BEHAVIOUR OF THE LARVAE OF Arrenurus fissicornis Marshall, A WATERMITE PARASITIC ON DRAGONFLIES

BY RODGER MITCHELLDepartment of Biology, University of Florida

It has been argued that the well known ten-dency of larval water mites of the genus Arren-urus to attach to specific sites on their odonatehosts (Miinchberg, 1935, et seq .) is related to theway in which the larvae re-enter the water afterfeeding on their host (Mitchell, 1959) . The at-tachment of mites to their hosts is non-random,so some mechanism must limit the mites toparticular sites. This study deals with thatmechanism and with the sequence of eventsduring a mite's larval life . A single species,Arrenurus fissicornis Marshall, is considered butother observations, that will be published in acomparative study, indicate the behaviourdescribed below to be typical of many speciesassigned to the subgenus Arrenurus .

All the field work was done on the EdwinS. George Reserve of the University of Michigan,located near Pinckney, Michigan . The variousofficers of the Reserve have given me a very widemeasure of support in the form of Grants-In-Aid from the Edwin S . George Scholarship Fundwhile permitting the greatest freedom in re-search .

IntroductionArrenurus fissicornis is a member of the sub-

genus Arrenurus . Through an extensive series ofrearings (see Miinchberg, 1959, for citations tomost. of this work), it is known that larvae of thissubgenus are typically parasitic on dragonflies .The life cycle of all known Arrenurus speciesfollows the basic water mite pattern with the firststage, the larva, parasitic on an insect imago ;this is followed by two stages, the nymph and theadult, which prey on microcrustacea . To date thedate on life cycles of Arrenurus species are basedon rearings of engorged larvae from field col-lected hosts. The larvae are removed from thehost and reared through subsequent stages inthe laboratory .

Such studies commence after larvae completetheir period of greatest activity, and nothingworthy of note has been seen in the behaviour ofthe nymph and adult under these circumstances .Engorged larvae exhibit some reactions whichhave been considered recently . Engorged larvaemay be thin-skinned and respond to moisteningor they may develop a thick skin and be entirely

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unresponsive . Thick-skinned larvae are usuallyon the thorax of the host ; thin skinned larvaeare usually on the last abdominal segments . Itwas concluded from these data that someparasites have adaptations for leaving the hostwhen it oviposits and these are the thin-skinned,responsive larvae . Larvae of other species rideon their host until its death, which must occurin or over water if the parasites are to re-enterthe water (Mitchell, 1959). This work demon-strated that the larval attachment site on the hostwas one of the important adaptations related tothe way the larvae re-enter the aquatic habitat .

Larvae attach to their host when the hostimago emerges from the naiad skin. Thus attach-ment occurs within a narrow span of time andcan be observed rather easily. The observationsreported below deal with the parasitism ofLibellula luctuosa Burm . and Er vthemis sim-plicollis (Say), by Arrenurus fissicornis . This miteattaches to the terminal segments of the abdomenand drops from the host at the time of ovi-position or pseudo-oviposition (Mitchell, 1959) .Unengorged larvae cannot be specifically identi-fied or reared through, but reliable presumptiveassociations could be made because all observa-tions were made at one pond (Burt Pond) wherelong term studies had shown As frssicornis to bethe only common parasite of the above hosts .

Host Emergence and Normal Activity of the MiteLarvae

If terminal naiads of either odonate host arecollected in the pond or just as they leave thewater, they are often found to have clusters ofmite larvae on the posterior surface of the heador on the anterior surface of the prothorax . Themite clusters are generally very assymetricalunless the larvae are so numerous as to competefor resting sites. The larvae are inactive andattached to their mouthparts, but the larvae donot appear to be feeding on the naiad .

On leaving the water the naiad climbs someobject and there the imago emerges from the oldskin. The skin first splits forward along the mid-dorsal line from the base of the forewings to theanterior margin of the thorax . The split thenextends over the head and, at a central position,divides into two lateral splits extending down

MITCHELL : BEHAVIOUR OF THE LARVAE OF A WATER MITE PARASITIC ON DRAGONFLIES

over the eyes . The imago expands its bulkwhile the naiad skin splits and, after the splittingof the skin is complete, movements of the imagoraise it dorsally out of the old skin . Once thehead and thorax are free, the abdomen is movedso that the imago rises upward through thesplit in the naiad skin. In order to tabulate thedata conveniently, the time from the beginningof the split to the completion of the split isdesignated `Stage 1' . As the imago moves out ofthe skin it is said to be in `Stage II' . When only afew terminal segments of the abdomen remainin the naiad skin the imago ceases all activityfor a period of time and this period of inactivityis designated `Stage I I1' . At the end of this stagethe imago crawls free of the old skin .

Larvae on the host naiad are not easily dis-turbed, and even if the host spends considerabletime searching out a site for emergence there isno activity among the larvae . The larvae evenremain quiet, except for the twitching of a fewlegs, for a period of five to six minutes afterthe naiad skin splits and host emergence begins .By this time the imago has been free of the skinwhere the larvae are situated for at least two orthree minutes and only the posterior of theabdomen is in contact with the naiad skin.

Data on the timing of the events during hostemergence are given in Table 1 . If the times ofstages are compared with the time of miteactivity, it is seen that mite activity is not co-ordinated with any particular physical event ofemergence ; but it is clear that mite activityalways begins after the head and thorax of theimago are free of the nymphal skin . In Fig . I thevarious events during an emergence are graphed .The part of the host that will be contacted by amite larva crawling from the nymphal skin tothe imago at various times during emergence isindicated by the shaded areas . All these datashow that the membranes to which mite larvaenormally attach are on the part of the host thatthe larvae strike when they first crawl on to theimago. Hence, there is no necessary reason topostulate any attachment site recognition on thepart of the larvae .

The Movement of Larval Mites on to the HostImago

Clusters of larval mites on the posterior sur-face of the head or on the anterior face of thethorax of the host tend to be near the mid-dorsalline with the larger clusters extending furthestdown the lateral surface. When the larvae be-come active during the emergence of the host, afew of the peripherally placed mites may wander

larval ad-vIty

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. ~ In M nules

Fig . 1 . A graphic representation of the events during theemergence of an adult Erythemis simplicicollis and the co-ordinated activity of the mite larvae . The shaded area isan approximate indication of the parts of the host thatwill be contacted by a larva crawling from the naiad skinat the various times during emergence . The numbersalong the ordinate give the percentage of the mite larvaeattached to the various abdominal segments in a sampleof 14 E. simplicicollis collected on June 20th, and 21st,1959. The graph is based on observation 59-13 .

about in most any direction, but the majorityof the cluster mill about in the same generalarea. Larvae that wander dorsally over the splitand touch the inner surface of the naiad skinnever return to the cluster . Consequently, thecluster appears to move dorsally even thoughthere is no clear orientated movement of in-dividual larvae toward the split . This loss oflarvae in one direction is the simplest explana-tion for the apparent movement of clustersdorsally .

When a larva is inside the naiad skin it isvirtually certain to contact the host imago in itswanderings . There does not appear to be aspecific stimulus attracting the larvae to the hostimago, but the larvae do seem to recognize theimaginal integument by touch for they begin toprobe for attachment sites with their mouthpartsas soon as the imago is touched . No larva wasever seen to leave the host .

When there are very few mites the larvae un-load from the naiad to the imago very slowlyand have less success in finding the imago . Onlya few such cases were observed and more datamust be collected, but it appears that if there arefewer than fifty larvae the unloading is quite in-efficient. It is as if an unloading pressure resultedfrom many individual kineses acting together .When too few mites are present the weak in-dividual kineses may prove to be inadequate .

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Table 1. The Timing of Events in a Dragonfly Emergence. All records were taken between May 31st and June 7th (1959and 1960) from specimens observed in the field . The stages are arbitrary divisions defined in the text and the time is givenin minutes since the splitting of the nymphal skin . Where a question mark is entered the time of splitting was not accurately

known but was estimated . The time of the end of the stage is given .

Locomotor Responses of the Larvae

Two kinds of locomotor activity can be elicitedfrom larval mites : the slow milling about oflarvae that is seen during host emergence orwhen larvae on the naiad are disturbed, and arapid swarming response which results in larvaeswimming from the naiad, if the host is in water.This reaction can be seen only if a naiad iswounded or damaged and the advantage of sucha response is obvious. The stimulus for this re-action is unknown .

In order to test for the various reactions dur-ing emergence, the exact time the naiad skin

ANIMAL BEHAVIOUR, IX, 3-4

began to split was carefully noted . Then atvarious intervals the mid-dorsal line of theemerging imago was pierced with a tiny hookedscalpel which was moved about so as to destroythe thoracic tracheal sacs . This stopped allmovements of the emerging dragonfly . All theexperiments were done on E. sitnplicirollisnaiads bearing a heavy load of mites .

Four hosts were damaged either before emerg-ence or within 15 seconds of the time the naiadskin had split and the mites on these hosts showeda rapid locomotor response within 60 seconds ofthe wounding. When 30 or more seconds ofemerging time had elapsed the larvae on the

StageI

StageII

StageIII

1st mite

Ist hostactivity

contactAll miteson host

Erythemis simplicicollis `~

59-12a 4 1/2 8 24 1/2 - -

59-12b 3 5 1 /2 19 -

59-12c 3 5 1/2 24 1/2 -

60-45 41/2 8 1/2 24 1 /2 -

60-64 4 8 1 /2 1 23 -

60-58 3 6 20 -

59-11 2 5 20 6 7 9

59-12 4 7 23 5 - 13

59-13 3 6 15 1/2 5 1/2 6

59-14 4 6 1/2 5 1/2 71/2 10 1/2

59-15 4 6 5 1 /2 6 11

59-16 4(?) 61/2 221/2 6 81/2 111/2

59-26 41/2 8 1/2 17 1/2 61/2 -

59-56 5 9 28 5 1/2 7 1/2

Libel a luctuosa

59-07 2 1/2 61/2 221/2 - -

59-24 5 1/2 91/2 341/2 -

59-25 4 1 /2 9 25 9 12

59-27 4 7 - -

59-30 4(?) 7 1/2 27 1/2 9 10 1/2 14 1/2

59-31 4(?) 7 1/2 25 7 7 1/2 12 1/2

MITCHELL : BEHAVIOUR OF THE LARVAE OF A WATER MITE PARASITIC ON DRAGONFLIES 223

wounded host generally remained quiescent untilabout the normal activity time . In 9 experimentsthe wounding was done 30 to 800 seconds afterskin splitting ; 7 experiments showed normalslow activity of the larvae 210 to 330 secondsafter skin splitting of the host (mean 270). Thisis slightly earlier than normal activity time (300to 390 seconds after skin splitting) but it is anactivity more closely correlated with the begin-ning of host emergence than with the woundingfor the interval between wounding and larvalactivity varied from 30 to 295 seconds (mean 164) .

Thus it appears that normal larval activitywill not be shown unless some 30 seconds ofemerging time have elapsed and that a stimulusduring this time sets off a series of larval re-sponses that cannot be altered by subsequentmanipulation .

Two exceptional experiments were eliminatedfrom the above discussion as due to mishandlingor some unrelated phenomena. One woundingat 30 seconds resulted in slow larval activity 120seconds after splitting and a wounding at 90seconds resulted in slow larval activity 750seconds later . A second case of extreme delay inlarval activation was noted when no manipula-tion was involved ; a Libellula luctuosa tooknearly twice the normal time to completeStage I and in this case the activation of thelarvae was delayed an equal amount . Perhapsthe stimulus affecting activity of the larvae isnormally produced over a brief period of timebut under some circumstances the stimulus ismodified so as to lengthen the period of larvalquiescence .

Mites clustered on a terminal naiad can bestimulated to activity if forcibly detached but aslong as the larvae are in contact with the naiadthey show a slow crawling response and willshortly reattach themselves to the naiad . Thegeneral mode of locomotion when disturbed butstill in contact with the host is similar to theslow activity during emergence, and these maybe identical responses that can be elicited underdifferent circumstances .

Attachment of Larvae to the Host Imago

Because of the delay in activation the larvaealways contact the host abdomen when theyfirst leave the naiad skin and very shortly attachto a nearby membrane. If mite larvae are trans-ferred from the abdomen to the thorax thereseems to be no difference in behaviour . Larvaecontinue to test the membranes with theirmouth-parts and soon attach to a thoracicmembrane. Evidently there is no discrimin-

ation of membranes on the part of the larvae .The hosts cannot be kept in confinement and itis not known whether normal development willensue on the thorax .

The number of parasites per host is extremelyvariable, but if imagos are collected as theyemerge there is a certain constancy in the levelof parasitism at a specific location. Seven E.simplicollis from the north side of Burt Pondcarried an average of 3 .2 mites (range 0-16) ;nine hosts from the south side (less than a hun-dred feet away) carried an average of 54 .2 mitesper host (range 13-100). There is doubtless arandom introduction of engorged larvae aroundthe entire margin of Burt Pond for the hosts arenot restricted in their activity nor is there anydistinct localization of the mite adults in thepond. Perhaps the explanation for non-random-ness of larval parasitism will be found in thedifferential success of either eggs or larvae incertain situations .

Discussion

It is now possible to outline the sequence ofevents in the parsitism of a libelluline host byArrenurus fissicornis. All of the larval activitiesobserved to date have been taken into account .The precise stimuli perceived by the larvae areunknown, but various experiments fix the cir-cumstances existing at the time of the responsesand show that there is a defined sequence ofevents. The data on experiments and observa-tions have been given and in the following para-graphs the conclusions are put together in sum-mary form .

Nothing is known about the various elementsinvolved in the `searching activity' of newlyhatched larvae. In the laboratory this appears tobe an incessant activity that is not modified in thepresence of a host naiad . It may only be a modeof locomotion involving no distance perceptionof the host . Larvae cease swimming on contactwith the host and quickly come to rest on thehost nymph. Local differences in the level ofhost parasitism could be the result of a searchingactivity that is efficient in bringing about para-site-host contacts under a limited set of cir-cumstances . Local variation in the rate ofparasitism would result from this unless thehosts were in situations where parasite searchingactivity was uniformly successful .

The stimulus eliciting larval quiescence on thehost is specific for healthy last instar naiadsand may be increasingly effective as last instarnaiads mature. Cast skins, naiads with unre-paired wounds, and early instars do not evoke a

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ANIMAL BEHAVIOUR, IX, 3-4

response. But a variety of hosts may be acceptedby the larvae in the field so it is probable thatsome general property of healthy terminal naiadsis perceived by the larvae at the time of hostcontact.

Once the larva is on the host it remains quietunless disturbed by abrasion or host grooming .Such disturbances are quite frequent on allsurfaces except the deep cervical groove betweenthe head and thorax . Clusters of larvae may cometo lie on the protected cervical and thoracicsurfaces because they are constantly disturbeduntil, by chance, they enter the groove betweenthe head and thorax . Larval clusters are dorsallyplaced and this may be the result of a specificorienting behaviour . When there are less than150 larvae on a naiad the clusters are almostalways assymetrical . This too may be the conse-quence of a random selection of the four un-disturbed areas (the right or left sides of theposterior of the head or the anterior of theprothorax) by the first larva to attach and atendency of other larvae to cluster around aquiescent larva. Precise data on larval clusterscould not be collected without interfering withsubsequent observations and these reflectionsstand as unverified speculations .The second response of quiescent host-

attached larvae is elicited by damage to the host(i .e. wounding) and body fluids escaping fromthe wounded host could provide the stimulus .The mite reaction is a prompt resumption ofwhat appears to be normal `searching activity' .

This abandoning of the host can be elicited inquiescent larvae up until about 30 seconds aftersplitting of the naiad skin during normalemergence of the imago . From that time onneither disturbance nor wounding of the hostcan break larval quiescence or modify the subse-quent chain of behaviour .

There is no evidence as to what the `emergencestimulus' may be. Apparently there is somequantitative relationship between the stimulusand the length of quiescence . Normally thelarvae are quiescent for four to five minutes afterthe emergence stimulus and then begin slowmovements that tend to bring them into con-tact with the host imago . These events have beendiscussed in detail and it was concluded that :(1) timing of larval activity, not specific siterecognition, explain the non-random attachmentof larvae to the host, (2) discovery of the imagoinvolves no distance perception, and (3) imagosare recognised only through touch .

Once attached to the imago the larvae feedand engorge. There is no thickening of the larvalcuticle and engorged larvae can be stimulated

to slow activity by moistening. As discussedelsewhere (Mitchell, 1959) this response resultsin the larvae tending to drop in the water duringhost oviposition . The libelluline hosts involveddip their abdomens into the water when ovi-positing and the males of L. luctuosa regularlypseudo-oviposit (Jacobs, 1955) . When the larvais back in the water it transforms into thequiescent nymphochrysalis stage from whichthe nymph will emerge.

SummaryLarvae of Arrenurus fissicornis become active

and move on to the emerging dragonfly hostonly after five minutes of emerging time haselapsed and the membranes they must en-counter first are those of the terminal abdominalsegments. Larvae attach to these membranes .If the emergence of the host is stopped (bymanipulation) thirty seconds or more after hostemergence begins the entire sequence of normalmite activity is unaltered ; earlier manipulationcauses larvae to abandon the host . Larvae willattach to any host membrane they are placedupon. Thus, it appears that timing alone is re-sponsible for site specificity and that the stimulusevoking the behaviour of mite larva during hostemergence is perceived during the first thirtyseconds of host emergence .The lack of strong orientation among larva

before they encounter the naiad, when theycluster on the cervical membranes of the naiad,or when they transfer from the naiad to theimago suggest that distance perception is notinvolved. Random movements and touch per-ception can adequately explain most of theobserved behaviour of the mite larvae .

AcknowledgmentI offer this as a token of my appreciation for

the wise counsel Irving J . Cantrall has lavishedon me during his tenure as Curator of the GeorgeReserve .

REFERENCESJacobs, M. E . (1955) . Studies on territorialism and sexual

selection in dragonflies. Ecology, 36, 566-586 .Mitchell, Rodger (1959) . Life histories and larval be-

havior of arrenurid water-mites parasitizingOdonata . J. N. Y. ent . Soc., 67, 1-12 .

Munchberg, Paul (1935) . Zur kenntnis der odonaten-parasiten, mit ganz besonderer Berachsichtigungder Ocologie der in Europa an Libellen schmaro-tzenden Wassermilben-Larven . Arch. Hydrobiot.,29, 1-120 .

Munchberg, Paul (1959) . Dritter beitrag uber die anafricanischen Libellen schmarotzenden Arrenurus-Larven (Hydrachnellae, Acari) . Arch. Hvdrobiot.,55, 264-275 .

Accepted .for publication 6th December, 1960.