Taxonomy, Acari, Oripodoidea, epiphyte, microhabitat, rainforest, Eucalyptus woodland, Queensland

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1 A novel association between oribatid mites and leafy liverworts (Marchantiophyta: Jungermanniidae), with a description of a new species of Birobates (Acari: Oribatida: Oripodidae) Matthew J. Colloff 1* and Andi Cairns 2 1 CSIRO Entomology, GPO Box 1700, Canberra, ACT 2601, Australia 2 School of Marine and Tropical Biology, James Cook University, Townsville, QLD 4811, Australia * Corresponding author Matt.Colloff@csiro.au Abstract This paper describes a new species of oribatid mite, Birobates hepaticolus sp. nov. from eucalypt woodland and rainforest in North Queensland, Australia. Adults and immatures of B. hepaticolus live completely enclosed within the ventral lobules of the corticolous liverwort Frullania ferdinandi-muelleri Steph. The ventral lobes, which sequester and store water, provide a protected, moisture-buffered microhabitat on tree bark that would otherwise be subject to extremes of wetting and drying. Analysis of gut contents indicates that B. hepaticolus appears to feed on liverwort tissue. To our knowledge this is the first documented example of an association between an oribatid mite and a leafy liverwort based on the provision of food and habitat. The genus Birobates is redefined and diagnosed. Key words Taxonomy, Acari, Oripodoidea, epiphyte, microhabitat, rainforest, Eucalyptus woodland, Queensland INTRODUCTION Oribatid mites, containing almost 10,000 described species, are often the most numerically abundant and diverse group of arthropods in soils and leaf litter, though many taxa are also

2 arboreal. Most are particulate microbivore-detritivores or mycophages. Some are opportunistic predators and a few feed on live plant tissue (Norton & Behan-Pelletier 2009). The arboreal microhabitats of oribatid mites include the bark (Proctor et al. 2002) and the canopy (Walter 1999; Walter & O Dowd 1995), as well as amongst epiphytic cryptogamic plants on trunks, branches, twigs and leaves (Walter & Behan-Pelletier 1999). Associations between oribatid mites and cryptogams are well-known, particularly those of mosses (reviewed by Gerson 1982; Lawrey 1987) and lichens (reviewed by Seyd & Seaward 1984). However, almost nothing is known about the association between these mites and liverworts. Oribatids have been recorded from corticolous and saxicolous liverworts from the Massane Forest in the eastern French Pyrénées, though most of the species were common and widespread in mosses and lichens also (Travé 1963). Hammer (1958; 1966) recorded oribatid mites from liverworts from Argentina, Bolivia and New Zealand. This paper describes a novel, intimate association in which oribatid mites belonging to a new species of the oripodid genus Birobates were found living inside pocket-shaped lobules of a corticolous leafy liverwort in Eucalyptus woodland and forest and notophyll vine forest in northern Queensland. MATERIALS AND METHODS Liverworts - Material Examined Frullania aff. ferdinandi-muelleri Steph. All specimens were collected by S. & T. Pócs, accompanied by A. Cairns, E.A. Brown & C. Cargill: 1) on exposed live bark, 2 m above ground, Eucalyptus-Alstonia woodland with Xanthorrhoea understorey, car park above Wallaman Falls, Girringun National Park, Queensland, Australia S E., elevation 542 m., coll. 19.vi.2001 (01106/A); 2) on live bark, cleared area surrounded by simple notophyll vine forest, McLelland s Lookout, Paluma Range National Park, Queensland, Australia, S E, elevation 897 m., coll. 19.vi.2001 (01109/L); 3) on live bark, open, wet Eucalyptus and Leptospermum forest, Bentham s track near Hermit Creek crossing, above Benhams Falls, Paluma Range National Park, Queensland, Australia, S E, elevation 910 m., coll. 17.vi.2001 (01116/A); 4) on live bark, edge of simple notophyll vine forest, amongst irrigated granitic boulders, Birthday Creek Falls, Paluma Range National Park, North Queensland,

3 Australia, S E, elevation 785 m., coll. 19.vi.2001 (01119/D); 5) on live bark, edge of simple notophyll vine forest, Lake Paluma Road, 1.06 km from turn-off, W. of Paluma village, Paluma Range National Park, North Queensland, Australia, S E, elevation 903 m., coll. 19.vi.2001 (01122/B). Samples in Herbarium of James Cook University (JCT), Townsville, Queensland. Oribatids Mites were removed from liverworts, placed in a cavity slide and macerated in lactic acid (70% aqueous) with 50% glycerol (1:1) on a hot plate at 50 C. Body length was measured in ventral view from the tip of the rostrum to the posterior margin of the opisthosoma, excluding the apophyses. Breadth was measured in dorsal view at the point of the widest part of the notogastral plate. All measurements are given in micrometres. Preliminary drawings of specimens were made with a camera lucida before adding more detail under highmagnification interference contrast optics. Generally, the morphological terms used herein are those of Hunt et al. (1998) and Norton & Behan-Pelletier (2009). For examination of gut contents, faecal pellets were examined in squash preparations of whole mites using high-resolution interference contrast optics ( 100 oil immersion lens), and by fluorescent microscopy using a 63 planapo lens and an excitation wavelength of 488 nm. TAXONOMY Birobates Balogh, 1970 Definition and Diagnosis Oripodid mites with the following combination of character states: rostrum with prominent naso, typically delineated by paired lateral notches; costulae narrow, positioned on lateral margins of prodorsum. Sensillus with club-shaped head, smooth spiculate; sensillus short, subequal to head. Bothridium almost concealed by anterior margin of notogaster. Pteromorphs immovable; notogaster smooth or punctate, with one to four pairs of sacculi and ten pairs of setae. Venter smooth or punctate; epimeral setal formula 2/ ; three pairs of

4 genital setae, aggenital setae absent, one pair of anal setae, three pairs of adanal setae, pori iad in the adanal position. Legs monodactylous. Remarks The genus Birobates was established by Balogh (1970) for B. reductus (the type species) and B. fenicheli, both from New Guinea, as monodactylous oribatulid mites with immovable pteromorphs, a pair of rostral incisions, one or two pairs of sacculi, ten pairs of notogastral setae, three pairs of genital setae, no aggenitals, one or two pairs of anals, three pairs of adanal setae, and with pori iad in the adanal position. Family placement of Birobates has been confused by the instability of the family-group classification of the Oripodoidea (Norton and Behan-Pelletier, 2009). Birobates was placed in the Oripodidae by Aoki & Okhubo (1974) within the subfamily Benoibatinae. Balogh & Balogh (1984) established Nanobates to accommodate those species that matched the definition of Birobates but had two pairs of anal setae (B. fenicheli, Trischeloribates latus Hammer, 1971; T. rotundus Hammer, 1971 and B. payatosensillus Corpuz-Raros, 1979). Birobates sensu Balogh & Balogh (1984) has only one pair of anal setae. However, Balogh & Balogh (1984) placed Nanobates within the Scheloribatidae and established the family Birobatidae for Birobates. Neither of these families can be differentially diagnosed and their constituent genera reconciled on the basis of the family-group definitions provided by Balogh & Balogh (1984). In a preliminary phylogenetic model of the Oripodoidea, Lee (1991) relegated Birobatidae to a subfamily of the Scheloribatidae, the sister-group of the Oripodidae. Subias (2004) and Norton and Behan-Pelletier (2009) consider Birobatidae to be a junior synonym of Oripodidae, and this classification is followed herein. Birobates hepaticolus sp. nov. (Fig. 1) Dimensions: holotype female length 262; breadth 151. Paratype females (n = 8): mean length 247 (range ), breadth 145 (range ); paratype males (n = 14): mean length 231 (range ), breadth 137 (range ).

5 Female. Prodorsum: rostrum with prominent naso and broad lateral incisions (Fig. 1c). Smooth setiform rostral seta (ro) inserted sub-apically on narrow lateral carina (Fig. 1a). Narrow costulae extending over half length of prodorsum, sharply incurved apically; lamellar seta (le) smooth, 33 inserted on incurved apex of costula. Interlamellar seta thin, smooth, setiform almost twice length of le. Bothridium almost completely covered by anterior margin of notogaster; sensillus with smooth, club-shaped head and short (13) stalk. Notogaster: smooth; ratio of length to breadth: 1.32; widest at level of seta lm (Fig. 1a). Ten pairs of fine, flagelliform notogastral setae; three pairs of small rounded sacculi (sa, s 1, s 2 ). Lyrifissurae im and ip long, straight. Setae p 3 positioned anterior of insertions of setae h 3. Venter: epimeral setal formula (Fig. 1b). Ventral surface smooth. Genital plates surrounded by more heavily-sclerotised cuticle. Three pairs of genital setae; one pair on anterior margin, two pairs on posterior portion of genital plate. Aggenital setae absent, one pair of anal setae positioned on anterior part of anal plates, three pairs of adanal setae. Preanal organ narrow, elongated, with shallow cup-shaped caput; pori iad in adanal position. Legs: monodactylous (Fig. 1d). Setation of leg I: 1-5-1(1)-3(2)-11(2). Femur II with five setae. Male. As for female but shorter and narrower (cf. dimensions above). Etymology: the specific name, hepaticolus, is Latinised Greek and refers to the liverwortdwelling habit of this species. Material Examined and Type Designation: Holotype and 22 paratypes, Wallaman Falls (see materials and methods for detailed locality data). Holotype and 14 paratypes deposited in the Australian National Collection of Insects (ANIC), CSIRO Entomology, Canberra. Eight paratypes in the Queensland Museum, Brisbane. Remarks Birobates hepaticolus sp. nov. can be differentiated from other members of the genus by the following combination of character states: 1) naso with broad lateral notches; 2) elongated thin interlamellar setae; 3) thin flagelliform notogastral setae; 4) setae p 3 positioned anterior of setae h 3 ; 5) all ventral setae very thin, short, curved, flagelliform. Birobates as redefined herein contains the following species (Subías 2004; updated April, 2009): B. reductus from corticolous moss in montane forest in Papua New Guinea (Balogh 1970), B. acutus (Hammer 1971) from forest litter on Viti Levu, Fiji, B. makinisus Corpuz-

6 Raros 1979 from forest litter in the Philippines and B. nasutus Aoki 2006 from moss (Plagiochila pulcherrima Horik.) on a tree trunk on Yaku Island, Ryuku Archipelago. RESULTS AND DISCUSSION Frullania ferdinandi-muelleri is a common epiphyte in tropical and sub-tropical Australia and grows appressed to bark, often in exposed situations such as forest edges or on isolated trees (Fig. 2a). The Frullania leaf typically has a large dorsal lobe and a ventral helmet-shaped lobule that holds water (Hattori 1979). These structures are also referred to as 'water sacs' (Malcolm & Malcolm 2006). The ventral lobule forms an enclosed microhabitat in which the mites are confined (Fig. 2b). Aggregations of predominantly adult male and female mites were found in lobules along branches of the liverwort. Only two nymphs were recorded, compared with well over a hundred adults. Most occupied lobules contained one (occasionally up to four) mites. Frequency of occurrence varied from contiguous lobules occupied to at least every thirtieth. Samples of F. ferdinandi-muelleri from all locations (cf. Materials & Methods above) contained mites, though their density showed considerable variation within and between samples. The accumulation of faecal pellets within the lobules suggested B. hepaticolus occupied the lobule for an extended period of time Dorsal lobes of stem-leaves F. ferdinandi-muelleri are widely-spreading and densely imbricate (Hattori 1979), completely concealing the ventral lobules beneath. The tunnels so formed by the overlapping leaves provide protected and, presumably humid, microhabitats for the mites. Lobules of Frullania and other leafy liverworts house a variety of microfauna, including protists, rotifers, tardigrades, crustaceans and nematodes (Barthlott 2000, Puterbaugh et al. 2004). Rotifers and nematodes were recorded from Lejeuneaceae lobules after they had passed through the guts of flying foxes (Parsons et al. 2007). No evidence of grazing damage was observed on Frullania leaves near to mite aggregations. Liverworts are considered unpalatable due to secondary metabolites stored in the oil bodies (Mues 2000). Frullania species synthesise diverse sesquiterpenes, diterpenoids and bibenzyl derivatives which may have anti-fungal, anti-microbial or anti-herbivore functions (Asakowa et al. 1981; 2003). However, oribatid grazers often exhibit host specificity (Walter & Behan-Pelletier 1999) and oribatids are known to be abundant and diverse on a range of lichen species that produce secondary metabolites (Colloff 1988; Meier et al. 2002; Seyd & Seaward 2004).

7 So does Birobates hepaticolus feed on Frullania ferdinandi-muelleri? The faecal pellets are of lightish brown colouration under interference contrast optics, as opposed to dark brown or black typical of the pellets of microbivorous-detritivorous oribatids and derived from humic acids from soil organic matter and from melanin in fungi. The absence of fungal spores, sections of hyphae and particulate detrital material from the faecal pellets of B. hepaticolus suggests that is not a microbivore-detritivore. Instead the pellets and midgut contain a series of solid, polygonate structures, ca µm long, containing a relatively uniform granular material (Fig. 2c). These structures are in the same size range as cells of F. ferdinandi-muelleri (Fig 2b) though they lack the characteristically crenellated structure of the cell wall. The particles in the faecal pellets and gut show yellow autofluorescence at 488 nm, (Fig. 2d), compatible with cellulose and chitin, though chlorophyll autofluoresces red following excitation at this wavelength. The mites had been removed from material that was collected almost ten years earlier and kept dry in a herbarium during the intervening period, so the absence of red autofluorescence could be due to chlorophyll degradation during storage. We suggest the most likely identity of the gut contents of B. hepaticolus is partiallydigested liverwort cells and that these mites are probably phytophagous. Isolated corticolous epiphytes, particularly mosses and lichens, are important habitats for oribatid mites (Travé 1963; Walter & Behan-Pelletier 1999). F. ferdinandi-muelleri provides habitat and probably food for B. hepaticolus. These minute oribatid mites thus can live in otherwise exposed and potentially desiccating environments by inserting themselves into lobules of liverworts where they are at least partially protected from dehydration. Even if at some stage the liverwort dries out completely and the mites are killed, eggs may survive within the dead gravid females. ACKNOWLEDGEMENTS We thank Tamás Pócs (Botany Department of the Eszterházy Károly College, Eger, Hungary) for the identification of Frullania ferdinandi-muelleri, as well as Eric Hines and Bruce Halliday (CSIRO Entomology, Canberra) for assistance with photomicrography. We thank the Environmental Protection Agency, Queensland, particularly the staff in the Cairns office of Queensland Parks and Wildlife Service in , for collection permits and access to national parks and protected areas in northern Queensland. Prof. Pócs was commissioned by

8 the Australian Biological Resources Study (ABRS) to collect specimens of Frullania and other liverworts, for taxonomic studies within the Flora of Australia project. REFERENCES Aoki J-I. & Ohkubo N A proposal of new classification of the family Oripodidae (s. lat.) with description of new species. Bulletin of the National Science Museum, Tokyo Series A 17, Aoki J-I New and newly-recorded Oribatid mites (Arachnida, Acari, Oribatida) from the Ryuku Islands, Japan. Bulletin of the National Science Museum, Tokyo, Series A 32, Asakawa Y, Matsuda R, Yoyota M, Hattori S. & Ourisson G Terpenoids and bibenzyls of 25 liverwort Frullania species. Phytochemistry 20, Asakawa Y, Toyota M, von Konrat M. & Braggins JE Volatile compounds of selected species of the liverwort genera Frullania and Schusterella (Frullaniaceae from New Zealand, Australia and South America: a chemosystematic approach. Phytochemistry 62, Balogh J New oribatids from New Guinea. II. Acta Zoologica Academiae Scientiarum Hungaricae 16, Balogh J. & Balogh P A review of the Oribatuloidea Thor, 1929 (Acari: Oribatei). Acta Zoologica Academiae Scientiarum Hungaricae 30, Barthlott W, Fischer E, Frahm J-P & Seine R First experimental evidence for zoophagy in the hepatic Colura. Plant Biology 2, Colloff MJ Species associations of oribatid mites in lichens on the Island of Ailsa Craig, Firth of Clyde (Acari: Cryptostigmata). Journal of Natural History 22, Corpuz-Raros LA Philippine Oribatei (Acarina). I. Preliminary list of species and descriptions of forty new species. Philippine Agriculturalist 62, Gerson U Bryophytes and invertebrates. In: Bryophyte Ecology (ed AJE Smith), pp Chapman and Hall, New York. Hammer M Investigations on the Oribatid fauna of the Andes Mountains. I. The Argentine and Bolivia. Biologiske Skrifter det Kongelige Dansk Videnskabernes Selskab 10(1),

9 Hammer M Investigations on the Oribatid fauna of New Zealand. Part I. Biologiske Skrifter det Kongelige Dansk Videnskabernes Selskab 15(2), Hammer M On some oribatids from Viti Levu, the Fiji Islands. Biologiske Skrifter det Kongelige Dansk Videnskabernes Selskab 16(6), Hattori S A revision of the Australasian species of the genus Frullania, Hepaticae, I. Journal of the Hattori Botanical Laboratory No. 45, Hunt GS, Norton RA, Kelly JPH, Colloff MJ & Lindsay SM Oribatid Mites: An Interactive Glossary of Oribatid Mites, CD-ROM. CSIRO Publishing, Melbourne. Hubert J, Žilová M & Pekár S Feeding preferences and gut contents of three panphytophagous oribatid mites (Acari: Oribatida). European Journal of Soil Biology 37, Lawrey JD Nutritional ecology of lichen/moss arthropods. In: Nutritional Ecology of Insects, Mites, Spiders and Related Invertebrates (eds. F Slansky & JG Rodriguez) pp John Wiley, New York. Lee, D.C. (1991) A modified classification of the Oripodoidea (Acarida: Cryptostigmata) based on a preliminary phylogenetic model. In: Modern Acarology Vol. 2. (eds F Dusbábek & V Bukva) pp Academia, Prague & SPB Publishing, The Hague. Malcolm W. & Malcolm N. (2006) Mosses and other Bryophytes: An Illustrated Glossary. Second edition. Micro-Optics Press, Nelson. Meier FA, Scherrer S & Honegger R Faecal pellets of lichenovorous mites contain viable cells of the lichen-forming ascomycete Xanthoria parietina and its green algal photobiont, Trebouxia arboricola. Biological Journal of the Linnean Society 76, Mues R Chemical constituents and biochemistry. In: Bryophyte Biology (eds AJ Shaw & B Goffinet) pp Cambridge University Press, Cambridge. Norton RA & Behan-Pelletier VM Suborder Oribatida. In: A Manual of Acarology Third edition. (eds GW Krantz & DE Walter) pp Texas Tech University Press, Lubbock. Parsons JG, Cairns A, Johnson CN, Robson SKA, Shilton LA & Westcott DA Bryophyte dispersal by flying foxes: a novel discovery. Oecologia 152, Proctor HC, Montgomery KM, Rosen KE & Kitching RL Are tree trunks habitats or highways? A comparison of oribatid mite assemblages from hoop-pine bark and litter. Australian Journal of Entomology 41,

10 Puterbaugh MN, Skinner JJ, Mille JM A nonrandom pattern of rotifers occupying lobules of the hepatic, Frullania eboracensis. The Bryologist 107, Siepel H & de Ruiter-Dijkman EM Feeding guilds of oribatid mites based on their carbohydrase activities. Soil Biology and Biochemistry 25, Seyd EL & Seaward MRD The association of oribatid mites with lichens. Zoological Journal of the Linnean Society 80, Subías LS Listado sistemático sinonímico y biogeográfico de los ácaros oribátidos (Acariformes, Oribatida) del mundo ( ). Graellsia 60 (supplement), Updated April, 2009: Accessed 9th September, Travé J Ecologie et biologie des Oribates (Acariens) saxicoles et arboricoles Vie et Milieu, Supplement 14, Walter DE Living on leaves: adaptations of Australian rainforest mites. In: Acarology IX: Volume 2, Symposia. (eds GR Needham, R Mitchell, DJ Horn & WC Welbourn) pp Ohio Biological Survey, Columbus. Walter DE & Behan-Pelletier V Mites in forest canopies: Filling the size distribution shortfall? Annual Review of Entomology 44, Walter DE & O Dowd DJ Life on the forest phylloplane: hairs, little houses and myriad mites. In: Forest Canopies (eds. M Lowman & N Nadkarni) pp Academic Press, New York.

11 Figure Legends Fig. 1. Birobates hepaticolus sp. nov., adult female; a) dorsal; b) ventral; c) squash preparation of rostrum; d) right leg I, axial view. Fig. 2a) Frullania ferdinandi-muelleri (Steph.): habitus photograph growing on bark at an exposed site above Wallaman Falls, North Queensland (scale bar 5 cm); b) a pair of adjacent ventral lobules (vl) of F. ferdinandi-muelleri containing a total of seven adult Birobates hepaticolus (scale bar 250 µm); dl = dorsal lobe; c) adult female Birobates hepaticolus showing gut contents (scale bar 50 µm); d) gut contents showing yellow autofluorescence following excitation at 488 nm (scale bar 50 µm).

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13 a) vl vl c) d) b) dl