Xibalbanus cozumelensis, Olesen & Meland & Glenner & Van Hengstum & Iliffe, 2017

Olesen, Jørgen, Meland, Kenneth, Glenner, Henrik, Van Hengstum, Peter J. & Iliffe, Thomas M., 2017, Xibalbanus cozumelensis, a new species of Remipedia (Crustacea) from Cozumel, Mexico, and a molecular phylogeny of Xibalbanus on the Yucatán Peninsula, European Journal of Taxonomy 316, pp. 1-27 : 9-20

Xibalbanus cozumelensis sp. nov.

urn:lsid:zoobank.org:act:B1758E15-23A9-4432-A9D5-DBD10EF11233

Figs 3–10

Speleonectes sp. – Yañez-Mendoza et al. 2007: 54.

Diagnosis

Xibalbanus cozumelensis sp. nov. is a slender and comparatively large species ( Fig. 3 ), up to 35 mm in length; largest specimens with 39 (38 limb-bearing) trunk segments. The species is very similar to Xibalbanus tulumensis ( Yager, 1987) , but is genetically different from this species and is so far only known from Cozumel.

Etymology

The specific epithet refers to the type locality of Cozumel.

Material examined

Holotype

MEXICO: 33 mm, 39 trunk segments (38 bearing trunk limbs), T. Iliffe and P. Van Hengstum leg., 7 Jul. 2014 ( ZMUC-CRU-4791 ).

Paratypes

MEXICO: 2 specimens (bearing 37 and 38 trunk limbs respectively), same locality as holotype, part of one individual removed for molecular analysis, other parts dissected for SEM and mounted separately on stubs, T. Iliffe and P. Van Hengstum leg., 7 Jul. 2014 (ZMUC-CRU-4792); 2 specimens, same locality as holotype, T. Iliffe and P. Van Hengstum leg., 3 Jul. 2014 (ZMUC-CRU-4793 and ZMUC-CRU-4794).

Type locality

MEXICO: Cueva Quebrada, a flooded cave system in Chankannaab National Park on the west coast of Cozumel in Quintana Roo, Mexico at 20°26′ N, 86°59′ W ( Fig. 2 ).

Description

BODY. Elongate, without eyes or pigment ( Fig. 3 ). Maximum length of specimens examined 35 mm. The shortest specimen examined is 30 mm. Cephalic shield small, tapering anteriorly with two lateral notches, about 1/12 of the total body length; cephalic shield partly covering first trunk segment and proximal parts of cephalic appendages; with distinct transverse suture in the region of maxillae 1, and another transverse but weaker suture in the region of antennae 1 ( Figs 3C , 10A ). Trunk elongate, maximum number of trunk segments of specimens examined 39 (38 limb bearing). Most trunk segments with similar subrectangular tergites with rounded lateral margins ( Fig. 10B ); posteriormost segments reduced with posteriorly pointing lateral margins of tergites ( Fig. 10I ). Appendages are lacking on posteriormost segment ( Fig. 4F ). Sternal bars very narrow, isomorphic.

FRONTAL FILAMENTS. Long, distally bifurcated into a large anterior branch and a smaller posterior branch ( Fig. 5 E–F).

ANTENNA 1 ( Figs 3B , 4A , 5B ). Two-branched, slender, relatively short, about 1/6 of body length. Protopod 2-segmented; proximal segment is largest with rows of dense, long ribbon-like aesthetascs along median margin; distal segment continues into a long dorsal/lateral branch and a shorter ventral/median branch. Dorsal branch with 11 slender segments most of which have clusters of aesthetascs along medial margin, and small scattered setae, terminal segment with fine terminal setae. Ventral ramus short, less than ½ the length of dorsal ramus, 9 segments, basal segments weakly divided, clusters of distomedial aesthetascs and short setae on margins; distal segment with terminal setae.

ANTENNA 2 ( Fig. 4B ). A paddle-like biramous appendage. Protopod divided in two segments, a coxa (proximally) and a basis; coxa with 4 medial setae, basis with 9 medial setae. Endopod 3-segmented and curves laterally; segment 1 with 10–11 setae on lateral (outer) margin; segment 2 with 7; segment 3 ovoid, bearing about 27–28 setae along entire margin, including a terminal double row of about 10 setae. Exopod an unsegmented, large oval plate with about 29–35 setae along margin. All setae plumose with long setules.

LABRUM ( Fig. 5E ). Prominent, bulbous, subdivided by a transverse suture in an anterior trapezoid shaped part and a posterior (distal) subrectangular part rounded laterally; distally is a dense tuft of fine setae.

MANDIBLES ( Fig. 5 H–K). Well developed with a gnathal edge consisting of three parts, a molar, a lacinia mobilis, and an incisor; only mandible of left side has been examined in detail. Left molar process occupies approximately ⅔ of the gnathal edge; in apical view the molar is crescent-shaped, composed of a dense row of multi-tipped setules bending towards each other forming a large cavity in the center of the molar; on the functionally anterior side of the molar are clusters of short setules and one cluster of longer. Left incisor broad, flattened, distal margin subdivided into four cusps of subequal morphology (three are pointed, one spade-shaped). The lacinia mobilis is positioned between the incisor and the molar as an extension of the latter, subequal in length to incisor but more narrow terminating in three cusps.

FIRST MAXILLA ( Figs 4C , 6 ). 7-segmented, uniramous, robust. Point of flexion between segments 4 and 5. Segment 1 ( Fig. 6 A–B) relatively short and drawn out medially in a flattened endite with 7 robust setae, posteriormost seta largest, anteriormost serrated; subterminally with row of 4 setules. Segment 2 ( Fig. 6A, D ) narrow, of subtriangular shape, with elongate, plate-like endite articulated to the segment and directed obliquely medially/anteriorly; terminal margin with one row of 7 robust spines and another more disorganized row of about 17 moderately long or smaller setae; at the posterior margin is a cluster of 4 long setae; at the anterior margin is a row of 5 long setae. Segment 3 ( Fig. 6 A–B) is trapezoid shaped with a well-developed conical medial endite bearing 2 robust, broad-based cone-shaped setae, each with tiny papilla-like projections on distomedial surface ( Fig. 6F , G–I); anteriorly on endite is a row of 5 long, slender setae, posteriorly is 5 setae of different lengths. Segment 4 ( Fig. 6A ) as large as the three preceding segments, bearing a well-developed conical median endite with 2 large cone-shaped setae as on segment 3, also with tiny papilla-like projections on distomedial surface; anteriorly on endite is a double-row of 9 setae, posteriorly on endite is a cluster of 9 setae, 4 relatively long and 5 relatively short. Segment 5 ( Fig. 6A ) about the same length as segment 4 but more slender; cluster of about 12 slender setae in medio-distal corner of segment. Segment 6 ( Fig. 6A, C ) very short not clearly separated from segment 5 dorsally, with two rows of setae anteriorly and posteriorly, about 8 setae in each. Segment 7 ( Fig. 6 A–C) short, not clearly separated from segment 6 dorsally, terminating in stout fang-like claw with visible subterminal duct opening, more than 3 times the length of segment 6; a cluster of about 6 long simple setae basally at segment 7.

SECOND MAXILLA ( Figs 4D , 7 ). 7-segmented, uniramous, longer and more slender than maxilla 1; point of flexion between segments 3 and 4; segments 4–7 decreasing in size distally. Segment 1 with 3 digitiform endites ( Fig. 7A , D–E) increasing in size anteriorly; all endites with 1 long apical spine-like seta, a row of short, spine-like setae medially (least on endite 1, most in endite 3) and a row of long setae laterally (least on endite 1, most in endite 3). Segment 2 ( Fig. 7A, F ) short, wedge-shaped, ‘squeezed in’ between segments 1 and 3 with the broad end of the ‘wedge’ facing medio-anteriorly, medially bearing 1 short, stout, curved medial spine, with a short row of about 4 median setae and short row or cluster of about 5 short to moderately long slender setae at medio-distal corner. Segment 3 ( Fig. 7A, F ) elongate, rounded medially with row of about 11 long setae and 8 shorter setae. Segment 4 ( Fig. 7A ) slightly shorter than segment 3, with small distomedial lobe terminating in a cluster of about 10 short to long, thin setae; distolateral corner with 4 slender setae of varying lengths. Segment 5 ( Fig. 7A ) shorter than segment 4 with approximate same configuration of setae. Segment 6 ( Fig. 7A, F ) bearing a large cluster of about 15 setae at distomedial corner and a pair of clusters at the disto-lateral corners (about 6 setae in each). Segment 7 ( Fig. 7A, C ) very short, about half the length of segment 6, with terminal claw complex consisting of fused arch of at least 17 denticles and 1 long, stout anterior spine; 1 short, stout anterior spine subterminal to fused arch; opposable thumb-like pad bearing many (at least 40) setae which fan under claw complex.

MAXILLIPED ( Figs 4E , 8 ). 8-segmented, generally similar in shape but longer and more slender than maxilla 2, with one more segment beyond point of flexure. Segment 1 ( Fig. 8A, C ) is short with 5 long and 2 short setae along median margin and about 3–4 small setae in a row more proximally. Segment 2 is large and undivided in anterior view ( Fig. 8A ), but in posterior view it is subdivided by an oblique furrow giving the appearance of two separate triangular segments ( Fig. 8C ); at the medio-distal margin is a row of 12 setae of varying length. Segment 3 as long as the combined length of segments 1–2; with round medial margin with about 15 slender setae of varying length in a dense row in the middle of the segment. Segment 4 ( Fig. 8A, C ) the same length as segment 3, subtriangular in shape, with a cluster of about 15 setae of varying size at disto-medial corner, and a small cluster of about 4 short setae in latero-distal corner. Segment 5 ( Fig. 8A, C ) approximately the same size as segment 4 but more rectangular; about 12 setae in a cluster at disto-medial corner, 5 in latero-distal corner. Segment 6 ( Fig. 8A, C ) very similar to segment 5 with respect to setation, but only slightly more than half as long. Segment 7 ( Fig. 8A, C ) about the same length as segment 6 with rows of short setae along distal margin of segment: two rows at the disto-lateral corners of the anterior and posterior side of segment, each with 4–6 setae, and two rows at the disto-medial corners with about 10 (anterior side) or 5 (posterior side) setae. Segment 8 ( Fig. 8B, D ) similar to claw complex on maxilla 2, with stout anterior spine subterminal to arched claw complex and with opposable setae-bearing pad.

TRUNK. Limbs biramous ( Figs 9–10 ), natatory, with large protopod, 4-segmented endopod and 3-segmented exopod; long plumose setae along margins; size of limbs varies along body, increasing in size from trunk limb 1 to approximately trunk limb 7, decreasing in size approximately from trunk limb 29 onwards; trunk limbs 37 and 38 are significantly reduced in size ( Fig. 4F ); in the most anterior trunk limbs the exopod is longer than the endopod, in the middle range of trunk limbs the rami are sub-equal in size, around trunk limb 30 onwards the endopod is clearly larger, while in the last two reduced trunk limbs (37 and 38) the exopods are largest ( Fig. 9 ).

CAUDAL RAMI. Very slender, about 4–5 times length of anal segment with small terminal setae ( Figs 4 F–G, 10H–I).

Remarks

Unidentified suctorians of varying shapes were found attached at the proximo-ventral parts of antennae 1 and at the trunk limbs ( Figs 5 C–D, 10F–G).

Remipedia CO1 and 16S mtDNA distance matrices

Table 2 shows uncorrected genetic distances of CO1 and 16S mtDNA among populations of Xibalbanus cozumelensis sp. nov. obtained in this study and other Remipedia of which data are available in GenBank (see also Neiber et al. 2012; Hoenemann et al. 2013). The CO1 gene was sequenced for three specimens of X. cozumelensis sp. nov. yielding a 0–3% pairwise genetic distance between the individuals. The X. cozumelensis specimens are genetically (CO1) closest to populations of X. tulumensis from the ‘mainland’ Yucatán Peninsula with a 9–11% genetic distance. The genetic distance between X. cozumelensis and other remipedes varies between 13% and 25%. The genetic distance (CO1) among species of Remipedia in general varies between 12% and 31%, but only with few values in the low end of the spectrum, e.g., the distance between two species of Cryptocorynetes ( C. longulus Wollermann, Koenemann & Iliffe, 2007 and C. haptodiscus Yager, 1987 ) and two species of Godzillius ( G. fuchsi Gonzalez, Singpiel & Schlagner, 2013 and G. robustus Schram, Yager & Emerson, 1986 ), which are 13%, and the distances between two species of Morlockia ( M. ondinae García-Valdecasas, 1984 and M. atlantida ( Koenemann et al., 2009)) , which is 12%. The rest of the CO1 genetic distances between species of Remipedia based on sequences available in GenBank are included for completeness but will not be described further here ( Table 2 ). 16S was sequenced for one specimen of X. cozumelensis sp. nov. The specimen is genetically (16S) closest to X. tulumensis showing genetic distances of 14–19%. The genetic distances in the 16S gene between species of Remipedia generally are between 20–30%, but with the distance between a few species being lower and at the same level as between X. cozumelensis sp. nov. and X. tulumensis (e.g., Cryptocorynetes haptodiscus and C. elmorei Hazerli, Koenemann & Iliffe, 2009 at 16%, and Speleonectes lucayensis Yager, 1981 and S. kakuki Daenekas, Iliffe, Yager & Koenemann, 2009 at 17%). CytB was compared to CytB extracted from the complete mitochondrion of X. tulumensis ( AY456190 ). The X. cozumelensis sp. nov. sequences were identical and had a 15% genetic distance from X. tulumensis .

Phylogeny of Remipedia based on Bayesian analysis of CO1 and 16S mtDNA genes

The phylogenetic tree of Remipedia in Fig. 11 is based on a Bayesian analysis of the CO1 and 16S mtDNA genes. New sequences of both CO1 and 16S have been obtained for Xibalbanus cozumelensis sp. nov. Sequences from other species of Remipedia are from GenBank and were previously used in Neiber et al. (2012) and Hoenemann et al. (2013). In the phylogeny ( Fig. 11 ) all included species of Xibalbanus were in the same clade (monophyletic). Xibalbanus cozumelensis sp. nov. appeared as sister species to X. tulumensis , and these two together appeared as sister of X. fuchscockburni . The remaining part of the phylogeny was largely similar to the topology obtained by Hoenemann et al. (2013) and is not further described here as the focus was on Xibalbanus .

Figures

Fig. 3. Xibalbanus cozumelensis sp. nov., light microscopy. A. Holotype, adult specimen, lateral view (ZMUC-CRU-4791). B. Holotype, cephalon, lateral view. C. Paratype, cephalon, dorsal view (ZMUC- CRU-4793).

Fig. 4. Xibalbanus cozumelensis sp. nov., holotype (ZMUC-CRU-4791), light microscopy. A. Antenna 1, left side from anterior. B. Antenna 2, left side from anterior. C. Maxilla 1, left side from anterior. D. Maxilla 2, left side from anterior. E. Maxilliped, left side from anterior. F. Caudal rami and posterior part of trunk. G. Caudal ramus, left side seen from median.

Fig. 5. Xibalbanus cozumelensis sp. nov., paratype (ZMUC-CRU-4792). Cephalon and cephalic structures. Scanning electron microscopy. A. Cephalon with cephalic shield and appendages. B. Antenna 1, right side, proximal parts of dorsal and ventral branches. C–D. Unidentified suctorians attached at the proximo-ventral parts of antenna 1. E. Labrum, frontal filaments, and parts of antennae 1 and 2, right side. F. Frontal filaments. G. Antenna 2, left side from anterior. H. Mandible, left side from anterior. I. Mandible, left side from posterior. J. Mandible, left side, apical view on gnathal edge. K. Mandible, left side, apical view on molar process.

Fig. 6. Xibalbanus cozumelensis sp. nov., paratype (ZMUC-CRU-4792), maxilla 1 (mx1), left side, scanning electron microscopy. A. Complete mx1 from anterior. B. Median view. C. Close-up of median structures (e.g., endites) and distal claw from anterior. D. Distal setation of plate-like endite of segment 2 seen from ‘below’. E. Distal setation of endite of segment 1 seen from ‘below’. F. Close-up of two robust, broad-based cone-shaped setae of segment 3. G. Close-up of papillae of cone-shaped seta. H. Close-up of median structures (e.g., endites) and distal claw from posterior. I. Fang-like claw with visible subterminal duct opening.

Fig. 7. Xibalbanus cozumelensis sp. nov., paratype (ZMUC-CRU-4792), maxilla 2 (mx2), left side, scanning electron microscopy. A. Complete mx2 from anterior. B. Close-up of terminal claw-complex from anterior (segment 7). C. Close-up of terminal claw-complex from lateral (segment 7). D. Median side of segments 1 and 2 with endites (e1–3) from anterior. E. Endites of segment 1 (e1–3) from median. F. Complete mx2 from median.

Fig. 8. Xibalbanus cozumelensis sp. nov., paratype (ZMUC-CRU-4792), maxilliped (mxp), left side, scanning electron microscopy. A. Complete mxp from anterior. B. Close-up of terminal claw-complex from anterior (segment 8). C. Complete mxp from posterior. D. Close-up of terminal claw-complex from posterior (segment 8). E. Close-up of terminal claw-complex from lateral (segment 8). F. Close-up of small cluster of setae along distal margin of segment 7. G. Close-up of pore at close to latero-distal margin of segment 7. H. Close-up of cluster of setae at latero-distal corner of segment 4. I. Close-up of cluster of setae at latero-distal corner of segment 5.

Fig. 9. Xibalbanus cozumelensis sp. nov., holotype (ZMUC-CRU-4791), trunk limbs, left side from anterior, light microscopy. A–J. Selected trunk segments (number specified on figure). All to the same scale.

Fig. 10. Xibalbanus cozumelensis sp. nov., paratype (ZMUC-CRU-4792), cephalon, body segments, and trunk limbs, scanning electron microscopy. A. Cephalon, cephalic shield, and head appendages from lateral. B. Trunk segments 5–10. C. Trunk limb 2, right side. D. Close-up of serrated setae in latero-distal corner of exopod segment 1. E. Close-up of serrated setae in latero-distal corner of exopod segment 2. F–G. Two unidentified suctorians attached to exopod of trunk limb 3. H–I. Posterior body segments, trunk limbs, and caudal rami from ventral and lateral.

Fig. 2. Maps of the Yucatán Peninsula showing the known distribution of four species of Xibalbanus (Remipedia) and water depths around Cozumel. A. Yucatán Peninsula showing Xibalbanus localities (1–10) in the northeastern region of the Yucatán Peninsula and one locality in Belize further south (11). B. Close-up of the northeastern region of the Yucatán Peninsula with the positions of 10 Xibalbanus localities indicated. C. Close-up of eastern Cozumel with the branches of the anchialine cave “Cueva Quebrada” indicated as an overlay, derived from Yañez-Mendoza et al. (2007). The collecting site of Xibalbanus cozumelensis sp. nov. is indicated as “10”. Numbers refer to the following cenotes/caves: 1 = Cenote Crustacea; 2 = Cenote Chac Mool; 3 = Cenote Ponderosa (= Cenote Jardín del Edén); 4 = Cenote Tajma Ha; 5 = Cenote Carwash (=Cenote Aktun Ha); 6 = Cenote Vaca Ha; 7 = Cenote Temple of Doom (Cenote Calavera, Cenote Esqueleto); 8 = Cenote Naharon (Cenote Cristal); 9 = Cenote Maya Blue (Cenote Escondido); 10 = Cueva Quebrada; 11 = Caye Chapel Cave. 1–9 are in the northeastern Yucatán Peninsula, 10 is on the island of Cozumel, 11 is in Belize.

Fig. 11. Phylogenetic position of Xibalbanus cozumelensis sp. nov. based on a Bayesian analysis of partial CO1 and 16S rDNA sequences of X. cozumelensis sp. nov. and other remipedes available from GenBank.