1997 . The Journal of Arachnology 25 :321–325
MATING BEHAVIOR OF PHYSOLIMNESIA AUSTRALIS (ACARI, LIMNESIIDAE), A NON-PARASITIC , ROTIFER-EATING WATER MITE FROM AUSTRALIA
Heather C . Proctor : Department of Biology, Queen s University, Kingston, Ontari o K7L 3N6 Canad a
ABSTRACT. The diversity of sperm transfer behavior shown by water mites (Acari, Hydrachnidia) i s among the highest in the Arthropoda . However, sperm transfer has been described in fewer than 10% o f water mite genera, all of them being Holarctic or cosmopolitan taxa . Here I describe mating behavior i n Physolimnesia australis (Halik 1940), the sole representative of an Australian genus . P. australis is unusual in having larvae that do not parasitize insects, and in including rotifers in its diet . The highly dimorphic P. australis male responds to female presence by taking up an "embrace" posture in which he orients hi s opisthosoma and legs III toward approaching females . The female is caught in the embrace and her leg s IV are secured by the modified tips of the male s legs IV. The male deposits a glutinous mass on the female s back, which she grooms towards her genital opening after being released . This mode of transfer differs from members of the confamilial genus Limnesia Koch 1836 in which males and females do no t pair.
Chelicerates show the greatest diversity of venter copulation (e .g., Midea Bruzelius 1854 , sperm transfer modes in the Arthropoda. In Eylais Latreille 1796) to complete dissociation some taxa, males transfer sperm directly with in which the sexes never meet (e .g., Hydrod- a penis (Opiliones) or with secondarily de - roma Koch 1837) . Despite this amazing rang e rived genitalia (e .g., palps in Araneae) . In oth- of behavior, water mites have been poorly er groups, males transfer sperm indirectly by studied and mating observations have been depositing spermatophores on a substrate, and published for only 24 of the more than 340 either encouraging females to move over the genera of water mites (Proctor 1992a,b) . sperm packets (e .g., Scorpionida) or allowing These observations have been limited almos t females to discover and take up sperm on their entirely to species from North America and own (e .g., many Pseudoscorpionida) (Proctor Europe, and there are no descriptions of sperm et al . 1995). Finally, the horseshoe crab s transfer in a non-holarctic genus . Here I de- (Merostomata) have external fertilization of scribe mating behavior in a monotypic genu s eggs (Ruppert Barnes 1994) . Within the of Australian water mites together with casua l Chelicerata, some taxa exhibit greater behav- observations of its life cycle and diet. ioral diversity than others . For example, all spiders pair whereas pseudoscorpions may or METHOD S may not have close associations between th e Physolimnesia australis (Limnesiidae) is a sexes. The greatest variety of sperm transfer small (<_ 1 mm) water mite found in the lit- behavior occurs among the mites (Subclas s toral zone of standing and slowly running wa- Acari), and within this group the most diverse ter in Queensland and New South Wales (M behavior is shown by the water mites (Sub - . Harvey pers . comm. order Prostigmata, Hydrachnidia) . With the ; Proctor pers . obs.). This exception of external fertilization, all possible species shows a strong sexual dimorphism in modes of sperm transfer occur in the Hy- which males have a ventrally concave opis- drachnidia from direct transfer via venter-to - thosoma and flattened terminal segments o f legs III and IV (Fig. 1). Females are morpho- Current address: AES, Griffith University, Nathan logically similar to species in the confamilial 4111, Queensland, Australia. genus Limnesia and were previously described 321
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as a species in this genus (Limnesia trituber- 1896, a cosmopolitan epizootic species of culata Viets 1955) . I collected and observed 200–380 µm in length (Koste Shiel 1987) . P. australis on two occasions in 1995 : in Thus to a 250 µm deutonymph, a single rotife r March from Cedar Creek approximately 50 would be a substantial meal . Adult male and km south of Brisbane, Queensland ; and in Oc- female P. australis were observed eating B. tober from a large pond on the University o f variabilis, as well as feeding on cladocerans Queensland campus, St. Lucia. All observa- and dipteran larvae . Neither the deutonymph s tions were made using a dissecting micro - nor the adults appeared to forcibly remove the scope and took place at the Department of En- rotifers from their moinid hosts ; rather, the tomology, University of Queensland . I mites captured rotifers that had detached fro m separated mites according to sex and stag e the cladocerans and were swimming freely i n (adult and deutonymph) and maintained thes e the wells . groups in large well plates (well diameter = Mating behavior . When a male P. aus- 35 mm, depth = 19 mm) . Dipteran larvae tralis was placed in a well that held females , (Culicidae, Chironomidae) and cladoceran s he initially stood on the substrate and (Moinidae) collected from a small pond on the groomed himself vigorously by moving leg s University of Queensland campus were in- III and IV back over his dorsum and around cluded as potential prey for the mites. I made to his venter. After a bout of grooming, the behavioral observations on mites that had male was very still relative to the females , been collected as adults as well as those raised which were constantly crawling and swim- from deutonymphs in the lab. Voucher speci- ming close to the substrate. In P . australis, as mens are deposited in the University o f in most linmesiids (pers . obs.), crawling lo- Queensland Insect Collection, Department of comotion is accomplished by the first three Entomology, St. Lucia, Australia, 4072 . pairs of legs, with legs IV moving in a con- stant fanning motion over the mite s back, pre- RESULTS sumably aerating the dorsal integument fo r Life-cycle and predation. Most water gas exchange purposes . When a femal e mites have a complex life-cycle with three ac- bumped into the male or passed near him h e tive stages: the six-legged larva parasitizes immediately took up the "embrace" posture adult aquatic insects, and is followed by tw o (Fig. 1). In this position the male s opistho- eight-legged predatory stages, the deuto- soma was tilted at approximately 30° to th e nymph and the adult (Smith Cook 1991) . substrate, the flattened tips of legs III were Physolimnesia australis is an exception to this touching and pressed against the substrate rule in that its larvae forgo the parasitic phase. (thereby forming the circular "embrace"), and Adult females collected from the field readily legs IV were held rigidly and vertically. The laid small clutches consisting of 1–8 eggs o n male oriented his embrace towards any fe- the sides and bottoms of the wells . The eggs males that passed behind him. He also orient- were large relative to the female (mean = 134 ed towards other passing males and occasion - µm, SD = 8 pm, n = 4). I observed that P. ally to swimming cladocerans . While in thi s australis larvae remain within the coating o f posture the male was often approached by a the egg clutch and transform directly into pre- female that -by accident or intent -crawled up daceous deutonymphs (via the inactive pro- behind the male and placed her capitulum tonymph). over the flattened tips of the male s legs II I The newly emerged Physolimnesia deuto- (Fig. 2). The male responded by elevating his nymphs were very small (body length 25 0 opisthosoma to about 50° to the substrate and µm) and were unable to handle the large cla- attempting to capture the fanning tips of th e doceran and dipteran prey I provided. Never- female s legs IV in the flattened, scoop-like theless, they increased in size and transforme d tips of his own fourth legs (Fig. 2). It wa s into adult mites . This energetic mystery was unclear how this capturing was achieved ; pos- solved when I observed deutonymphs captur- sibly, the long apical seta at the tip of the fe- ing and eating large phoretic rotifers that had male s leg IV is secured by the groove in the been inadvertently introduced along with thei r male s tarsus. moinid cladoceran hosts . The rotifers were When the male had captured both of th e identified as Brachionus variabilis Hempel female s legs she typically began to struggle .
PROCTOR—MATING BEHAVIOR OF PHYSOLIMNESIA 323
Figures 1—4 .—Mating behavior of Physolimnesia australis . 1, Male in the "embrace" posture wit h female approaching from behind ; 2, Female within male s embrace, male has captured the tip of her left leg IV in the tip of his modified leg IV; 3, Male has captured both leg tips and the pair is swimmin g jerkily; 4, Female grooms sticky material deposited by male on her back towards her ventrally locate d genital aperture .
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However, the male gripped the female in th e of Physolimnesia australis appears to fall be- region of her 2nd or 3rd coxal plates with th e tween the third and fourth categories, as the tips of his legs III (Fig . 3). The pair typically male places the sperm on the female (as in left the substrate at this point and swam abou t copulation), but she must move it to her gen- in a jerky fashion. I observed at least 20 pair- ital opening (as in pairing, indirect transfer) . ings that reached this stage; however, all but This suggests that the categories of sperm three were terminated when the female es- transfer outlined by Proctor (1992a) may be caped from the male s grip after a few seconds too rigid to easily encompass all transfer be- of swimming . For the pairs that continued haviors. swimming, which usually lasted less than on e It is not clear what motivates the P . aus- minute, the male rubbed the concave ventra l tralis female to enter the embrace of th e surface of his opisthosoma on the female s male s legs . In the water mite Neumania pap- dorsum . The male s genital opening is locate d illator (Unionicolidae), the female orients to - just behind the coxal plates of legs IV, and th e wards the male s courtship signals becaus e rubbing of his venter against the female s bac k they resemble vibrations caused by pre y probably represents deposition of the ejacu- (Proctor 1991) . It is possible that male Phy- late. In two of the three complete matings ob- solimnesia australis engage in similar "sen- served, the male slid around backwards to - sory trapping" (sensu Christy 1995), perhaps wards the end of the female s opisthosoma by producing chemicals that mimic the scent just before the pair separated . After the female of prey animals. escaped or was released from the male s grip , The water mite Family Limnesiidae con- she perched on the substrate and vigorously tains 23 genera, five of which are compose d groomed back over her dorsum and around of species that are strongly sexually dimorphi c towards her ventrally located genital opening (Physolimnesia, Timmsilimnesia K.O. Viets (Fig. 4). In two of the three complete matings , 1984, Centrolimnesia Lundblad 1935, Ptero- I observed opaque white material on the fe- limnesia Viets 1942 and Acantholimnesia male s dorsum after she separated from the Viets 1954) (Cook 1974, 1980, 1986, 1988 ; male (Fig. 4). Viets 1984) . No two genera share the same types of male modifications, suggesting tha t DISCUSSION sperm transfer with close contact between th e The mating behavior of Physolimnesia aus- sexes has evolved repeatedly in this family tralis is very different from that of species i n from an ancestral non-paired state, as has oc- the genus Limnesia, the only other limnesiid curred in many other families of water mites genus for which reproductive behavior i s (Proctor 1991) . known. Limnesia species show no sexual di- Physolimnesia australis is an unusual water morphism save in body size (female larger ) mite in other aspects of its biology . Whereas and degree of fusion of genital plates . In Lim- most Hydrachnidia have a parasitic larva tha t nesia spp., physical or chemical contact be- acts as both a feeding and a dispersal stage , tween males and females is not required fo r the larva of P. australis transforms to a pred- spermatophore production and transfer (Witt e atory deutonymph without parasitizing an in - 1991 ; Proctor 1992a). Rather, males main- sect host. Suppression of the parasitic phas e tained alone will deposit spermatophores on a has been recorded in 29 species scattered substrate, and females that later encounte r through distantly related families of water them will take up sperm if so inclined . Procto r mites, including a few confamilials in the ge- (1992a) called this mode of sperm transfer nus Limnesia (Smith Cook 1991 ; Smith in "complete dissociation", and contrasted it press; H. Proctor pers . obs.). Like many spe- with three other modes : incomplete dissocia- cies with non-feeding larvae, P. australis has tion (physical or chemical contact between th e a small adult body size, small clutch size and sexes required for spermatophore depositio n relatively large eggs for its body size (Cook , but no pairing between the sexes) ; pairing, in - Smith Brooks 1989 ; Smith in press) . Al- direct transfer (male courts a given female , though the loss of larval parasitism has inde- spermatophores deposited on substrate) ; and pendently arisen many times, it does not see m copulation (male places sperm in female s conducive to cladogenesis, as such lineage s sperm-receiving structure) . The transfer mode consist of single species (or populations)
PROCTOR—MATING BEHAVIOR OF PHYSOLIMNESIA 32 5
whose closest relatives retain parasitic larva e Cook, D.R. 1974. Water mite genera and subgen - (Smith in press) . Although one might expec t era. Mem . American Entomol . Inst., 21 :1-860 . that loss of dispersal via parasitic larvae Cook, D.R. 1980. Neotropical water mites . Mem. would occur in lineages that inhabited per- American Entomol . Inst., 31 :1-645 . Cook, D manent water bodies, there is no apparent pat- .R. 1986. Water mites from Australia. Mem . American Entomol . Inst ., 40 tern in relation to habitat : lineages without lar- :1-568 . Cook, D.R. 1988. Water mites from Chile. Mem. val parasitism occur in streams, temporar y American Entomol . Inst ., 42 :1-356 . ponds, and both littoral and planktonic habi- Cook, W.J ., B .P. Smith R .J . Brooks . 1989. Al- tats within lakes (Smith in press) . It is not location of reproductive effort in female Arren- clear how, or indeed if, water mites with non- urus spp . (Acari : Hydrachnidia ; Arrenuridae) . feeding larvae mites disperse to new bodie s Oecologia, 79 :184-188 . of water. Koste, W. J . Shiel . 1987. Rotifera from Austra- The final strange aspect of P . australis bi- lian inland waters . II. Epiphanidae and Brachion- ology is the inclusion of rotifers in its diet . idae (Rotifera : Monogononta) . Invert. Taxon ., 1 : 949-1021 Confamilials in the genus Limnesia have been . Proctor, H.C. 1991 . The evolution of copulation i n observed feeding on a variety of invertebrate s water mites : a comparative test for nonreversin g (crustaceans, insects, other mites) and even characters . Evolution, 45 :558-567 . vertebrate prey (fish eggs) (Proctor Prit- Proctor, H.C. 1992a. Mating and spermatophore chard 1989) ; but to my knowledge, this is only morphology of water mites (Acari : Parasitengo- the second observation of arachnids feeding na). Zool . J . Linn. Soc ., 106 :341-384 . on rotifers. One other species, an undescribed Proctor, H .C . 1992b . Sensory exploitation and the oribatid mite in the genus Aquanothrus En- evolution of male mating behaviour : a cladistic gelbrecht 1975 (Ameronothridae), is believed test using water mites (Acari : Parasitengona) . to feed on rotifers based on the presence o f Anim. Behay., 44 :745-752 . Proctor, H .C ., R.L. Baker D undigested trophi (rotifer mouthparts) in the .T. Gwynne . 1995 . Mating behaviour and spermatophore morphol - mites guts (R .A. Norton pers . comm.). ogy : a comparative test of the female-choice hy- Note added in proof : (a) Adults and pothesis . Canadian J . Zool ., 73 :2010-2020. nymphs also prey on nematodes and oligo- Proctor, H . G. Pritchard. 1989. Neglected pred- chaetes . (b) It is also possible that the male ators : water mites (Acari: Parasitengona: Hy- deposits spermatophores on his own legs III drachnellae) in freshwater communities . J . North prior to taking up the embrace posture; sperm American Benthol . Soc ., 8 :100-111 . could thereby be inserted in the female s gen- Ruppert, E.E. R.D. Barnes . 1994. Invertebrat e ital opening during the "nuptial swim," an d biology, 6th ed . Saunders College Pubi ., New the gelatinous substance on her dorsum ma y York. 1102 pp . Smith, B .P. In press. Loss of larval parasitism i be residual spermatophore material . n parasitengonine mites . Exp . Appl ., Acarol., 21 : ACKNOWLEDGMENTS 00-00 . Smith, I.M . D .R. Cook. 1991 Many thanks to Dave Walter (Entomology, . Water mites . Pp. 523-592, In Ecology and Classification of North University of Queensland) who offered la b American Freshwater Invertebrates (J .H. Thorp space, room and board, and chauffeur service . A.P. Covich, eds .). Academic Press, New Mark Harvey (Western Australian Museum ) York. kindly provided me with access to his volu- Viets, K . O . 1984. Ober Wassermilben (Acari, Hy - minous water mite library, and both he and drachnellae) aus Australien . Arch. Hydrobiol ., Bruce Smith (Ithaca College, New York) sent 101 :413-436 . me copies of their own unpublished manu- Witte, H. 1991 . Indirect sperm transfer in prostig- scripts . This research was supported by a matic mites from a phylogenetic viewpoint . Pp. Queen s University ARC grant. 107-176, In The Acari : Reproduction, Develop- ment and Life-history Strategies . (R . Schuster LITERATURE CITED P.W. Murphy, eds .). Chapman Hall, New York. Christy, J .H. 1995. Mimicry, mate choice, and the sensory trap hypothesis . American Nat ., 146: Manuscript received 30 April 1996, accepted 5 171-181. March 1997.