First Records of Lohmanniidae (Acari, Oribatida) from the Bermuda Islands

Records of nine species of the family Lohmanniidae from the Bermuda Islands, belonging to six genera, are presented and discussed (Haplacarus foliatus Wallwork, 1962, Lohmannia banksi Norton, Metz et Sharma, 1978, L. jornoti Mahunka, 1985, L. similis Balogh, 1962, Meristacarus porcula Grandjean, 1934, Nesiacarus granulatus Hammer, 1972, Papillacarus incompletus (Mahunka, 1985), P. spinosus Bischoff de Alzuet, 1972, Torpacarus omittens omittens Grandjean, 1950). Morphological characteristics, ecology and zoogeographical relationships are analysed. Most Lohmanniidae species were found in terrestrial habitats, a few species colonize the salt-spray area of the supralittoral zone or even the upper eulittoral zone, mainly in mangrove leaf litter. Almost all Lohmanniidae species found on Bermuda occur also in Central or South America. Dispersal by hydrochory can be assumed for most species.


INTRODUCTION
The knowledge of the oribatid mite fauna from the Bermuda Islands is still very poor. Prior to this study 23 species have been recorded. Sellnick (1952) published the first three species collected on Bermuda. Oripoda longiseta Woolley, 1966 was discovered in the slide series from the U.S. National Museum, which was originally found on plant material ("unknown cuttings") at Boston, introduced from Bermuda without detailed site records (Woolley 1966, Balogh andBalogh 1990). Niedbala (2002) recorded 18 "Ptyctimous" oribatid species from Bermuda. Among them, three species (Atropacarus paraclavatus Niedbala, 2002, Mesoplophora paragaveae Niedbala, 2002, Phauloppia gracilis Sellnick, 1952 were found exclusively on Bermuda up to now. Recently a new species of the family Fortuyniidae, Fortuynia atlantica Krisper et Schuster, 2008 was described which is hitherto only known from the Bermuda Islands, occurring in many localities along the rocky coastlines (Krisper and Schuster 2008). An additional study, also about littoral oribatid mites, was published by Pfingstl and Schuster (2012). In the course of two collecting trips made by the second author to the Bermudas in the summers of 1977 and 1981, numerous Lohmanniidae species were collected. These taxa are presented in the present paper.

ENVIRONMENTAL SETTING
The Bermuda Archipelago, located near the western edge of the Sargasso Sea in the Atlantic Ocean, consists of about 150 islands with a total terrestrial surface of 55 km 2 , the largest island of which, called "Main island" or "Bermuda" covers about 40 km 2 . Most of the other islands are very small and devoid of dense terrestrial vegetation. The islands are of oceanic origin, a land bridge to the American continent has never existed. The nearest distance to Cape Hatteras, North America, is about 960 km. Originally formed by a volcanic seamount the subaereal part is covered by coralline limestone, partially broken down into sand and fused to aeolian sandstone. The islands are largely flat, the highest point is Town Hill on Main island with an altitude of less than 100 m. There is no mountainous region. On the other hand, the islands have more than 100 km of coastline, surrounded by coral reefs. Ecologically the shoreline can be divided into three different parts: sandy beaches, rocks, and remains of a typical mangrove vegetation on some coastal sections. The inland environment is poor and characterized by sandy soils with low amounts of organic matter, small forests, bushes and grassland. Rivers or brooks are absent. Remarkable are numerous Karst caves.
The climate of the Bermudas is subtropical. It is largely influenced by the Gulf Stream which represents an important climatic factor. Additionally, this ocean current arising in the Caribbean region, is a significant factor for the colonization of the Bermuda islands by plants and animals.
The terrestrial vegetation includes different trees and shrubs, forming forests in some places. Endemic plants are rare (e.g. Juniperus bermudiana, "Bermuda Cedar" or Sabal bermudana, "Bermuda Palmetto", the only native palm). Since discovery by humans in 1503, numerous species have been introduced to the islands, deliberately or accidentally, which were responsible for the remarkable changes in the native flora and fauna of the archipelago as well as the subsequent changes in the original vegetation and landscape. A characteristic introduction is the Australian Casuarina-tree.

Haplacarus foliatus
Remarks: The specimens from Bermuda correspond to the original description (Wallwork 1962) and are considered conspecific. The description by Wallwork (1962) is based on one adult and one tritonymph. Haplacarus foliatus is very similar to H. javensis Hammer, 1979. Main differences between the two species are: The notogastral setae are thicker in adults of H. foliatus, but more slender in H. javensis (this character could not be observed in the studied juvenile instars); notogastral setae e1 are longer than f1 in H. foliatus; transverse band s7 is incomplete in H. foliatus, but complete in H. javensis. A comparison with adults and tritonymphs of H. javensis from Belize and Cocos Island, Costa Rica (Schatz 1994b), was possible. Haplacarus foliatus is also morphologically similar to H. bengalensis Bhattacharya, Bhaduri et Raychaudhuri, 1974, but the latter species has shorter notogastral setae.

Lohmannia banksi Norton, Metz et Sharma, 1978
Remarks: A comparison with the paratype of this species was possible. The adult and juvenile specimens found on Bermuda correspond to this type (adult) and the original description (Norton et al. 1978) and are considered conspecific. Leaf-like notogastral setae of different shape are found in several species of the genus. In their key of the genus Lohmannia, Balogh and Balogh (1987) state the notogastral setae of this species "without midrib" but apparently they misinterpreted the drawing of Norton et al. (1978), where the midribs of the notogastral setae are barely indicated and not specially mentioned in the text. The body size of all instars from the population in Bermuda are in the range of the population from North Carolina.
Remarks: A direct comparison with specimens from Galapagos was possible. The specimens from Bermuda correspond to those and the original description (Mahunka 1985a) in most respects and are considered conspecific. The body size of the specimens from Bermuda is in the range of the population from Guadeloupe (length 794 -826 µm) but considerably smaller than the population from the Galapagos Islands (930 -1020 µm, Schatz 1993). Also the deutonymph is smaller than in specimens from Galapagos (680 -725 x 355 -380 µm, Schatz 1993). The species is very similar to L. banksi Norton et al., 1978. It differs mainly in having smaller posterior exobothridial setae, smaller and differently shaped notogastral setae, and setiform posterior medial genital setae.
General distribution: Antilles, Guadeloupe: under shrubs near the sea (Mahunka 1985a); Ecuador, Galapagos Islands: under Sesuvium shrubs in the littoral zone on Santa Cruz Island, in leaf litter of a dense elfin-forest on Volcán Alcedo (Isabela Island), in fern litter and moss near a fumarole on Fernandina Island (Schatz 1993); Central America: Belize Light House Reef: Half Moon Cay, in leaf litter (Schatz 1994b: 276;Schatz 2006); Cuba Ciudad de La Habana, Santiago de las Vegas, sugar cane (Saccharum spp.), leaf litter and soil (Prieto and Calderón 1992); first record for Bermuda.
Remarks: A direct comparison with specimens from Galapagos was possible. The specimens from Bermuda correspond to those and the description given in Schatz (1993) in most respects and are considered conspecific. Differences are the smaller body size in most of the population from Bermuda (Peru 830 µm, Galapagos 800-930 µm), and slightly shorter notogastral setae. The two specimens from sample BE 301 have a larger body length of 830-860 µm. Differences between Lohmannia similis Balogh, 1962 and the similar species L. lanceolata Grandjean, 1950 resp. L. bifoliata Willmann, 1936 are given in Schatz (1993).

Remarks:
The single specimen found in Bermuda corresponds to the original description (Grandjean 1934) and to the specimens found in Galapagos and Central America (Schatz 1994b) in most respects and are considered conspecific. The body size of the Bermuda specimen is slightly smaller than the population from the Galapagos Islands (length 1020 -1070 µm) and from Cocos Island (990 -1065 µm). Grandjean (1934) reports a length of 950 -1030 µm; Balogh and Balogh (1987) of 940 -1090 µm.
Remarks: The specimens found in Bermuda correspond to the original description (Hammer 1972) and to the specimens found in Central America (Schatz 1994b) in most respects and are considered conspecific. The body size of the population from Bermuda is slightly smaller, but in the range of the populations from Tahiti and Central America.
General distribution: Tahiti, along the coast in Cyperus vegetation beneath a hedge (Hammer 1972); Japan, leaf litter from an evergreen broadleaved forest on a seaside hill near the southern end of Kasado-jima Island (Wada 1987), Ryukyu Islands (Aoki 2009); Central America: Belize and Guatemala: in moist, decayed leaf litter under dense tree and bush vegetation as well as in hardwood tropical rain forest (Schatz 1994b(Schatz , 2006; first record for Bermuda.
The specimens found in Bermuda were identified by comparison with the type specimens of this species. The populations of this species from St. Lucia, Antilles, and Bermuda are conspecific. The suture between the anal and adanal plates is undoubtedly complete, but weakly developed in the posterior part.
Remarks: The specimens found in Bermuda correspond to the original description (Bischoff de Alzuet 1972) in most respects and are considered conspecific. A difference is the smaller body size of the adult specimens in Bermuda (614 x 305 µm in the specimen from Argentina).
2. Sensillus: The number of branches on sensillus is variable: 9 in specimens from Venezuela, 10-14 in specimens from Bermuda; 15-16 in other described subspecies.
3. Transverse lines on notogaster: Among the described subspecies this character is present only in T. omittens omittens. In most specimens from Bermuda the transverse lines are present but very weakly developed; in some specimens the lines are invisible.

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Schatz H. and Schuster R. 4. Length of notogastral setae: The size ratio of c2 : c3 is about 1 : 2 in most Bermudan specimens, as is usual in T. omittens omittens, but in specimens of sample BE 308 the setae c2 are very long, causing a ratio of almost 1 : 1 (in adult and tritonymph). In the other described subspecies the setae c2 are maximally half as long as setae c3. The setae f1 are long in all Bermudan specimens as is usual in T. omittens omittens and T. omittens paraguayensis.
5. Shape of inner epimeral setae: The epimeral setae of the median row (1a, 2a, 3a, 4a) are long and smooth in most Bermudan specimens as is usual in T. omittens omittens, but in one adult of sample BE 288 setae 1a are long and ciliate. In the other described subspecies these epimeral setae are long and ciliate in T. omittens paraguayensis resp. short and smooth in T. omittens galapagensis.
6. The solenidion ω1 on tarsus I has a distinct dilation distally in all populations of T. omittens omittens investigated in this respect, but one additional weaker basal dilation in most specimens in the population on Bermuda. The other described subspecies have 2 weaker dilations each.
These differences do not justify the separation of the population or part of the population of T. omittens omittens on Bermuda as a separate taxon. However, the variability of characters in different populations of this widespread species might be explained by isolation and the parthenogenetic reproduction mode of the Lohmanniidae (Norton and Palmer 1991 Grandjean 1950, Wallwork 1962, Mahunka 1985a, 1985b, Schatz 1994a, 2006, Starý 1998, Prieto and Schatz 2004, Subías et al. 2004); first record for Bermuda. Balogh (1962) and Bischoff de Alzuet (1971) recorded T. omittens also from Peru and Argentine. It is uncertain whether these individuals belong to T. omittens paraguayensis Balogh et Mahunka, 1981 or to T. omittens omittens Grandjean, 1950(Schatz 1994a).

ECOLOGICAL NOTES
The Bermuda Islands are predominantly low without much ecological diversity. Most Lohmanniidae species occur in different rather terrestrial habitats, in sandy soils and leaf litter (Lohmannia jornoti, Meristacarus porcula, Nesiacarus granulatus, Papillacarus incompletus, P. spinosus, Torpacarus omittens omittens). Lohmannia banksi was the most frequent species on the islands (11 samples, 15 adults and 31 juvenile instars) in a wide range of habitats, from terrestrial locations in the interior with leaf litter and sandy soils to the edges of brackish and salty pools and the salt-drenched supralittoral zone. Haplacarus foliatus (2 samples, 5 juvenile instars) and Lohmannia similis (3 samples, 17 adults and 25 juvenile instars) were mainly found in sandy or muddy samples from the supralittoral zone.
Some Lohmannidae species (adults and juveniles) colonize the salt-spray area of the supralittoral zone and were even found in lower regions of the littoral zone, mainly in leaf litter near Avicennia mangroves (Haplacarus foliatus, Lohmannia similis). On the Galapagos Islands a total of 13 Lohmanniidae species was found (Schatz 1998, Schatz unpublished data), among them six species prevailing in the littoral zone, mainly in leaf litter under mangroves (including Lohmannia similis and Meristacarus porcula). Some of those species were even collected from the sea surface between the islands, washed from the shore (Peck 1994). But despite those findings in the border area between land and sea Lohmanniidae cannnot be considered to be exclusively thalassobiotic. Several members of the family seem to have a certain tolerance towards saline conditions, but as yet no species was found spending its whole life cycle in periodically inundated littoral zones. Furthermore Lohmanniidae species seem to avoid the littoral zone of rocky coasts. It is possible that their occurrence in saline conditions within the littoral zone is linked to the leaf litter of mangroves (Schuster, unpublished data of studies in Central and South America).

ZOOGEOGRAPHICAL REMARKS
Previous to this study no single Lohmanniid species was recorded from the Bermuda Islands. All species except Haplacarus foliatus were previously known from North, Central or South America: (North America, North Carolina: Lohmannia banksi. Central America: L. banksi, L. jornoti, Meristacarus porcula, Nesiacarus granulatus, Papillacarus incompletus, P. spinosus, Torpacarus omittens omittens. South America: Lohmannia similis, Meristacarus porcula, Papillacarus spinosus). Since the Bermuda Islands are situated in the Gulf Stream a hydrochorous dispersal from Central America can be assumed for most species, but also a zoochorous (by migrating birds and their nesting material) and anthropochorous dispersal with plant material seems possible.