Mating Behavior of Physolimnesia australis (Acari, Limnesiidae), a Non-Parasitic, Rotifer-Eating Water Mite from Australia

5 Pages·1997·5.2 MB·English

by  Heather C Proctor

1997. The Journal ofArachnology 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, Ontario
K7L 3N6 Canada
ABSTRACT. The diversity of sperm transfer behavior shown by water mites (Acaii, Hydrachnidia) is
among the highest in the Arthropoda. However, sperm transfer has been described in fewer than 10% of
water mite genera, all of them being Holarctic or cosmopolitan taxa. Here I describe mating behavior in
Physolimnesia australis (Halik 1940), the solerepresentativeofanAustraliangenus. P. australisisunusual
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 his
opisthosoma and legs III toward approaching females. The female is caught in the embrace and her legs
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 oftransfer
differs from members of the confamilial genus Limnesia Koch 1836 in which males and females do not
pair.
Chelicerates show the greatest diversity of ventercopulation (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 range
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 almost
females to discover andtake up spermontheir entirely to species from North America and
own (e.g., many Pseudoscorpionida) (Proctor Europe, and there are no descriptions ofsperm
et al. 1995). Finally, the horseshoe crabs transfer in a non-holarctic genus. Here I de-
(Merostomata) have external fertilization of scribe mating behavior in a monotypic genus
&
eggs (Ruppert Barnes 1994). Within the ofAustralian water mites together with casual
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 METHODS
may not have close associations between the
Physolimnesia australis (Limnesiidae) is a
bseexheasv.ioTrheocgcruerastesatmovanrgiettyheofmistpeesrm(Sturbacnlsafsesr small (^ 1 mm) water mite found in the lit-
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.; Proctor pers. obs.). This
order Prostigmata, Hydrachnidia). With the
species shows a strong sexual dimorphism in
exception of external fertilization, all possible
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 of
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 werepreviouslydescribed
321
322 THE JOURNAL OF ARACHNOLOGY
as a species in this genus (Limnesia trituber- 1896, a cosmopolitan epizootic species of
culata Viets 1955). I collected and observed 200-380 fjim in length (Koste & Shiel 1987).
P. australis on two occasions in 1995: in Thus to a250 pmdeutonymph, a single rotifer
March from Cedar Creek approximately 50 would be a substantial meal. Adult male and
km south ofBrisbane, Queensland; and in Oc- female F. australis were observed eating B.
tober from a large pond on the University of variabilis, as well as feeding on cladocerans
Queensland campus, St. Lucia. All observa- and dipteran larvae. Neither the deutonymphs
tions were made using a dissecting micro- nor the adults appeared to forcibly remove the
scope and took place at the DepartmentofEn- rotifers from their moinid hosts; rather, the
tomology, University of Queensland. I mites captured rotifers that had detached from
separated mites according to sex and stage the cladocerans and were swimming freely in
(adult and deutonymph) and maintained these 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 cladocerans he initially stood on the substrate and
(Moinidae) collected from a small pondon the groomed himself vigorously by moving legs
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 of in most limnesiids (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-
stantfanning motion overthe mite’sback, pre-
RESULTS
— sumably aerating the dorsal integument for
Life-cycle and predation. Most water gas exchange purposes. When a female
mites have a complex life-cycle with three ac- bumped into the male or passed near him he
tive stages: the six-legged larva parasitizes immediately took up the “embrace” posture
adult aquatic insects, and is followed by two (Fig. 1). In this position the male’s opistho-
eight-legged predatory stages, the deuto- soma was tilted at approximately 30° to the
nymph and the adult (Smith & Cook 1991). substrate, the flattened tips of legs III were
PhysoUmnesia australis is an exception to this touching and pressed against the substrate
rule in that its larvae forgo theparasitic 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 on 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-
fxm, SD = 8 jam, n — A). 1 observed that P. ally to swimming cladocerans. While in this
australis larvae remain within the coating of 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 III
The newly emerged PhysoUmnesia deuto- (Fig. 2). The male responded by elevating his
nymphs were very small (body length « 250 opisthosoma to about 50° to the substrate and
|xm) and were unable to handle the large cla- attempting to capture the fanning tips of the
doceran and dipteran prey I provided. Never- female’s legs IV in the flattened, scoop-like
theless, they increased in size andtransformed tips of his own fourth legs (Fig. 2). It was
into adult mites. This energetic mystery was unclearhow 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 their male’s tarsus.
moinid cladoceran hosts. The rotifers were When the male had captured both of the
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 with
female approaching from behind; 2, Female within male’s embrace, male has captured the tip ofher left
leg IV in the tip of his modified leg IV; 3, Male has captured both leg tips and the pair is swimming
jerkily; 4, Female grooms sticky material deposited by male on her back towards her ventrally located
genital aperture.
324 THE JOURNAL OF ARACHNOLOGY
However, the male gripped the female in the of Physolimnesia australis appears to fall be-
region of her 2nd or 3rd coxal plates with the 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 about copulation), but she must move it to her gen-
in ajerky 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 afterafew seconds too rigid to easily encompass all transfer be-
of swimming. For the pairs that continued haviors.
swimming, which usually lasted less than one It is not clear what motivates the P. aus-
minute, the male rubbed the concave ventral tralis female to enter the embrace of the
surface of his opisthosoma on the female’s male’s legs. In the water mite Neumaniapap-
dorsum. The male’s genital opening is located illator (Unionicolidae), the female orients to-
just behind the coxal plates oflegs IV, and the wards the male’s courtship signals because
rubbing ofhis venter againstthe female’sback they resemble vibrations caused by prey
probably represents deposition of the ejacu- (Proctor 1991). It is possible that male Phy-
late. In two ofthe 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
justbefore the pair separated. Afterthe 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 composed
groomed back over her dorsum and around ofspecies that are strongly sexually dimorphic
towards her ventrally located genital opening {Physolimnesia, Timmsilimnesia K.O. Viets
(Fig. 4). In two ofthe 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 that
DISCUSSION
sperm transfer with close contact between the
The mating behavior ofPhysolimnesia aus- sexes has evolved repeatedly in this family
tralis is very different from that of species in 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 is (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 offusion ofgenital plates. In Lim- most Hydrachnidia have a parasitic larva that
nesia spp., physical or chemical contact be- acts as both a feeding and a dispersal stage,
tween males and females is not required for the larva of P. australis transforms to a pred-
spermatophore production and transfer (Witte atory deutonymph without parasitizing an in-
1991; Proctor 1992a). Rather, males main- sect host. Suppression of the parasitic phase
tained alone will deposit spermatophores on a has been recorded in 29 species scattered
substrate, and females that later encounter through distantly related families of water
them will take up sperm ifso inclined. Proctor 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 orchemical contactbetweenthe a small adult body size, small clutch size and
sexes required for spermatophore deposition 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 seem
copulation (male places sperm in female’s conducive to cladogenesis, as such lineages
sperm-receiving structure). The transfer mode consist of single species (or populations)
PROCTOR—MATING BEHAVIOR OF PHYSOLIMNESIA 325
whose closest relatives retain parasitic larvae Cook, D.R. 1974. Water mite genera and subgen-
(Smith in press). Although one might expect 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.R. 1986. Water mites from Australia.
manent water bodies, there is no apparentpat- Mem. American Entomol. Inst., 40:1-568.
tern in relation to habitat: lineages withoutlar- Cook, D.R. 1988. Water mites from Chile. Mem.
val parasitism occur in streams, temporary 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 bodies Oecologia, 79:184-188.
of water. Koste, W. & J. Shiel. 1987. Rotifera from Austra-
The final strange aspect of P. australis' bi- lian inlandwaters. II. EpiphanidaeandBrachion-
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 ofcopulation in
observed feeding on a variety ofinvertebrates
water mites: a comparative test for nonreversing
(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); butto my knowledge, thisis only morphology of water mites (Acari: Parasitengo-
the second observation of arachnids feeding na). Zook 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 of ProActnoirm,.H.BCe.h,av.R,.L4.4:B7a4k5e-r75&2.D.T Gwynne. 1995.
undigested trophi (rotifer mouthparts) in the
Mating behaviour and spermatophore morphol-
mites’ guts (R.A. Norton pers. comm.).
ogy: a comparative test ofthe 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 freshwatercommunities. 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. Invertebrate
ital opening during the “nuptial swim,” and biology, 6th ed. Saunders College Publ., New
the gelatinous substance on her dorsum may York. 1102 pp.
Smith, B.P. In press. Loss of larval parasitism in
be residual spermatophore material.
parasitengonine mites. Exp. AppL, AcaroL, 21:
ACKNOWLEDGMENTS 00-00
Many thanks to Dave Walter (Entomology, Smith, I..M. & D.R. Cook. 1991. Water mites. Pp.
523-592, In Ecology and Classification ofNorth
University of Queensland) who offered lab
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. UberWassermilben (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. m1e0n7-t1a76n,d ILinfeT-hheisAtcoarryi:StrRaetpergoidesu.ct(iRo.n,ScDheuvsteelrop&-
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Christy, J.H. 1995. Mimicry, mate choice, and the
sensory trap hypothesis. American Nat., 146: Manuscript received 30 April 1996, accepted 5
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