Freshwater halacarid mites (Acari: Halacaridae) from Madagascar. New records and the description of a new species

In recent years the numbers of aquatic mite species from Madagascar has increased considerably (Gerecke 2004a, b, 2006, 2009; Goldschmidt 2008; Tuzovski and Gerecke 2009), but the area is still a white spot with respect to knowledge of its freshwater halacarid (Halacaridae) fauna. Recently, some halacarid specimens were extracted from sandy deposits of the banks of streams and creeks. These samples included four species, namely Limnohalacarus cultellatus Viets, 1940, Limnohalacarus novus Bartsch, 2013, Lobohalacarus weberi (Romijn and Viets, 1924), and a new species of the genus Ropohalacarus. The new species, Ropohalacarus pallidus n. sp., is described, and the characters of the other species are outlined. The three genera collected in Madagascar are cosmopolitan and the Lobohalacarus and Limnohalacarus species are wide-spread. The halacarid fauna of Madagascar seems to be poor in endemic species, which is contrary to the situation for the freshwater Hydrachnidia mites. Future studies will certainly increase the number of halacarid species but not the percentage of endemics.


INTRODUCTION
Madagascar with its diverse aquatic mite fauna (Gerecke 2004b;Goldschmidt 2008) is a terra incognita as to the knowledge of its freshwater halacarids. From the African continent, most records and descriptions of halacarids are from the 1950th to 1970th (Walter and Bader 1952;Bader 1967Bader , 1968Green et al. 1974). Reasons for absence of halacarid records from Madagascar may be the size of the mites, their colour and life-style. Most of the adults have an idiosomal length of distinctly less than 600 µm, often the species are pale and lack conspicuous pigment spots, and halacarids are benthic, crawling rather slowly amongst a substratum.

MATERIALS AND METHODS
The halacarid mites were extracted from the banks of small streams and creeks by digging pits into the sandy deposits and filtering the seeped water (Karaman-Chappuis Method). Collectors are Drs R. Gerecke and T. Goldschmidt. The mites were cleared in lactic acid, rinsed in glycerine and mounted in glycerine jelly. The holotype, paratypes and voucher specimens are deposited in the Zoological Museum, Hamburg (ZMH), additional material in the author's collection.
Rarely occurring numbers of setae or acetabula are in parentheses. The legs are numbered I to IV, the segments are trochanter, basifemur, telofemur, genu, tibia, and tarsus. The number of setae on the tarsi includes the solenidion but excludes the parambulacral setae. In the illustrations marginal setae are shown either in the dorsal or in the ventral aspect but not in both. Drawings were done with a drawing tube.

RESULTS
Four species were extracted from sandy deposits of banks of rivers, Limnohalacarus cultellatus Viets, 1940, Limnohalacarus novus Bartsch, 2013, Lobohalacarus weberi, and a new Ropohalacarus species, R. pallidus n. sp. GENUS Limnohalacarus WALTER, 1917 Type species -Halacarus wackeri Walter, 1914. Diagnosis (adults) -Plates delicately and evenly punctate. Dorsum with anterior and posterior dorsal plate and pair of ocular plates, five pairs of gland pores and three to four pairs of very short dorsal setae. Ocular plate and sclerite with third gland pore often fused. Venter with anterior and pair of posterior epimeral plates and genital plate. Either plates separated or all fused to a shield. Anterior epimeral plate with three pairs of setae, posterior plates with a dorsal, lateral and ventral seta. Acetabula arranged along lateral margins of genital plate (or part corresponding to this plate). Females with 3-10 pairs of perigenital setae, males with 17-30 pairs of setae. Female genital opening near posterior margin of genital plate and covered by large genital sclerites. Male genital opening smaller, removed from posterior margin of genitoanal plate. Anal sclerites much smaller than genital sclerites. Base of gnathosoma wide, rostrum conical. Palps four-segmented, attached dorsally. Second palpal segment with short basal and long distal seta, third segment with large ventral spine, fourth segment with six setae and apical spine. Leg segments slender, in general bearing conspicuously long setae. Genua I and II shorter than these legs' telofemora. Tibia III with four ventral setae, mostly two of them bipectinate. Tarsi I to IV with 1, 0, 0, 0 ventral setae and 4, 4, 4, 3 dorsal setae. Tarsi I to III with solenidia in dorsolateral position. Paired claws of tarsi with pectines. Arrangement and size of tines on claw I different from those of following tarsi.
Comments -The genus in spread on all continents except Antarctica. Records are from fresh water as well as from coastal and inland saline waters. Limnohalacarus includes at present 13 species (Bartsch 2009(Bartsch , 2013.
Diagnosis (female, Madagascar individual) -Idiosoma pale, its length 274 µm. Dorsal plates with reticulate ornamentation. Anteriormost part of anterior dorsal plate smooth and separated from reticulate major part; anterior dorsal plate rectangular, 1.1 times longer than wide. Ocular plates sub-circular, 1.1 times longer than wide. Sclerite with gland pore triangular, not fused with ocular plate. Posterior dorsal plate elongate, 1.7 times longer than wide and 2.4 times longer than anterior dorsal plate. With four pairs of dorsal setae, second pair of setae in striated integument between anterior dorsal plate and ocular plates; adanal setae on anal cone, in ventrolateral position. Ventral plates (anterior, pair of posterior epimeral plates and genital plate) separated. Genital plate with four to five pairs of acetabula, three pairs of perigenital and two pairs of subgenital setae. Gnathosoma 1.7 times longer than wide. Rostrum slender. Both pairs of maxillary setae slender. Pharyngeal plate removed from basal margin of gnathosoma by more than half the length of pharyngeal plate. Second palpal segment basally abruptly increased in height; its dorsal margin straight. Telofemora I to III 1.8-1.9 times longer than high. Leg chaetotaxy, from trochanter to tarsus: leg I, 1,4,4,6,7,5;leg II,1,3,4,6,6,4;leg III,1,2,3,4,7,4; leg IV, 1, 1, 3, 3, 6, 3. Ventromedial seta on tibia I and II and both ventromedial setae on tibia III bipectinate, all other setae smooth. All tarsi with pair of single parambulacral setae. Each claw with lamellar ventral process. Claws on tarsus I slender, with about eight delicate tines near apex. Claws of following tarsi with J-shaped arranged pectines, each with about 15 -18 tines.
Distribution -Records are from North, Central and South America, from Europe (Hungary) and India (Bartsch 2011b(Bartsch , 2013.
Remarks -Adults of the two species at present known from Madagascar can easily be separated because of (1) the shape of the ocular plates, including versus excluding the sclerite with the gland pore, (2) the ventral plates, separated versus fused to a shield, (3) the length of the rostrum, short versus elongate, and (4) the claws on tarsus I, with numerous long tines versus a few delicate ones. The size of the rostrum and the shape of claw I can be used to separate the nymphal and larval stages of the two species.

GENUS Lobohalacarus VIETS, 1939
Type species -Walterella weberi Romijn and Viets, 1924 Diagnosis (adults) -Idiosoma often with frontal spine. Dorsum with anterior and posterior dorsal plate, pair of ocular plates and seven pairs of idiosomatic setae. Gland pores inconspicuous. Ocular plate with two setae. Ventral plates fused to a shield. Area corresponding to anterior epimeral plate with three pairs of setae and one pair of epimeral pores, area of posterior epimeral plates with one dorsal, one marginal and one ventral seta. Female genitoanal plate with three to seven perigenital setae on either side of genital opening and 79 one to three acetabula on each genital sclerite; no acetabula outside genital sclerites. Gnathosoma slender. Four-segmented palps attached laterally. Second palpal segment with single seta, third palpal segment with small spur, fourth palpal segment basally with three setae. Leg I slightly more robust than leg II. Telofemora and genua of legs almost equal in length. Genu and tibia I with ventral spurs. Tarsi I to IV with 4, 4, 3-4, 3(-4) dorsal and 3, 0-1, 0-1, 0-1(-2) ventral setae. Tarsus I with enlarged lateral fossa membrane. Solenidion on tarsus I in dorsolateral, on tarsus II in dorsomedial position. Paired claws distinct, central sclerite with dent-like process.

Lobohalacarus weberi (Romijn and Viets, 1924)
Material examined -One female ( Diagnosis (female, Madagascar individuals) -Length 284 -304 µm. With frontal spine. Dorsal plates uniformly foveate. Genital sclerites with two and three acetabula, genital area with five pairs of perigenital setae. Telofemora III and IV with 2/0 dorsal/ventral setae. Ventral flank of genu I on one leg with spur and seta, on other leg with two spurs; each ventral flank of tibiae II to IV with one smooth and two pectinate setae, tarsi III with 4/1 dorsal/ventral setae, and tarsi IV with 3/1 setae. Length of deutonymphs 234 -244 µm.
Remarks -In Lobohalacarus weberi in general, character states are known to vary in individuals from different localities but also within a population (cf. Bartsch 2007bBartsch , 2011b. From Madagascar only two adults were available for study.

GENUS Ropohalacarus BARTSCH, 1989
Type species -Porohalacarus uniscutatus Bartsch, 1982. Diagnosis -Anterior and posterior dorsal plate fused, ocular plates reduced to minute sclerites or absent. Gland pores reduced. Dorsum with four to five pairs of idiosomatic setae; adanal setae lacking. Anterior and posterior epimeral plates and genitoanal plate fused. Area representing anterior epimeral plate with three pairs of setae, posterior epimeral plates with two to three setae. Female with three pairs of acetabula, all on genital sclerites, and two to three pairs of perigenital setae on genitoanal plate. Subgenital setae lacking. Palps foursegmented, attached dorsolaterally. Second palpal segment with one to two similar-sized setae, third palpal segment with small medial spur, fourth palpal segment with conspicuously wide seta. First and second pair of legs similar in shape. Genua of all legs shorter than both telofemora and tibiae. Tarsi I to IV with 4, 3-4, 3, 2 dorsal and 0-1, 0-1, 0, 0 ventral setae. Solenidia on tarsi I and II in dorsolateral position. Paired claws large, central sclerite with small, dent-like process.
Description (female) -Length of idiosoma 217 -238 µm, length of holotype 238 µm, width 132 µm. Idiosoma about 1.8 times longer than wide; its colour pale, without spots of eye pigment. Inter-val between insertions of legs II and III equalling almost half the length of idiosoma. Anterior and posterior dorsal plate fused to a shield, 215 µm long, 80 µm wide (Figure 1a). Ocular plates reduced, marginal parts incorporated into dorsomarginal parts of ventral shield. All ventral plates fused to a shield, its length 212 µm (from camerostome to end of anal cone). Ventral shield extending dorsad, forming frontal margin of idiosoma with its short, obtuse frontal process. Surface of dorsal shield with delicate porosity and faint foveate ornamentation (Figure 1a Gnathosoma short, wider than long, its length 37 µm, width 40 µm. Rostrum wider than long, triangular in ventral aspect (Figure 1d). Tectum truncate. Palps extending beyond rostrum. Second palpal segment with single seta in apical half. Third palpal segment with spur in medial position (Figure 1c). Ventral seta of fourth palpal segment wider than dorsal seta.
All legs distinctly shorter than idiosoma. Legs III and IV slightly longer and more slender than legs I and II. Telofemora I and II about 1.5 times longer than high, telofemora III and IV 1.6 times. Leg chaetotaxy from trochanter to tarsus (parambulacral setae excluded): legs I and II, 0, 2, 3, 3, 7, 4; leg III, 1, 1, 2, 2, 5, 3; leg IV, 0, 0, 2, 3, 5, 2 (Figure 2a-d). Ventral spine on genu I slightly longer than length of that segment. Tibiae I to IV with 3, 3, 2, 2 ventral spines and 2, 2, 1, 1 short dorsal spurs. Tarsi I and II each with three fossary setae, a dorsolateral clavate solenidion but no ventral setae. Tarsus I with delicate porus that may be remnant of a famulus ( Figure  1e). On tarsi I and II paired fossary setae unequal in length, dorsolateral seta somewhat thicker and longer than dorsomedial seta (Figure 1f). Tarsus III with three dorsal setae, one of setae in dorsolateral position and equalling a solenidion (Figure 1g). Tarsus IV with two dorsal setae, both equal in size. On tarsi III and IV dorsal fossary seta lacking. Paired claws with a slightly widened apical process, each process with four delicate tines. No tines on shaft of claw. Median claw slender, hook-like.
Variants -Tarsus II of one of the paratype females without dorsal fossary seta (Figure 1h).
Remarks -Ropohalacarus pallidus is the second species of this genus. Characters which separate R. pallidus from R. uniscutatus are: (1) dorsal plates delicately foveate versus reticulate, (2) anterior margin equivalent to dorsal portion of anterior epimeral plate versus to anterior part of dorsal shield, (3) second pair of dorsal setae within dorsal portion of anterior epimeral plate versus in striated integument, (4) second palpal segment with single seta versus two setae, (5) genu I with three versus four setae, (6) tarsi I and II without versus with a ventral seta.

CHARACTERS
The two presently known Ropohalacarus species have the anterior and posterior dorsal plate and the anterior and posterior epimeral plates and genitoanal plate fused. Most halacarids have a pair of ocular plates, plates which often bear corneae and eye pigment, in R. pallidus the ventral shield extends dorsad and includes remnants of the ocular plates, whereas in R. uniscutatus the ocular plates are reduced to minute sclerites which are situated in the dorsal integument. Within several halacarid genera a fusion of two or more plates on either the dorsal or ventral flank is a common phenomenon, but a fusion of both the dorsal and ventral plates is at present known only in the two Ropohalacarus and a few Rhombognathus species (e.g., R. aspidotus Bartsch, 2006, R. conjunctus Bartsch, 1986, R. parvulus Viets, 1939, R. peltatus Viets, 1939, R. similis Bartsch, 1977, R. scutulatus Bartsch, 1983).
In general a fusion of plates seems to be correlated with a life in an environment with mechanical stress (Bartsch 2010). In adults of the above mentioned genus Lobohalacarus all ventral plates are fused, but not the dorsal plates. Due to the fusion of the plates to a dorsal and ventral shield, the two Ropohalacarus species have a solid exoskeleton. Both species are expected to live in subterranean or hyporhithral sandy deposits. The plates of the two nymphal stages of R. pallidus are, if at all, separated by only few striae of soft integument and the surface of the plates is not as smooth as in the adults. In contrast, almost all halacarid nymphs have the dorsal and ventral plates distinctly separated by striated integument and the ornamentation of the plates is less conspicuous than in adults. In general the growth during a juvenile stage is by a dilatation of this striated integument, in R. pallidus the textured surface of the plates of nymphs may allow a slight dilatation.
The two Ropohalacarus species have their hind legs far in the posterior half of the idiosoma, the insertions of legs III and IV are at about 0.7 and 0.8 (with reference to the length of idiosoma, from anterior to posterior), the gap between insertions of legs II and III is somewhat less than half the length of the idiosoma. A similar posterior position of the legs is present in the marine genera Anomalohalacarus, Arenihalacarus, Australacarus, and Parhalixodes (Abé 1991;Bartsch 1987Bartsch , 1993Laubier 1960). Anomalohalacarus and Arenihalacarus live in sandy deposits (Abé 1991;Bartsch 2006), species of these two genera have small, delicate dorsal and ventral plates, the plates are separated by large areas of striated integument, their legs are slender, leg I is longer than the other legs. Anomalohalacarus has been watched alive, it moves rapidly on the convex surface of grains, the body is extremely flexible, able to turn back within minute interstitia. The two genera Australacarus and Parhalixodes, too, have small, reduced dorsal and ventral plates; their mode of living is not known but representatives of these genera are expected to feed as ectoparasites (Laubier 1960;Bartsch 1987Bartsch , 1993. The two Australacarus species studied by the author had a dark body content; rostrum and chelicerae are slender, bristle-and stylet-formed, the palps form a trough (Bartsch 1987(Bartsch , 1993. The dark body content is expected to represent the remnants of a diet of, e.g., haemolymph. One may speculate that the ancestors of Australacarus have been interstitially living forms which got used to stick to a sedentary macrofauna and feed on the body fluids. In contrast to the above mentioned genera, the idiosoma of Ropohalacarus is less slender and both the dorsal and ventral plates are fused to shields. The legs of the Ropohalacarus species are rather short, with only small differences in the length between the anterior and posterior legs, the gnathosoma is short. Anomalohalacarus and Arenihalacarus are restricted or bound to the interstitia amongst sediment particles but Ropohalacarus is expected to push particles out of the path rather than wriggling around them.
Ropohalacarus pallidus has an unusual low number of setae. The chaetotaxy of the legs is reduced when compared with other halacarids. There are no setae on the trochanters I and II, whereas in R. uniscutatus, as well as in species of other halacarid genera, these leg segments bear a seta, in the adults as also in the juveniles (Bartsch 1982a(Bartsch , 2003(Bartsch , 2007a(Bartsch , 2011a. A reduction of the number of setae on the legs is documented in the genus Copidognathus. This genus holds one-third of all halacarid species, it is spread world-wide, records are from all depth and temperature zones, from marine and even freshwater habitats, from the mesopsammal as well as from the surface of sediment, algae and colonial organisms, the genus also includes a few parasitic living forms (Bartsch 2004). The more than 340 described species demonstrate a uniformity in the number of setae on idiosoma and legs. In general the genua I to IV bear 4, 4, 3, 3-4 setae, the tibiae I to IV 7, 7, 5, 5 setae, and in most species the telofemora I and II have five setae each. Only a few species have a reduced number of setae, e.g., C. cerberoideus Bartsch, 1991 andC. consobrinus Bartsch, 1991, both known from Hong Kong, C. cribellus Bartsch, 1993 andC. psammobius Bartsch, 2008, known from western and eastern Australia, respectively (Bartsch 1991(Bartsch , 1993(Bartsch , 2008b. All four species were extracted from sandy deposits, they are small in size (174 -232 µm), the number of setae on the genua is reduced to 2-3, 2-3, 2-3, 3, the tibiae I and II of C. cribellus and C. psammobius bear six setae. Another species with a reduced number of setae on the genua I and II (three setae each) and tibia I (six setae) is C. inusitatus Bartsch, 1989. This species has very long and slender legs; it was extracted from a depth of 1508 m (Pacific Ocean) (Bartsch 1989) and does certainly not live within sandy deposits. The long-legged C. curiosus Bartsch, 1982, from about 800 m depth (Indian Ocean), bears three and two setae on genua I and II, respectively (Bartsch 1982b). As demonstrated by species of the algae-inhabiting genus Isobactrus (Bartsch 2010), a reduction of the number of setae on the legs is not restricted to species living in and on a sediment. According to the though sparse data set, several of the Isobactrus species living in habitats exposed to long-term or severe desiccation have a lower number of setae on the legs than those living in almost permanently wet habitats. In general, reduction of setae seems to be correlated with life in a 'harsh' environment, with unfavourable biological (food intake) and chemical parameters. Though speculative, as the regime of dissolved and solid inorganic and organic matter in the interstitial water of the Madagascar river banks is unknown, the condition R. pallidus meets is expected to be meagre and may have led to a reduction of the number of setae on the legs.

FAUNA
Four halacarid species, in three genera, are now known from Madagascar. The four species are from running water; no samples have been taken in standing water. All three of the freshwater halacarid genera collected in Madagascar are cosmopolitan and three of the four halacarid species are known from outside Madagascar and outside Africa, the continent closest to Madagascar.
Lobohalacarus weberi is mentioned from the northern and southern hemisphere, from North and South America, Europe, Asia, Australia, Oceanic Islands, and also from Africa. Limnohalacarus cultellatus was first described from islands off the northern coast of South America, in the meantime there are records from North, Central and South America, Europe and India (Viets 1940;Bartsch 2011bBartsch , 2013. Representatives of the other Limnohalacarus species from Madagascar (L. novus) have been found in Australia, Queensland, Moreton Bay (Bartsch 2013). The fourth species, Ropohalacarus pallidus, may be restricted to Madagascar, though one should keep in mind, studies on halacarids in adequate habitats of the nearby Africa or India are lacking. Notewor-thy is that R. uniscutatus, the second species of this genus, has records from North America, northern Africa and eastern Australia (Bartsch 2009).
In contrast to the sparse number of halacarids, the fauna of Hydrachnidia seems to be rich in species and numbers, obviously including a high percentage of endemisms. A recently updated list of Madagascar Hydrachnidia mentioned 63 species or subspecies, 35 species (56 %) were only known from Madagascar, 24 species (38 %) from both Africa and Madagascar, and four species (6 %) had an even wider distribution (Gerecke 2004b). Since, several more species have been described (Gerecke 2006(Gerecke , 2009Goldschmidt 2008;Tuzovsky and Gerecke 2009). Goldschmidt (2008), who concentrated the studies on the family Anisitsiellidae (Hydrachnidia), found 24 species, 23 of which were new to science. A striking difference between the presence of halacarid and hydrachnid endemisms in the freshwater mite fauna is documented from New Zealand. At a species level almost all species of the Hydrachnidia are exclusively taken in New Zealand, and in respect to the genera, 35 out of 59 (59 %) are endemic; no more than 12 genera (20 %) of the New Zealand fauna are widespread, seven genera (12 %) are cosmopolitan (Sirvid et al. 2010). By contrast, the New Zealand freshwater halacarid fauna is surprisingly similar to that found in equivalent habitats in Europe and North America (Bartsch 2007b). Four species, in three genera, are at present known from New Zealand, and all genera and three of the species are cosmopolitans (Bartsch 2007).