Leptalpheus degravei, Scioli & Robles & Felder, 2024

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 : 40-44

Leptalpheus degravei n. sp.

( Figs. 22–24 , 25a–g )

Leptalpheus forceps .— Pachelle et al., 2016: 12 , fig. 6C.— Rosário et al., 2020: 63 , figs. 2–6 [not L. forceps Williams, 1965 ].

Leptalpheus cf. forceps .— Anker, 2008: 788 , figs. 4, 5, 6A, B.— Anker, 2011: 6 , figs. 3A, B; De Grave & Anker, 2017: 12; Chow et al., 2021: fig. 3 [not L. forceps Williams, 1965 ].

Leptalpheus aff. forceps .— Almeida et al., 2012: 15 , figs. 5A–D.

? Leptalpheus forceps .— Christoffersen et al., 1998: 361.—Riul et al., 2007: 7.

Type material. Holotype: male (cl 5.1 mm), ULLZ 18510 [ USNM 1705360 ], Panama, Caribbean coast, Bocas del Toro, Isla Colón, Boca del Drago, at mouth of small creek south of Playa de Estrellas , with Lepidophthalmus richardi (host catalog no. ULLZ 18514 [ USNM 1706529 ]), 0–0.5 m, coll. J.A. Scioli, 03.07.2018 . Paratypes: 1 male (cl 3.6 mm), ULLZ 18511 [ USNM 1705361 ], same locality as holotype, with L. richardi (host catalog no. ULLZ 18515 [ USNM 1706530 ]), coll. J.A. Scioli, 03.07.2018 ; 1 male (cl 3.6 mm), ULLZ 18505 [ USNM 1705355 ], same locality as previous, coll. J.A. Scioli, 18.05.2018 ; 1 ovigerous female (cl 3.6 mm), ULLZ 18507 [ USNM 1705357 ], same locality as previous, coll. J.A. Scioli, 25.05.2018 ; 1 male (cl 3.9 mm), ULLZ 18508 [ USNM 1705358 ], same locality as previous, coll. J.A. Scioli, 09.06.2018 ; 1 female (cl 3.1 mm), ULLZ 18509 [ USNM 1705359 ], same locality as previous, coll. J.A. Scioli, 09.06.2018 ; 1 ovigerous female (cl 4.7 mm), ULLZ 18512 [ USNM 1705362 ], same locality as previous, coll. J.A. Scioli, 03.07.2018 ; 1 female (cl 3.7 mm), ULLZ 18506 [ USNM 1705356 ], same locality as previous, coll. J.A. Scioli, 25.05.2018 ; 1 male (cl 6.0 mm), 1 female (cl 3.2 mm), UF 51702 , same locality as previous, collected from burrow of Lepidophthalmus richardi , 0.5 m, coll. M. Leray & P.P.G. Pachelle, 05.04.2019 ; 1 male (cl 4.8 mm), MNHN-IU-2011-5238, Panama, Caribbean coast, Bocas del Toro, Isla Bastimentos , near main village, sand flat near mangroves, 0–0.2 m, collected from burrow of Lepidophthalmus sp. , coll. A. Anker, 03.05.2007 .

Additional material examined. 1 male (cl 6.1 mm), UCRMZ 2420-01 , Costa Rica, Caribbean coast, Cahuita, Punta Uva, small mangrove river, coarse sand, with Lepidophthalmus richardi (host catalog no. UCRMZ 2420-02 ), coll. A. Anker, I. Wehrtmann & L. Harris, 26.11.2005 .

Description. Frontal margin of carapace broadly rounded, without rostral projection or orbital crests ( Fig. 22a, b ). Carapace glabrous; branchiostegal margin with narrow folded lip; lip broadest posteriorly and gradually tapering in breadth anteriorly; pterygostomian angle rounded, not strongly projecting anteriorly. Telson 2–4 times as long as basal breadth, gradually tapering in breadth throughout length; distal margin arcuate, 0.4–0.6 times as broad as basal margin; dorsal surface with two pairs of spiniform setae; anterior pair inserted at 0.25–0.5 length of telson from base; posterior pair inserted at 0.5–0.7 length of telson from base; posterolateral margins with two pairs of spiniform setae; mesial pair 5–6 times length of lateral pair ( Fig. 22d ).

Antennular peduncles stout; stylocerite somewhat appressed against first article, with subacute tip not reaching distal margin of first antennular article; ventromesial carina bearing subacute, anteriorly directed ventral tooth; second antennular article 2–3 times as long as broad; secondary ramus of lateral flagellum furnished with aesthetascs beginning on article 4–7 ( Fig. 22a–c ). Antennal peduncles subequal in length to antennular peduncles; basicerite bearing broad, subacute ventrolateral tooth, tip of latter not reaching distal margin of stylocerite; scaphocerite broad, oval-shaped, 2–3 times as long as widest breadth, bearing minute, subacute distolateral tooth; carpocerite broad, 2–5 times as long as widest breadth, distally overreaching scaphocerite ( Fig. 22a, b ).

Mouthparts somewhat typical for genus. Mandible with two-segmented palp; molar process small, bearing rows of minute, stiff setae; incisor process bearing five teeth ( Fig. 22e ). Maxillule with bilobed palp ( Fig. 22f ). Maxilla with dorsal endite bearing deep groove; scaphognathite somewhat broad, palp present ( Fig. 22g ). First maxilliped with small palp; exopod with expanded caridean lobe; epipod bilobed ( Fig. 22h ). Second maxilliped with broad, roughly oval-shaped epipod ( Fig. 22i ). Third maxilliped with well-developed arthrobranch; lateral plate slender, elongate, distally overreaching half-length of antepenultimate article, with subacute tip; exopod long, tip reaching or nearly reaching distal margin of antepenultimate article; ultimate article shorter than antepenultimate article, bearing transverse rows of setae on mesial face, with blunt tip ( Fig. 22j ).

Major cheliped slender; ischium bearing subacute subtriangular projection on ventromesial margin; merus slender, 4.5–7 times as long as maximum breadth, with ventral margin concave to accommodate chela when folded; ventrolateral, ventromesial and dorsal margins of merus all lined with minute tubercles throughout length; carpus short, cup-shaped, with two subtriangular projections on distoventral margins; chela slender, tapering in breadth distally, bearing numerous minute tubercles throughout ventral half; adhesive disks absent; fingers 0.2–0.25 palm length; dactylus bearing 4–7 rounded, subacute teeth in proximal two-thirds of length, with distal third strongly curving ventrally to ventrally-pointed subacute tip; pollex bearing 5 rounded subacute teeth in proximal half, distalmost tooth directed anterodorsally, tip slightly curving dorsally; fingers crossing at tips when closed ( Fig. 24 ).

Minor cheliped distinctly smaller than major cheliped; ischium unarmed; merus relatively slender, 5.5–8 times as long as maximum breadth, with concave ventral face to accommodate chela when folded; ventrolateral, ventromesial and dorsal margins smooth; carpus short, cup-shaped; chela slender, 4–6 times as long as maximum height; fingers subequal in length to palm; ventral margin slightly concave at base of fingers; dactylus and pollex both with raised cutting margins bearing minute, subacute medial projections; tips distally crossing when closed ( Fig. 23a, b ).

Second pereopod slender, with merus longer than ischium; carpus subdivided into five articles, with article ratio approximately 9: 2: 3: 2: 6; fingers of chela subequal in length to palm, bearing sparse setal tufts ( Fig. 23c ). Third pereopod laterally compressed; ischium unarmed; merus unarmed, 2.5–4.5 times as long as maximum height; carpus 0.4–0.5 length of merus, bearing distoventral spiniform seta, with distodorsal margin projecting over carpo-propodal articulation; propodus bearing three spiniform setae along ventral margin; dactylus tapering in breadth to acute, simple tip ( Fig. 23d ). Fourth pereopod similar to third, but slightly slenderer ( Fig. 23e ). Fifth pereopod slender, not compressed; ischium short, unarmed; merus slender, 3.5–6 times as long as maximum height; carpus slender, with distodorsal margin slightly projecting; propodus bearing 3–6 transverse rows of grooming setae on lateral face and minute spiniform seta in middle of ventromesial margin; dactylus simple, with acute tip ( Fig. 23f ).

Male second pleopod with long, slender appendix masculina, latter 1.5–2 length of appendix interna, bearing apical setae ( Fig. 22k ). Uropod with bilobed protopod; lateral lobe of protopod with shallow concavity on distal margin; uropodal exopod with truncate distal margin; uropodal endopod with or without distal appendix composed of 1–5 articles ( Fig. 22l ).

Variation. Some, but not all, specimens of L. degravei n. sp. had caudal appendices on the distal margins of the uropodal endopods. Specimens with caudal appendices were larger-bodied (cl 4.7–6.0 mm) than those that lacked them (cl 3.2–3.9 mm).

Color in life. Semitransparent with sparse red chromatophores throughout body, arranged into diffuse transverse rows on dorsal surface of abdomen; walking legs without chromatophores; ovaries and eggs yellow-green ( Figs. 25a–g ; also see Anker 2011: fig. 3A, B; Pachelle et al. 2016: fig. 6C; Rosário et al. 2020: fig. 2).

Etymology. Named in honor of our colleague Sammy De Grave (Oxford University Museum of Natural History, Oxford, UK), for his significant contributions to the biology and taxonomy of caridean shrimps, including those of Caribbean Panama.

Type locality. Isla Colón, Bocas del Toro , Caribbean Coast, Panama.

Distribution. Southwestern Atlantic and Caribbean Sea: Brazil ( Pachelle et al. 2016; Rosário et al. 2020); the Caribbean coasts of Panama ( Anker 2011; De Grave & Anker 2017; present study) and Costa Rica ( Anker 2008; present study).

Ecology. Obligate burrow cohabitant of callichirid ghost shrimps in the genus Lepidophthalmus : associated with L. richardi in Panama and Costa Rica ( Anker 2008; present study), Lepidophthalmus cf. sinuensis Lemaitre & Rodrigues, 1991 in Panama ( Anker 2011; De Grave & Anker 2017), and Lepidophthalmus siriboia Felder & Rodrigues, 1993 in Brazil ( Pachelle et al. 2016; Rosário et al. 2020).

Remarks. Leptalpheus degravei n. sp. is morphologically very similar to L. forceps and was previously reported as L. forceps , L. cf. forceps , and L. aff. forceps ( Anker 2008; 2011; Almeida et al. 2012; Pachelle et al. 2016; De Grave & Anker 2017; Rosário et al. 2020; Chow et al. 2021). Anker (2008) first expressed some doubt that specimens collected in Costa Rica were conspecific with L. forceps described from North Carolina, most notably because of the presence of caudal appendices on the uropodal endopods of Costa Rican specimens, which are absent in the type specimens of L. forceps . The same author continued to report Caribbean specimens as L. cf. forceps in a later study based on Panamanian material, although the Panamanian specimens lacked caudal appendices, on the basis of the proportions of the antennular peduncle resembling the Costa Rican specimens and differing somewhat from the description of L. forceps , as well as the smaller body size of mature adult specimens compared to L. forceps from the Atlantic coast of the USA ( Anker 2011). A specimen reported as L. aff. forceps from Canavieiras, Bahia, Brazil was compared with a specimen from the Atlantic coast of Florida and differs in the dentition of the major cheliped and the proportions of the antennular peduncle ( Almeida et al. 2012). Later records of L. forceps from Brazil included remarks that they more closely resembled specimens of L. cf. forceps from Costa Rica and Panama ( Anker 2008; 2011) than L. forceps from the Atlantic coast of the United States ( Rosário et al. 2020). The morphological variation and taxonomic uncertainty expressed in these records motivated our genetic investigation of material identified as or resembling L. forceps .

Our genetic results clearly delimited specimens from the Caribbean coast of Panama and Brazil ( L. degravei n. sp.) from specimens from the Atlantic coast of the USA and Gulf of Mexico ( L. forceps sensu stricto). Pairwise COI distances were significantly greater between the two species (15.2–16.9% divergence) than within each species (0–0.8% divergence in L. forceps , 0–1.7% divergence in L. degravei n. sp.). The same pattern was true for 16S sequences (0–0.9% intraspecific divergence vs. 3.0–4.8% interspecific divergence) and 12S sequences (0–0.6% intraspecific divergence vs 2.5–3.2% interspecific divergence).

There are few reliable morphological characters that distinguish L. degravei n. sp. from L. forceps . Although some authors noted the presence of caudal appendices on the uropods of L. degravei n. sp. ( Anker 2008; Rosário et al. 2020), which has not previously been reported in L. forceps from the Gulf of Mexico or Atlantic coast of the USA, these structures do sometimes occur in L. forceps sensu stricto (see remarks on L. forceps below). Anker (2008) also noted differences between the relative proportions of the scaphocerite between Costa Rican specimens of L. degravei n. sp. and the description of L. forceps . These proportions, however, are also somewhat variable in L. forceps sensu stricto. Variation in the dentition of the fingers of the major cheliped overlapped between the two species. The only morphological character that consistently separates the two species is the proportions of the antennular peduncle: the second antennular article is shorter in L. degravei n. sp. (2–3 times as long as broad) than in L. forceps (3.5–6 times as long as broad) (compare Fig. 22a vs. Fig. 21i, j ). L. degravei n. sp. also appears to be a smaller-bodied species, as specimens of L. degravei (cl 3.1–6.1 mm) did not reach as large body sizes as L. forceps (cl 3.0– 10.5 mm). Leptalpheus degravei n. sp. can be distinguished from all species of Leptalpheus and related genera other than L. forceps , including L. ankeri n. sp., by the dentition pattern of the fingers of the major cheliped, which bear series of subacute teeth proximally and gape distally.

Based upon our results, we consider the identity of all records of L. forceps from the Caribbean Sea as L. degravei n. sp. We were able to confirm that the material reported by Pachelle et al. (2016) as L. forceps from Ceará, Brazil, is L. degravei n. sp., as the genetic sequence from this material published by Chow et al. (2021) matches sequences of L. degravei n. sp. Furthermore, we can say with confidence that specimens reported as L. forceps from Bahia and Pará, Brazil, are in fact L. degravei n. sp. based on the proportions of the antennular peduncle in the accompanying illustrations (see Almeida et al. 2012: fig. 5A; Rosário et al. 2020: fig. 3A). Records from Sergipe ( Christoffersen 1998) and Paraíba ( Riul et al. 2008), Brazil, are likely also L. degravei n. sp., but as there are no accompanying illustrations or genetic data, we cannot ascertain their identity beyond reasonable doubt.

Figures

FIGURE 21. Leptalpheus azuero Anker, 2011 (a–e), Leptalpheus felderi Anker, Vera Caripe & Lira, 2006 (f–h), and Leptalpheus forceps Williams, 1965 (i–k). Leptalpheus azuero: ovigerous female (cl 4.7 mm), ULLZ 11823 [USNM 1545912], from Las Peñitas, Nicaragua (a, b) and ovigerous female (cl 6.4 mm), ULLZ 5917 [USNM 1541195], from Estero Aserradores, Nicaragua (c–e): a, major chela, lateral; b, same, mesial; c, major chela, dorsolateral; d, same, dactylus and pollex, dorsolateral; e, same, fingers opened, lateral. Leptalpheus felderi: male (cl 8.5 mm), UF 48038, from Wachapreague, Virginia, USA: f, major chela, mesial; g, same, dorsolateral; h, same, dactylus and pollex, dorsolateral. Leptalpheus forceps: male (cl 8.8 mm) (i), female (cl 5.3 mm) (j), ULLZ 18053 [USNM 1706385], from Bay St. Louis, Mississippi, USA and female (cl 6.0 mm) (k), ULLZ 5593 [USNM 1541048], from Nuevo Campechito, Mexico: i, frontal margin, dorsal; j, same; k, uropod with caudal appendix, dorsal.

FIGURE 22. Leptalpheus degravei n. sp., holotype male (cl 5.1 mm), ULLZ 18510 [USNM 1705360], from Bocas del Toro, Panama: a, frontal margin, dorsal; b, same, lateral; c, ventromesial carina of first antennular article, lateral; d, telson, dorsal; e, mandible, mesial; f, maxillule, mesial; g, maxilla, lateral; h, first maxilliped, lateral; i, second maxilliped, lateral; j, third maxilliped, lateral; k, second pleopod with appendix interna and appendix masculina, mesial; l, uropod, dorsal.

FIGURE 23. Leptalpheus degravei n. sp., holotype male (cl 5.1 mm), ULLZ 18510 [USNM 1705360], from Bocas del Toro, Panama: a, minor cheliped, ventrolateral; same, chela, ventrolateral; c, second pereopod, lateral; d, third pereopod, lateral; e, fourth pereopod, lateral; f, fifth pereopod, lateral.

FIGURE 24. Leptalpheus degravei n. sp., holotype male (cl 5.1 mm), ULLZ 18510 [USNM 1705360], from Bocas del Toro, Panama: a, major cheliped, dorsolateral; b, same, ventromesial, c, same, dactylus and pollex, lateral; d, same, fingers opened, mesial.

FIGURE 25. Color patterns of Leptalpheus degravei n. sp. and Leptalpheus forceps Williams, 1965. Leptalpheus degravei n. sp.: a, paratype male (cl 3.6 mm), ULLZ 18511 [USNM 1705361], from Bocas del Toro, Panama, dorsal; b, same, lateral; c, holotype male (cl 5.1 mm), ULLZ 18510 [USNM 1705360], from Bocas del Toro, Panama, dorsal; d, same, lateral; e, paratype female (cl 3.7 mm), ULLZ 18506 [USNM 1705356], from Bocas del Toro, Panama, dorsal; f, same, lateral; g, paratype ovigerous female (cl 4.7 mm), ULLZ 18512 [USNM 1705362], from Bocas del Toro, Panama, lateral. Leptalpheus forceps: h, ovigerous female (cl 5.9 mm), ULLZ 5818 [USNM 1541154], from Ft. Pierce, Florida, USA, lateral. Photographs by the first author (a–g) and third author (h).