Biffarius botterae, Hernáez & Miranda & Tavares, 2020

Hernáez, Patricio, Miranda, Marcel S. & Tavares, Marcos, 2020, A new species of Biffarius Manning & Felder, 1991 (Decapoda: Axiidea Callianassidae) from the intertidal coast of northeastern Brazil, Zootaxa 4759 (4), pp. 575-583 : 576-582

Biffarius botterae sp. nov.

( Figs. 1–3 )

Type material — Holotype, male, cl 4.6 mm, tl 20.3 mm, pereiopods detached, Praia de Tutóia , 02°45’40”S, 42°15’45”W, lower intertidal, Tutóia, Maranhão, Brazil, P. Hernáez coll., 7 July 2017, MZUSP 39002 . Paratypes: 2 males, cl: 4.0– 4.6 mm and 1 female, cl 4.1, same locality data as holotype, MZUSP 40375 ; 1 male, cl 5.6 mm, 1 female, cl 5.0 mm, mangrove, 04°40’55”S, 37°21’30”W, lower intertidal, Icapuí , Ceará, P. Hernáez coll., 16 July 2016, MZUSP 40376 .

Comparative material examined— Biffarius biformis ( Biffar, 1971) : holotype, male, tl 24 mm, mouth of Doboy Sound, lower intertidal, south end of Sapelo Island, McIntosh County, Georgia, USA, R. W. Heard coll., 1 June 1969, USNM 135052 . Paratypes: 18 males, tl: 15–29 mm and 14 females, tl: 20–26.5 mm, same locality data as holotype, USNM 135053 ; 4 males, tl: 27–32 mm and ovigerous female, tl 26 mm, same locality as holotype, R . W. Heard coll., July 1969, USNM 135054 . Biffarius delicatulus Rodrigues & Manning, 1992 : holotype, male, cl 6.8 mm, Praia do Araçá , 23°40’S, 45°20’W, São Sebastião, São Paulo, Brazil, S.A. Rodrigues coll., 18 May 1985, MZUSP 10582 ; male, cl 3.1 mm, Praia do Tremembé , 04°44’05”S, 37°17’24”W, Icapuí, Ceará, P. Pachelle coll., 19 August 2012, MZUSP 27620 ; 3 males, cl: 4.5—5.0 mm and 2 females, cl: 4.4—4.7 mm, Praia da Casa Caiada , 07°58’59.8”S, 34°50’06”W, Olinda, Pernambuco, M. Botter-Carvalho coll., 27 February 2013, CRUSTA 130001 .

Diagnosis —Carapace lateral margin emarginate on central part, rostrum short and triangular, distinct lateral projection absent. Antennular peduncle shorter than antennal peduncle; penultimate antennal article 1.2 times longer than distal article. Crista dentata absent. Male major cheliped massive, ischium with row of well spaced acute teeth from midlength to articulation with basis. Male pleopod 2 present. Uropodal endopod widening distally, inner lateral margin convex. Anterodorsal plate of uropodal exopod absent. Posterior margin of telson convex.

Description —Shrimp small in size, carapace length of adults from 4 to 5.6 mm. Carapace smooth, dorsal oval, cervical groove and linea thalassinica distinct, cardiac prominence absent, lateral margin emarginate on central part; rostrum short and triangular, lateral frontal projections absent ( Fig. 1A, B ). Branchial formula as shown in Table I.

Ocular peduncle ( Fig. 1B ) subtriangular, distal margin with triangular projection, exceeding first article of antennular peduncle (A1), cornea subterminal, darkly pigmented. A1 peduncle shorter than A2 peduncle; lower margin of antennular peduncle articles 2 and 3 setose, distal article about twice as long as penultimate article; flagellum dorsal ramus slightly shorter than ventral ramus, with 16-23 smaller articles vs 14-20 larger articles, both ramus with sparse, long tufts of setae. A2 peduncle with penultimate article 1.2 times longer than distal article; basal article with excretory pore produced laterally; second article with tuft of setae distolaterally; third article narrower than second; fourth article with sparse and long setae, fifth article with tuft of long setae distolaterally, scaphocerite reduced.

Mandible ( Fig. 1C ) with molar process developed, consisting of one calcareous acute tooth projected laterally; incisor process well calcified, distal margin armed with seven acute corneous teeth; palp trisegmented, terminal article longest, external surface covered with dense, short, stiff setae. Maxillulle ( Fig. 1D ) with bi-articulated, narrow palp (endopod), terminal article deflected proximally at articulation; proximal endite kidney-shaped, external margin with row of short, stiff setae; distal endite elongate, hatchet-shaped, distal margin with short, sharp stiff setae. Maxilla ( Fig. 1E ) foliaceous; proximal and distal endite deeply bilobed, external surface of both heavily setose; endopod narrowing terminally, slightly flexed distally; exopod forming large, broad, scaphognathite.

Maxilliped 1 ( Fig. 1F ) foliaceous; proximal endite reduced, rounded, setose distally; distal endite developed, subrectanglar, external surface heavily setose; endopod subrectanglar, reduced; large exopod, marginally setose, with marked notch on mesial margin, setose marginally; epipod large, posterior lobe broad, anterior end narrowing terminally. Maxilliped 2 ( Fig. 1G ) with long, narrow endopod; dactylus short, less than half as long as propodus, with terminal brush of short, thick, stiff setae; propodus less than half of merus, slightly arcuate; carpus subtriangular, short; endopod merus more than five times as long as broad, flexor margin with dense fringe of long, simple setae; exopod rounded, heavily reduced. Maxilliped 3 ( Fig. 1H ) without exopod and epipod; ischium-merus operculiform, length about 1.2 times its width, marginally setose; ischium without crest or teeth on mesial surface, 1.3 times length of merus; distal margin of merus projecting beyond carpo-meral articulation; carpus as long as propodus; dactylus digitiform, slightly shorter than propodus.

Chelipeds (pereopods 1) greatly unequal and dissimilar in male but similar in female. Male major cheliped ( Fig. 2A ) heavy and strongly calcified; ventral margin of ischium with row of well spaced acute teeth from midlength to articulation with basis, dorsal margin arcuate; merus with strong hook proximo-ventrally, margin of hook strongly serrate with sparse setae, acute distally, remainder of ventral margin with irregular rounded denticles, dorsal margin smooth with sparse setae; carpus length about 1.5 times than half of palm, carpus about 1.3 times longer than width, dorsal margin straight, unarmed, ventral margin smooth with sparse setae; palm rectangular, longer than width, dorsal and ventral margin smooth, with sparse setae on ventral margin; fixed finger arcuate, cutting edge unarmed; dactylus slightly arcuate with tip curved downward, slightly longer than fixed finger, shorter than palm, cutting edge with large rounded tooth proximally and distally with one small blunt tooth. Male minor cheliped ( Fig. 2B ) slender; ischium longer than merus, ventral margin with row of well spaced acute teeth from midlength to articulation with basis, dorsal margin slightly arcuate; merus with hook proximo-ventrally, proportionally smaller from that of major cheliped, margin of hook slightly serrate, acute distally, remainder of ventral margin with small denticles, dorsal margin smooth; carpus longest, with dorsal margin straight, unarmed, ventral margin keel-like, with spaced and short setae; length of palm about 1.4 times its width, dorsal margin unarmed, ventral margin with spaced tufts of setae; fixed finger about as long as dactylus, cutting edge weakly dentate, tuft of setae distally; dactylus strongly arcuate, unarmed, tuft of setae on tip.

Female chelipeds slender, both less heavy than in male. Female left cheliped ( Fig. 2C, D ) differing from right cheliped as follows: presence of meral spine on ventral margin; cutting edge of fixed finger with blunt teeth on central part. Ischium generally longer than merus, margins unarmed; length of merus about twice its width, ventral margin straight, sparse short setae, dorsal margin slightly rounded, unarmed; carpus longest, about 2 times longer than palm, ventral margin with spaced setae; ventral margin of propodus with tufts of spaced setae, palm slightly longer than fixed finger; dactylus slightly longer than fixed finger.

Pereopod 2 ( Fig. 2E ) chelate, densely setose ventrally; length of ischium about 1.4 times its width; merus more than twice as long as carpus, proximo-ventral expansion with dense long setae, dorsal margin slightly straight; carpus subtriangular, widening distally, dorsal and ventral margin with well spaced tufts of setae; palm shorter than carpus, fixed finger subtriangular, cutting edge micropectinate; dactylus lanceolate, densely setose dorsally. Pereopod 3 ( Fig. 2F ) pediform; ischium widening distally, unarmed; merus about 1.4 times longer than ischium, ventral margin with weak expansion on central part, margins non-setose; carpus subtriangular, widening distally, dorsal margin with sparse tufts of setae; propodus expanded ventrally, keel-like, setose, length of dorsal margin shorter than ventral margin, densely setose; dactylus reduced, digitiform, margins covered with dense setae. Pereopod 4 ( Fig. 2G ) simple; ischium about as long as merus, unarmed, margins non-setose; merus slightly wider than ischium, arcuate ventrally; carpus conical distally, almost equal in length with propodus, a few setae scattered disto-dorsally; propodus rectangular, margins almost straigth, dorsal margin densely setose, tuft of dense and short setae distoventrally; dactylus reduced, digitiform, length about 3.3 times less than propodus. Pereopod 5 ( Fig. 2H ) chelate, fingers not gaping; ischium conical, unarmed; merus longest, about 2.7 times longer than ischium, unarmed; carpus subtriangular, widening distally, unarmed; inner and outer surface of propodus densely setose from central part to fixed finger; surface of dactylus covered with dense setae.

Pleon ( Fig. 1A ) smooth, glabrous dorsally except for setose subcircular patches of setae on lateral margins of somites 3 to 5. Somite 2 longest, with isolated tuft of short setae on proximal lateral margin. Somite 6 saddle-like, longer than telson; uropod with protopod smooth dorsally; endopod and exopod uropodal setose marginally; endopod widening distally, about 1.1 times longer than wide, inner lateral margin convex; anterodorsal plate of exopod absent, distal margin sinuous.

Telson ( Fig. 3A ) tapering distally; broadest at lateral lobes on anterior half, slightly wider than long, posterior margin convex, unarmed, setose. Pleopod 1 ( Fig. 3B, C ) uniramous in both sexes; two-segmented in males, tri-segmented in females. Pleopod 2 ( Fig. 3D, E ) sexually dimorphic; heavily reduced and uniramous in male, consisting of two segments, distal segment with short apical setae; biramous and unsegmented in female, endopod and exopod with long and plumose setae. Pleopods 3 to 5 ( Fig. 3F ) biramous, leaf-like, endopod broadened, with subtriangular appendix interna projected from mesial margin of endopod in both sexes.

Distribution – Maranhão (Tutóia) and Ceará (Icapuí), northeastern Brazil.

Habitat — Biffarius botterae sp. nov. builds its galleries in the intertidal zone of fine-grain size sandy beaches, among the galleries of other burrowing shrimps, such as Neocallichirus maryae Karasawa, 2004 , with whose juveniles it can be easily confused in the field.

Etymology —The specific epithet is given in honor of our colleague and friend, Mônica Botter Carvalho, in recognition of her many contributions to the biology of ghost shrimps of Brazil.

Color— Generally translucid except for the whitish chelipeds, and yellow orangish subcutaneous abdominal dorsal surface.

Remarks — Biffarius botterae sp. nov. is herein assigned to Biffarius , whose diagnostic characters (cf. Manning & Felder 1991; Poore et al. 2019) are readily recognized in the new species. They are as follow: rostrum obsolete or obtusely triangular, flat, not reaching cornea ( Fig. 1B ); antennular peduncle exceeded by most to all of antennal peduncular article 5 ( Fig. 1B ); crista dentata absent; major cheliped upper margins of ischium and merus, lower margins of merus and carpus beaded, propodus with deep notch at base of fingers ( Fig. 2A ). Biffarius now consists of four species ( Poore et al. 2019), namely: B. biformis (known from Massachusetts, USA to Pernambuco, Brazil), B. botterae sp. nov. (from Maranhão to Ceará, Brazil), B. delicatulus (from Ceará to São Paulo, Brazil) and B. limosus (currently known from southeastern Australia). Biffarius botterae sp. nov. raises to three the number of western Atlantic species in Biffarius , all of which also known from Brazilian waters ( Rodrigues & Manning 1992; Souza & Borzone 1996; Botter-Carvalho et al. 2012; Pachelle et al. 2016).

The new species is morphologically closest to the southwestern Atlantic B. delicatulus , with which it shares a number of characteristics including vestigial male pleopods 2, absence of crista dentata, and uropodal endopod widening distally (cf. Rodrigues & Manning 1992, figs. 1d–i, r, w; see also Figs. 1 C–H, 3A, D).

However, the two species can be easily separated from each other by the shape of the male major cheliped, much more massive in B. botterae sp. nov. ( Fig. 2A ) than in B. delicatulus (cf. Rodrigues & Manning 1992, fig. 1j). Biffarius botterae sp. nov. also differs from B. delicatulus in the armature of the male major cheliped, whose ventral margin of ischium is armed with a row of well spaced acute teeth, carpus falling short of maximal length of palm (fixed finger excluded), and in the cutting edge of dactylus armed with two strong teeth ( Fig. 2A ), whereas B. delicatulus stands apart in having the ventral margin of the ischium smooth, the carpus longer than the palm and the cutting edge of the dactylus minutely serrated (cf. Rodrigues & Manning 1992, fig. 1j). The two species further differ from each other 1) in the shape and ornamentation of the male minor cheliped, much stronger and with the ventral margin of the merus armed with a large meral hook in B. botterae sp. nov. (versus merus weaker and with a minute spine on the meral ventral margin in B. delicatulus ); 2) in the number of articles of the pleopod 1 of the female, trisegmented in B. botterae sp. nov. (versus bisegmented in B. delicatulus ); and 3) in the absence of anterodorsal plate on the uropodal exopod in B. botterae sp. nov. (versus anterodorsal plate incomplete in B. delicatulus ) (cf. Rodrigues & Manning 1992, figs. 1k, t, w; see also Figs. 2B , 3A, C ).

Biffarius botterae sp. nov. can be distinguished from both, B. biformis and B. limosus , in having vestigial male pleopods 2 (versus male pleopods 2 absent in B. biformis and consisting of a minute papilla in B. limosus ), and the uropodal endopods widening distally (versus uropodal endopod subrectangular in B. biformis and subtriangular in B. limosus ) (cf. Biffar 1970, fig. 3l; Poore 1975, fig. 4b; see also Figs. 3A, B ). It additionally differs from B. limosus in the absence of crista dentata (crista dentata present in B. limosus ), in the female pleopod 1 trisegmented (versus pleopod 1 bisegmented in B. limosus ) and in the anterodorsal plate of uropodal exopod absent (versus anterolateral plate of uropodal exopod present and incomplete in B. limosus ) (viz. Poore 1975, figs. 4b, 5fg; see also Fig. 3A, C ).

Poore et al. (2019) were uncertain as to whether B. delicatulus shares with B. biformis and B. limosus a long antennal peduncle and the lower margins of the major cheliped merus and carpus being beaded and with a dense row of long fine setae. In the B. delicatulus males and females examined (see above under comparative material), the antennal peduncle reaches slightly beyond the tip of the penultimate segment of the A2 peduncle, and the lower margins of the major cheliped merus (not including the meral hook) and carpus are slightly beaded but without setae. Also, Poore et al. (2019) proposed the antennular peduncle length of about 2.5–3 times the width of both eyestalks, and the maxilliped 3 dactylus ovate with a dense brush of long setae over most of the upper-distal margin, and with a few setae along the lower margin towards uniquely diagnosing the genus Fragillianassa (type species Callianassa fragilis Biffar, 1970 ). Whereas the ratio antennular peduncle length/eyestalks width is about the same for Biffarius biformis and F. fragilis , the maxilliped 3 dactylus indeed strongly differs between the two species, being distinctly ovate in F. fragilis and digitiform in B. biformis .

The following key facilitates the identification of the species of Biffarius .

Key to the western Atlantic species of the genus Biffarius .

1.- Male pleopod 2 absent. Uropodal endopod subrectangular, lateral margins subparallel...................... B. biformis - Male pleopod 2 present. Uropodal endopod widening distally; endopod inner lateral margin convex................... 2 2.- Maxilliped 3 crista dentata present. Male pleopod 2 consisting of a papillae............................... B. limosus - Maxilliped 3 crista dentata absent. Male pleopod 2 uniramous, vestigial.......................................... 3 3.- Male major cheliped massive. Anterodorsal plate on uropodal exopod absent....................... B. botterae sp. nov. - Male major cheliped slender. Anterodorsal plate on uropodal exopod present, incomplete.................. B. delicatulus

Figures

FIGURE 1. A–H, Biffarius botterae sp. nov., A, B, holotype, male, cl 4.6 mm, tl 20.3 mm, MZUSP 39002; C–H, paratype, male, cl 5.6 mm, tl 23.1 mm, MZUSP 40376. A, body, pereopods not represented, lateral view; B, carapace front, eyestalks, and antennular and antennal peduncles, dorsal view; C, left mandible, external surface; D, left maxillulla, external surface; E, left maxilla, external surface; F, left maxilliped 1, external surface; G, left maxilliped 2, external surface; H, left maxilliped 3, external surface. Scale bars: A, B = 2 mm; C, D = 0.5 mm; E–H = 1 mm.

FIGURE 2. A–H, Biffarius botterae sp. nov., A, B, E–H, holotype, male, cl 4.6 mm, tl 20.3 mm, MZUSP 39002; C, D, paratype, female, cl 4.1 mm, tl 19.3 mm, MZUSP 40375. A, B, major and minor chelipeds, respectively, lateral view; C, D, major and minor chelipeds, respectively, lateral view; E–H, pereopods 2 to 5, respectively, lateral view. Scale bars: A, B = 2 mm; C–H = 1 mm.

FIGURE 3. A–F, Biffarius botterae sp. nov., A, B, D, F, holotype, male, cl 4.6 mm, tl 20.3 mm, MZUSP 39002; C, E, paratype, female, cl 4.1 mm, tl 19.3 mm, MZUSP 40375. A, abdominal somite 6, uropods, and telson, dorsal view; B, C, male and female pleopods 1, respectively, external surface; D, E, male and female pleopods 2, respectively, external surface; F, pleopods 3 to 5, external surface. Scale bars: A, F = 1 mm; B–E = 0.5 mm.