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Mating and Spermatophore Morphology of Water Mites (Acari: Parasitengona)

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Mating and Spermatophore Morphology of Water Mites (Acari: Parasitengona) <oological Journal of the Linnean Society (1992), 106: 341-384. With 7 figures Mating and spermatophore morphology of water mites (Acari: Parasitengona) HEATHER C. PROCTOR* Department of <oology, Erindale College, Universily of Toronto, Mississauga, Ontario, Canada L5L IC6 Received June 1991, accepted March 1992 In this paper I synthesize original and published studies of sperm transfer behaviour of 23 genera of water mitrs from 15 families. The morphology of spermatophores from 16 genera (12 families) is described. Behaviour and/or spermatophores are described for the first time for the following species: Hydrachna magniscutata Marshall, Hydrachna hesperia Lundblad, Hydrachna sp. nr. leegk Koenike, Limnochares ampricana Lundblad, Limnesia undulata (Miiller), Neumania distincta Marshall, Unionicola (three species in the I/. crassipes-complex), 'Thyas stolli Koenike, Lcbertia annae Habeeb, Lcbertia sp., Piona sp. nr. debilis (Wolcott), Tip$s uernalis (Habeeb), Arrenurus dentipctiolatus Marshall, Arrmurus marshalli Piersig and Arrenurus birgei Marshall. On the basis of proximity of male and female during sperm transfer, 1 divide water mites into four groups: complete dissociation, involving no physical or chemical contact between the sexes (nine genera); incomplete dissociation, requiring distance- or contact-chemoreception but not involving pairing behaviour (five genera); pairing with indirect transfer, involving pairing behaviour with females controlling sperm uptake (three genera); pairing with direct transfer ( = copulation), involving pairing behaviour and male placement of sperm in the receiving structure of the female (12 genera). Four genera have representative species in more than one category of sperm transfer. Factors possibly leading to the diversity of water mite mating behaviour include an evolutionarily flexible mode of sperm transfer in the ancestral water mite, and the development of planktonic and endoparasitic habits in many mites. Morphological features of spermatophores that improve physical stability, probability of females taking up sperm and resistance against osmotic stress are discussed. Finally, I present implications of mating behaviour and spermatophore morphology for phylogenetic relationships within water mites and between this group and terrestrial Acari. KEY WORDS:-Acari - water mites - mating behaviour - spermatophores - evolution. CONTENTS Introduction ................... 342 Methods .................... 342 Collection and maintenance of mites ............ 342 Spermatophore illustrations .............. 343 Behavioural observations and descriptions ........... 343 Experimental methods ............... 343 Statistical analyses ................ 343 Modes of sperm transfer ................ 343 Complete dissociation. ............... 346 Incomplete dissociation ............... 356 Pairing with indirect transfer .............. 362 Pairing with direct transfer (copulation) ........... 366 *Present address: Department of Biological Scienres, University of Calgary, Calgary, A1 berta, Canada T2N I N4. 34 I 0024-4082/92/120341+44 SOE.OO/O 0 1992 The Linnean Society of London 342 H. C. PROCTOR Discussion ................... 375 Comparison of mating behaviour between water mites and other arachnids. .. 375 Functional morphology of water mite spermatophores ........ 378 Spermatophore structure, mating behaviour and water mite phylogeny. ... 380 Acknowledgements ................. 382 References ................... 382 INTRODUCTION Although arachnids show the greatest diversity of sperm transfer behaviour of all arthropods (Thomas & Zeh, 1984), there are few reviews of mating in any groups other than scorpions (Polis & Sissom, 1990), spiders (Austad, 1984) and pseudoscorpions (Weygoldt, 1966, 1970). Within the class Arachnida most orders are monotypic in their mode of sperm transfer (e.g. all spiders copulate); however, one monophyletic group, water mites, exhibits all modes of sperm transfer from complete dissociation of the sexes to intromission. Possibly because there has been no synthesis of early work, water mite behaviour has been overlooked in comparisons of mating systems. In this paper I compile previous studies of mating behaviour, present my own experiments testing the importance of female presence for spermatophore production in non-pairing species, and describe spermatophore morphology (where possible) of water mites in 15 families. Finally, I compare the diversity of water mite mating to that of other arachnids, discuss functional morphology of spermatophores, and describe patterns in behaviour and spermatophore structure that may help to elucidate phylogenetic relationships in this diverse group of animals. METHODS Collection and maintenance of mites Water mites were collected from several sites in southern Ontario, Canada, from April to November 1989 and April to September 1990 (Table 1). Samples were taken by sweeping a dipnet (250 pm mesh) through aquatic vegetation or by holding it downstream while disturbing rocks and gravel. I maintained mites TABLE1. Collection sites in Ontario. Authorities for species' names are in text Location and type of water body Latitude Longitude Species Burlington, flooded quarry 43" 15' 79" 45' Hydrachna hespcria; Anmum birgei Valens Conservation Area, pond 43" 20' 80" 05' Limnesia marshallac Milton, permanent pond 43" 31' 79" 56' Hydrachna magniscutata; Limnochares americana; Hydrodroma despicicns; Limnesia fulgida; Neumania distincta; Unionicola sp. 4 Erindale Campus, Mississauga 43" 33' 79" 40' (a) permanent 43" 33' 79"40' Limnesia undulata; Neumania papillator; Piona sp. nr. debilis; Anenurw marshalli (b) temporary pond 43" 33' 79" 40' Thyas stolli; Tiphys uemalis Credit River, river 43" 35' 79" 42' Lcbertia sp.; Atractidcs nodipalpis Warnock Lake, pond 43" 40' 79" 57' Limnesia undulata Caledon Hills, pond 43" 50' 79" 55' Hydrachna baculoscutata Indian Lake, pond 44" 40' 76" 20' Hydrachna sp. nr. lcegei Lake Opinicon, bay 44" 40' 76" 20' Limnesia undulata; Lcbcrtia annac; Unionicola sp. 3 Plastic Lake, lake 45" 11' 78" 50' Unionicola sp. 4 MATING AND SPERMATOPHORES OF WATER MITES 343 individually in 17-mm deep tissue-culture well plates (large: diameter = 35 mm; small: diameter = 11 mm) at 19-21°C, 12 h light: 12 h dark. Except for Thyas and Hydrachna, whose food was unavailable, I fed mites according to their preferences (Proctor & Pritchard, 1989). Representative specimens of new or unidentified species are deposited with Ian Smith at the Biosystematics Division of Agriculture Canada, Ottawa. Spermatophore illustrations Spermatophores were removed gently from their sites of deposition with minuten pins and pipetted on to a depression slide. Specimens were photographed through a compound microscope. Technical pen drawings were made by projecting slide images on to a mirror angled at 45”C, and placing a glass plate covered with tracing paper above the mirror. Terms applied to spermatophore morphology are illustrated in Fig. 1 a. Behavioural observations and descriptions Mating and spermatophore deposition were observed under a stereomicroscope or videotaped with a Panasonic CCTV chip camera (model WV-BL200) attached to a stereomicroscope and recorded to a Panasonic SVHS time lapse video cassette recorder (model AG-6720). Morphological terms used in descriptions of mite behaviour include (1) idiosoma: the fused ‘thorax’ and ‘abdomen’ of the mite, i.e. its body exclusive of mouthparts; (2) legs: are numbered from fore to hind with roman numerals (legs I to IV). Experimental methods When possible, experiments were performed to determine the importance of female presence for spermatophore deposition in non-pairing species or to compare deposition rate of males held with con- and heterospecific females. Details are outlined in Table 2. For each experiment mites were initially maintained individually for several days; I then paired some males with females, maintained other males alone, and sometimes provided males with female chemical cues. Substrates for spermatophore deposition were taken from the species’ habitat (vegetation), except for Hydrodroma (chironomid egg masses) and Unionicola (scratched well bottom). Trial durations were based on preliminary observations of spermatophore deposition. Statistical analyses Tests were performed with the STATISTIX I1 software package (NH Analytical Software). All measures of central tendency are mean k SE. MODES OF SPERM TRANSFER With the exclusion of Hydrovolzioidea, water mites comprise a monophyletic group of six superfamilies in the prostigmatid cohort Parasitengona (Barr, 1972; Cook, 1974; but see Witte, 1991). Because water mites evolved from a non- W L TABLE2. Experimental procedures and results from tests of the importance of female presence for spermatophore production by males. Time alone = time mites maintained separately prior to the experiment; duration = duration of treatment; m = male; f = female Number of males ZkSE Species Time alone (days) Substrate Treatments N Duration depositing Spermatophores/male - H$raCh 3 M~~ophyffumstem m alone 6 3 hours 4 - magniscuhh m+2mL f H20 6 4 - m+f 6 3 - Limnochres americana' I1 Oak leaf m alone 8 5 days' 0 - m+f 9 5 - Limnochres am'cana' 4-9 Oak leaf m alone 12 5 days 0 - m+f 11 5 - m+m I 0 - Limnochres americana' I1 Oak leaf m alone 17 5 days 0 - m+f 14 9 - m+m 9 6 - Limnochres amnicana' 10 Oak leaf m+f 2 5 days 1 - m+m 10 8 - - Hgdrodrmna' 4 chironornid egg mass m alone 9 32 hours 7 &SpiCitnS m+f 6 6 - m+m 8 7 - Limnesia undulah 3 1 x 1 cm reed' m alone 23 I hour
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