Batillipes brasiliensis, Santos, Erika, Da Rocha, Clélia M. C., Jr, Edivaldo Gomes & Fontoura, Paulo, 2017

Santos, Erika, Da Rocha, Clélia M. C., Jr, Edivaldo Gomes & Fontoura, Paulo, 2017, Three new Batillipes species (Arthrotardigrada: Batillipedidae) from the Brazilian coast, Zootaxa 4243 (3), pp. 483-502 : 485-491

Batillipes brasiliensis sp. nov.

( Figs 2–3 ; Table 1)

Diagnosis. Small sized Batillipes with tubular undivided primary clavae and papillar secondary clavae. Cephalic cirri with swollen distal tips. Sensorial spines on all legs. Toes 3 and 4 of legs IV with different lengths. Distinct head separated from the body by a neck constriction followed by well-developed lateral processes (“auricles”). Small lateral processes between legs I–III each with a small digit-shaped apex. Processes between legs III and IV fringed with digit-shaped expansions. The caudal apparatus consists of a wide ala-like cuticular expansion covered with detritus. A small semicircular cuticular projection is also present on the coxal region of each leg. Punctate cuticle comprised of small pillars. Rosette-like female gonopore surrounded by a four-valved cuticular structure. Males with circular gonopore with a cuticular crescent-shaped fold.

Type locality. Gunga Beach , Alagoas, Brazil (9°51'45"S, 35°54'17"W).

Type material. Holotype: adult, female (slide CVII-80) collected at Gunga Beach, mounted in glycerol. Allotype: adult, male (slide TARD/UFRPE 02-11) collected at Amor Beach, mounted in glycerol. Paratypes: 8 females collected at Sossego Beach, mounted in polyvinyl alcohol (slides TARD/UFRPE 02-03 to 02-06 and 02- 14); 2 females and one four-toed larva collected at Forte Orange Beach, mounted in polyvinyl alcohol (slides TARD/UFRPE 02-14); 5 specimens collected at Gunga Beach (3 females, 1 male and 1 juvenile), mounted in glycerol (slides TARD/UFRPE 02-08, 02-09 and CVII-81); and 14 specimens collected at Amor Beach (4 females, 4 males and 6 juveniles), mounted in glycerol (slides TARD/UFRPE 02-10 to 02-13, 02-24 and CVII-82).

Type repository. The type material (slides CVII-80–82) is deposited in the collection of the Department of Biology, Faculty of Sciences , University of Porto , Portugal, and all the other slides in the collection of Tardigrades—UFRPE ( Laboratory of Meiofauna , Department of Biology , Universidade Federal Rural de Pernambuco, Brazil) .

Etymology. The name brasiliensis refers to the locus typicus, Brazil.

Ecological note. B. brasiliensis sp. nov. was found in shallow sublittoral medium to coarse, gravels and quartz sands, in low energy (Sossego Beach) and estuarine beaches (Forte Orange Beach and Gunga Beach) and in reef pools of high energy beaches (Amor Beach).

Description of the holotype. Female with a body length 124 µm (142 µm including the caudal apparatus) and 45.4 µm wide between the third and fourth pair of legs ( Fig. 2 A, B). Trapezoid head with eleven cephalic appendages: Internal cirri inserted dorsally on the frontal margin of the head are 18.6 µm long, bearing cirrophores (about 2.2 µm long). External cirri 12.7 µm long, with indistinct cirrophores, inserted more ventrally, near the lateral cirri and primary clavae. The median cirrus, with cirrophore, is 15.5 µm long ( Fig. 2 C). Lateral cirri (26.6 µm long) are located dorsally in relation to the unconstricted tubular primary clavae (12.9 µm long). These two appendages share a common pedestal. A van der Land’s organ is present at the base of the primary clava that exhibits a terminal hole ( Fig. 2 D). An indentation is present in the frontal edge of the head between the external cephalic cirrus and the pedestal bearing the primary clava and lateral cirrus. In the frontal edge of the head papillar secondary clavae ( Fig. 2 D) are also well visible (major diameter 2.9 µm). All cephalic cirri, including external cirri, and lateral cirri have swollen tips. Eye spots not recognized. Ovoid pharyngeal bulb 19.7 µm long and 17.7 µm wide. Ventral mouth opening in a protruded triangular cone. Placoids not visible after slide mounting.

Four pairs of ventro-lateral body processes are present: a blunt lateral expansion, 4.1 µm long, between the head and the first pair of legs ( Fig. 2 D). Lateral processes are also present between all leg pairs. Between the first two pair of legs these blunt processes (6.0, 4.6 µm between legs I–II and II–III respectively) exhibit a thin digitshaped apex ( Fig. 3 A). Between legs III and IV ( Figs 3 B, C) lateral processes are larger, 5.8 µm long and 10.8 µm wide. In these lateral processes the cuticle is punctated except for the membranous fringed external edge constituted by five digit-shaped expansions ( Fig. 2 A, B). The caudal apparatus is an ala-like structure, protruding 17.5 µm and covering almost all the posterior edge of the body. The precise shape of this structure cannot be described because it is covered by detritus ( Figs 2 A, B, 3 C, D). Small semicircular cuticular projections, decreasing in length from the first to the third leg (3.5, 3.3 and 2.1 µm respectively), are also present on the coxal region of legs I–III. This structure is particularly evident in the first leg pair ( Figs 2 D, 3 A) and difficult to see in legs III. Lateral processes between legs and cuticular projections on legs often covered by detritus also.

Sensorial spines present on all legs, increasing in length from leg I to leg IV (5.1; 8.2; 9.6, and 12.8 µm long on leg I, II, III and IV respectively). All leg sense organs with swollen tips. The sense organ on leg IV divided into a pronounced cirrophore (5.8 µm long) and a spine-like distal portion (7.0 µm long) with a basal van der Land’s organ ( Fig. 3 B). Sharply pointed and short (13.1 µm long) cirri E with small cirrophores. Cirri E are dorsally placed between lateral processes and leg IV.

Telescopic legs with toes of different lengths. On the first three pair of legs ( Fig. 2 B), toe 2 is the shortest (considering toe 1 the most cephalically), toes 3 and 5 are the longest, and toes 1, 3 and 4 are medium sized (in leg II toe 1 is 7.0 µm long, toe 2 is 3.2 µm, toe 3 is 13.0 µm long, toe 4 is 6.2 µm, toe 5 is 14.1 µm, toe 6 is 7.3 µm). On the fourth pair of legs toes ( Fig. 3 D) conform the pattern of the D group of species proposed by Kristensen and Mackness (2000), with toes 3 and 4 of different lengths (6.4 and 10.4 µm long respectively for toes 3 and 4). In those legs toes 1 and 6 are similar in length (respectively 11.3 and 11.0 µm long); toes 2 and especially toes 5 are the longest (16.3 and 20.5 µm long respectively). Toes have the distal stalk enlarged distally (about 2.2 µm wide), ovoid suction discs (3.3 long x 2.8 µm wide measured on toes of leg IV) with conspicuous braces and well developed peripheral thickenings.

Dorsal cuticle punctated, about 10 pillars/10 µm (each pillar about 1.4 µm high), without evident transverse folds. However, the large amount of detritus covering the dorsal region of the body can hide those lines. Transverse cuticular folds are visible ventrally where the cuticle punctation is more delicate.

Rosette-shaped gonopore ( Fig. 3 C) separated from the anus by a weakly defined groove. The gonopore is surrounded by a four-valved cuticular structure. Two larger divergent valves are located posteriorly and two narrow valves are located anteriorly to the gonopore ( Fig. 3 E). The anus is 10.9 µm distant from the gonopore.

Remarks. Sexual dimorphism is not evident. Males are similar to females in both qualitative and metric characters (table 1), except for their circular gonopore with a cuticular crescent shaped fold ( Fig. 3 F) located nearer the anus (4.5 µm distant for the anus in the allotypic male). Juveniles, with six toes on each leg but without a visible gonopore, are also similar to adults. The four-toed larva differs from the other juveniles and the adults in having reduced lateral projections without digit-shaped apices; in particular the one located between legs III and IV which lacks the fringed edge. Moreover, the caudal apparatus of this larva is constituted by a conical process without any membranous ala. However, small projections on the coxal region of the three first legs, characteristic of the new species, are present.

On the other hand, among adults, the development of the caudal apparatus (see Fig. 3 B, C, F) and the shape of the fourth lateral projection (between legs III and IV), especially in the number (from 2 to 7) of digit-shaped membranous expansions, are very variable ( Figs 3 B, C). Variability in other projections is not relevant.

Differential diagnosis. The taxonomy of the genus Batillipes is particular problematic due to the reduced number of taxonomic characters traditionally used to distinguish species. Intraspecific variability exhibited by some of those characters and deformations caused by slide mounting are also a source of taxonomic difficulties (cf. McKirdy 1975; Kristensen 1978; Morone De Lucia et al. 1988; Villora Moreno and de Zio Grimaldi 1993). In this genus, one of the more reliable taxonomic characters is the relative dimension of toes. This indicator was introduced by Pollock (1970) and modified by Kristensen and Mackness (2000) who proposed four patterns of toe lengths on the fourth foot, corresponding to four species groups. Batillipes brasiliesis sp. nov. in having toes 3 and 4 of different lengths and respectively different from toe 1 and toe 2, belongs to the D group of species. Only five species exhibit this toe pattern on leg IV: B. africanus Morone De Lucia, D’Addabbo Gallo and Grimaldi de Zio, 1988 ; B. lesteri ; B. tubernatis ; B. similis Schulz, 1955 and B. acuticauda .

The new species, in having lateral projections, can be clearly distinguished from B. africanus and B. tubernatis . Batillipes brasiliensis sp. nov. differs from B. similis in the shape of lateral processes and the caudal appendage that, despite variability, are always conical in the last species. In addition, the primary clava of B. similis , in having a swollen tip, is drumstick-like and not uniformly tubular as in the new species. On the other hand, the sense organ on leg IV is much longer, almost twice the length, in B. similis than in the new species; 18% of the body length in B. similis (mean values, according to Gallo d’Addabbo et al. 1999) and 10% in the new TABLE]. Measurements (in µm) of selecteđ morphological structures of specimens of Batillipes brasiliensis sp. nov. (Holo—Holotype; SD—Stanđarđ đeviation; Range refers to the smallest largest measuređ specimen/structure; N—number of specimens/structures measuređ; Allo—Allotype).

FEMALES MALES JUVENILES LARVA

adults adults 6-toed 4-toed

STRUCTURES Holo Mean ± SD (Range); N Allo Mean ± SD (Range); N Mean ± SD (Range); N

......continued on the next page TABLE]. (Continueđ) species. Batillipes acuticauda , in contrary to the new species, has an acute spiky caudal appendage, cephalic appendages sharply pointed, and very different shaped lateral projections that are flattened between legs III and IV.

Batillipes brasiliensis sp. nov. in having swollen external cephalic cirri and the caudal apparatus consisting of an ala-like cuticular expansion covered with detritus is most similar to B. lesteri . However, B. brasiliensis sp. nov. exhibits different shaped lateral projections with digit-shaped apices and the one between leg III and IV distally fringed. In addition, external cephalic cirri are horn-shaped in B. lesteri and terminated by a swollen tip in the new species. The two species, that have comparable body lengths, differ in the length of cirri E (the longest cirrus E in the new species is 13.1 µm long while in B. lesteri the shortest cirrus E is 19.0 µm long) and leg sense organs that are shorter in the new species. In particular, the sense organ of leg IV is much shorter in the new species (10% of the body length) than in B. lesteri where it is comprised of between 20 and 26 % of the body length. Cuticular valved structures associated with the female gonopore are present in both species, but in B. lesteri only two valves are present posterior to the gonopore, while there are four in the new species, two anterior and two posterior. Moreover, the new species differs from B. lesteri (and from all Batillipes species) by a peculiar character: the presence of small semicircular cuticular projections on the coxal region of legs I–III. This character, that cannot be confused with the coxal swelling of the leg articulation, is also present in specimens previously collected in Brazil and attributed to B. lesteri (da Rocha et al. 2013) . The re-examination of those specimens, which also have external cephalic cirri with swollen tips, led to the conclusion that they should be attributed to the new species. In those specimens mounted in glycerin, eyes were observed which seem to confirm the presence of these structures in the new species. Eyes are soluble in some mounting media, as the glycerol. The re-examination also confirms the intraspecific variability of the caudal apparatus and lateral projections located between legs III and IV that, together with the large amount of adherent detritus were the reason of misidentification. With this correction, B. brasiliensis sp. nov. is also recorded for Cupe Beach, Pernambuco State (8°25'S, 34°55'W), and for the continental shelf, in medium sands at 35 m depth, of Ceará and Rio Grande do Norte States (4°20'– 4°50'S; 36°00– 37°15' W), (see da Rocha et al. 2013).

Figures

FIGURE 2. Batillipes brasiliensis sp. nov. A. Drawing (ventral view); B. Habitus (ventral view); C. Detail of the head showing cephalic appendages (cm—median cirrus; ci—internal cirrus; cl—lateral cirrus); D. Anterior portion of the body showing clavae (pc—primary clava; sc—secondary clava), first body projection (pr 1) and leg projection of the first leg (lpI). Scale bars: A – B = 50 µm; C – D = 10 µm.

FIGURE 3. Batillipes brasiliensis sp. nov. A. Detail of the two first legs of a paratype showing first body projections (pr 1; pr 2), leg projections (lpI; lpII) and first leg spine (pI); B. Posterior portion of the body of a paratype showing the body projection between legs III and IV (pr 4) and sensorial organ of leg IV (pIV); C. Caudal ala (ca) and body projection between legs III and IV (pr 4) of the holotype; D. Toes (t 1 – t 6) of the leg IV of the holotype; E—Detail of the female gonopore (go) and anus (an) of the holotype; F. Detail of the gonopore (go) and anus (an) of the allotypic male. Scale bars = 10 µm.