Phimochirus holthuisi ( Provenzano, 1961 ), 2019

Felder, Darryl L., Lemaitre, Rafael & Craig, Catherine, 2019, Two new species of the Phimochirus holthuisi complex from the Gulf of Mexico supported by morphology, color, and genetics (Crustacea: Anomura: Paguridae), Zootaxa 4683 (4), pp. 531-551 : 535-539

Phimochirus holthuisi ( Provenzano, 1961) s.s.

( Figs 1 ; 2A, B ; 3 ; 4 ; Tab. 1 )

Pylopagurus operculatus .— Holthuis, 1959: 157 (in part?), not fig. 31 (= Phimochirus formani nov. sp.); Hazlett, 1966: 86; Rodríguez, 1980: 234. [See Remarks].

Pylopagurus holthuisi Provenzano, 1961: 162 , fig. 3 (type locality: 4.5 miles Southeast of Ram’s Head, St. John, U.S. Virgin Islands, 15–18 m) (in part); Felder, 1973: 30, fig. 13 (in part). [See Remarks].

? Pylopagurus holthuisi .— Coelho & Ramos, 1973: 165; Coelho & Santos, 1980: 143; Coelho & Ramos-Porto, 1986: 42.

Pylopagurus samariensis Sánchez, 1978: 215 , figs 1–5; Sánchez & Campos, 1978: 58, fig. 22.

Phimochirus holthuisi .— McLaughlin, 1981a: 5; McLaughlin, 1981b: 342, figs 4c, 6a–c, 7c (in part); Williams, 1984: 225 (in part), not fig. 161 (= Phimochirus formani nov. sp.); Abele & Kim, 1986: 34, 383 unnumbered fig. c, d (in part); Lemaitre & McLaughlin, 2003: 466, tab. 1 (in part); Mejía-Ortíz et al., 2008: 232; Felder et al., 2009: 1071 (in part); McLaughlin et al., 2010: 34. [See Remarks]; Martínez-Campos et al., 2017: 292 (unnumbered figs a–c), 293, figs 4.75, 6.35 [see Remarks]; Poupin, 2018: 166, fig. 170.

? Phimochirus holthuisi .— Gore & Scotto, 1983: 93, figs 1–6 [larvae]; Hernández-Aguilera et al. 1996: 49; Rieger, 1998: 421; Melo, 1999: 140, figs 81, 82; Martínez-Campos et al., 2012: 248, tab. 4; Rodríguez-Almaraz et al., 2005: 322, not fig. 40 (= Phimochirus formani nov. sp.); Wicksten, 2005: 32, tab. 1; Coelho et al., 2007: 10, tab. 4; Nucci & Melo, 2011: 36 , figs 1J, 2J, 3J; Lemaitre & Tavares, 2015: 454, tab. 1. [See Remarks].

Type material. Holotype: male, sl 4.2 mm ( USNM 107155 ), 4.5 miles Southeast of Ram’s Head, St. John , U. S. Virgin Islands, sand patch on coral rock bottom, 15–18 m, 3 Feb 1961.

Additional material. Southeastern United States. 1 ov female, sl 2.7 mm ( USNM 191093), 91 m, Cape Lookout, North Carolina, Oct 1963 ; 1 ov female, sl 2.4 mm ( USNM 191094) 24° 54’ N, 75° 32’ W, 51 m, off North Carolina, R/ V Silver Bay, sta 2926, 23 Mar 1967 ; 3 males, sl 1.6–2.2 mm, 1 female, sl 2.1 mm, 2 damaged specimens ( USNM 150224), 31° 26.53’ N, 79° 42.22’ W, 252–291 m, off Sapelo Island , Georgia, 6 Aug 1963. Caribbean Sea. 1 male, sl 3.7 mm ( USNM 1111037 ) Jamaica, Drax Cove, St. Ann’s Bay , intertidal/shallow water, 14 May 2005; 1 male, sl 3.3 mm ( USNM 1542650 = ULLZ 3564 ), patch reef behind crest, 2.0 m, Carrie Bow Cay , Belize, 27 Apr 1983; male, 3.3 mm ( USNM 1558313 = ULLZ 16588 ), rubble atop spur on reef front, 4.0 m, Carrie Bow Cay , Belize, 28 Apr 2015 .

Diagnosis. Carapace shield approximately as long as broad; rostrum broadly subtriangular, rounded. Antennular and antennal peduncles at most reaching to distal margin of corneas; antennal flagella with short setae 1 or less flagellar article in length. Right chela with dorsal surface of fixed finger with small, low nearly obsolete tubercles; palm with dorsal surface smooth, lateral and mesial margins sharply defined by weakly crenulate ridge, mesial margin expanded distally and terminating in strong, blunt spiniform angle. Carpus with dorsomesial margin weakly defined by low ridge armed with 1 proximal spine and 2 or 3 small, blunt spines distally. Dactyls of second and third pereopods approximately 1.7 times longer than propodi; dorsomesial margins each with usually 5 corneous spinules, ventromesial margins each with row of usually 5 or 6 corneous spinules. Anterior lobe of sternite between third pereopods subsemiovate, with simple setae; sternite between fourth and fifth pereopods with simple setae. GenBank sequence accession numbers for Belize specimen (USNM 1558313 = ULLZ 16588): (H3) MK830047 ; (12s) MK848210 ; (16s) 848227.

Color. In life ( Fig. 2A, B ), body overall color whitish to pale yellow-brown to rust, with primary patterning of narrow brown lines, carapace overall marked by dark narrow broken longitudinal lines of brown on whitish background; major chela almost entirely white to off white; ocular peduncle with narrow band of brown proximally.

Habitat. Occupying variety of medium sized gastropod shells, including faciolariids, turbinids, and muricids; coral reefs, on coralline sand and rubble substrates of spur and groove reef front to backreef lagoon rubble, sands, and seagrass beds; reef crests and shallow adjacent subtidal waters; inner continental shelf; most commonly 2–18 m, to 91 m off North Carolina, perhaps to 291 m off Georgia.

Distribution. Western Atlantic: East coast of the United States, off North Carolina and Georgia; Caribbean, including Quintana Roo (Cozumel), Belize, Virgin Islands, Jamaica, Guadeloupe, and Colombia; questionably northeastern coast of South America, Suriname to Brazil.

Remarks. The study of numerous specimens considered to be members of the Phimochirus holthuisi complex has shown that, in addition to coloration, a number of subtle yet diagnostic characters can be used to redefine and restrict Provenzano’s (1961) taxon. In the absence of coloration, P. holthuisi s.s. can be differentiated, with caution, from the two new congeneric species described herein by several reliable, albeit subtle, characters that include the shape of the rostrum (rounded in P. holthuisi s.s. vs. acute in the new species); the length of the antennular peduncles relative to the ocular peduncles (not exceeding the corneas when extended in P. holthuisi s.s. vs. clearly exceeding the corneas in the two new species); and the armature of the dactyls of the second and third pereopods (with dorsomesial and ventral rows of 5 spines in P. holthuisi s.s. vs. usually 9 or 10 in the two new species). In general appearance, the habitus of P. holthuisi s.s. is stouter and less armed than in the two new species, having less elongate ocular peduncles, slightly more dilated corneas, a shorter and broader right cheliped, and a nearly smooth dorsal surface on the right palm.

The color pattern described by Provenzano (1961) for the holotype from St. John, U. S. Virgin Islands, rather accurately applies to other shallow water specimens herein assigned to P. holthuisi s.s., especially in terms of the “carapace with symmetrically placed pairs of short longitudinal dark stripes….eyestalks with thin ring of brownish pigment on proximal third….major manus white distally….major carpus diffusely colored with purple”, along with striping on the walking leg articles “imposed on a diffuse yellow background which forms a band around each segment.” Unfortunately, this color description for specimens from the type locality, which was repeated by Williams (1984), has been assumed by subsequent workers to generally apply to materials assigned to this species from throughout its presumed accepted broad range. Despite some similarity in patterning, this previously reported coloration in fact bears little resemblance to striking carapace, ocular peduncle, and appendage colors seen in related species. Given this color information, most of what McLaughlin (1981b) listed from the Gulf of Mexico region as P. holthuisi is not likely that species, as evident from extensive subsequent collections of fresh materials from the same or nearby localities. Unfortunately, external anatomy alone does not, as yet, provide much in the way of definitive non-color characters to underpin this conclusion. The distribution stated above is conservatively limited to those specimens that can for now be assigned with reasonable confidence to P. holthuisi s.s., but the species likely ranges much more widely into shallow tropical waters, perhaps including those of the Bahamas, Florida Keys, southeastern Gulf of Mexico, if not more generally throughout the Caribbean and northeastern South America. Accepted records include a report from Isla Cozumel off the Caribbean coast of Quintana Roo, Mexico by Mejía-Ortíz et al. (2008). Provenzano (1961) considered Holthuis’ (1959) report of Pylopagurus operculatus (Stimpson, 1859) to be synonymous with his new species, P. holthuisi , but concluded that Holthuis’ color account of the Suriname materials appeared to differ from his own Virgin Islands type materials “…probably because of the more faded condition of the Suriname material at the time of its description.” In retrospect, given the significance now placed on coloration, rereading of the Holthuis (1959) account almost certainly excludes its applying to P. holthuisi s.s., and instead suggests that it more closely applies to the first of two new species in the descriptions that follow (see comments for that species). At the time, Holthuis applied it to some materials he had with reservation assigned to Pylopagurus operculatus , which as mentioned, Provenzano (1961) later included in his synonymy for his P. holthuisi despite the color differences he observed. However, it is evident that the Suriname materials came from substantially deeper waters (48–49 m) and different substrate than did the holotype from St. John (15–18 m). Recent collections of fresh material for which color establishes the identity as P. holthuisi s.s., all came from less than 18 m depth, with one from <2 m, and all were taken from the immediate vicinity of coral reefs. It is uncertain as to whether larval descriptions by Gore & Scotto (1983) apply to P. holthuisi s.s., but the striking colors they described for postlarvae are more like those of the closely related congeners.

The precise range of Phimochirus holthuisi s.s. is difficult to determine with certainty, given the paucity of specimens with color information available from large portions of the western Atlantic, including from the east coast of the United States to the Caribbean and northeastern South America to Brazil. This leaves in question the precise identity of paratypes assigned by Provenzano (1961: 161), which include fragments found in fish stomachs at the U.S. Virgin Islands, and two specimens from the coast of Suriname. Based on genetic data, coloration, and the limited usefulness of morphological characters, we can herein confirm distribution of this species to include a northern range on the eastern coast of the United States off North Carolina, Central American Gulf of Mexico and Caribbean coasts from Quintana Roo and Belize, and from the Lesser Antilles in the U.S. Virgin Islands and Guadeloupe (Poupin 1986). Various reports of P. holthuisi from the Gulf of Mexico (Hernández-Aguilera et al. 1996; Rodríguez-Almaraz et al. 2005; Wicksten 2005), the southern Caribbean ( Martínez-Campos et al. 2012), and Brazil (three as Pylopagurus holthuisi: Coelho & Ramos 1973 ; Coelho & Santos 1980; Coelho & Ramos-Porto 1986; and others as Phimochirus holthuisi: Rieger 1998 ; Melo 1999; Nucci & Melo 2011; Martínez-Campos et al. 2012; Lemaitre & Tavares 2015), all must be reevaluated to determine the extent to which they indeed may represent P. holthuisi s.s.

Abele & Kim’s (1986) report of Phimochirus holthuisi is herein considered to in part represent this species as the authors used what is considered the sensu lato concept of this taxon. The report and information on P. holthuisi provided by Martínez-Campos et al. (2017) from the Caribbean coast of Colombia is, regarded to be fully consistent with P. holthuisi s.s. as herein defined. However, these authors reproduced McLaughlin’s (1981: fig. 6) photographs of right chelipeds from three specimens whose identities remain in question, as they were originally published without additional morphological details or locality data for the photographed specimens.

Figures

FIGURE 1. Maximum Likelihood phylogeny inferred in RAxML based on H3 nuclear DNA, 12s mtDNA, and 16s mtDNA. Bootstrap support values (bs) and Bayesian posterior probabilities (bp) with values greater than 50 are displayed above branches at tree nodes with the notation bs/bp. Clades I and II, assigned a priori to Phimochirus cf. holthuisi, are delimited by vertical black bars and correspond to two new species herein described. For branch labels, taxon name is followed by voucher catalog number (see Table 1) and collection locality. Abbreviations: eGMx = eastern Gulf of Mexico, ePac = eastern Pacific, neGMx = northeastern Gulf of Mexico, nwGMx = northwestern Gulf of Mexico, seGMx = southeastern Gulf of Mexico, swGMx = southwestern Gulf of Mexico.

FIGURE 2. Phimochirus holthuisi (Provenzano, 1961) s.s.: A, male, sl 3.3 mm (USNM 1542650 = ULLZ 3564), Belize; B, male, sl 2.9 mm (USNM 1558313 = ULLZ 16588), Belize. Phimochirus formani nov. sp.: C, male paratype, sl 3.1 mm (USNM 1547566 = ULLZ 14352), northeastern Gulf of Mexico; D, male paratype, sl 2.8 mm (USNM 1543170 = ULLZ 7711), northeastern Gulf of Mexico. Phimochirus tunnelli nov. sp.: E, male paratype, sl 4.1 mm (USNM 1545269 = ULLZ 10611), northwestern Gulf of Mexico; F, ov female paratype, sl 3.9 mm (USNM 1541146 = ULLZ 5789), northwestern Gulf of Mexico.

FIGURE 3. Phimochirus holthuisi (Provenzano, 1961) male holotype, sl 4.2 mm (USNM 10515), U. S. Virgin Islands. A, cephalothorax, eyes, and frontal appendages, dorsal surface; B, left second pereopod dactyl, lateral surface; C, left second pereopod dactyl, mesial surface; D, left third pereopod dactyl, lateral surface; E, left third pereopod dactyl, mesial surface; F, telson, dorsal surface. Scale bars = 1.0 mm.

FIGURE 4. Phimochirus holthuisi (Provenzano, 1961) male holotype, sl 4.2 mm (USNM 105155), U. S. Virgin Islands, major cheliped. A, dorsal surface; B, ventral surface; C, mesial surface; D, lateral surface.