Revealing the diversity of a once small taxon: the genus Selenoribates (Acari, Oribatida, Selenoribatidae)

Abstract Three new intertidal oribatid species, Selenoribates elegans sp. n., Selenoribates quasimodo sp. n. and Selenoribates satanicus sp. n. are described from the archipelago of Bermuda. Selenoribates elegans sp. n. is characterized by its slender body shape, Selenoribates quasimodo sp. n. possesses a hunchback in lateral view and Selenoribates satanicus sp. n. exhibits two horn-like projections on its anterior gastronotic region. Based on these new findings, the number of Selenoribates species doubled at once and the distribution of this genus, formerly limited to the Mediterranean and the Red Sea, includes now occurrences in the Atlantic and Indo-pacific Ocean as well. The morphology of Selenoribates quasimodo sp. n. and Selenoribates satanicus sp. n. deviates conspicuously from the other known members of Selenoribates, thus indicating that not only the number of species but also the anatomy of this genus is more diverse than formerly supposed. Nymphs of Selenoribates quasimodo sp. n. show an interesting case of ontogenetic neotrichy, with gastronotic setae being duplicated with each moult.


introduction
The family of Selenoribatidae represents a group of littoral oribatid mites. These mites are air-breathing terrestrial organisms, but they have managed to colonize marine associated habitats and are now exclusively confined to intertidal zones of coastal areas (Pfingstl 2013). They show a transoceanic distribution and occur on shores of the tropics and subtropics (e.g. Schuster 1989, Procheş andMarshall 2001). At present, this family consists of seven genera, namely Arotrobates Luxton, 1992, Carinozetes Pfingstl and Schuster, 2012, Psednobates Luxton, 1992, Rhizophobates Karasawa & Aoki, 2005, Schusteria Grandjean, 1968, Selenoribates Strenzke, 1961and Thalassozetes Schuster, 1963. Rhizophobates and Schusteria have been subject to taxonomic debates (e.g. Karasawa andAoki 2005, Pfingstl andSchuster 2012) and the discreteness of some members of these genera is still unclear. The other genera are yet well delimited and the same applies to the genus type Selenoribates. Strenzke (1961) described the first species of this taxon, Selenoribates foveiventris, then Grandjean (1966) discovered S. mediterraneus, and finally Abd- El-Hamid (1973) added the third species, S. ghardaqensis. Since that time no further species have been detected and not even a single record of the already known species has been published. Accordingly the genus Selenoribates, with only three species, was supposed to be a small taxon with a restricted distribution in the Mediterranean and the Red Sea. The descriptions of the known species provided ample data on the morphology of the adults (Strenzke 1961, Grandjean 1966, Abd-El-Hamid 1973 but only one author (Grandjean 1966) described the nymphs of S. mediterraneus. Concerning the ecology and biology, virtually nothing is known about these species.
In the course of a recent study on intertidal oribatid mites from Bermuda, three new Selenoribates species could be discovered and this finding changes biogeographic and morphological aspects of this genus dramatically. Therefore this paper describes the morphology of the three new species, modifies the distribution pattern and tries to answer the question why the genus Selenoribates has vanished into thin air for more than forty years.

Material and methods
Intertidal algae growing on sandy and rocky substrate, as well as on roots of the black mangrove (Avicennia germinans) were collected on the archipelago of Bermuda during low tide and afterwards put in a Berlese-Tullgren apparatus for the extraction of mites. For investigation in transmitted light all animals were stored in ethanol (70% or pure ethanol), then heated in lactic acid (80°C for about 20 minutes) and afterwards embedded in BERLESE mountant. Observations, photographs and drawings were made with an Olympus BH-2 Microscope equipped with a drawing attachment. Image stacks were obtained by an Olympus E1 digital camera and layered with the Combine ZP software. Inscriptions of drawings were done according to Grandjean (1966Grandjean ( , 1968.

Selenoribates quasimodo
Prodorsum. Rostrum rounded in dorsal view, but slightly projecting anteroventrally in lateral view. Rostral setae (ro) short and smooth. Lamellar setae (le) and interlamellar setae (in) simple, short and smooth. Exobothridial setae (ex) minute. Lamellar ridge conspicuous, but short, not reaching insertions of lamellar setae. Bothridium large cup exhibiting a strongly projecting posterior ridge with three lobe-like protrusions overhanging anterior border of gastronotic region. Sensillus long (ca. 50µm) and flagelliform. Tutorium developed as slightly dorsally curved ridge.
Lateral aspect (Figs 2C,3C). Pedotectum I small but thick, pedotectum II absent. Lateral parts of anterior margin of notogaster broad and deep, showing conspicuous granules. Enantiophyse consisting of two strong triangular teeth orientated against each other. Discidium developed as strong rectangular bulge between acetabulum III and IV.
Ventral region of idiosoma (Figs 2B, 3B). Epimeral setation 1-0-1-1, seta 1b long reaching trochanter II, setae 3b normal length and 4a short. Internal borders of all epimera well visible, sternal apodemes II, sejugal and III well developed. A densely granulated median sternal cavity on epimeron I. Three pairs of short and fine genital setae, arranged in longitudinal rows, anterior two pairs close to each other. Insertion of tendon β next to anterior corners of genital orifice. Aggenital setae absent. Anal plates triangular. Preanal organ triangular in ventral view. Two pairs of short anal setae, an 1-2, present. Two pairs of short and simple adanal setae ad 1-2 present, ad 3 absent. Lyrifissure iad obliquely, adjacent to anterior corners of anal orifice.
Legs. Monodactylous. Long hook-like claws with one conspicuous proximoventral and one minuscule proximodorsal tooth. Trochanters III and IV with an obvious triangular dorsodistal projection. Femora with slightly projecting ventral carinae. All tarsi with one proximal lyrifissure. No porose areas on femora discernable. Solenidia φ 1 on tibia I long and orientated backwards. Chaetome and Solenidia see Table 1.
Etymology. The specific name refers to Quasimodo, the famous bell-ringer of Victor Hugo's historical novel "Notre-Dame de Paris" (1831). This appellation is due to the hunchback of this species shown in lateral view (that does not necessarily mean the species is as ugly as the bell-ringer was supposed to be). The name is given as noun in apposition.
Juvenile instars -common features. Apheredermous. Colour light brown. Integument strongly plicate, except for centrodorsal plate. Thick layer of cerotegument covering whole body. Prodorsum triangular, rostrum rounded. Rostral and lamellar setae short and smooth. Exobothridial setae reduced to a circular vestigial structure. Interlamellar setae very short. Sensillus long and flagelliform. Bothridium large cup, laterally opened. Gnathosoma no obvious differences to adult instar. Hysterosoma slightly concave, plateau-like. Slightly plicate centrodorsal plate occupying two thirds of dorsal hysterosoma, bearing centrodorsal setae. Hysterosomal cupules not discernable in any instar. Large folds framing centrodorsal plate completely, showing fine granular surface. Orifice of opisthonotal gland laterad of seta ad 2 . Integument surrounding anogenital area folded. Dorsal setae of tibiae and genua absent. No porose areas detectable in any stage.
Prodorsum. Rostrum rounded in dorsal view, but slightly projecting anteroventrally in lateral view. Rostral setae (ro), lamellar setae (le) and interlamellar setae (in) short and simple. One pair of minute exobothridial setae (ex). Lamellar ridges conspicuous, reaching insertions of lamellar setae. Bothridium large cup with a projecting   Gnathosoma. Pedipalp pentamerous 0-2-1-3-9 (including solenidion). Solenidion erect, not fused with eupathidium acm. Chelicera chelate, in lateral view forceps-like and each digit with two teeth, whereas from frontal view most distal teeth split into two symmetrical teeth. Distal part of rutellum developed as thin triangular slightly curved inward membrane. Setae a and m long and smooth. Mentum regular, setae h simple, thin and long.
Notogaster (Figs 7A, 8A). Rounded in dorsal view, concave in lateral view. Anterior margin of notogaster incomplete, medially interrupted. On anterior border of notogaster a pair of strongly anteriorly projecting horn-like structures, situated directly posterior of bothridia. Three notogastral depressions on anterior third of notogaster, framed by longitudinal ridges reaching transversal line of setae la and da. Cerotegument of depressions strongly granular. Fourteen pairs of notogastral setae, c 1-2 , da, dm, dp, la, lm, lp, h 1-3 , p 1-3 (approximate length 10-13 µm); c 3 absent. Setae da-dp, slightly serrate, all other setae smooth. Porose areas or distinct pores absent. Five pairs of notogastral lyrifissures present; ia anterior to seta c 2 , in dorsal view hidden under anterior notogastral horn-like projection; im posterior of seta c 2 ; lyrifissures ih, ip and ips laterally close to lateroventral border of notogastral plate. Orifice of opisthonotal gland (gla) next to setae la.
Lateral aspect (Figs 7C, 8C). Pedotectum I small but thick, pedotectum II absent. Lateral sejugal furrow broad and deep, showing conspicuous granulation. Enantiophyse consisting of two strong triangular teeth orientated against each other. Anterior tooth slightly rounded. Discidium developed as strong triangular bulge between acetabulum III and IV.
Ventral region of idiosoma (Figs 7B, 8B). Epimeral setation 1-0-1-1, seta 1b long reaching trochanter III, setae 3b and 4a short. Internal borders of all epimera well visible, sternal apodemes II, sejugal and III well developed. A densely granulated median sternal cavity on epimeron I and a second circular median cavity on a level with apodemes III. Three pairs of short and fine genital setae, arranged in longitudinal rows, anterior two pairs of setae close to each other. Insertion of tendon β next to anterior corners of genital orifice. Aggenital setae absent. Anal valves triangular. Preanal organ shaped triangular in ventral view. One pair of short anal setae, an 1 , located on posterior half of anal valves. Three pairs of short and simple adanal setae ad 1-3 . Lyrifissure iad obliquely, adjacent to anterior corners of anal orifice. Legs (Fig. 9). Monodactylous. Long pointed hook-like claw with one conspicuous proximoventral and a minute proximodorsal tooth. Trochanters III and IV with a triangular dorsodistal projection. Femora exhibiting slightly projecting ventral carinae. All tarsi with one proximal lyrifissure. No porose areas on femora discernable. Solenidion φ 1 on tibia I long, orientated backwards. Chaetome and Solenidia see Table 1.
Etymology. When the author regarded S. satanicus in dorsal view for the first time, the oval contour of the notogaster with its two anterior horn-like projections reminded him of the silhouette of the devil's face, therefore the specific name refers to the Hebraic name Satan and is given as adjective in the nominative singular. Integument. Colour light brown. Cuticle showing dotted pattern. Cerotegument of notogaster granular, larger granules in centre of gastronotic plate. Cerotegument of lateral parts granular, with larger granulation in areas surrounding acetabula. Ventral region finely granular, denser granulation laterad of anal orifice.
Gnathosoma. Pedipalp pentamerous 0-2-1-3-9 (solenidion included). Solenidion erect, not fused with eupathidium acm. Chelicera chelate, forceps-like in lateral view, each digit with two teeth, whereas from frontal view most distal teeth split into two symmetrical teeth. Distal part of rutellum a thin triangular slightly inward curved membrane. Setae a and m long and smooth. Mentum regular, setae h simple, thin and long.
Notogaster (Figs 11A, 12A). Rounded in dorsal view, slightly concave in lateral view. Anterior margin of notogaster complete. On anterior part of notogaster a pair of small X-shaped ridges, close to seta c 1 . Fourteen pairs of simple notogastral setae, c 1-2 , da, dm, dp, la, lm, lp, h 1-3 , p 1-3 (approximate length 17-20 µm), setae c 3 absent. Porose areas or distinct pores absent. Five pairs of notogastral lyrifissures present; ia anterior to seta c 2 ; im posterior and laterad of seta la; lyrifissures ih, ip and ips laterally close to lateroventral border of notogastral plate. Orifice of opisthonotal gland (gla) posterior to seta c 2 . Lateral aspect. Pedotectum I small but robust, pedotectum II absent. Enantiophyse consisting of two strong triangular and pointed teeth orientated against each other. Discidium developed as strong triangular projection between acetabulum III and IV.
Ventral region of idiosoma (Figs 11B, 12B). Epimeral setation 1-0-1-1, seta 1b long reaching trochanter III, setae 3b and 4a of normal length and simple. Internal borders of all epimera well visible, sternal apodemes III and IV well developed. Median sternal cavity on epimeron I divided into two anterior symmetric parts and one unpaired posterior part, all parts strongly granulated. A second triangular median cavity on epimeron III on a level with apodeme 3. Three pairs of short and fine genital setae, arranged in longitudinal rows, anterior pairs close to each other. Insertion of tendon β adjacent to anterior corners of genital orifice. Aggenital setae absent. Anal plates triangular. Preanal organ triangular. Two pairs of short anal setae, an 1-2 . Two pairs of short and simple adanal setae ad 1-2 , ad 3 absent. Lyrifissure iad obliquely, next to anterior corners of anal valves.
Legs. Monodactylous. Long acute hook-like claw with two obvious proximoventral teeth, one close to the base of claw and one proximodorsal tooth. Cuticle finely granular. Femora with projecting ventral carinae. All tarsi with one proximal lyrifissure. Porose areas absent. Solenidia φ 1 on tibia I long, orientated backwards. Chaetome and solenidia see Table 1.
Etymology. The specific name is derived from the Latin word elegans meaning elegant and refers to the slender and delicate shape of the whole body. The name is given as adjective in the nominative singular.

Discussion
Grandjean (1966) mentioned three depressions separated by two X-shaped ridges on the anterior part of the gastronotic region as diagnostic character of the genus Selenoribates.
The new species possess anterior notogastral depressions and sometimes ridges, but they differ in shape and size (Fig. 13). Especially S. quasimodo sp. n. diverges in this respect, showing a single large deepening without any ridges. Notogastral depressions may represent a synapomorphic character of this genus, but the detailed configuration has evolved in different ways. Moreover, Pfingstl and Schuster (2012) described Carinozetes trifoveatus, another selenoribatid species, also exhibiting three anterior gastronotic depressions and two X-shaped ridges, similar to that shown in most of the Selenoribates species. As C. trifoveatus is subject to the same selective constraints of the littoral environment, this character may have evolved convergently. However, median epimeral cavities are also present in Carinozetes Pfingstl &Schuster, 2012 andin Thalassozetes riparius Schuster, 1963, but the possession of two cavities is unique to the genus Selenoribates. Accordingly, this character state represents another synapomorphy of this taxon, whereas the specific shape of the cavities varies among species (Fig. 14), and hence represents a valuable trait for species discrimination. Comparing the new species with the already known members of Selenoribates, one interesting fact becomes obvious (Table 2). Selenoribates elegans sp. n. shows conformity in most of its morphological features with S. foveiventris, S. mediterraneus and S. ghardaqensis, whereas S. quasimodo sp. n. and S. satanicus sp. n. deviate conspicuously from the others as well as from each other. Although S. elegans sp.   on the other hand, may represent members of another lineage within the genus Selenoribates. However, the new species are unambiguous members of Selenoribates and based on their morphology, the genus diagnosis provided by Grandjean (1966) should be slightly adjusted as it was done here in the results part. Knowledge about juvenile morphology of this taxon is largely incomplete and only Grandjean (1966) gave a detailed description of the deuto-and tritonymph of S. mediterraneus. Unfortunately, only the proto-and tritonymph of S. quasimodo sp. n. and the larva of S. satanicus sp. n. were available for the present study, so a comprehensive comparison and analysis of the ontogeny is not feasible. Nevertheless, the instars of S. quasimodo sp. n. and S. satanicus sp. n. posses a centrodorsal plate framed by lateral and ventral folds, the typical habitus of selenoribatid juveniles, and further exhibit conformity in most aspects with the nymphs of S. mediterraneus, confirming the familial and generic relationship of the species. Besides that, the nymphs of S. quasimodo sp. n. show an interesting case of ontogenetic neotrichy with most of the gastronotic setae being duplicated with each moult so that their number increases from stage to stage. This type of neotrichy should be classified as a cosmiotrichy, as the placement of secondary setae follows a distinct arrangement (van der Hammen 1981). Neotrichy shown in juvenile stages is a rare but not unknown phenomenon in oribatid mites. Nymphs of Hydrozetes parisiensis exhibit secondary notogastral setae (Grandjean 1948), the juveniles of Tricheremaeus nemossensis also show neotrichy (Grandjean 1963) and the number of secondary setae is increasing from stage to stage in the lohmanniid Annectacarus mucronatus (Grandjean 1950). But in all these examples the neotrichy persists throughout the adult stage, whereas in S. quasimodo sp. n. all the secondary setae get lost in the adults. However, to clarify the nature and the occurrence of this phenomenon in the genus Selenoribates it is necessary to investigate the complete development of all species.
The biogeographic distribution of the genus Selenoribates was formerly limited to the Mediterranean and the Red Sea, but the records of new species from Bermuda clearly demonstrate that members of this genus also exist on coasts of the Western Atlantic. Moreover, littoral samples from Singapore, kindly provided by Ilse Bartsch, also contained specimens of a yet undescribed Selenoribates species. These new findings suggest that members of this genus show a much wider distribution than formerly supposed (Fig. 15) probably occurring on most coasts of tropic and subtropic regions. However, not only the biogeography, but also the diversity of Selenoribates must be reconsidered based on the present data. Bermuda is, with ca. 55 km 2 , one of the smallest countries of the world and harbours just as much Selenoribates species as the whole Mediterranean and the Red Sea together. Of course the Bermudian intertidal mite fauna may be derived from the Caribbean region and the species found on Bermuda may show a much wider distribution, but this clearly indicates that the real number of species may exceed the presently documented number by far. Pfingstl and Schuster (2012) already stated that within the Caribbean area, with its numerous islands, a relatively high diversity of selenoribatid species should be assumed and the same may apply to many other similar geographic regions, as for example the Indo-pacific area. However, if the genus Selenoribates is much more diverse than formerly known, the question arises why only a few species have been discovered yet and there are several possible answers to this question. First, Selenoribates specimens are relatively small for oribatid mites and may be easily overlooked, second, the littoral environment has been sampled only marginally in matters of oribatid mites and third, it is still unclear which microhabitat within the intertidal zone is usually occupied by Selenoribates species. Even in the present study specimens of this genus were found infrequently and in very small abundances. Accordingly it was not possible to assess if these mites are specifically associated with rocky or sandy substrate or with a specific alga etc. Nevertheless, further studies should answer the question of ecological needs and preferences and maybe then it will be easier to sample Selenoribates and reveal further species.