Records of the Western Australian MIISellnl Supplement No. 52: 13-24 (1995).

The behavioural ecology of Latrodectus hasselti (Thorell), the AustralianRedback Spider (Araneae: Theridiidae): a review

Lyn Forster

McMasters Road, RD 1, Saddle Hill, Dunedin, New Zealand

Abstract - Aspects of the biogeographical history and behavioural ecologyof the AustralIan Latrodectus hasseIti provide support for the endemic statusof this species. Cannibalism, prey stealing and short instar lengths are growthstrategies for. female spiders whereas early maturation, small size, hidingand scavengmg are useful survival tactics for males. Moreover malecomplicity is an important component of sexual cannibalism which is ~hownto be a highly predictable event. Latrodectus hasseIti males hybridize withfemale L. katlpo (a New Zealand species) and fertile Fl and F2 generationsImply genetic relatedness. Hence, it is likely that L. hasselti and L. katipoevolv~d from a common ancestor in ancient Pangaea, a feasible explanationonly If L. hasseItl IS endemic to Australia. It is concluded that L. hasseItiwould have been able to persist in outback Australia for millions of years,with ItS mtraspeClfJc predatory habits aiding subsistence and the evolution ofsexual cannibalism providing a way of coping with infrequent meeting andmatmg opportunities.

INTRODUCTION

Many stories and articles have been writtenabout the redback spider (McKeown 1963; Raven1992) with considerable attention being devoted toits venomous nature (Southcott 1978; Sutherlandand Trinca 1978). But, behaviourally, this spiderposes one of nature's most intriguing riddles for,instead of the North American black widow, it isactually the Australian redback female whichca~ibalises its mate (Fig. 1). The events precedingthIS deed and set in motion during courtship, aremaster-minded by its genes (Forster 1992a).

The redback is undoubtedly Australia's mostwidely known spider (Main 1965). Hence thesuggestion that it could be an introduced species(Raven and Gallon 1987) aroused interest amongstthe news-hungry public (Harris 1988; Mitchell1988) as well as arachnological scientists. The mainreasons for this proposition were (1) that it had notbeen recorded until 1870, long after many otherindigenous species were known, and (2) that itspreference for human-modified habitats followed apattern known in other introduced species.

However, in 1993, Barbara York Main drewattention to the diary record and colouredillustration of a readily identifiable redback spidercollected by Edward Snell from the "AdelaideHills" in 1850 (Snell 1988). Moreover, by tracingseveral derivations of the words meaning "spider"in aboriginal languages, Downes (1993) raised thepossibility that the redback was known to theindigenous people of Australia. While these reportsdo not offer "proof positive" of L. hasselti's

indigenous status, Main (1993) notes that, (as aconsequence of its supposed introduction), "theabsence of Latrodectus in the Australian region,prior to human habitation, poses a curiouszoogeographic dilemma". This comment raises aninteresting point which will be given furtherattention later in this paper.

The "introduction" theory, nevertheless, gainsqualified support from a paper by Cariaso (1967)about black widows in the Philippines (thenbelieved to be L. mactans) in which it is stated that"after some time the male turns its abdomentowards the venomous fangs ...of the female."Later, Cariaso adds " ...a majority of the males aredevoured by the females." No further details aregiven but these comments infer that this spidercannibalises its mate in the manner described for L.hasselti (Forster 1992a, see below). Because this,otherwise unique, mating behaviour occurs in aPhilippine Latrodectus species, can we assume thatit is L. hasseIti. If so, then did it colonise Australiaat some stage, or was it introduced into thePhilippines as Sloggett (1946) noted?

This paper portrays the life style and habits l ofthis spider, poses some questions and offers somepossible explanations. For example, did it once ekeout a living in the outback of Australia or perhaps

I Unless otherwise stated many of the new observations Idescribe here are the result of rearing hundreds of redbackspiders in captivity but there is no reason to suppose that, ifspacious enough, captive webs present any discernibledifferences from wild webs to their inhabitants. Observations inthe field were also carried out in Queensland, Australia in 1988and in Wanaka, New Zealand in 1981, 1983 and 1990.

14 L. Forster

Figure 1 Immediately after inserting his embolus into the female epigynum, the male raises himself into a headstand- shown here - then turns over in a complete somersault (see Figs 5 and 6). This highly predictable act, notknown in any other Latrodectus species, ultimately leads to his demise. (Embolus = male reproductiveorgan; epigynum = female reproductive opening).

some other land and then find a comfortablelivelihood in Australian suburbia? And was itperhaps a gravid female emigrating to NewZealand in somebody's luggage that led to afounding colony on the lower slopes of Mt Roy inWanaka, central Otago, New Zealand, and thusbegin the events which led to this story (Forster1982, 1984)?

HABITAT, DEVELOPMENT AND DISPERSAL

HabitatPrimarily a ground-dwelling spider, the redback

occupies a wide range of microhabitats, the mainrequirements being shelter from wind and rain,adequate warmth for breeding and a plentifulsupply of suitable food. These conditions weremore readily met in Australia with the coming ofEuropean settlers whose lighted dwellingsattracted both spiders and prey, so that Lntrodectushasselti has prospered (Forster 1988). Within asuitable site the redback builds a conical webretreat linked by threads to a catching structure(Main 1965) which is laced with sticky globules.Together occupying an area ranging from 5 to 20cm2 they are anchored by a series of dry trap lines

to a nearby substrate. The cone retreat becomesmuch thicker during cooler temperatures « lO°C)and the spider withdraws to its uppermost area(Forster, personal observations).

Despite its denser populations in warmer areas(Forster 1988), Lntrodectus hasselti is able to toleratea wide range of climatic conditions. In parts ofAustralia, temperatures fall below freezing attimes; in other places redbacks have been seen inthe open at 41°C (Softly and Freeth 1970). In NewZealand, snow lies on Mt Roy for short intervalsduring the winter but redbacks, hiding under rocksor logs, are buffered against the cold. Duringvideotaping of females and young spiderlingsmoving freely about on uncovered webs, ambienttemperatures from the studio lights required forsuch close-up work led to the death of two femalesalthough all spiderlings remained fully active.Measured at 43°C, one explanation may be that thefemales' heat-absorbing blackness and greater massled to their deaths whereas the whitish sheen ofthe young reflected the heat and enabled them tosurvive (see Robinson and Robinson 1978). In thewild, dispersal could expose spiderlings to a widerange of thermal conditions, hence their pale colournot only makes them inconspicuous but may alsoshield them against heat extremes.

Behavioural ecology of Latrodectus hasselti

18

16>-~

14I-:::l~ 1210E

0 10~

l/1 8>-10\J

6c:10Q)

4:x:

2

0

CA females

CB females

• Males

15

2 3 4 5 6 7 8

Number of instarsFigure 2 Developmental trends in male and female redback spiders. Males generally mature in the 5th instar while

females mature in (A) the 7th, or (B) the 8th mstar. (Mean data only - for standard deviations see Forster(1984)).

DevelopmentTemperature has been shown (Forster 1984,

Downes 1987) to influence the growth rate of thesespiders. In the laboratory, males mature in 28 to 45days and females take 45 to 74 days when kept at aconstant temperature of 25°C and a light/ darkregime of 12/12 hours (Forster 1984, Kavale 1986).These conditions appear to be close to optimalsince Downes (1987) found that when reared at30°C, their development rate is not markedlygreater. At temperatures below 25°C, however, thetime taken to reach maturity increases. Below lOOCgrowth apparently ceases and spiders enter a stateof quiescence during which they are able towithstand cold conditions while sheltered withintheir now-denser conical retreats (Forster 1984).

Figure 2 shows that the duration of the secondinstar in females is considerably less than that ofmales, an advantage maintained throughoutdevelopment, and a trend also noted by Downes(1987). Note that most males mature at the 5thinstar and females mature at either the 7th or 8thinstar (Forster 1984). Thus, although females takealmost twice as long as males to reach maturity,they become larger, more quickly. Clearly thisgives them the competitive edge with respect tomales and smaller siblings in prey capture andcannibalism.

While L. hasselti has been largely regarded as asub-tropical species, it is well adapted to endureadverse circumstances. This is no doubt why it isable to tolerate the snowy winter weather in centralOtago, New Zealand. The most important factor is

that, here, hot summers of 4-months or more allowthem to breed. Since 1980 the population in thisrather desolate uninhabited area has slowlyincreased and, recently, females have beendiscovered in the small Wanaka township some 12km away.

DispersalPrior to dispersal, neonatal spiderlings track the

light and climb to the upper limits of nearby logs,stones or vegetation. Tests (Forster 1984 andunpublished data) show that this positivephototactic behaviour persists during the secondinstar but that subsequently spiderlings andjuveniles are less likely to be attracted to light. Ifnewly hatched spiderlings are kept in the dark, forexample, they remain within 5-6 cm of the eggsacand do not climb upwards. Thus the likelihood ofwidespread dispersal at later instars is reduced.Perhaps this shows that, in the wild, somespiderlings may be uplifted for varying distanceswhile others remain near their hatching site.

Under the right conditions, spiderlings arecooperative climbers. As the first echelon movesupwards, each spiderling holds a line of silk awayfrom the substrate with a fourth leg andperiodically attaches it. These primary lines arequickly climbed by other spiderlings, in turn layingstill more silk. However, the 'lead' spiderlingsprovide the most direct path for others, and theascent gathers momentum. Inevitably, clusters ofspiderlings are formed, each cluster intent on itsupward urge. Once at the summit of a rock or bush

16

spiderlings are ready to balloon, the aerial mode oftransport usually adopted by redback spiderlings(Raven 1992). One method of 'taking off' mayutilise loose strands of silk which seem to appearas spiderlings climb, somewhat similar to the'second line' technique of airborne initiationdescribed by Eberhard (1987). Perhaps they alsotake to the air in clusters since their usual refuge iswithin a communal network of silk (Forster 1984).

These days, however, it is most likely that largerredbacks travel by car, or boat or plane, even inAustralia. The introduction of these spiders intoNew Zealand clearly involved sea and air transportsince they were found in their dozens in containersduring the early 1980s (Forster 1984). Whether, inthe wild, juveniles and/ or female spidersperiodically leave established webs, move toanother site, and build anew, has not beenascertained with certainty. But many householdersin Australia testify to the sudden appearance ofredbacks in a tool-shed, letter box or underneathplayground equipment, for example, where nonehad been seen a few days earlier. In Texas, U.S.A.,Gary Polis (personal communication) has observedblack widows (L. mactans) walking on the desertsands at night.

The mobility of males is more of a mystery. Theirsmall size and pale colouration make theminconspicuous, hence their movements gounnoticed. But finding females is not likely to beleft to chance. Undoubtedly, female pheromonesprovide important locational signals as Ross andSmith (1979) showed for L. hesperus but how domales travel? Perhaps, if they balloon together asspiderlings they take up residence near a female atan early age, lurking nearby until she is mature.Laboratory studies also show that, as juveniles,males tend to hide behind twigs or under debriswhen communally reared with females (Forster,personal observation). Another strong possibility isthat, because of their small size, adult males arestill able to balloon. Perhaps larger distances arecovered in this way and the male is then guidedlocally by pheromones. In L. reviviensis, forinstance, Anava and Lubin (1993) found malesmoved from one female web to another and wereprobably directed by web-borne pheromones.

PREDATORY BEHAVIOUR

EntrapmentLatrodectus hasselti spiders enjoy a varied diet,

trapping some 60-70% of beetles as well as otherkinds of insects, spiders, small mice andoccasionally lizards which blunder into their stickytrap lines (Forster 1988). When alerted by suchdisturbances, the redback rushes to the site, andpauses just a leg's length from the target.

L. Forster

Stretching out a front leg to touch it, the spidergives the impression that it is assessing the target'sdistance and direction and perhaps its identity andpalatability. Such tactile behaviour may provideimportant diagnostic information for the spiderwhich has to take the risk of turning its back beforesquirting a swathe of viscous silk over its target.When directed at a small house fly, for instance,this 'super glue' may instantly bind both legs andwings to its body, effectively immobilising it(Forster, personal observation). Liquid 'super glue'emanates from greatly modified aggregate glandsand passes via short ducts to the posteriorspinnerets (Kovoor 1987) from which it isdisgorged through extra wide spigots (Coddington1989). Perhaps a sudden increase in intra­abdominal pressure which forces liquid silk fromthe glands through the short duct and spigots isresponsible for the swiftness of this action.

Biting and trussingOnce restrained, the spider bites its prey

repeatedly on the head, body and leg joints.Usually bites are interspersed with further bouts ofboth sticky and dry silk wrapping, threads beingdrawn from the spinnerets by the alternatemovements of the hind legs. Although 'super glue'appears wet and viscous whereas sticky silkconsists of globules adhering to a thread, thisdifference may be the result of variation in themethod of application. Most often wrapping iscarried out while the spider hangs vertically, itsunderside directed towards the victim, andabdomen bent inwards thus allowing the silk to bemore carefully targeted towards the victim's body(Fig. 3) (Forster, in preparation). Prey is notrotated, hence this wrapping technique differs fromthat employed by araneids, for example. Theeffectiveness of 'glueing and biting' enables thespider to tackle large and often dangerous animals.

Provided with a torpid mealworm as prey,however, redbacks may tap it with the palps first,then bite. The bite invariably activates themealworm and its subsequent wriggling triggerssilk throwing by the spider. Silk is the primaryimmobilising medium used by L. hasselti andmovement of prey the impetus for its use; the moremovement from the prey, the more silk is tossed totruss it up (Forster, personal observation).Apparently, venom is only employed after theinitial subjugation of prey has been achieved,except in the event of prey sluggishness.

An important function of biting and theaccompanying action of the mouthparts involvesthe injection and infusion of digestive enzymes.These enzymes lead to the liquefaction of theinternal tissues of the prey, a process which takessome time to accomplish. During biting andtrussing, the spider periodically abandons its prey

Behavioural ecology of Latrodectus hasselti

Figure 3 After spurting sticky silk at prey, the redbackspider throws more silk and partially wrapsit before biting.

some 6 to 10 times, these egresses graduallyincreasing in duration from two to three seconds toup to 10 minutes. The interval between first biteand ingestion may be from 5 to 20 mins, thisvariability depending to a large extent on therelative size of prey and spider as well as thedegree of prey resistance (Forster in prep.). This'elapsed time' is assumed to be a measure of thevenom and enzyme reaction time required prior toingestion.

Transport and IngestionWhen trussing and biting have been completed

the spider cuts its well-wrapped prey free from thesurrounding web. Then, with its prey securelysupported with a thread from its spinnerets andheld between the back legs, the spider climbs backto its lair. Feeding commences at once, the spideringesting the contents from several places aroundthe head, body and leg joints. All availablenutrients are extracted, leaving the carcasecompletely desiccated.

Prey stealingSneak feeding by spiderlings (see below) and

prey stealing amongst larger females are commonoccurrences (N)25). Gravid females areparticularly assiduous in gathering up as muchfood as possible and storing it within their retreats.When prey is readily available, the spider will trussand bite its own victim and then, alerted by anearby spider's activity, it will move through theweb and seize this spider's already trussed andbitten prey. Its success is mainly by reason of its

17

larger size, since even a slightly smaller conspecificwill quickly abandon its catch as soon as themarauder is within touching distance. The victormay gather up several extra items in this way,cutting them free and transporting them all back toits lair. Occasionally, if the seized item is leftunattended while the marauding spider stealsanother, the original owner may steal it back(Forster in prep.).

There are considerable advantages to thisstrategy. The larger spider gains extra food at amuch lower cost, there being less energyexpenditure and a greatly reduced use of silk. Thespider will consume most of this food over the nextfew days, items such as meal worms oftenrequiring 24 hours or more to ingest. During thistime, the spider swells visibly, its black velvetsleekness being replaced by a dull brownish-orangehue. Mealworms and other larvae, in particular,affect the colour of the spider if large quantities areconsumed (Forster, personal observation).

CANNIBALISM

Often cannibalism is regarded as an artefact ofcaptivity. But in a web-building spider, captivity isless likely to influence behaviour than in, say,hunting spiders because a web is always thespider's natural environment wherever it isconstructed. This is demonstrated by the fact thatredbacks appear equally at home in the glove boxof a car (Forster 1985) as they are under a log wellaway from human habitation. Moreover,cannibalism has never been observed in Steatodagrossa (Theridiidae), a related genus with similarappearance and habits, when maintained inequivalent captive conditions. It is likely, therefore,that L. hasselti is innately predisposed towardscannibalistic behaviour.

First mealsMost redback spiderlings emerge from the

eggsac within 12 hours of each other but up to 10%remain within the sac for 2-5 days. This lattergroup tend to be the "stay-at home" spiderlingswho do not disperse with the others (Forster 1984).First meals for some of these may consist of siblingsor they may "sneak feed" from the female's catch.As the female begins to devour her catch, two orthree spiderlings approach cautiously, usuallyassuming feeding positions on the far side of herprey. Sneak feeding is not condoned by the femalewho periodically conducts exploratory sweepswith her front legs, actions which often deter them.Some of the "super glue" thrown by the femalemay miss its target and can be seen in globularform attached to a silk thread. These globules arefrequently imbibed by spiderlings still in the femaleweb (Forster 1992b).

18

In captivity, spiderlings readily catch Drosophilabut initially the direction and distance needed forswathing prey may be astray. Accuracy quicklyimproves. Since several spiderlings may attack asingle fruit fly it is almost inevitable that some fallvictim to the "super glue" attacks of others. Abundle consisting of one Drosophila and two tothree spiderlings may ensue and this food parcel isthen shared by several spiderlings, not necessarilythose which initiated the attack. Indeed, those firston the scene are more likely to be victims.

First meals for spiderlings dispersed in the wildhave not been observed but it is reasonable tosuppose that midges and other small insects formthe basis of such meals. Since spiderlings quicklyconstruct a communal silk network it is probablethat opportunistic cannibalism is also a feature oftheir wild existence. In captivity, cannibalism ofsluggish individuals by more active spiderlings is afrequent occurrence but does not generally takeplace until neonatals are more than ten days old(Forster 1992b).

Juvenile cannibalismIn captivity, juvenile cannibalism is a regular

feature (Forster 1984) regardless of the starvationlevel (Forster and Kavale 1989) exhibited by thecannibal. While it is more common that largerspiders prey upon smaller companions, the reversesituation has also been observed. The victim of acannibalistic attack is treated as prey. Initially,there is an encounter between spiders fromadjoining webs. Each spider may attempt toimmobilise the other with silk but the larger one ismore likely to be successful. After wrapping,injecting and the 'venom/digestive time-lapse', thehapless spider is consumed, its carcase cut fromthe web and discarded. Should the target spiderflee after first being struck with sticky silk, it isable to remove this silk by first wiping its legs withthe mouthparts and then using its legs to clear theabdomen of silk (Forster, personal observation).

Studies have shown (Forster 1992b) thatcannibalism is a growth strategy for femaleLatrodectus spiders. From the neonatal stage toadulthood, cannibalistic females grow morequickly and reach maturity earlier than lesscannibalistic siblings. Once a particular femalegains the advantage, she will prey on smallerindividuals and steal their catches. In thiscompetitive environment young males aredisadvantaged. However, by hiding and feedingon prey remains, many survive. Moreover, becausethey soon need much smaller food items than thefemale, they are no longer competing, nor indanger. As adults, males do not catch preyalthough they often imbibe water and have beenseen on discarded prey carcases.

LForster

Adult cannibalismDespite the prevalence of juvenile cannibalism,

adult females may be surprisingly tolerant of someyounger females in the same web structure,preferring to steal their prey rather thancannibalise them. It could be argued that space andhunger are limiting factors and that once apopulation equilibrium has been reached,cannibalism is minimised (Forster 1984).Experiments with L. mJldims (Forster 1992b) showthat conspecifics and prey items less than 150/0 thesize of a female are mostly ignored. This meansthat a juvenile spider the size of an adult male isnot treated as prey. Close scrutiny reveals thatfemales are unresponsive to small movements inthe web. This observation has importantimplications for interpreting the behaviour of amale in the female web.

SEXUAL CANNIBALISM

Pheromonal cuesFor 2-3 days before moulting, sub-adult females

may be courted by mature males. Most of thisactivity consists of pre-copulatory behaviour (seeForster 1992a) and is conducted in the vicinity ofthe epigynum. Prior to this, resident males subsistaround the perimeter of the female web. Moultingfemales were not observed to attract males andmale courtship did not generally begin until at least24 hours after this moult. However, malesperformed courtship in fresh webs made byfemales which had been removed as Anava andLubin (1993) also found in L. reviviensis.

Functions of courtshipIn Latrodectus hasselti, the onset of courtship

precedes copulation by several hours (5.03 ± 0.84h).A number of acts peculiar to Latrodectus courtship(Forster 1992a; Anava and Lubin 1993) areperformed by males, these eliciting leg-flicking,lunging and/or chasing from females. Most maleacts relate to particular stages of courtship, e.g, (i)when he first enters the web (ii) after contact withthe female and (iii) upon mounting the femaleventer (Forster 1992a). Female rejection responsesusually diminish with time and ultimately sheadopts a suspended docile posture in or near herretreat.

Platnick (1971) suggested that the principalfunctions of courtship are to (i) reduce thelikelihood of the male being attacked by the female(ii) provide signals indicating the male's potentialreproductive status and (iii) allow for physiologicalpriming in both partners. Experimental studiesreveal some modifications to the first of thesenotions. Like L. mactans, L. hasselti females aresimilarly unresponsive to small prey judged to be

Behavioural ecology of Latrodectus hasselti

less than or equal to the body weight of males(mean 6.83 ± 2.41 mg, n = 85) (Kavale 1986).Moreover, during trials in which 17 females wereeach courted by one male it was found that, in allcases, males were only assaulted after copulationand somersaulting (Forster 1992a). Of 13 malesintroduced into non-virgin female webs 96 h afterfemales had mated, two mated within 24 h andwere also cannibalised. The other 11 males did notcourt or mate after this 96 h period, were notattacked by females and were removed unharmedafter 14 days (Forster, unpUblished data). Hence itappears that mated females become unresponsiveto males in the web within four to five days aftermating regardless of whether such males are, orare not courting, the inference being that redbackmales in the web are not in danger of being treatedas prey.

It is likely, therefore, that L. hasselti courtship isnot designed to enable the male to approach thefemale with caution but rather to attract herattention, since his normal web movements do not.No doubt, male acts such as abseiling, runningaway, web-cutting and web bouncing led observersto interpret this behaviour as constituting aprudent approach. Whereas it may be that certainfacets of male courtship are designed as deterrentsor distractions to competing males. H, for instance,a potential mate has less chance of a successfulcopulation in the presence of other males, how,then, can this competition be minimised?

Since courtship is a genetically programmedevent, activated by web pheromones (Ross andSmith 1979; Anava and Lubin 1993) would it not beselectively advantageous to have male-impedancecomponents incorporated within it? Moreover,because there are several reports of two or moremales being seen in the periphery of a female'sweb in the wild (e.g. McKeown 1963, Forster,personal observation) it makes evolutionary sensefor male courtship to cater for this probability.Hence, it may be erroneous to describe courtshipas being directed solely at the female. Rather, someelements, such as web cutting and web-bundling,may delay or impede the activities of another male.Once selected by the female, elements thatdisadvantage other males and hence benefit the"successful" suitor, will persist regardless ofwhether other males are actually in the web or notduring courtship.

The fact that courtship is almost always a lengthyprocedure supports the contention thatphysiological priming is one objective. Femalechoice may be another (Forster 1992a). Moreover,male web activities, such as bouncing, jerking, legwaving stimulate the female either into activity ordocility. Female responses to male acts includeflicks of the legs, lunges or short chases. But,during courtship, females never throw silk at

19

conspecific males or behave in a distinctlypredatory fashion. Males may repeat their web­related acts for many hours until female priming/choice is achieved, probably demonstrated whenfemales adopt the mating posture. Oncecomplaisance occurs and males make contact withthe female, she submits to having silk, usuallyreferred to as the 'bridal veil', thrown over legsand body. Videotaping of L. hasselti females show,however, that part of this "bridal veil" actuallyforms a cradle beneath the abdomen and, as weshall see, provides leverage for both male andfemale during subsequent events.

Precopulatory eventsMales add a number of acts to their repertoire

once they climb on the venter of a submissivefemale (Forster 1992a). Many of these utilisemovements of the palps which tap vigorously inthe vicinity of the epigynum. For example,"knocking" with the 'selected intromittent' palp(usually the left one first) against the epigynummay have a stimulatory effect on the female."Scraping" the edge of this palp at the epigynalrim eventually leads to the 'freeing' of the embolustip (video obs.) from its protected position (Fig. 4).Perhaps "rubbing" the distal parts of the palpstogether conditions the emboli for insertion."Nibbling" at the epigynal orifice with themouthparts coincides with the appearance of fluids

Figure 4 Lateral SEM view of palp of an unmatedmale Latrodectus hasselti (courtesy of J.Kavale, 1986). The distal portion of theembolus is tucked protectively behind thecymbium and must be "sprung" beforeintromission can take place.

20

which flow over the epigynum and seem likely tohave originated from the male (video obs.). Arethey digestive juices and is their function alubricative one?

During these episodes of palpal foreplay, the. male pauses periodically while the abdomen

vibrates rapidly up and down (8-12 cycles/sec) forID-IS secs. Intervals of 3D-120 secs separate theseintense vibratory phases (Forster, unpublisheddata) which accompany a gradual mid-abdominalconstriction and shrinkage of the posteriorabdomen. This pre-copulatory phenomenon is notknown in any other Latrodectus species.Apparently, abdominal constriction and release ofthe embolus tip foreshadow penetration of theepigynal duct and the associated hematodochalinflation (Forster 1992a).

Copulation and somersaultingUp to this stage, the copulatory posture of the

male is as for other Latrodectus species (see Kaston1948, fig. 2009). But then, a unique event occurs.The male raises himself into a headstand position(see Fig. I) and somersaults towards the female'ssternum. The somersault is conditional uponhematodochal inflation and is apparently initiatedby this event (Forster 1992a). But it is also assisted

L. Forster

by an upward push from the female abdomenwhich is supported by the web cradle below (videoobs.). This somersaulting behaviour has occurredin all observed trials (n = 86) (Forster 1992a andunpublished data) .

The male comes to rest with his abdomen againstthe female's mouthparts (Fig. 5) from whichdigestive fluids are exuded at once; his surrenderis complete when the female secures his abdomenwith her fangs. Although it has not been possibleto determine whether the female injects poison atthis time, it ·seems unlikely. One reason is, that forthe female to benefit from a second insemination,the male must survive the first one. Second, inmating observations involving just a single

~ intromission (n = 11), the male remained active forperiods of up to 24 hours (Forster 1992a).

The first signs, some 5 to 20 mins later, that malewithdrawal is imminent come when he begins toflex and jerk his legs. These movements accentuateand eventually the female releases him. Sometimesshe restrains him with a single fang and at othertimes she seizes a leg. Once the male achieves somepurchase against the female abdomen with three orfour legs, he is able to tug his embolus free. Themale's release is usually accompanied by theappearance of a pellet of white guanine at the

Figure 5 The "somersault" results in the redback male falling backwards against the female's mouthparts (also seeFig. 1). Immediately she grasps him and exudes digestive juices onto his abdomen.

Behavioural ecology of Latrodectus Izasselti

female's mouthparts (Forster 1992a). This happensbecause the first digestive phase consists of thedissolution of the outer chitin and sub-dermalguanine layers of a portion of the male's dorsalabdomen. These particles are too large to beingested and are filtered out by a "palate plate"and regurgitated (Bartels 1930). Perhaps it is theneed for the disposal of this pellet that induces thefemale to liberate the male. Moreover, thisintermission also provides for pre-digestiveprocessing, the male normally returning for the

9 passive

21

second insemination in about 10 to 15 minutes(Forster 1992a).

Sexual cannibalismAfter the next somersault the female begins to

suck up his internal body fluids, and the malegenerally becomes too weak to escape a secondtime. Timing is critical, with two different digestivephases being controlled by distinctive behaviours.But "slip-ups," occur; males sometimes do not, orcannot, return for a second insemination,

0011 venter ~------..,

PRECOPULATORYBEHAVIOUR

embolusinserted

COPULATION

SOMERSAULT

ograsped

1hematodocha

inflated

1headstand

1800

somersault (1.2)

SEXUALCANNmALISM

first stagedigestion

1oescapes

2 second stagedigestion

o discarded

Figure 6 Key events which determine the fate of the male L. hasselti. Abdominal vibration (abd.vib) appears to belinked to abdominal constriction (abd. constr), the latter probably ensuring that vital organs are not initiallydamaged (see Forster 1992a). This process only occurs during the first precopulatory stage. Each of the twosomersaults (1, 2) presages a particular digestive phase. Each digestive phase accompanies an insemination,most commonly with the left palp first and the right palp second. See text for details.

22

sometimes they escape after the secondintromission although the female may later find,wrap and devour her wounded mate (Forster1992a).

The sequence of events described here reveals afin~ly ~uned strategy during which the matingoblIgations of these two spiders and the pre­digestive conditions of female predation areintricately interwoven (Fig. 6). Thus, sexualcannibalism by L. hasselti females incorporatespredictable elements of male complicity, a geneticstate of affairs (Forster 1992a) found in relativelyfew other species2

•

HYBRIDIZATION

Cross-mating experimentsNew Zealand has two indigenous Latrodectus

species, one of which is L. katipo. When L. katipomales were introduced into L. hasselti webs, theresident redback female always attacked the katipomale (n = 10) (Forster 1992a). Mating was notinduced even when several ploys, such as"switching males and/or webs" and "waxing thetarsi to prevent female attack", were attempted(Kavale 1986). A likely explanation relates to thefact that a katipo male weighs some 12 ± 2.78 mg(n = 50), twice that of a redback male (loc. cit.).~ence his greater "noise" in the web sends preysIgnals to the redback female which reactsaccordingly.

However, redback males readily mated withfemale katipos (100% success, n = 22)(Forster 1984,Kavale 1986), a unidirectional reproductiveph~~omenon noted in some other species, e.g.PhldlPPUS spp. (Edwards 1980). Apparently, theiralmost identical courtship regime overcomes anotherwise, relatively "noiseless" approach, therebydeceiving the katipo into mate acceptance. As inconspecific matings, redback males somersault andlie against the katipo mouthparts but are notcannibalised (Forster 1992a).

These interspecific matings produced viable F1hybrids from which F2 generations were bred(Kavale 1986). Fecundity in hybrids was found tobe intermediate between the parent stock (Fig. 7)indicating a genetic 'bias', although it is knownthat factors such as nutritional state of the femaletemperature and adult size (Kavale 1986) are als~influential. There was, moreover, a skewed ratio(ca. 3:1) of females to males in the F1 generation.Visually, hybrids looked more like katipos but

2 Elgar (1992) lists some 87 invertebrate species in which sexualcannibalism has been recorded, but in many of these the eventdoes not appear to be stereotyped and predictable. Moreover,there is little evidence relating to the circumstances, e.g.starvation, misadventure, mistaken identity, etc., under whichsuch predation occurred.

L. Forster

120

if> 100enen.,ci 80cc

'".,-.::. 60

>-..,.-"0C 40::JU.,

lI..

20

Latrodectus "species"

Figure 7 Comparison of mean fecundity data in L.katipo (n = 56), F1 hybrid (n = 36) and L.hasselti (n = 16). (For original data andstandard deviations see Kavale (1986»).

other characters such as leg length, hair type anddensity, etc., were quite variable. Fertility was verylow (3%) in the F1 generation but improvedsubstantially (83%) in the F2 generation (Kavaleand Forster, in prep.). This high F2 fertility ratemeans that the hybrids must have been capable ofexchanging genes which, in turn, implies that theirallopatric biparental stock possess commonfertilization systems, and hence a high degree ofgenetic relatedness. (For more details of thisargument, see Templeton 1992 and Paterson 1993.)

Perhaps these findings are best explained byproposing a common origin for these two speciesarising from the juxtaposition of Australian andNew Zealand land masses during the "gondwana"era some 150 million years ago (Stevens 1985). If,therefore, L. hasselti and L. katipo are siblingspecies, their long geographical isolation has led tospecific changes in mating behaviour, habits andsome morphological characters (Kavale 1986) butnot to other heritable features. Such an explanationis only tenable if we accept that redbacks areindigenous to the Australian region and not arecently introduced species. In which event,Sloggett's (1946) account of the introduction of L.hasselti into the Philippines in boxes and cratesfrom Australia is supported.

BIOGEOGRAPHICAL PERSPECTIVES

Only a few spider genera are as widelydistributed as Latrodectus. Relatively minordifferences occur in their general appearance, theiroverall habitat requirements, their behaviour and,quite significantly, their genitalia. Understandably,

--- ----------------------------------------------.

Behavioural ecology of Latrodectus hasselti

these resemblances led Levi (1958, 1959) to group35 species into six, a finding which, in 1983, heacknowledged to be incorrect.

The belief, now, that most of the earlier speciesare valid taxa raises as interesting point. Sincethere is no longer a case for six taxa to have beenintroduced into various host cQuntries by humanagency or other mechanisms, we must assume thatmost are endemic to their present countries. Theirevident affinities imply that all these species havesprung from a common ancestor. The onlyconceivable explanation is that this commonancestor, a theridiid, must have evolved inPangaea before its breakup into separate landentities at the end of the Palaeozoic, about 400million years ago (Stevens 1985). Moreover,another theridiid genus, Steatoda, also Widespreadand with many similar characteristics, can belinked to this common ancestor. The conclusionreached here is that theridiids have an ancienthistory, a view which may be inconsistent with thatof Coddington (1986) who considers that thisfamily derived its cobweb from the orbweb group.

Perhaps the key to the question of 1. hasselti'sindigenous status lies in Barbara York Main'scomment (loc.cit.) about the zoogeographicdilemma of the Australian region if this spider wasproved to be introduced. Given Australia'sbiogeographical history, it would be extraordinaryif that country had not spawned its own endemicspecies especially since Latrodectus occurs in allother continents as well as there being two species(1. katipo and 1. atritus) in New Zealand. The closegenetic relationship suggested between 1. hasseltiand 1. katipo adds weight to this argument.Moreover, it has been shown here that 1. hasseltihas an adaptable lifestyle, one which permits it tolive in a range of habitats and climatic conditions.Hence, it would have been able to subsist inoutback Australia for millions of years, with itsintraspecific predatory habits aiding subsistenceand the evolution of sexual cannibalism providinga way of coping with infrequent meeting andmating opportunities.

ACKNOWLEDGEMENTS

This review is dedicated to Barbara York Mainwhose important contribution to Australasianspider knowledge spans many years. Hercomments regarding the endemicity of Latrodectushasselti in Australia provided the underlying themefor this paper.

Field studies on 1. hasselti in Australia in 1988were made possible by a Prince and Princess ofWales Science Award from the Royal Society ofNew Zealand. A grant from the Exline-FriznelFund, California Academy of Sciences, enabled meto undertake a study of black widows in the USA

23

in 1989. I am grateful to these two institutions aswell as the American Museum of Natural History,NY, and the Smithsonian MNH, Washington, DC,for space to carry out the black widow studies. Ithank Henry Kavale for comments and help withsome illustrations. I acknowledge the expertise ofthe TVNZ Natural History Film Unit invideotaping the mating sequence of Latrodectushasselti.

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Manuscript received 14 January 1994; accepted 28 June 1994.