g, same, mesial; h, minor cheliped, lateral; i, same, chela, ventrolateral.

FIGURE 20. Color patterns of the Leptalpheus axianassae species group. Leptalpheus hendrickxi Anker, 2011: a, male (cl 7.7 mm), ULLZ 5810 [USNM 1541151], from Paso Caballos, Nicaragua, lateral; b, female (cl 9.4 mm), ULLZ 6036 [USNM 1541281], from Las Peñitas, Nicaragua, lateral. Leptalpheus corderoae Salgado-Barragán et al., 2014: c, female (cl 8.3 mm), ULLZ 18237 [USNM 1706503], from Las Peñitas, Nicaragua, lateral. Leptalpheus axianassae Dworschak & Coelho, 1999: d, ovigerous female (cl 8.4 mm), ULLZ 18173 [USNM 1706443], from Ft. Pierce, Florida, USA, lateral; e, male (cl 7.3 mm), ULLZ 18173 [USNM 1706443], from Ft. Pierce, Florida, USA, lateral; f, male (cl 7.1 mm), UF 51713, from Bocas del Toro, Panama, lateral; g, same, dorsal; h, same, close-up of major chela, lateral. Photographs by the third author (a–e) and Paulo P.G. Pachelle (f–h).