The Life History of Climacia Areolaris (Hagen), a Neuropterous 'Parasite' of Fresh Water Sponges Author(S): Harley P

Home , Climacia, Climacia areolaris, Spongilla

The LifeHistory of Climaciaareolaris (Hagen), a Neuropterous'Parasite' of FreshWater Sponges* HarleyP. Brown Departmentof ZoologicalSciences, University of Oklahoma,Norman

Climaciaareolaris is an insectbelonging to the FamilySisyridae, of the OrderNeuroptera. The larvaeof all knownmetmbers of this family occur as parasitesupon fresh water sponges of theFamily Spongillidae, Order Demo- spongiae,hence the common name applied to thesisyrids by Needham-"spon- gillaflies." (However,the larvae may be found,at times,upon bryozoans or algae.) Accordingto thepresent scheme of classificationand stateof knowledge, thereare but two representativesof the familywhich normally occur in temperateNorth America: Climacia areolaris (Hagen), and Sisyravicaria Walker. Bothof thesespecies are widelydistributed in the UnitedStates, occurringfrom the Gulf of Mexicoto Canada,and fromthe Atlantic coast at least as farwest as New Mexico (*Carpenter,1940). In the regionwhere the presentwork was carriedon bothspecies occur. Despite theirwide distribution,and the fact that severalinvesigators have becomeinterested in them.,the life history of neitherof theseAmerican sisyrids has been workedout. In fact,the only extensivelife historystudy of any memberof the family,so faras I have been able to discover,is thatof Withy- combe,upon a Britishspecies of Sisyra (Withycombe,1922). Mating,eggs, and firstinstar larvae of Climaciahave neverbeen described. The investigationsupon whichthis articleis based were initiatedin the summerof 1941, continuedduring parts of the summersof 1942, 1944, and 1945, and carriedon intensivelyfrom June 16 throughAugust, 1949. All significantwork was done at the Franz Theodore Stone Laboratory,which is located at Put-in-Bay,Ohio, on an island in the westernend of Lake Erie, withina fewmiles of the Canadian boundaryline. I wishto acknowledgemy indebtednessto: Prof.Nathan Banks foridentification of specimens;Prof. M. W. Boesel for advice and assistancethroughout the work; Profs. H. B. Hungerford,M. C. Old, and R. C. Smi"thfor helpful suggestions; Prof. T. H. Langloisfor the use of the facilitiesof the Franz Theodore Stone Laboratory; Mr. Bert Millen for the use and care of the tank at the Ohio State Fish Hatchery. HISTORICALREVIEW Adult sisyridswere first described by Degeer in 1771, as membersof the the Genus Hemerobius. In 1829, the Genus Sisyrawas createdby Burmeister for these European forms. In the same year,the late instarlarvae were describedby Westwood. A quotationfrom Needhatn (1901) is of interest:

* Contributionfrom the Franz TheodoreStone Laboratory,Put-in-Bay, Ohio. 130 1952 BROWN: LIFE HISTORY OF CLIMACIA AREOLARIS 131

"A discussionwas then raging in thelearned societies of theold worldas to whether spongesbelong to theplant or to theanimal kingdom, and the Sisyra larva was dragged, an innocentvictim, into this controversy. Dujardin, maintaining that sponges are animals, toldthe French academy that he foundin thesponge body numerous fine filaments that movedto and fro. JamesHogg, on theother hand, believing that sponges are plants, maintainedbefore the Linnaean society of Londonthat the filaments seen by Dujardin were thesetae on theback of these larvae, which had crawled,as is theirwont, into the spcnge throughthe open osteoles. "The larvapossessed two structures, also, so uniquein characterthat interest in them hassurvived the sponge controversy, andon accountof which the original figures of West- woodand Grubeare handed down in textbooksof thepresent day. Thesepeculiar parts are1) paired,jointed appendages beneath the abdominal segments, and 2) long,dezurved, piercingmouth parts, of a uniquesuctorial type. "Notwithstandingtheinterest attaching to thislarva, it seemsnot to havebeen reared." Needham rearedthe larvae of the specieshe found at Saranac Inn, New York--i.e.,he placed spinninglarvae in vials,obtaining from them both pupae and adults. He describedthis species as Sisyra umbrata. He also reared adults of Climacia frompupae withincocoons collectedfrom the hatchery supplytrough. These he describedas Climacia dictyona. Needham supplied one of his students,Miss Anthony,with preserved material, from which she workedout some details of the metamorphosisand anatomicalstructures of Sisyra,publishing her results in 1902. Banks (1906) relegatedboth of Needham'snew speciesto synonymy,with Sisyra vicariaWalker (1853), and Climacia areolaris (Hagen) (1861), respectively. The latterwas originallyplaced in the Genus Micromus,until the genericname Climaciawas introducedby MacLachian (1869). In 1906, Handlirsch createdthe Family Sisyridae,including therein the then-known speciesof Sisyra,Climacia, and Neurorthus. Priorto thattime (and, by some authors,after that time), these generahad been generallyassigned to either the Osmylidae or the Hemerobiidae. Since then, a fourthgenus, Sisyrella (= Nopia), has been describedand includedin the family (Kruger, 1923; Navas, 1935). Kruger(1923) considersthe Balticgenus Rhophalis as belong- ing to the Sisyridae. Navas (1935) outlinesthe systematicsof the family,and presentsa table indicatingbroadly the geographicdistribution of the variousspecies. He lists fivespecies of Ncurorthus:two in Europe,two in Asia, and one in the islands of the PacificOcean. Of the threespecies of Climacia,two occur in South (and Central ?) America,the other in North America. Of the nineteen speciesof Sisyra,four are European,eight Asiatic, one African,three from the Pacificislands, anid three "American." Of the last three,I gatherthat only one occursnorth of the tropicsand Caribbeanislands. The two species of Sisyrellaare Asiatic. His supplement,listing species of Spongillidaewhich serveas food for sisyrids,appears, rather, to be a fragmentarycompilation of data on the distributionof freshwater sponges. His materialon Climacia is taken fromthe publicationsof Needham and Banks. His sectionson larval sisyridsand on the biologyof sisyridsare drawnentirely from Withycombe 132 THE AMERICAN MIDLAND NATURALIST 47 (1)

(1922), althoughhe misinlterpretedan item or so. Thus,he mistookWithy- combe'sfigure of an egg-breaker,although it is so labeledeven in hisreproduc- tionof it, for a pupalstructure, and states that it is a heavilychitinized mandi- blewhich serves in themanner of a sawin liberatingthe pupa from the cocoon. Botharticles by Withycombe(1922, 1924) presentexcellent descriptions of the lifehistory of Sisyrafuscata in England,with pertinent information uponrelated groups. As previouslymentioned, they represent the most extensivelife history study upon members of theSisyridae. In theUnited States, the only investigation relating to thelife history of sisyrids,other than that of Needhain,was reported by Old (1932b). Work- ingat DouglasLake, Michigan, he collectedfrom sponges 38 larvae,placed themin-"finger bowls containing water, a thinlayer of sand,and a pebble largeenough to extendabove the water. Piecesof freshsponge replaced old piecesevcry day. The larvaesometimes fed on the sponge,sometimes not. Oftenthey showed no evidenceof even being aware of itspresence.... About 60 percent of them died within two to tendays. Of theremaining 40 percent whichpupated, 80 percent emerged in fromeleven to fifteendays. At pupa- tionthe larvae had a lengthof 3.5 to 4.0 mm." He foundabundant cocoons ofboth Sisyra and Climacia,and speculated thus: "The purposeof thisloosely wovennet (on Climaciacocoon) is notknown. It mightserve as a protection fromcertain parasitic insects. It doesnot, however, protect the pupa from be- comingwiet during submergence, as was shown by experiment." He describedthe swimmingmovements of sisyridlarvae as follows:"A larvaswims about by a peculiarbody movement. It holdsitself in a verticalposition, head up, arches tlhebody, and then,by slnappingback into the verticalposition, produces a forwardmovement." His attemptsat breedingsisyrids were as fruitlessas mostof myown: "Pupae broughtinto the laboratoryemerged and affordedmaterial for experimentson life-history. Twenty-five cocoons were placed in a naturalposi- tionover an aquariumcontaining sponges and waterplants, the latter project- ingabove the surface of thewater. A cageof clothnetting was adjustedover the aquarium.As the imagoesemerged, they flew to the top of the cage, soughta secludedcorner, and remainedthere, rarely flying about. Fromthree to fivedays later the flies could be pickedfrom the surface of thewater, where theyhad fallen. Theyappeared very weak in flight,and theslightest wetting renderedthem unable to extricatethemselves. Examination of thewater and plantsrevealed no evidenceof eggs. Repeatedobservations yielded no results. Flashinga lighton imagoesat nightcaused them to flyabout toward the light andexhibit positive phototropism." The onlyother significant point made by Old was thatnot all sponges seemto serveas hosts,since he had foundno sisyridlarvae upon Ephydatia fluviatilis,Heteromeyenia repens, or H. argyrosperma,although he had col- lectedniumerous specimens of at leastthe first of these. Both Comstock(1940) and Ward & Whipple(1918) presenta brief accountof theAmerican sisyrids, based solely upon Needham's work. The 1952 BROWN: LIFE HISTORY OF CLIMACIA AREOLARIS 133 sectionin Ward & Whipple on aquatic insects(written by Needham) includes a key to both adults and larvae,and is more readilyavailable than the paper by Needham & Betten (1901), in whichkeys are includedfor larvae,pupae, and adults. Both books also summarizeMiss Anthony'sdescripticn of the anatomyof thelarval Sisyra, so I need not recountany detailshere. Killington(1936) and Balduf (1939) presentrather detailed accounts of the familySisyridae, based primarilyupon the literatureavailable. Stitz (1931), Tillyard (1916), and Van der Weele (1909) probablypresent per- tinentinformation, but I have not had access to their papers. Klingstedt (1929) merelydiscusses the taxonomyand distributionof a Eturopeanspecies, Sisyrajutlandica. Crampton(1921) figuredfrointal views of the heads of adult Sisyra and Climacia,and a ventralview of part of the head of whatappears to be a third instarClimacia 1.arva which has recentlyundergone ecdysis. Peterson(1945) figuresthe dorsal aspect of a thirdinstar Climacia larva with only nine abdominalsomites and exhibitingantennae and mouthparts unlike those I have observed. His statementconcerning the nutritionof sisyridsis somewhatpuzzling: "By means of theirlong needlelikemouthparts theyfeed on the individualsponge organisms- in a spongecolony." Townsend(1935) depictsa Sisyralarva in whichthe threeterminal abdominal somitesare not distinguishable.I suspectthat the specimensdrawn by Petersonand Townsendhad been incompIetelyextended.

MATERIALS AND METHODS Collectingand Rearing.-Eggs maybe obtainedin any one of severalways, all of whichwere utilized at one timeor another: (1) Eggs may be squeezed or dissectedfrom gravid females. (2) Eggs may be collectedfrom various objectsoverhanging water, by examinationof such objectsfor the tinywhite sheetscovering the eggs and subsequentremoval of appropriateportions of the substratebearing the eggs. I have thus collectedeggs fromthe undersides of kinnikiniiickleaves (Cornus obliqua Raf.), thoughnone fromgrape or mulberryleaves nearby,which were also overhangingthe water.I have found them in abundancein depressionsand crevicesof dead twigsand branches, beneathboards (painted or bare) formingthe laboratoryboat dock, and on boththe rustedand paintedportions of an ironpipe. In fact,I firstdiscovered eggs by detectinga femaleovipositing upon the ironsupport of the lake-level- recordingbox beside the Ohio State Fish Hatcherydock. In such a case, of course, the eggs had to be seen beforebeing removedto the laboratory, whereas,in the case of such portablestructures as leaves and twigs,the objects may be broughtinto the laboratoryfor carefulexamination. (3) Eggs may be obtainedby havingthe gravidfemale oviposit in the laboratory.Perhaps the simplestmeans of accomplishingthis is to collect ovipositingfemales (several hours aftersunset) in a vial or wide-mouthbottle having a cork stopper.The surfaceof the cork to which the capturedfemale has access shouldhave a numberof shallowgrooves, in whichthe eggsmay be deposited. 134 THE AMERICAN MIDLAND NATURALIST 47 (1)

The containershould be kept in the dark, preferably,and should be left undisturbeduntil morning.Many females,once interruptedin theiroviposit- ing activity,promptly terminate oviposition and cannotbe inducedto resume it, no matterhow accommodatingtheir captor may be. Other substratesupon whichoviposition has occurredin vials, bottles,and testtubes include Cornus leaves,pieces of black paper and piecesof cellophanefolded like an accordion bellows,and the innershoulder of a glass vial, In orderto observethe developmentof the eggs withoutdisturbing their silkencovers, or tents,I wantedeggs ovipositedupon a transparentsubstrate. Although this was accomplishedin the aforementionedcases of cellophane and the glass vial, the most satisfactoryresults were obtainedwith Petri dishes. By placings,everal small, elongateobjects (pins, pieces of toothpick and capillaryglass tubes and rods were used) on the innersurface of the Petridish lid, thensticking them down witha stripof cellulosetape (Scotch tape or Texcel), I could produce crevicesin whichfemales would oviposit. Most of the eggs were depositedat the pointsof contactbetween glass and tape, and werereadily visible from above or below. They could be examined under the high power of the compoundmicroscope, by use of transmitted light. On all of tlhenaturally-occurring substrates, only directillumination could be employedin examiningthe eggs. Many of the females,collected in the act of ovipositionand promptlyplaced in a Petri dish preparedas describedabove, would proceed to ovipositwithin a shorttime. By carefully transferringthe dish to the stage of a binoculardissecting microscope, and by employingnot too brighta light,I could observethe processesof egg- laying and net-spinningin considerabledetail. Eggs were also depositedabundantly in the rearingcages to be described below. After acquiringeggs, it is a relativelysimple matterto get first-instar larvae-by allowinigthc eggs to developand hatchunder reasonably favorable conditions.After suspendingegg-bearing leaves, etc., over water in bottles, fingerbowls, watch-glasses,and such, I developed a more fool-prooftech- nique. This, again, involvedthe use of Petri dishes and an adhesive. By stickingthe egg-bearingobject to. the innersurface of the Petri dish cover, and adding waterto a depthof severalmillimeters in the bottomof the dish, a chamberis produced-in which all larvae emergingfrom the eggs may drop directlyupon the water surface.They may then be collected either beforeor afterthey have penetratedthe surfacefilm of the water,the dish beingplaced upon,the stage of the microscope.Of course,with a Petri dish in which the eggs were originallydeposited upon the innersurface of the lid, one has but to add water-to the lower half of the dish, afterremoving the adult sisyrid(s). Although first-instarlarvae are seldom found upon sponges examined eitherin the field,or in the laboratory,second- and third-instarlarvae may readily be collected thus. 1 have seen as many as six third-instarlarnae, along with at least one or two second-instarlarvae upon a single sponge 1952 BROWN: LIFE HISTORY OF CLIMACIA AREOLARIS 135

which covered part of the undersideof a rock which was no largerthan my fist. Third-instarlarvae also may be collected in fair numbersfrom rockswhich do not bear sponges,but whichoccur in the vicinityof sponges. These, apparently,are larvae whichare preparingto leave the water.After the larvae leave the water-whichthey usually do well aftersundown-they may be collectedas theyare crawlingabout in search of a cocoon site, so to speak. Since a numberof them spin theircocoons at distancesranging fromthirty to fiftyfeet fromthe water'sedge, it is obvious that specimens may be taken at some distancefrom the water. I have found them to be most numerous,however, along thieedges of the dock, or climbingsuch objects as posts, a net-drier,or the lake level box. I have taken withina minuteor two as many as a dozen migratinglarvae fromone surfaceof a signboardabout 15"x15". I have easilycollected climbing specimens by touch- ing theirrear ends with the lip of a shell vial, into whichthey will usually drop. The third-instarlarvae may also be collectedwhile in the act of spinning, beforethey have pupated. However, as will be explainedin the section on the larva, thereare relativelygross differencesin the anatomyand appearanceof those third-instarlarvae taken from the water,those taken during migration,and those taken duringthe pre-pupalresting stage. The pupal stage is more easily obtainablethan any other.One need but look about among the objects near the water's edge to find the whitish cocoons,which are about the size of an ordinarymatch head-and usually enclosedwithin a whitenet, as describedand figuredbelow (Fig. 11). The cocoons occur upon rocks,trees, grass, etc., but are usually most numerous in crevicesor otherprotected places, e. g., beneathstones or in rockycaves or old pipes. Here at the laboratory,the cocoons are abundant in some unusual places, such as on the protectedsides of the mooredboats, on the mooringropes, on the indoor side of the windowscreens, and beneaththe windowsills. At mid-season(July 18, 1949), I counted75 freshcocoons on one. side of a 3"x155 wooden strip inside the lake level box, to which the larvae had access througha crack. Since I wishedto know the exact age of all of the pupae under observa- tion, I generallycollected migrating larvae, whichwere most numerousbe- tweenone and six hoursafter sunset, and allowed themto spin theircocoons in the laboratory.Of the various containersutilized for this purpose,from test tubes to fingerbowls, Petri dishes,once more, turnedout to be most convenient.In each Petri dish, or bottomhalf thereof,were placed two or threesquares of black paper, about 20 to 25 mm. on a side. E,ach square of paper was folded along two parallel sides, about 4 mm. fromthe edges, so that these two edges stood at 90? angles fromthe plane of the paper square, which rested flat upon the bottom of the dish. The larvae were placed in such a dish, usually 10 or 15 per dish, and kept in darkness,e. g., by coveringthe dish with an invertedcardboard box. Within 1 to 3 hours, most of the larvae were spinningalong the folded edges of the paper,pro- ducingbeautiful white nets and cocoons on a black background.The remain- 136 THE AMERICAN MIDLAND NATURALIST 47 (1) inglarvae (10 to 40%) wouldspin on theglass, either against a paperwall or a glasswall. Only one out of theseveral hundred so treatedspun on the open surfaceof the dish,away from any wall. In the cocoonsspun upon glass,the insect within can be seenfairly distinctly, and observedunder the microscope. Adultsmay be readilycollected at nightat lighttraps or upon lighted windows.A secondlikely nocturnal collecting site is ovipositionterritory. In the immediatevicinity of the laboratory,they may be takenovipositing beneaththe kinnikinnickleaves overhanging the wateror, in greaternum- bers,beneath the boardsof the dock. Duringdaylight hours, of whichI saw all-too-fewduring this study,the adultsmay be takenby sweeping withan insectnet among the bushes near the sponge-inhabited water. How- ever,the easiest way to obtainadults of knownage is to collectthe cocoons, and allowthe adultsto emergein anyhandy receptacle. For maintainingadults in th-elaboratory, I utilized cages avaitable in our stock-room.These are 5?/2"0x5?/"x9"in dimensions,with removable glass top and bottom.Three of theremaining, long sides are madeof screenwire, the fourthof glass. I suspendedfrom the top a couple of kinnikinnick leaves (by meansof cellulosetape), and placed beneaththem an open Petridish of water-intowhich hatching larvae may drop, and fromwhich the adultsmay drink. A gumdropprovided food forthe adults.In each suchcage wereplaced 20 to 30 newly-emergedadults, some of whichsur- vivedover three weeks. Within these cages, courtship, mating and oviposi- tionoccurred, and the larvaedropped from the egg-bearingleaves into the Petridish. These larvae were transferred to culture dishes containing sponges. As manyas 25 to 30 livinglarvae were removed from a singlePetri dish at one emptying. The problemsencountered in culturingor maintainingthe larvaeunder laboratoryconditions were not so easilysolved. I succeededin keepingonly twolarvae alive for more than three weeks, though a numberof thethird- instarlarvae emerged and pupated.No singleindividual was keptalive from egg to adult.However, I did manageto rearsome spongilla flies from egg to secondlarval instar, others from second larval instar to adult.The first- instarlarvae were maintained chiefly in smallPetri dishes or Syracusewatch glassescontaining small sponges carefully removed from rocks by meansof a razorblade. In mostcases, I was able to slicebeneath the gemmule layer, damagingthe spongebut slightly,if at all. Nevertheless,these sponges seldom lastedmore than one or twodays, and had to be replacedwfith con- siderablecare, lest the larvae should get abovethe surface film of thewater -a mishapwhich was almostalways fatal. Few of the larvaesurvived long enoughto reachthe second instar, none to reachthe third. The waterutilized was unfilteredlake water,pumped from a depthof aboutfive feet. Lake waterdipped up in glass containersand transferreddirectly to the culture dishesseemed no moresalutary than the tap water. Some of the later-instarlarvae were kept as longas twoweeks in a bat- 1952 BROWN: LIFE HISTORY OF CLIMACIA AREOLARIS 137

teryjar containinga single small sponge, and into which tap water was kept drippingat a rapid rate. The sponge had died beforethe end of the second week, and the survivorswere third-instarlarvae which had deserted the sponge. Similar jars containingseveral sponges on algae-coveredrocks becamefoul withina few days to a week. The most nearly successfulmethod of maintainingliving sponges and sisyridlarvae was also the most awkward,from the standpointof the in- vestigator.It involvedthe use of a large,wooden rearingtank in the Ohio State Fish Hatchery.The tank,in its inside dimensions,is about 23"" deep, 31" wide,and 14' long. It was coated witha worncoat of aluminumpaint. The water employed was the aforementionedunfiltered lake water, kept flowingat a rate of approximatelytwo litersper minute,and kept at an average depth of about four inches. Sponge-bearingpieces of wood, back, and stonewere scattered here and therein the tank. They seemedto do best near the water inlet,which was also about the best-lightedportion of the tank, receivingplenty of light-thoughlittle or no directsunlight-through a large east window.In this tank,a fewsponges and larvae survivedbeyond the thirdweek, although neither could have been said to thrive.A narrower, unpaintedtank or trotigh,kept in an ill-lightedplace, failed to keep the sDongesalive beyond the firstweek. Two large light-bulbswere suspended above this troughto augment the illumination.However, since the light bulbs merelyattracted insects which dropped into and perhapsbefouled the water,they were not replaced after they had burned out. This tank was markedoff as a failure,although it may providea hintas to the significance of light as an ecologicalfactor in sponge distribution.In my opinion,such tanks and troughshardly represent laboratory conditions, but rathersome- thing intermediatebetween laboratory and outdoor conditions. The real problemin rearingsisyrid larvae, as suggestedby both Withy- combe (1922) and Old (1932b), is that of keepingthe sponges alive for extendedperiods. I believe that a shallow 10-gallonor 20-gallonaquarium mightserve the purpose if it were well-aerated,kept in a well-lightedplace (but exposed to little direct sunlight), filled with pond or streamwater never exposed to metal, with evaporatedwater replaced by glass-distilled wateronly, and firstbalanced with a fishor two and sparse aquatic plants, e. g., Myriophyllumand Vallisneria.The fish should be removedbefore adding larva-bearingsponges. One or two small spongeswould, I think,be optimum. Preservaiion.-Variousmethods were experimentedwith for the preservation of eggs, larvae, pupae, cocoons,and adults. The effectsof som-eof the killingtechniques upon third-instarlarvae are, perhaps,worth mentioning. Formalin,phenol vapor, carbon tetrachloride,chloroform, and various con- centrationsof ethylalcohol from30% to 95% are fairlygood, but result in contractedor curledlarvae. K.A.A.D. solution (1 part kerosene,10 parts 95%o ethylalcohol, 2 partsglacial aceticacid, and 1 part dioxane) is better, yieldingstraighter larvae. Best resultsare obtainedby immersinglarvae in 138 THE AMERICAN MIDLAND NATURALIST 47 (l1) moderatelyhot water (50' to 70?C.) for several minutes,then gradually runniingthem througlhthe alcohol series for sterage at 9519i. Aside from those specimensmounted on slides in eitherdiaphane or balsam, I prefer to storeall of my materialin 95%'rethyl alcohol, to whichseveral drops of glycerolper vial are added in case of accidentaldrying. Cocoons and nets are best kept dry; some I have enclosedin glass cells, coveredby a circular coverglass, and mountedupon a microscopeslide.

RESULTS Egg.-The egg (Fig. 1) is similarin formto the average hemerobiid egg, being more or less oval in outline,averaging about 340,u in lengthand about 160,t in its greatestwidth. The micropylarknob or cap averagesabout 8,u in heightand about 20,u in width. The egg, when freshlylaid, is a glistening,whitish, semi-transparent body. The reticulationof the chorionic shell is hardlyperceptible, although it becomes evidentin the emptyshell afterhatching (Fig. 4). The egg, as it appears when squeezed or dissected fromthe female,is whiterand more granular,translucent rather than transparent. At room temperaturesaround 800F., tlheeggs develop rapidly. At 70

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Figs. 1-3.--1. Egg of Climacia, shortly after deposition; 2. Egg of Climacia, shortly before hatching. The eyespots may be seen to consist of 6 ocelli. Appendages are vaguely discernible, lying along the mid-ventralsurface and overlapped distally by the curled tip of the abdomen. The egg-saw is beneath the bulging nrdgewhich extends along the mid- line between the eyes; 3. Larva within amnion, immediatelyafter emergencefrom egg shell. Appendages are still enclosed, but are more clearly discernible than in the egg. The egg- saw is now exposed, lying betweenthe eyes. 1952 BROWN: LIFE HISTORY OF CLIMACIA AREOLARIS 139

hours afterdeposition, reddish eye-spots are appearing,and the egg is as- suminga yellowishor ambercolor. At 100 hours,the eyespotshave turned black. On the eighthday, 6 blackishdorsal scleritesare visible.During the night of the eighthday, hatchingoccurs. At lower temperatures,a longer incubationperiod is required,as would be expected.In the laboratory,the rangewas from8 to 10 days. As long as 6 to 12 hours beforehatching, pulsations or pumpingmay be observedalong the mid-dorsalline of the larva withinthe egg. Some- times these pulsationsseem directedanteriorly, at other times posteriorly. This pumpingoccurs at intervalsof 1 to 20 secondsfor a periodof a minute or so, then may cease for severalminutes. The periodsof pumpingappear to become more frequentas the time of hatchingapproaches. After a few hours,vibrations are noticeablein the frontalregion of the larva, slightly posteriorand ventral to the micropylarknob. Now the head may turn fromside to side withinthe egg. The processof hatchingis quite similar to that describedby Withycombe(1922) for Nothochrysacapitata, a Brit- ish chrysopidor lacewing.Blood is forcedinto the labrum-clypeus,which lies in the aforementionedfrontal region of the head of the larva, beneath the amnionicegg-breaker (Figs. 3, 4, 5). Through the consequentswelling of the underlyingtissues, the egg-sawis pressedagainst the chorionor egg shell. Since the underlyingtissues are now rapidly pulsating,the egg-saw is vibrated,and serveseffectively in rippingor cuttingthrough the shell- at times even penetratingthe sheet of silk which covers the eggs. Mean- while,the anteriorportion of the larva is pushingout of the egg shell. It may now be seen that the larva is still encased withinthe amionicskin or membrane,of whichthe egg-sawis a part. Within a shorttime, the amnion splits down the mid-dorsalline of the head, and the larva extractsitself fromthe skin, leavingthe latterextending from the hole in the egg-tentor stretchedupon the substratenearby (Fig. 4). The egg-sawis slightlyout of focus in Fig. 4, althoughlittle could be seen of its structureat this magnification.It is the portionwhich resembles a lowerjaw, if the emptyamni- onic skin be likenedto a fishwith dorso-lateralbars. Fig. 5 representsthe appearanceof the egg-sawat a high magnification.The numberof teethis not absolutelyconstant. Two of the blunter teeth near the base seem characteristicallyto be lighterin color,probably being less heavilysclerotized. The eggs are ordinarilylocated in a creviceor depression.On the kinnikinnickleaves, they were invariablytucked in the crotchesof the veins on the under surfaces.As mentionedpreviously, no eggs were found on nearby grape or mulberryleaves. Perhaps these leaves were too pubescent.The numberof eggs coveredby a single egg-tentranged from0 to 22, though the averageseemed'between 2 and 5. Larva withinA mnion (EmbryonicSkin). -The larva,as it emergesfrom the egg, appears maggot-like,since all of its appendagesand setae are enclosed withinthe thin amnionicskin (Fig. 3). It is as if the larva were 140 THE AMERICAN MIDLAND NATURALIST 47 (1)

hog-tiedand crammedinto a cellophanebag. Creepingout of the egg shell, now and then extendingits body to a lengthof 0.4mm., it pushes- and perhaps cuts with its egg-saw--throughthe egg tent beneath which it is imprisoned.While escaping throughthis hole in the egg-tent,or shortly thereafter,as describedabove, the larva emergesfrom its amnionic skin (Fig. 4) . Accordingto Killington(1936), Sisyra and other neuropterons shed the embryonicskin when hatching. First-InstarLarva.-Upon emergingfrom the amnion,the larva ordinarily drops upon the surface of the water. Here it encountersan obstacle whichmany larvae,in the laboratoryat least, fail to surmount.The task of gettingthrough the surfacefilm into the water beneath is a difficultone. By bendingthe tip of the abdomen to the dorsal surfaceof the head or beyond,it may manage to get the posteriorsetae caughtin the film,achieving sufficientpurchase so that the anteriorportion of the body is forced throughbeneath the filmas the larva straightensout. Then it withdrawsthe exposed partsbeneath the surfacefilm and sinks slowly.Since many of mv specimensfailed to squirm throughsuccessfully, I tried various means of assistingthem. Occasionally I succeeded in pushingthem throughwith a finecamel's-hair brush, or by droppingwater upon themfrom a finepipette. The most nearly successfulmethod consistedin loweringthe water level so that part of a sponge barelyprojected above the surface,with the larva strandedupon this small island. When it had gained a foothold,I could raise the waterlevel carefully(by adding waterthrough a pipetteinserted beneaththe surface), leaving the larva clingingto the sponge as it became graduallysubmerged. The same techniquewas helpfulin transferringolder

Fig. 4.-Empty egg shell,egg tent,and amnion.Note anglesof tentfibers at points of attachmentto substrate.These provideclue to problemof spinningtechnique. 1952 BROWN: LIFE HISTORY OF CLIMACIA AREOLARIS 141 larvae to freshsponge dishes, since they experiencedthe same hazardous difficultieswhenever they happened to get above the surfacefilm of the water. Their setae appear to be decidedlyhydrophobic, or unwettable. Once beneaththe surfacefilm, the larva sinksslowly, as a rule. One gets the impressionthat the gas bubble or bubbleswithin the gut of this newly- hatched larva serve as a hydrostaticorgan-either by absorptionor com- pressionof the bubble,-since the larva can apparentlyeither sink or merely drift,suspended midway in the water. I referto any individuallarva; ap- parentlyit has some degree of controlover its specificgravity. If it were merely a matter of some larvae drifting,and others sinking,one could readily postulatediffering amounts of gas in the bubble. I have watched a larva for an hour or more at a stretch,and its activitieswere varied. Everynow and thenit would sink to the bottomand crawlabout for several minutesor longer,crawling up the sides of the dish to the surface film, upside down alosig the surfacefilm, or merelyhere and thereon the bottomn of the dish. It crawlsrather rapidly, with the mouthpartsextended anteriorly, and the antennaeextended antero-laterally. After thus wanderingabout for awhile,it would take to swimming.This involvedcurling the abdomen

0 0.1m 0.01mm

Figs.5-7.-5. Egg-saw,as; it appearson tip of castamnionic skin; 6. Driftingfirst- instarlarva after submergence in water, lateral aspect. After feeding a day or two,the larvaresembles more closely the second-instar larva, in bothsize and shape;7. Drifting first-instarlarva, dorsal aspect. At times,the abdomen is curledeven farther under, leaving onlythe first segment visible from above. Note that the mouthparts of the two sides are notunited in themid-line basally. 142 THE AMERICAN MIDLAND NATURALIST 47 (1)

ventrally,then snappingit back straight-repeatingthis process in a rapid seriesof jerkyflips. At the same time,the legs are activelyutilized. To the naked eye, the swimmingmovements seem quite similarto those of a small Cyclops,and the larva mighteasily be overlookedas such in an ordinary sample of water.The larva swimsthus for a momentor so, at timestrav- cling severalcentimeters. Then it drifts,resting awhile, before resuming its swimming.Or it may simplydrift for 10 to 20 minuteswithout appearing to move a muscle. In this criftingposition (Figs. 6, 7), the abdomen is curledventrally, at timesso completelythat only one or two abdominalseg- mentsare visiblefrom above. If disturbedwhile drifting,as by a currentin the water,the larva usually begins to swim. Whetherthere is any direc- tionalorientation in this swimming,I cannotsay. It appearsto be at random. If, in its travels,the larva -encountersa sponge, it may settle down promptly,piercing the sponge with its hypodermicneedle-like mouthparts, and suckingup the juice and cells of the sponge. Or it may simplyignore the sponge. I have been disgustedmany a time,when the larva I have so solicitouslyguided to or deposiWedupon a sponge obstinatelyrefuses to notice the juicy morsel,hurrying away fromit as if it were an ogre. The fault does not always lie with the sfonge, either,for other larvae may eagerlygo to workon it inmmediatelyupon its discovery. Once settledupon a sponge,the average larva does not readilyleave it, unless it dies. The larva commonlyfeeds for 1/2 to 2 minutes,then restsor wandersfor 1 to 5 minutesbefore reinserting its mouthpartsfor another meal. The descriptionsof the mouthpartsof Sisyra by eitherAnthony (1902) or Withycombe(1922, 1924) serve well for Climacia. (Miss An- thony'sdescription is that of the third-instarlarva, and not appropriateat this point.) I quote fromWithycombe (1924): "Owingto the small size of the larva (.5 mm long) and consequentdifficulty of dis- section,I am not quite sure as to whichportion of the jaw is the mandible,but I feel fairlycertain that it is themandible which is narrowand pointed.The maxillais enlarged in its basal half,and claspsthe mandible;apically it narrowssuddenly, and terminateswith a slightdilatation, which, no doubt,is sensory.I have foundno traceof labial palpi." Both mandibiesand maxillae are groovedalong one side, so that when the left mandible,for instance,is applied to its maxilla, a tube is formed betweenthem. Renderingthe tube more effectiveis the fact that each edge of the groovesis furtherridged or groovedso as to engage in complemen- taryfashion wilth the opposingmember. When food is being suckedthrough these parallel tubes-the rightand left being closely applied side by side- particlesof the sponge tissue may be seen flowingthroutgh them. As in other neuropterouslarvae (Withycombe,1922), the mandible and maxilla move longitudinallyupon each otherduring feeding. This tends to pre- vent clogging.The suckingmuscles of the head, whichdilate the walls of the pharynx,may be seen in action.After feeding, the antennaeand mouthparts are cleaned by means of the fore legs. Here, too, the mandibleand maxilla may be seen to move back and forthupon each other. 1952 BROWN: LIFE HIISTORY OF CLIMACIA AREOLARIS 143

It was amusingto watchlarvae emerge fkrom a sponge osculum through whicha strongcurrent of waterwas passing.Each larvabacked out with deliberationand dignityuntil the forepart of the bodywas struckbroad- side by thecurrent as themidpoint of thebody passed the rim of theoscu- lum. The hindtarsal claws had gaineda firmfoothold before this point was reached,so thatwhen the forepart of the body was suddenlyand forciblyexpelled, the larvaflipped quickly to the side of the osculum-out of thecurrent. A newly-hatchedlarva is usuallyfrom 350 to 500,uin -length, exclusive ofmouthparts. The jawsare about 125 to 140t in length.The greatestwidth of thehead is from75 to 100p.The head is oftenslightly broader than the thorax.The abdomentapers to a bluntpoint. The overallgeneral appear- ance of the larvaat thistime is reminiscentof a crayfish.Each segment of thethorax bears a pairof dorso-lateralblackish sclerites. The prominent eyespots,each composed of 6 blackocelli, represent the only other noticeably pigmentedportions of the body,although the long terminalsetae of the abdomenappear quite dark. The mouthpartshave beendescribed, though I mightmention that no signof a palp is visible,and thatthe jaws are almosttwice the length of the head. The antennaeare a littlelonger than the jaws,and are composedof 5 joints.The basal jointis broadest,the second,third, and fourthjoints being progressivelya little longer anrd rarrower. A spine arisesdistalyr fromthe thirdjoint, and extendsventro-medially parallel with, and almost as faras, thetapering fourth and pointed fifth joints. The legsare essentiallyalike. Each has butone tarsal joint and one tarsal claw,which is relativelylong and sharp,and slightlycurved. On each side of the head,there is an antero-dorsalseta. The prothorax bearsone anteriorand one posteriorseta on each side of the mid-dorsal line. The meso-and meta-thoraxeach bear symmetricallyone dorsaland one lateralseta. Each of thefirst 8 abdominalsegments bears, on eitherside, a dorsaland a lateralpapilla, each bearing a pairof setae.These setaeare progressivelylonger posteriorly, those of the seventhand eighthsegments beingthickest and longest.The ninthabdominal segment is encircledpos- teriorlyby 8 papillae,each bearinga long s.eta.The tenthabdominal seg- mentbears no setae. No gills are visible.As suggestedby Withycombe(1924), absenceof the gillsin the firstlarval instar indicates that the gills of laterinstars are probablynot vestigesof ancestralabdominal appendages. Afterfeeding for severaldays, the body lengthmay be doubled,the abdomenbecoming especially enlarged and elongated.Under laboratory conditions,ecdysis occurs about the end of the firstweek, if at all. Second-InstarLarva.-A well-fedsecond-instar larva is depictedin Fig. 8. The generalbody proportions are noticeablydifferent from those of the first-instarlarva. Otherdifferences include the following:the mouthparts 144 THE AMERICAN MIDLAND NATURALIST 47 (1) are longerand more flexible;the tips can be bent at the will of the larva. The antennaeare longer,and are comprisedof 6 joints. The long spine now arisesfrom the distal end of the fourthjoint, a small seta arisingfrom

I I~n Fig. 8.--Second-instarlarva, shortly before ecdysis. Dorsal aspect. 1952 BROWN: LIFE HISTORY OF CLIMACIA AREOLARIS 145

the distal end of the fifth.An additionalpair of setae has appeared on the head. Each thoracicsegment now bears 5 pairs of papillatesetae. Lateral papillae of the meso- and meta-thoraxand the first8 abdominalsegments now bear clustersof 3 setae. In each dorsal row of tubercles,the meso- and meta-thoraxand the firstabdominal segment each have 2 setae, whereas abdominalsegments 2 through7 each have 3 setae. Abdominal segments1 through7 now bear, on each side, a jointed trachealgill folded mediallyand posteriorlybeneath the body. These gills are transparentand are intermittentlyvibrated, so that the ventralsurface of the body, as seen frombelow or fromthe side, is blurred.These gills are kept vibratingmost of the time and are difficultto see, even when quiescent.For that matter,they are also ratherdifficult to observein detail in preservedmaterial. In life, they often extendbeyond the posteriorend of the abdomen almost as far as the long setae, althoughthey are easily overlooked.Each gill containstwo trachealtrunks. These trunkspass forward and medially,appearing to unite in the midlinein the prothorax.The general structureof the trachealgills of Climacia seems quite similar to those of Sisyra vicarid, as descri'bedand figuredby Anthony (1902). Third-InstarLarva.-Fig. 9 representsa migratingthird- or last-instar larva-i.e., ol1e which nas left the water,'but has not yet begun to spin. Among the ways in which the third-instardiffers from the second-instar larva are the following:the mouthpartsare now much more flexible,long, and slender.The antenna consistsof 16 joints, the firstof which is very short and broad, the second narrower,longer, and slightlytapering. Joints 3 through15 are yet more slender,all being of approximatelythe same diameter.They differconsiderably in length,the thirdbeing as long as any two otherscombined, and the sixth,seventh, tenth, eleventh, and twelfth being shorterthan the others.The sixteenthjoint is sharplypointed. The fifteenth,which tapers somewhattoward the tip, bears a small seta at its distal end. There is now interpolatedbetween the head and the prothorax, on the dorsal side only, a short pseudo-segmentwhich is ratherclearly- defined.In the dorsal row of tuberclesor papillae on eitherside of the mid- dorsal line, all remainingsegments but the firstabdominal have now added a third seta. The leg joints are much more liberallysupplied with hairs or setae. On eitherside of the mid-dorsalline of the eighthabdominal segment is a single more-or-lessmedian seta. The setae are noticeablyshorter on the ninthabdominal segment. Small hairs may be seen on the tenthabdominal segment.A patternof brown or blackishpigment spots, chieflyalong the mid-dorsalline, is obvious on many of the larvae, althoughdetails of the patterndiffer among various individuals. The color of the larva depends largelyupon the sponge fromwhich it came, greenlarvae comingfrom green sponges,etc. In almost any random sample of migratinglarvae, the body colorationranges from a rich green to a lightyellow-brown. In the paler specimens,the stomachcontents often give the mid-thoracicregion a red or orangecolor. 146 THE AMERICAN MIDLAND NATURALIST 47 (1)

While yet feedingupon the sponge, a third-instarlarva has the same numberand type of gills as describedfor the second-instarlarva. Upon leavingthe water,these gills disappear or shrink,so that only a lump re-

iNR*fi .

nmm

Fig. 9.-Third-instarlarva, migrating.Dorsal aspect. Note singlesmall seta arising fromsubterminal joint of antennae,and greatly-increasednumber of antennaljoints. If the terminalabdominal setae were relatively as largeas thoseof precedinginstars, they would seriouslyinterfere with the spinningof the cocoon. 1952 BROWN: LIFE HISTORY OF CLIMACIA AREOLARIS 147 mains to indicate the formerlocation of each gill base along the ventro- lateralsurface of each of thefirst abdotninal segments (Fig. 12). Upon the sponge, Climacia larvae are as deliberateand unaggressiveas aphids. Larvae of various instarsfeed calmly side by side, now and then even crawlingover one another.Occasionally, however, a larva will make a sudden jump or jerk-perhaps to dislodge irritatingmaterial which may have adheredto it. Many of the larvaehave theirsetae fairlywell coveredwith debris, and are quite inccnspicuousupon the sponge as they rest quietly upon its surface,blending harmoniously with the background. After leavinlgthe sponge, a third-instarlarva may crawl or swim to some objectupon whichit may climbout of the water.The numerouslarvae which emerge upon boat hulls attest to the importanceof swimmingin this firstlap of its migratoryjourney. The manner in which the larva swims has been adequately describedby Old (1932 b), as quoted in the historicalreview. The larva is now much more active than when upon the sponge, although its rate of progressionvaries considerablywith the sur- roundingtemperature. At a temperatureof about 800F., the average speed of a numberof timed larvae was about 1 cm. per second. Since the larvae may crawl for severalhours afterleaving the water,before settling to spin, it is not surprisingthat their cocoons are occasionallyover 50 feet from the water's edge. In climbing,the spinneretis used for temporaryattach- ment at times,resulting in a mode of locomotionresembling that of a geo- metridlarva, or "measuringworm." According to Withycombe(1922), this is commonamonlg neuropterous larvae.

Fig. 10. - Diagram to illustrate method of net-spinningby larva. Note that only the abdomen -3 - m changesposition, the fore part of _ - s~ 0 the body remainingin place. A B When the larva has selecteda site for the cocoon-often in a crevice or corner-it secures a firmfoothold, partially withdraws its head beneath the prothorax,and extendsthe abdomen.The abdomen exhibitstelescopic movements,and the spinneret,which may be seen in the median portionof the last few abdominalsegments, appears to undergocontractions. The tip of the abdomen is touched to the substrateand the viscid,semi-liquid silk oozes out, becomingattached to the surface.Now, by a seriesof shorttugs or pulls, the silk is drawnout into a fiber,looped over,and again attached to the substrate(Fig. 10 A). Next, the strand of silk is drawn up in anotherloop, attachedto the edge of the formerloop, and continueddown to the substrateon the otherside of the initialloop. This processis repeated, back and forthfrom one side over in an arc to the other side. Since the legs retaintheir original positions, with the head and thoraxremaining fixed, 148 THE AMERICAN MIDLAND NATURALIST 47 (1) a hemisphericnet is spun over the body-the radius of the arc being determinedby the lengthof the extendedabdomen. Toward the end of the spinning of the outer net, as shown in Fig. lOB, the tip of the abdomen is stretclhedforward beyond the aintennae.After the net is completed,the telescopictip of the abdomenenergetically explores most or all of the net, retracingpractically every strand,adding fine strands along the previous lines, thoughoften cutting corners. As it does so, it oftenvibrates up and down slightly,spinning the tiny narrowarches above the heavierfibers de- picted (along one of the mesh fibers) near the top of Fig. 11. On some nets, the entiremesh is thus ornamented,while on othersonly a few or none of the fibersbear these microscopicjiggles. When the net is thus finishedand reinforced,a numberof cross-fibresare spun directlyfrom top to bottomof the net, and fromone side to the other.With these strands as a framework,the larva now proceedsto spin the cocoon withinthe net. In the process of constructingthe cocoon, the larva firstspins awhile at one end, then reversesits position,cramped though its quartersbe, and continuesspinning at the oppositeend.

The completednet and cocoon are representedin Fig. 11, the darker centralportion of the cocoon being intendedto representthe larva within, vaguelyshowing through the layetr of silk. Actually,there are relatively ; fewerlongitudinal strands than are shown, and more criss-crossedhori- zontally-encirclingones. Some of the supportingfibers may be seen.

Fig. 11.-Cocoonand netof Climacia, viewedfrom above. Some of thesupport- ingor frameworkstrands may be seenex- tendingfrom the cocoon out to thenet.

Various cocoonIs and nets differmarkedly in neatnessand size, the latter dependingprimarily upon the size of the larva. The overalllength of most nets is between4 and 7 mm. In cases wherethe larva choosesa cocoon site lacking in adequate substrate,and sometimeseven when the substrateis perfectlyadequate, the outer net may be omitted.Examples in point are cocoons on spiderwebs, grass blades and stems,fibers of hemp rope, or the appendagesof other insect skins or corpses. I have found as many as 5 netless cocoons clusteredone upon the other on a projectinghemp fiber. 1952 BROWN: LIFE HISTORY OF CIIMACIA AREOLARIS 149

Dragonflynaiad and mayflysubimnaginal casts oftenbear clumps of Clima- cia cocoons. The rate of spinningvaries, of course,with the environmentaltempera- ture. At about 75?F., it requiredan average of around 7 seconds for the tip of the spinneretto spin a single mesh-arc-i.e., from one to another point of attachmentupon a previously-formedpair of consecutiveloops or waves of silk thread.It requiredbetween 40 and 75 minutesto completethe net, beforeretracing its meshes.From 2 to 5 more hourswere requiredfor the completionof the cocoon. From about 4 to 8 hours elapse betweenthe time the larva leaves the waterand the time when it has finishedits spinning. When a larva has settled,but not yet begun to spin, it will jump if crawled over or otherwisedistuibed by anotherlarva. Once spinninghas begun, however,this behaviorpattern is no longer exhibited;instead, the larva merelyhuddles down, maintainingits exact position,even though a second larva may go scurryingright over it. The net, even duringthe process of construction,is strongenough to supportthe weightof such wan- dering larvae as may clamberover it. On a smooth substrate,such as a glass Petri dish, the larva often experiencesdifficulty in maintainingthe position of the anteriorpart of the body while the abdomen is weaving to and fro above it. Under these conditions,the larva frequentlyslips, whereuponit will usually startall over again. Some of my specimensmade as many as 5 unsuccessfulattempts before achieving a completenet. Others turnedaround withintheir incomplete nets and constructeda second half, beginningat the substrateand workingupward to meet the firsthalf. These generallyproduced rathermessy-looking nets. Occasionallytwo larvae spin too close together,or the cocoon of one larva may obstructthe passage throughwhich anotheremerging individual must travel to escape. Individ- uals so trappedfail to emergefrom the pupal skin. At times an agitated larva,after a territorialsquabble, hurries away fromits unfinishednet, leaving a trail of silk wnercverit goes. These are but a few of the complica- tions whicharise. My attemptsto photographthe spinninglarva failed. As soon as the brightbeam of light struckthe larva, it would contractits abdomen.The constantmovements of the abdomenrendered slower photography with dim- mer light impractical.Of spinninglarvae immobilizedby the intenselight beam, 6 died withoutfurther spinning or pupating,whereas 8 othersdid no more spinning,but pupated with the unfinishednet. These 8 died in their pupal skins,although several of themdid not die unzil time for emergence as adults. Within the completedcocoon, the larva may spend from30 to 60 hours beforepupating-possibly longer at yet lower temperatures.Meanwhile, the head has been turnedbeneath the prothorax,the mouthpartsand antennae now being directedposteriorly and lyingalong the mid-ventralline between the flexedrows of legs (Fig. 12). In this bowingof the head, the chitinous 150 THE AMERICAN MIDLAND NATURALIST 47 (1)

coveringsof the eyes have separated fromand slipped ventralto the pig- mented portionsof the eyes, which now loom large and owlish within the prothorax.

cocoon,Fig. 12.-Restingbefore pupation. Climacia Ventral larva aspect.within This larva would never have pupated, since it had been stung by a parasitic pteromalid wasp, one egg of which lies near the right eye of the host. A newly- hatched larva of the wasp is feeding upo-1 ...... _.. :the abdomen of the host, sucking out its ...... : s;contents.;: Note the position of the eyes in the prothorax of the Climacia larva, th2 old eye shells being located medial to them. This position of head and appendages is characteristic. The ,i-es of the ;, 27tWs @)ventro-lateral gills may be seen on the first .v 1 \\seveis ab dominal segments.

1mm

Pupa and Emergence.-Upon pupation,the larval skin is tuckedinto the posteriorend of the cocoon as a prickly-lookingbrown wad. The pupa is characteristicof the Order Neuroptera,with the appendagesimmovable until shortlybefore emergence. It exhibitsthe charactersof the adult, exceptin proportions.The wings, in particular,are relativelymuch shorterthan in the adult. The head is tucked beneaththe prothorax.The sex may readily be determinedby examiningthe genitalia.The antennaepass dorsal to the eyes and lie along the anteriormargins of the fore-wings,extending beyond theirdistal extremities.The tarsi of the hind legs also extendposterior to the wing tips and slightlyposterior to the tips of the antennae. Fig. 13 depictsa pupa between6 and 12 hotursbefore emergence, prior to the libera- tion of the appendages.On the ventralsurface, between the eye and the second leg, may be seen the dark, heavilysclerotized mandible, with which the pupa chewsits way out of cocoon and net. Among the specimensreared in the laboratoryat various temperatures (uncontrolled),the time elapsingbetween emergence of the larva fromthe waterand emergenceof the adult fromthe cocoon rangedfrom 120 to 170 hours. Most adults emergedat the end of the fifthor sixth day, usually aftersunset. From 5 minutesto an hour or more beforethe onset of chewing,the antennae and other appendages may be seen to be free. Ordinarily,the pupa chewsand pushes its way out of the cocoon withina few minutes,and 1952 BROWN: LIFE HISTORY OF CLIMACIA AREOLARIS 151 promptlyproceeds to chew its way throughthe net. Beforegetting the entire body throughthe net, however,the abdomen begins to undergoa series of telescopic,peristaltic, movements. Internal movementsmay be observedon up to the head. Within 2 or 3 minutesafter this has commenced,the skin splits in the mid-dorsalline of the mesothorax.The split soon spreads to the metathorax,posteriorly, and to the prothoraxand head, anteriorly.With- in 2 or 3 moreminutes, the adult has completelyemerged from this slit,the antennaeoften being among the last structuresto be completelywithdrawn fromthe old skin. About 5 minuteslater. the wingsare being gentlyfanned as they finishuncurling and spread:ng.The wings are completelyunfurled and spread in 6 to 8 minutes.Meanwhile, the abdominal segmentshave been extending.Within about 15 minutes,the abdomen has reached its normaladult size and form,and withinabout 2 hours,its color darkensfrom green or tan to brown.The wingsand antennae,pale at emergence,darken to theirordinary adult colors within'-/2 to 11/2 hours. Within the firsthour or two followingemergence, often before leaving the vicinityof the cocoon, a dark brownfecal pellet is deposited.This probablycontains the accumu- lated waste solids fromthe entireprevious existence, and is enclosed within a peritrophicmembrane. I believethat Sisyra vicaria producesa similarfecal pellet,and that Miss Anthony (1902) inerelyhad no opportunityto observeit, since she worked only withpreserved material. Nievertheless,her remarksconcerning the larval alimentarytract are of interest:"In Siyra, thereis no such residuum,since the juices of the sponge are ready for comipleteabsorption. An extensive digestivetract being in this way renderedsuperfluous, nature has economized by modifyinga large part of the alimentaryapparatus into a silk-secreting organ.

1mm

Fig. 13. Climaciapupa 6-12 hoursbefore emergence, lateral aspect. This specimen maybe recognizedas a femaleby its genitalia.The appendagesare notyet free. 152 THE AMERICAN MIDLAND NATURALIST 47 (1)

14 15

I m

Figs.14, 15. 14. Posteriorportion of abdomenand genitaliaof gravidfemale, lateral aspect.Eggs may readily be seenbulging the side of the body wall. The structurebearing the spinneretis terminal,and is foldedvertically; 15. Posteriorportion of abdomenand genitaliaof adultmale, lateral aspect.

"The posteriorfourth of the stomach appears merelyas a solid cord of atrophiedcells, whichends in the walls of a dilatation-'silk receptacle,' it may be termed.The walls of this receptaclehave the structureof those of the Malpighiantubules. It appears to be the outlet of fivetubules, three of whichare attachedhere at both ends, and two of whichextend posteriorly and end in the body cavity.All are modifiedin theirmiddle portionsfor the secretion.After passing throughthis tube, the silk collectsin the spinneret, the walls of which are surroundedby bands of strong circular muscles,which aid in ejectingthe secretionwhen the cocoon is spun." Withycombe(1922) points out that Sisyra has 6 looped Malpighian tubes, instead of 3 (in additionto the 2 which are not looped), and that the conditionsdescribed above are similarto those in most neuropterouslarvae. Lampe (1911) also found8 Malpighiantubes, but statesthat theyend blindly. During the pupal stage, the gut becomes complete,the lumen of the alimentarytract now being continuousfrom mouth to anus. A vexingbehavior pattern was noted in the emergingpupae: if disturbed whilechewing through cocoon or net, the pupa "'freezes,"remaining motion- less for as long as an hour. An abruptchange in light intensityis sufficient to elicit this response. Adult.-There is littleneed in my describingthe adult, since it has been 1952 BROWN: LIFE HIISTORY OF CLIMACIA AREOLARIS 153 previouslydescribed by Hagen (1861), MacLachlan (1869), Needham (1901), Banks (1906), and Navis (1935). Fig. 16 portraysa fema!e afteroviposition. Figs. 14 and 15 representthe terminalabdominal segments and genitaliaof a gravid femaleand a male, respectively.From the dorsal or ventralaspect, tne femaleabdomen ends in a joint, whereasthat of the male is bluntlyrounded at the posteriorend. When at rest,the adult holds the antennaeside by side, directlyanterior, and ratherclose to the substrate.When alert,the antennaeare spread apart and directeddorso-latero-anteriorly, or kept w-avingabcut, the rest of the body remainingmotionless. Whetheranimal food is ordinarilytaken, I do not know. It is not neces- sary,however, since I have obtainedmating, eggs, and larvae fromindivid- ua!s rearedin the laboratoryand exposed to no food otherthan gumdrops and water.That adults under naturalconditions feed upon plant products such as nectaris indicatedby the fact that the fecal droppingsof captured adults may be largelycolnposed of polien grains.I intended,but nevergot around,to experinentwitlh such sourcesof animal food as aphids. Sisyrids mightreasonably be expectedto feed upon animals of this sort,when one considersthe foods of most of theirrelatives e. g., hemerobiidsand chryso- pids. Furthermore,the adults nave well-developedmouthparts (Crampton, 1921). What the naturallife span is, I cannotsay. It is conceivablethat a few adults mighteven survivethe winter.Under laboratoryconditions, with the restricteddiet mentionedabove, most of the adults die within2 or 3 weeks, althougha few lingeron anotherweek or so. If the presenceof the adults upon windowsat night (a sort of lighttrap) is a valid means of estimating abundanceand naturaloccurrence, I can state that thereis a rapid turnover. At least,the adults occurin numbersupon the windowsonly during,and for a fewdays after,the periodsof heavyemergence from the cocoons. This sug-

lmm

Fig. 16.-Adult female,after oviposition. Lateral aspect. The footof the adultClimacia maybe seen to have two tarsalclaws, whereas that of the larva had but one. 154 THE AMERICAN MIDLAND NATURALIST 47 (1)' gests,in the absence of otherfactors such as strongwinds, that the adults- either: (1) die offwithin a fewdays, (2) migrateaway fromthe waterfront aftera fewdays-perhaps into the more heavily wooded sections of the islands, (3) dispersein all directions,traveling considerable distances within a fewdays, or, (4) lose theirphototactic response after a few days. Or perhapsa com-- binationof some of tlhesefactors may be in operation. Mating may occur,apparently, several hours after emergence, or any time withinthe followingweek or two. At least,the males are stillexhibiting court- shipbehavior after two weeks or morein thecage. Courtshipand matingseems. to take place, as a rule,in subdued lightor in darkness-eitheron a cloudy day or duringthe eveningon past midnight.The air has usually also been humidwhen I have observedcourtship, but this factormay have been of no significance. The males,in general,are more activeand nervouisthan the females. If, in his excitedwandering, a male contactsa female-fromany direction-he evidencesimmediate interest. (Occasionally, two males, if they meet head- long,will take momentary interest in each other. The interestis fleeting.) He extendshis wingsand antennaelaterally, maneuvering into a positionat a 90' angle fromthe body of the female. He usuallyremains in thisposition for a few seconds,with his head about on a level withthe firstabdominal segment of the female,one of his antennaeextended beyond and touchingher wing-tip, the other antennaextended forward beyond her head, crossingone of her antennaeand touchingthe other.He may now partiallyfold his wings,except forhis forewingon theside towardher head, withwhich he appearsto be fan- ning towardher head. It may be that some portionof his anatomy-e.g.,a portionof his genitalia-producesa sort of aphrodisiacodor, whichis being waftedtoward the antennaeof the female. Perhapsthis is mere fancy. At any rate,keeping his head and antenlae fixedin theirpositions, he now bends his body around towardhers, curls the tip of his abdomenventro-laterally beneaththe loweredge of her wings,and contactsher genitaliawith his own. She oftenrepulses him at thispoint, if not sooner. (A femaleuninterested in the attentionsof a male, if flirtedwith by a male, usuallymakes a shortrush at him, wavingher antennaemeaningfully. He seems to get the idea, and promptlydeparts.) If not repulsed,the male remainsin this positionfor a shortwhile, then disengages and movesalong. A willingfemale remains mo- tionlessall this time,except for a few parrieswith her antennaeat the very outset. The intrusionof anotherindividual, usually some othereagerly roving male, immediatelybreaks up the affair,and both of the interruptedparties go away,unless the interruptedmale "locks antennae"with the intruder. In the lattercase, the interestof each in the otherwanes in a moment,and each goes his own way. Often severalmales simultaneouslyattempt flirtation with a singlefemale. She commonlyducks out of the huddle and goes about her business,leaving the excitedmales investigatingone another. In a successful copulation,the male appearsto deposita spermatophorewith the female. It is yellowish-whitein color,and less thana millimeterin any dimension. I have 1952- BROWN: LIFE HISTORY OF CLIMACIA AREOLARIS 155 foundseveral upon the surfaceof or withinthe waterin the open Petridishes in the breedingcages. Eitherthey had fallenthere from above, or one of the flieswith an exposedspermatophore had fallenupon the water,lost its sper- matophore,but managedto escapefrom the water. I have collectedmating adults but once in nature. They werecopulating in flight,at dusk. Ovipositionoccurs between 2 and 6 hoursafter sunset-sometimes, at least, withinbut a fewhours following copulation. As mentionedin the sectionon theegg, the eggsare depositedin depressionson objectsabove the water. The gravidfemale moves about with her abdonen curled forwardventrally, the blade-likestructure at its tip extendeddownward to the rearand lookingsome- whatlike a pocketknife three-quarters opened. With this blade-liketip, the femaleis exploringthe surfaceof the substrate,as she walks upside down or verticallyalong on the objectshe has chosen. When the tip discoversa depression or groovethat "feels right," an e"g or a groupof eggsis deposited.Then the blade, withthe openingof the silk or cementgland at its tip, describes lightning-likezig-zag vibrations to and frobetween the rimsor edges of the depressioncontaining the eggs. Afterspinning thus for a moment,the female shiftsher positionand continuesher spinningfrom another angle. Aftersev- eral such shifts,the eggs are ordinarilywell coveredby a sheetof silk,though occasionallythe aim is poor and the tent does not cover the eggs at all (Fig. 4). At firstI thought,as did Withycombe(1922), thatthe femalefirst spun one layerwith the fibers approximately parallel, then, upon shiftingher position, producedanother sheet with fibers at an angle to the first. However,by care- fullystudying such a tent,I discoveredthat this was not the case at all. The spinnerettip describesa letterZ, the line thenbeing carried back fromthe end of the Z to a pointjust belowits beginning,forming an angularfigure 8, then thewhole process is repeated,etc. The movementsof the tip are too rapid for the eye to follow,even thoughone managesto observethe processclearly at highmagnification. I include this particularphotograph (Fig. 4), in prefer- ence to otherswhich show the eggshelland amnionbetter, because it shows ratherwell the spinning pattern of theegg tent. Exactlyhow many eggs a femalemay produce, I have not determined.The number,however, is at least 45. One nightI collected2 femaleswhich had beenovipositing, brought them into the laboratory, and placed themin a corked 8-dramvial containinga singleclean Cornusleaf. By the followingmorning, theyhad deposited90 eggs upon the leaf,cork, and glass. It is obviousthat the minimumnum'ber of eggs prcducedovernight by a single one of these femalesmust have been 45. In ovipositingand spinningthe egg tent,the femaleswork with surprising rapidity. A singlefemale laid 2 eggs,spun theirtent, laid anotheregg else- where,and was in the processof spinningits tentwhen interrupted-all within slightlyless thanone minute. Mortalityand Natural Enemies.-Excessivewind, water, or directsunlight 156 THE AMERICAN MIDLAND NATURALIST 47 (1) are amongthe physical factors which may seriously reduce the population of Climacia. For instance,high winds may blow the adults out intothe lake or mayinterfere with the migrations of thelarvae either directly or indirectly-by churningup thewater and thuspreventing their successful emergence. Both waveaction and heavyrains destroy the animals within their cocoons, as also rm-aydirect sunlight. Hazards presented by the surface film of thewater have alreadybeen discussed. Amongbiological factors, a numbermay be listed. The eggsare often attackedby fungi.Both eggs andc emerging larvae appear to sufferfrom the activitiesof predatoryand egg-suckingmites, if not otherarthropods. The first-instarlarva must run the gamutof larger-planktonfeeders, including suchforms as Hydra,which is oftenabundant in thevicinity of thesponges, and the bladderwort,Utricularid. (On July 31, I opened Utricularia bladders,finding but an ostracod,an oligochete,and a fewprotozoans. How- ever,the materialhad stoodin the laboratorya numberof days.) In the laboratory,"sewage fungus" (which, I believe,is reallybacterial in nature) constitutesa major menace, either by destroyingthe sponge upon which the larvalives, or by actuallyentangling and killingthe larva-perhaps through suffocation,byusing up muchof theavailable oxygen. The third-instarlarva meets a phalanxof perils.While swimming through thewater, it is a likelytarget for predatory fishes, its mode of swimmingren- deringit ratherconspicuous. Once on land,there are myriadsof spiders, centipedes,and antsawaiting it. The antspatrolling the edge of the dock seizethe Climacia larvae and makeoff with them as if theyreally had been lookingfor these luscious tid-bits. At that,the larvae are oftenlarger than the antswhich carry them off. As forthe centipedes:I have counted3 specimensof Scutigerafeeding upon Climacic, larvae at one timeon thenet- drierin frontof thelaboratory. Indirectly, however, they are alliesof Cli- macia,in thatthey frequently devour the spiders-which, in turn,might have eatenmy larvae. I haveobserved one fat spider (an orb-weaver)holding two Climacialarvae with its feet-pinningthem down -, whileit was feeding upona third. Withinthe cocoon,both restinglarvae and pupae serveas host for Sisyridivora,a pteromalidwasp, of whicha detailedaccount has been publishedseparately (Brown, 1951). The wasp insertsits long ovipositor throughnet and cocoon, stings the larva or pupa,and deposits an egg.Fig. 12 representsa resting or pre-pupal Climacia larva upon which a waspegg is lying besidethe eye and a recently-hatchedwasp larva is feedingupon the ventral surfaceof the abdomen. By the time the wasp grub or larvais readyto pupate, thehost has been completely devoured-except for the skin. In placeswhere the Climacidcocoons are abundant,these wasps also becomenumerous. I have collected15 waspswithin approximately 1 square meter at thesame time on thenorth cliffs of Gibraltarisland. Somepupae seem to be simplytoo weakto emergeas adults,even though theymay manage to chewout of cocoonand net. Othersare overtakenby 1952 BROWN: LIFE HISTORY OF CLIMACIA AREOLARIS 157

fungi,especially in the damp caves along the northcliffs of Gibraltarisland. In the laboratory,I have noticedthat small grayjumping spiders (Atti- dae) get intothe adult rearingcage-one thathas a crackin it. These spiders seem to eat everythingbut the wings,as I have seen other attids do with soft-bodiedflies. Host sponges.-The only species of sponge upon which I have found Climacia larvae is Spongilla fragilisLeidy. My identificationswere based upon permanentslides preparedaccording to the directionsgiven in Ward & Whipple (1918), and identifiedby means of the key presentedin the same book. The sponges occurredat depths rangingfrom just beneaththe surface to over 6 feet. Most of themwere on the undersides of rocks. Those in relativelywell-lighted situations were green, the othersbeing yellowishbrown in color. Cultureof the spongesis describedin the sectionon materialsand methods. It was notedthat, although Spongilla fragilis occurs both in the relatively cool, clean lake and in the relativelywarm, polluted Haunck's Pond (on Middle Bass Island), sponges fromthe lake yielded only Climacia larvae, whereassponges from the warm,shallow pond yieldedonly Sisyralarvae. I am here consideringonly the sisyrids;actually the spongesalso had several differentkinds of mitesliving in and upon them,and oligochetes,chironomid and trichopterouslarvae, and perhapsa few otherorganisms, as well as the sisyridlarvae. Old (1932a) lists a nunmberof associatedmacro-organisms whichmight be added to thisgroup. I have not determinedthe extentof the damage,if any,caused the sponge by its sisyridparasites.

DISCUSSION A generalpoint or two remainto be considered. I have estimatedthat around 50,000 Climaciaeggs are depositedbeneath our woodenboat dock on a single nightduring a period of heavy emergence. This rate is maintained for about a week. Consequently,there should be a considerableshower of larvae fallingupon the watera week or so later. Since many of these will probablybe driftingfor a matterof hours,it seemslikely that some of them should be collectedin planktonnets. They have never,to my knowledge, been reportedin planktonsamples, although such have been takenduring the periodsof theirabtmdance by variouslimnologists. Why have theynot been detected? I suspectthat the answerlies in the samplingor collectingtech- nique. The larvae probablyseize and cling to the net, and are thus not washeddown into the concentratingreceptacle. So faras I know,sisyrid larvae have not been reportedfrom fish stomach analyses. I suspectthat they will be, afterthe analystbecomes acquainted withsuch unique diagnosticcharacteristics of sisyridlarvae as the singletarsal claw or the slendermouthparts. I hope to examinethe morelikely species of fishat some futuredate. Nevertheless,since sisyridsare, as yet,unreported 158 THE AMERICAN MIDLAND NATURALIST 47 (1)

in such studies,it is reasonablysafe to assume that theyplay no significant role as fishfood. All thingsconsidered, this is hardlysurprising. Lestage (1921) statesthat Sisyra larvae occur as parasitesupon filamen- tous algae and such bryozoaas Cristatellamucedo, as well as upon sponges. I have collectedthird-instar Climacia larvae upon algae-coveredrocks and beneathbare rocks,but theywere not feeding.The fully-grownthird instar larva leaves its host sponge and wandersabout or hides in protectedplaces duringits last day in the water. Not untilnightfall does it leave the water in quest of a pupation site. It is possible that such migratingor resting larvae, found upon algae or bryozoa,might provide the basis for Lestage's statement. I have encounteredno referenceto Climacia as a parasiteupon anythingother than sponges. Since I have not made a year-roundstudy of Climacia,I cannotstate posi- tivelywhat the overwinteringstage is, or how many broods there are. In England, Withycombe(1922) found Sisyra larvae throughoutthe winter. Killington(1936), however,states that Sisyra overwintersin the prepupal stage withinthe cocoon. Perhapsthe mode of overwintering,at least in some regions,is' contingentupon the conditionof the local host spongesduring the wintermonths. Thus, wherethe spongesremain alive and intactthroughout the winter,the sisyridlarvae might remain upon them,whereas in areas where the host spongesdisappear with the onset of winter,the sisyridsmight sur- vive in the prepupalstage. Furtherobservations must be made beforethe problemis settled. Regardingthe numberof broods,I should say thatthere are at least three per summerin the regionstudied. If overwinteringoccurs in the prepupal stage, I have probablymissed the firstemergence, which, I suspect,should appear in May. The adults, in the summerof 1949, were most numerous duringthe last week of June,the last week of July,and the last week of August. The August emergencewas morediffuse than the others,migration and pupationof larvae havingbeen seriouslyinterfered with by strongwinds and cool weather. Periodsof abundanceof migratinglarvae correspondwith those of the adults,coming about a week earlier. The observationsof Need- ham (1925) suggestthe occurenceof only two broods of Climacia a year in New York (Lake Geotge). The warmerwater of the Put-in-Bayregion may accountfor our greaternumber of broods. Withycombe'sstatement (1924) that Climacia larvae are less specialized than those of Sisyra was apparentlybased upon an erroneousimpression he gained concerningClimacia froman incompletefigure of the larval head presented by Crampton (1921). Several authorshave repeatedthis statement withoutinvestigating its basis. Actually,I should say that Climacia is quite as highlyspecialized as Sisyra-more so, in fact,if we considerthe cocoon rnet. This elevates Climacia to the exalted positionof having perhapsthe mosthighly specialized of all neuropterouslarvae. After remarkingupon the strikingsimigarity between sisyrid and osmy- lid first-instarlarvae, Withycombe (1924) continued: ". . . it appears to me very probablethat the Osmnylidlarval habit of probingmoss for Dipterous 1952 BROWN: LIFE HISTORY OF CLIMACIA AREOLARIS 159

larvaewas of such a kind as to lead to the discoveryof the freshwatersponge as a means of livelihood. Freshwatersponges as a rule containDipterous larvae,especially Chironomids, and the deeper the sponge in the water,the fewerlarvae are present. Now, the Sisyra larva must feed on the sponge itself." This speculationapplies equallywell to Climacia. (Killington,1936, discussesthe evolutionaryrelationship of sisyridsand osmylids,and reaches similarconclusions.)

SUMMARY Literatureon the biologyof sisyridsis reviewed. The egg, the threelarval instars,and the pupa are describedand figured, with notes concerningtheir collection, preservation, and developmentunder laboratoryconditions. All stages of the life cycle were reared in the laboratory. Details of methodsand resultsare presented. Activitiesof the adults are described,including courtship, mating, and oviposition. Genitaliaand an entireadult femaleare figured. Ecologicalfactors affecting distribution and abundanceare discussed Evidence is presentedindicating that three or more generationsmay developwithin a year. Relationshipsof Climaciato otherorganisms are considered. The host speciesin the area studiedis Spongillafragilis Leidy. The investigationsupon whichthis paper is based were conductedat the Franz Theodore Stone Laboratory,Put-in-Bay, Ohio-near the westernend of Lake Erie.

REFERENCES

ANTHONY, MAUDE H. 1902-The metamorphosisof Sisyra. The AmericanNaturalist 36: 615-631, 18 figs. BALDUF, W. V. 1939-The bionomicsof entomophagousinsects. Part IL. 384 pp., 228 figs.John S. SwiftCo., St. Louis, Mo. BANKS, NATHAN 1906 (sometimescited as 1905)-A revisionof the nearcticHemero- biidae. Trans. Amer.Ent. Soc. 32: 21-51,3 pls. BROWN, HARLEY P. 1951- Climaciaarealaris (Hagen) parasitizedby a new pteromalid (Hymenoptera:Chalcidoidea). rI. Life historyof the parasite. Ann. Ent. Soc. Amer.44(1): 103-110,8 figs. BURMEISTER, H. C. C. 1839-Handbuch der Entomologie.Berlin 2 (2). CARPENTER, F. M. 1940-A revisionof the nearcticHemerobiidae, Berothidae, Sisy- ridae,Polystoechotidae, and Dilaridae. Amer.Acad. Artsand Sci. Proc.74 (7): 193-280,75 figs.,3 pls. COMSTOCK, JOHN H. 1940-An introductionto entomology.Comstock Pub. Co., Inc., Ithaca,N. Y. CRAMPTON, GUY C. 1921-Scleritesof the head, and mouth-partsof certainimmature and adultinsects. Ann. Ent. Soc. Amer.14: 65-103,7 pls. DEGEER, CARL 1771-M6moire pour servira l'histoirenaturelle des insectes.Tome 2, part2. 160 THE AMERICAN MIDLAND NATURALIST 47 (1)

* GRUBE, E. 1843-Beschreibungeiner auffallenden, an Siisswasserschwammenlebenden Larve. Arch.Naturg. 9 (1): 331-337. HAGEN, H. 1861-Synopsis of the Neuropteraof North America. SmithsonianInsti- tution,Washington, D. C. HANDLIRSCH, ANTON 1906-1908-Die fossilenInsekten und die Phylogenieder rezen- ten Formen.Leipzig. KLINGSTEDT, H. 1929-Neuropterologischesaus FinnlandI. Die GattungSisyra mit besondererBeriicksichtigung von Sisyrajutlandica Esben-Petersen. Memnor. Soc. Fauna Flor. Fenn. 5 (1928-1929): 81-88,5 figs. KRUGER, LEOPOLD 1923-Sisyridae. Beitrage zu einerMonographie der Neuropteren- Familieder Sisyriden.Stett. ent. Zeit. 84: 25-66. LAMPE, M. 191I-Beitrage zur Anatomieund Histologieder Larve von Sisyrafuscatac Fabr. DoctoralDissertation, Friedrich-Wilhelms-Universitat, Berlin: 1-55. LESTAGE, J. A. 1921-(In E. Rousseau: Les larveset nymphesaquatiques des insectes d'Europe. Morphologie,Biologie, Syst6matique). 1: 337-342,3 figs. J. Lebegue & Co., Bruxelles. MACLACHLAN (also spelledMcLACHLAN), ROBERT 1869-New species,etc. of Hem- erobiina;with synonymic notes. Entomologist'sMonthly Mag. 6: 21-27, 1 fig. NAVAS, R. P. LONGINOS 1935-Monografia de la familiade los sisiridos(Insectos neur6pteros).Memoria 4.a Memoriasde la Academia de Ciencas Exactas, Fisico-Quimicasy Naturales de Zaragoza. NEEDHAM, JAMES G. 1925-Some aquatic neuropteroidinsects of Lake George. Ent. News 36: 110-116. AND C. BETTEN 1901-Aquatic insectsin the Adirondacks.New York State MuseumBull. 47: 383-612,42 figs.,36 pls. OLD, MARCUS C. 1932a-Contributionto the biologyof fresh-watersponges (Spongil- lidae). Papersof the Mich. Acad. of Sci., Arts and Letters17: 663-679. 1932b-Observationson the Sisyridae(Neuroptera). Ibid. 17: 681-684,1 fig. PETERSON, ALVAH 1945-Some insectinfants. Sci. Mo. 60 (6): 426-442,59 figs. * STITz, HERMAN N 1931-Planipennia. (in P. SchuLlze'sBiologie der Tiere Deutsch- lands. Berlin. Lief 33, Teil 35, pp. 67-304,figs. TILLYARD, R. J. 1916-Studies in AustralianNeu-roptera. No. IV. The families Ithonidae,Hemerobiidae, Sisyridae. Berothidae, and the new familyTrichomati- dae; witha discussionof theircharacters and relationships,and descriptionsof new and little-knowngenera and species. Proc. Linn. Soc. New South Wales 41 (2): 269-332. TOWNSEND, L. H. 1935-Key to larvaeof certainfamilies and generaof nearcticNeu- roptera.Proc. Ent. Soc. Wash. 37: 25-30, 1 pl. VAN DER WEELE, H. W. 1909-Mecopteraand Planipenniaof Insulinde.Notes from the LeydenMuseuLm 31: 1-100,5 pls., 41 figs. WALKER, FRANCIS 1853-Catalogue of the specimensof neuropterousinsects in the collectionof tlheBritish Museum. London. WARD, H. B. AND G. C. WHIPPLE 1918-Fresh-waterbiology. John Wiley & Sons, Inc., New York. WESTWOOD, J. 0. 1839-An anomalousinsect found in the Spongillaflivia:i is. Mag. Nat. Hist., 2nd series,3: 200. WITHYCOMBE, CYRIL L. 1922-Notes on the biologyof some BritishNeuroptera (Planipennia). Trans. Ent. Soc. London: 501-594,pls. 38-43. 1924-Some aspectsof the biologyand morphologyof the Neuroptera.With special referenceto the immaturestages and theirpossible phylogenetic significance. Trans. Ent. Soc. London: 303-411,pls. 39-44,2 textfigs. The University of Notre Dame

The Life History of Climacia areolaris (Hagen), a Neuropterous 'Parasite' of Fresh Water Sponges Author(s): Harley P. Brown Source: American Midland Naturalist, Vol. 47, No. 1 (Jan., 1952), pp. 130-160 Published by: The University of Notre Dame Stable URL: http://www.jstor.org/stable/2421701 . Accessed: 08/05/2011 11:09

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