Troglocaris (Troglocaris) anophthalmus

Sket, Boris & Zakšek, Valerija, 2009, European cave shrimp species (Decapoda: Caridea: Atyidae), redefined after a phylogenetic study; redefinition of some taxa, a new genus and four new Troglocaris species, Zoological Journal of the Linnean Society 155 (4), pp. 786-818 : 798-803

TROGLOCARIS (TROGLOCARIS) ANOPHTHALMUS – ADRIATIC CLADE ZAKŠEK ET AL., 2007.

Synonymy: Incl. Troglocaris schmidti auct. from Vjetrenica, p.p.; incl. Troglocaris schmidti schmidti forma typica Fage, 1937 p.p.; incl. Troglocaris anophthalmus Matjašicˇ, 1960; incl. Troglocaris ‘forma P’ (Pelješac) Franjevic´, 2006; incl. Troglocaris anophthalmus anophthalmus (Vjetrenica) Franjevic´, 2006; incl. Troglocaris ‘forma AA’ (Metkovic´) Franjevic´, 2006; incl. Troglocaris ‘forma A’ (coastal region) Gottstein Matočec, 2003;?incl. Troglocaris ‘forma A’ (Mandalina) Franjevic´, 2006.

Material examined (sequenced): Croatia, Biograd na moru, Vrana, Pećina kod Vrane cave, ‘Vrana_Tgc-53’; Zadar, Pirovac, Bikovica cave, ‘Bikovica_Tgc-59-60’. Bosnia and Herzegovina, Hercegovina SE, Popovo polje, Zavala, Vjetrenica cave, ‘Vjetrenica_Tgc-21, 63’. A number of other samples were inspected morphologically.

Remarks, distribution: We exposed this unnamed clade to show the phylogenetic position of the Vjetrenica population. This has been repeatedly regarded as belonging to the ‘typical’ T. anophthalmus (e.g. Matjašicˇ, 1960), or even explicitely as being T. a. anophthalmus ( Fage, 1937, as T. s. schmidti ; Franjevic´, 2006). It is a molecularly close but geographically distinct clade ( Zakšek et al., 2007) from a contiguous area along the Adriatic coast in Croatian Dalmacija (Dalmatia), and the neighbouring south Hercegovina of Bosnia and Herzegovina.

TROGLOCARIS (TROGLOCARIS) ANOPHTHALMUS – OTHER SOUTH- EASTERN LINEAGES

Synonymy: Incl. Troglocaris anophthalmus intermedia Gottstein Matočec, 2003 (Franjevic´, 2006, from Kukuruzovića špilja, nec T. a. intermedia from Mikašinovića pećina); incl. Troglocaris ‘forma P’, Gottstein Matočec, 2003; incl. Troglocaris anophthalmus E-Slovenian clade, Zakšek et al., 2007, p.p.

Material examined (sequenced): Slovenia, Črnomelj, springs in Jelševnik, ‘Jelsevnik_Tgc-9-10’; Vinica, Špeharji, Kobiljača cave, ‘Speharji_Tgc-5-6’. Croatia, Istra, Plomin, spring in artificial tunnel of Čepic´, sequenced ‘Krsan_Tgc-33’. A number of other samples were inspected morphologically.

Remarks, distribution: Some molecularly very close but geographically distinct clades could be identified ( Zakšek et al., 2007) within the area south to southeast of T. ( T.) a. anophthalmus , i.e. in Slovenian Bela Krajina, and in Croatian eastern Istra and Kordun. Some of the yet unsequenced populations in the Ogulin area ( Croatia) probably belong to T. ( T.) a. intermedia . A detailed study is in progress.

TROGLOCARIS (TROGLOCARIS) PLANINENSIS BIRŠTEJN, 1948

Synonymy: Troglocaris schmidti planinensis Birštejn, 1948 ; Troglocaris planinensis d’Udekem d’Acoz, 1999 ; T. anophthalmus W-Slovenian clade Zakšek et al., 2007; incl. Troglocaris anophthalmus anophthalmus from Jama pod krogom, Gottstein Matočec, 2003; incl. Troglocaris ‘forma A2’ (Plomin) Franjevic´, 2006; incl. Troglocaris ‘forma AN’ (Krog) Franjevic´, 2006; incl. Troglocaris hercegovinensis Sket, 1992 from Slovenia (Osp); see also Holthuis, 1956.

Type locality: Slovenia, Postojna, Planina, Planinska jama cave.

Material examined: Slovenia, type locality, sequenced ‘ Planina _Tgc-85’; dissected, Divača, Kačna jama cave, ‘ Kacna _Tgc-17-18, 110-116’; Koper, Osp , Grad cave, ‘ Osp _Tgc-28’; Sočerga , Jama pod krogom cave, ‘ Socerga _ Tgc 83’; Ilirska Bistrica, Novokračine , Novokrajska jama cave, ‘ Novokrajska _Tgc-87’; Divača, Kačiče , Mejame cave , ‘ Mejame _Tgc-118-120’; Planina , Laze , Najdena jama cave, ‘ Najdena _Tgc-121 ’.

Croatia, Istra, Plomin, spring in artificial tunnel of Čepic´, sequenced ‘Krsan_Tgc-34’.

Italy, Trieste, Trebiciano/Trebče, Grotta di Trebiciano/Labodnica cave, sequenced ‘Trebiciano_ Tgc-1, 19, 20, 23, 32’.

Diagnosis: Cave shrimps from western Slovenia and Italian Carso/Kras and Croatian Istra; morphologically not yet diagnosable.

Remark: The original description of this taxon is erroneous. Birštejn based the subspecies mainly on the differences in male pleopods I and II, which should put his T. s. planinensis morphologically ‘between (promežutočnoe položenie) T. s. inermis on one side and T. schmidti hercegovinensis and most transcaucasian subspecies on the other’. However, the drawings of pereopod IV and pleopods I and II clearly show that Birštejn described an immature male. Mature males from the same cave are hardly distinguishable from the type population of T. a. anophthalmus , but molecular differences are present. Some taxonomical characters, the rostrum length in particular, vary highly between populations of this clade: the differences within the clade are much higher than between topotype populations of both species.

See above for species distinctiveness [under Remarks for subgenus Troglocaris (Troglocaris) ].

Distribution: Populations west and south-west of Planinska jama, in Kras/Carso, and up to the central parts of Istra Peninsula (Labin) are related ( Zakšek et al., 2007). Populations in the lower reaches of the river Soča/Isonzo ( Italy), and from the southern and western parts of the Istra Peninsula ( Croatia), have not yet been molecularly investigated.

TROGLOCARIS (TROGLOCARIS) BOSNICA SP. NOV.

( FIGS 7 , 8 )

Synonymy: Troglocaris sp. nov. 2 of the Bosnian clade, Zakšek et al. (2007).

Holotype male: Bosnia and Herzegovina, Bosanska Krajina , Lušci polje, Suvaja cave; partially dissected, as ‘ Suvaja _Tgc-193m’, leg. R. Davidovic´, 1984.

Paratype male: Sequenced and dissected, ‘Suvaja _Tgc-168m’.

Paratype female: ‘Suvaja_Tgc-04f’, treated like paratype male.

Other material: Approximately 20 specimens from type locality; three specimens from Sanski Most, Dabarska pećina cave; ‘Dabarska_Tgc-08, 24’, sequenced and dissected.

Etymology: Named after Bosna, a region of Bosnia and Herzegovina.

Diagnosis: As for subgenus, rostrum 60% of CL or longer, usually with 15 ventral teeth; palp of maxilla I with more than three, moderately long setae; male pleopod-I endopodite with more than 30, partially grouped, and long, inner marginal setae.

Description of holotype male: Moderately stout animal of CL 7.7 mm without pigmentation, eyes (eye stalks) reduced to egg-shaped rudiments without facetting. Rostrum 70% of CL, wide and curved upwards, densely serrated, with a dentition formula of 34+6/17. Supraorbital spine long, antennal (suborbital) spine shaped as a short tooth of the carapace margin below orbit. Pleonite VI twice as long as pleonite V, much longer than half the carapace, and longer than the telson. Telson slightly shorter than half CL, 2.5 times as long as wide; side margins slightly converging in distal direction, straight, distal border strongly convex and regularly rounded; both pairs of dorsal spines nearly marginally positioned, 14 distal spines, most subequally long, only the marginal pair shorter, and the submarginal one slightly longer.

Antenna I stylocerite sharply pointed, distant, tip reaching to 85% of the length of the bearing article. Similarly-pointed distal projection of article 1 distant, reaching approximately 40% of article 2 in length. Antenna II scaphocerite narrow, 3.5 times as long as wide, with very long and jutting subdistal outer projection.

Maxilla I with larger endite, gradually narrowing in distal direction; palp rounded apically, with four setae, two approximately as long as width of the largest article, others very short. Maxilla II scaphognathite triangular, with many long setae distally.

Pereopods I– IV with long and flexible exopodites, pereopod V with shorter one. Lengths of pereopods II, III, and V: 84, 175, and 150% CL, respectively. Pereopod I chela slightly shorter and stouter than chela II, with pronounced proximal bulge; carpus shorter than chela, remarkably widened and excavated distally. 160% CL, respectively. Pereopod III in immature males and in females not widened distally, dactylus with up to seven inner spines. Exopodite on pereopod V apparently always present, in males and females; may be short and stiff in some specimens.

Remarks: The high molecular distance showed the independent species character of the clade from Bosanska Krajina (north-west Bosna), it is a sister clade to all other populations within the subgenus Troglocaris s.s. as conceived here.

The rostrum may be similarly long in some populations of T. anophthalmus , even in some individuals of the type population. However, the number of ventral teeth is diagnostic at approximately double the highest number found in T. anophthalmus . The setation of the maxilla-I palp is also distinctive, with between four and six short to medium long setae; in T. anophthalmus and in other subgenera there is only one very long and one or two very short setae. The marginal setation of male pleopod-I endopodite is denser and longer in T. (T.) bosnica sp. nov.

Chela II narrow, fingers longer than basal part, which has a very small basal bulge; carpus longer than chela, indistinctly widened and excavated distally. Pereopod III longer than V; article 6 slightly widened in distal third, part of widening with multiplied inner marginal spines; dactylus elongated and curved, with approximately 25 irregularly set inner spines. Pereopod V normally shaped, but dactylus with a comb of approximately 50 spines, and with evenly distributed setae along both margins. Pleopods I and II with about five very stout and moderately short setae along distal margin of sympodite, at endopodite base. Pleopod-I endopodite foliaceous, distally narrowed, slightly rolled, without a trace of appendix interna; along its folded inner margin 12 curved and strong, nearly spine-like setae; approximately 40 long and short setae along outer margin, partly in groups. Pleopod-II endopodite with AM plate-like, about five times as wide and twice as long as stick-shaped AI, which is appended at proximal quarter of AM length; with numerous small, rigid, setae on surface. Uropod with long spine at diaeresis, side tooth half as long as spine.

Variability: Rostrum 57–70% CL, with 11–17 ventral and 27–32 dorsal teeth. Pereopods lengths variable: pereopods II, III, and V in paratype male 93, 158, and Distribution : We only found these animals in the Suvaja in Lušci polje and Dabarska pećina caves near Sanski most, which are both in Bosanska Krajina (north-west Bosnia and Herzegovina) .

SUBGENUS TROGLOCARIS (XIPHOCARIDINELLA) SADOVSKIJ, 1930

Diagnosis: Rostrum moderate to very short, with between zero and 11 teeth dorsally; suborbital spine absent ( Birštejn, 1948: 7); male pleopod-I endopodite as flat ovoid lamina, extended medially distally or subdistally into finger-like AI, outer marginal row of long setae uninterrupted until reaching distal part of lamina or its distal lobe (when developed); male pleopod II with AM longer than AI, rod shaped to shield shaped; (pereopods in mature male differentiated or not).

Remarks: Mostly, the authors did not mention the carapace spines, except for T. jusbaschjani , which definitely has none; Birštejn (1948: 4,7) indirectly indicated the existence of supraorbital spines in all other taxa.

Reliable morphological distinction from subgenera Troglocaridella and Spelaeocaris could probably be traced after a detailed redescription of the Caucasian species. Molecular and biogeographical data support the phyletic peculiarity of this group.

Type species: Xiphocaridinella kutaissiana Sadovskij, 1930 from Kutaisi in Georgia.

Other taxa: Troglocaris ablaskiri Birštejn, 1939 ; Troglocaris fagei Birštejn, 1939 ; Troglocaris osterloffi Juzbaš’jan, 1940; Troglocaris birsteini Mugue, Zueva & Ershov, 2001 in Abhazetis (Abkhazia) in Georgia; Troglocaris jusbaschjani Birštejn, 1948 in Tatarstan in Russia.

Material: No samples were available. Phylogenetic relationships were based on molecular data provided by N. Mugue (pers. comm.).

Remarks. Sadovskij (1930) characterized his genus Xiphocaridinella in roughly this way: eyes strongly reduced; pereopods I– IV, and sometimes V, with exopodites; seven pairs of gills, seventh reduced. This would encompass close to any species of Troglocaris s.l.

The aggregate is not discussed further because of the lack of material. Most taxa were described as subspecies of either T. anophthalmus (in fact ‘ T. schmidti ’) or of T. kutaissiana . Mugue et al. (2001) demonstrated, by molecular analyses and by the sympatry of two taxa, that they are independent species. Position of this clade within the Troglocaris complex was shown by Zakšek et al. (2007). One must note, however, that neither of the two most aberrant species, the type species T. kutaissiana and T. jusbaschjani , have been included in molecular analyses. Troglocaris kutaissiana seems (the published drawings are quite sketchy) to have a T. anophthalmus - like male pleopod II; T. jusbaschjani seems to have a Typhlatya -like (or Spelaeocaris -like) spineless carapace. Nevertheless, this clade seems to be corroborated by its biogeographical compactness and by some degree of morphological similarity.

The phylogenetic affiliation of T. jusbaschjani to Typhlatya (as supposed by d’Udekem d’Acoz, 1999) is highly unlikely considering the biogeographical situation: the low number of morphological characters indicating this supposed relationship have been shown above. Both its male pleopod-I endopodite and the pleopod-II appendices show its close relationship with some other Xiphocaridinella spp. The non-lobate endopodite of the male I in T. fagei is similar to that of S. pretneri . However, this sole similarity of two geographically distant taxa is most probably an accidental convergence (or plesiomorphy).

Distribution: This group of taxa inhabits a compact area on the flanks of the western Caucasus in northwestern Georgia, mainly in the north-western autonomous republic Abhazetis (Abkhazia), and in the neighbouring Russian Tatarstan.

SUBGENUS TROGLOCARIS (TROGLOCARIDELLA) BABIĆ, 1922

Diagnosis: Troglocaris group with supraorbital spines (suborbital may be absent); distal extension of antenna I article 1 pointed, but short and not jutting out; maxilliped-I exopodital lobe ( Fig. 5 Th) narrow, and gradually narrowing into a distal flagellum; chelae and dactyli very narrow; pereopods III and IV widened distally in mature males; male pleopod-I endopodite ( Fig. 2 Th) with oval and lobate lamina elongated into finger-like AI, uninterrupted marginal row of setae, not along distal lobe (if developed); male pleopod II ( Fig. 4 Th) AM spindle-shaped, with numerous small spines in distal half, longer and wider than AI.

Type (and only) species: Troglocaridella hercegovinensis Babic´, 1922.

Remarks: The genus Troglocaridella was defined by an absence of exopodites on pereopods IV and V, and by its troglomorphy, and implicitly also by a short rostrum [‘Der Troglocaris ( v. intermedia ) sehr ähnlich, nur die drei ersten Pereopodenpaare mit Exopoditen; die zwei letzten Pereopodenpaare ohne exopodit. Blind, mit verkümmerten Augen’]. Even among molecularly identifiable topotypical specimens, one may have a developed exopodite IV, whereas most actually lack it.

Distribution: The only known species has been found within a comparatively small area within the southeastern merodinaric (sensu Sket, 1994) biogeographical area in south-eastern Hercegovina ( Bosnia and Herzegovina) and southern Montenegro.

TROGLOCARIS (TROGLOCARIDELLA) HERCEGOVINENSIS ( BABIĆ, 1922)

( FIGS 2 Th, 4Th, 5Th)

Synonymy: Troglocaridella hercegovinensis (Absolon) Babic´, 1922; Troglocaris Schmidti hercegovinensis or Troglocaris Schmidti Forma hercegovinensis Fage, 1937 ; nec Troglocaris hercegovinensis Sket, 1992 , from Osp in Slovenia; see also Holthuis, 1956.

Type locality: Bosnia and Hercegovina, Popovo polje, Zavala, Vjetrenica cave.

Material sequenced and dissected: Bosnia and Herzegovina, south-eastern Hercegovina, Popovo polje, Zavala, Vjetrenica cave, ‘Vjetrenica_Tgc-11-12’, only dissected ‘Tgc-127-129. Only dissected Bileća, Dejanova pećina, ‘Bileca_Tgc-06’; Dabarsko polje, Ljelješnica cave, ‘Ljeljesnica_Tgc-133’; Dabarsko polje, Sušica cave, ‘Sušica_Tgc-134’; Fatničko polje, Obod cave, ‘Obod_Tla-186-187’.

Montenegro, Rijeka Crnojevića, Obodska pećina cave, ‘Rij-Crn_Tgc-56, 58’; only dissected ‘Rij- Crn_Tgc-82’.

Diagnosis: With characteristics of the subgenus; suborbital spine usually present; chelae and dactyli very narrow; pereopods-III and -IV article 6 in mature males differentiated, dactylus sparsely pectinate.

Remarks: Babić (1922) ascribed this species to Absolon, but Absolon (1916: 609) only introduced the name ‘ Troglocaris hercegovinensis n. sp. ’, without any description and without any exact locality data. Babić (1922) described the species as ‘ Troglocaridella hercegovinensis (Absolon) ’ mentioning the taxonomically less useful short rostrum with 7–10 upper and 0–3 lower teeth, but also describing the male pleopods I and II; his drawing enables us to recognize this taxon with certainty among shrimps from Vjetrenica.

Although Babić (1922) did not emphasize it, he presented a good drawing of the male pleopods I and II. Therefore, Fage (1937) also correctly interpreted these appendages. Confusion was evidently brought into the taxonomy when ‘normal’ T. anophthalmus was also found in samples from the cave Vjetrenica. It caused different interpretations: (1) only T. anophthalmus lives in Vjetrenica, variations are produced by age differences ( Stammer, 1932, 1933; Birštejn, 1933); (2) either two species or one species with dimorphic males in Vjetrenica ( Stammer, 1935); (3) Fage (1937) decided to consider this taxon as ‘ forma hercegovinensis ’; (4) Matjašič (1960) clarified the situation, presenting a number of differences between populations of both species from this locality.

Distribution: As well as in Vjetrenica, southern Hercegovina, this species could also be molecularly (and morphologically) proven for Obodska pećina near Rijeka Crnojevića in southern Montenegro, whereas morphologically identical or very similar specimens originate in the caves Ljelješnica and Sušica in Dabarsko polje. Animals from Bileća and from Fatničko polje, both in eastern Hercegovina, have a much longer rostrum, approximately 60% CL; they could not be molecularly identified, and could (but do not necessarily) represent another taxon.

Figures

Figure 2. Endopodites of male pleopods I: Dv, Dugastella valentina from Mijares River; Gi, three aspects of Gallocaris inermis from Grotte de Cambous; Th, Troglocaris (Troglocaridella) hercegovinensis from Vjetrenica; Sp, Troglocaris (Spelaeocaris) pretneri from Dejanova pećina;?Sp, T. (S.) cf. pretneri from Ljelješnica. Scale bars: see Fig. 4; sE for Sp, Th, iTh; sG for Dv, Gi.

Figure 4. Endopodite appendices of male pleopods II: Dv, Dugastella valentina from Mijares river; Gi, Gallocaris inermis from Grotte de Cambous; Th, Troglocaris (Troglocaridella) hercegovinensis (jTh, immature male) from Vjetrenica; Sp, Troglocaris (Spelaeocaris) pretneri from Dejanova pećina; Ta, Troglocaris (Troglocaris) anophthalmus from Kompoljska jama, CL 7 mm; jTa, an immature male T. (T.) anophthalmus, CL 6.4 mm. See the Appendix for a list of abbreviations. Scale bars: see Fig. 4: sA-sH scale bars; sE for Sp, Ta, jTa; sG for Dv, Th; sH for Gi, jTh.

Figure 5. Distal articles of pereopods III and V, and maxilliped I. Dv, Dugastella valentina, male from Mijares river; Gi, Gallocaris inermis, male from Grotte de Cambous; Th, Troglocaris (Troglocaridella) hercegovinensis, male from Vjetrenica; fTh, T. (T.) hercegovinensis, female from Vjetrenica. See the Appendix for a list of abbreviations. Scale bars: see Fig. 4: sD for mx and mxp; sG for pp of Gi and fTh; sH for other pp.

Figure 7. Troglocaris (Troglocaris) bosnica sp. nov. holotype and paratype males. See the Appendix for a list of abbreviations. Scale bars: see Fig. 4: sA for all complete pp; sB for cp; sC for both a, t, up; sD for mx, mxp, distal parts of pp.

Figure 8. Troglocaris (Troglocaris) bosnica sp. nov., holotype male. See the Appendix for a list of abbreviations. Scale bars: see Fig. 4: sD for mx, pp; sE for plp.