sign in sign up
<<
Home , Alopecosa, Aphonopelma chalcodes, Araneomorphae, Atypoides, Chelicerae, Euagrus

1998 . The Journal of 26 :317-329

BEHAVIOR, LIFE CYCLE AND WEBS OF MECICOBOTHRIUM THORELLI (ARANEAE, , MECICOBOTHRIIDAE)

Fernando G . Costa and Fernando Perez-Miles : Division Zoologia Experimental, Instituto de Investigaciones Biologicas Clemente Estable, Av . Italia 3318, Montevideo,

ABSTRACT. A comprehensive study of the of Mecicobothrium thorelli Holmberg 1882 was carried out in the laboratory and in the field (Sierra de Animas, Maldonado, Uruguay) . The is found in shady riparian sites under trees . M. thorelli builds sheet-and-funnel webs under stones, logs, roots and in crevices . In the laboratory, developmental data indicated that the have an inactive phase in summer and probably another in winter. Adults emerged in the fall and the males die during late winter. Three -clutches of about 30 were observed in the laboratory at the end of winter and the beginning of spring (August-September) . Juveniles emerged from one of the clutches 27 days after ovi- position . A three- lifespan was estimated . Males started (body vibrations and palpal drum- ming) upon contacting the female web . Females showed high tolerance during the entire sexual interaction . An unusual clasping mechanism was observed before and during : the female engaged her cheliceral fangs into grooves on the male . Twenty-eight copulations were observed . Mean copulation duration was 24 .7 min, while males performed a mean of 10 alternate palpal insertions . The complex insertion pattern is described and analyzed . Half of the copulated males pursued females after uncoupling. These males expelled females from the web and remained there . Mated males aggressively defended the female's web from other males . The reproductive strategy, cheliceral clasping and palpal insertion pattern are discussed in detail . Phylogeny and biogeography of mecicobothriid genera are also considered .

The Mecicobothriidae was estab- (Maldonado, Sierra de las Animas (Capoca- lished by Holmberg (1882) to include small- sale et al . 1989)) . Other Mecicobothriidae oc- sized mygalomorphs found in . cur only in North America . Biological data on These spiders have unique morphological fea- North American mecicobothiid species were tures (abdominal tergal plates, longitudinal fo- given by Gertsch & Platnick (1979) . M. tho- vea and elongated posterior lateral ) . relli was found in Uruguay in hilly zones in Mecicobothriid was supported by riparian woods under stones, roots and trunks, Gertsch & Platnick (1979) and by Raven and in holes in the tree bases (Costa et al . (1985) . Recently, Goloboff (1993) placed Me- 1991 ; Perez-Miles et al. 1993) . Lack of cicobothiidae as a sister group of the non-aty- knowledge of the biology of this group, to- poid Mygalomorphae . Following Barrow- gether with the presence of enigmatic cheli- clough (1992) this characteristic justifies ceral male apophyses, challenged us to con- giving high priority to the conservation of the duct field and laboratory studies on the Mecicobothriidae, considering the importance biology of M. thorelli . of this family to studies of phylogeny . Our objective was to describe and analyze The geographic distribution is also crucial be- the development, life cycle, phenology, webs cause these spiders are only known from tem- and, especially, the sexual behavior of M. tho- perate regions of North and . relli . This last aspect, poorly known in My- Mecicobothrium thorelli Holmberg 1882 galomorphae, is unknown in Mecicobothri- (Figs. 1, 2) is the only mecicobothriid known idae . from the Southern Hemisphere . It was origi- METHODS nally recorded from Argentina (Buenos Aires : Tandil, Balcarce and Sierra de la Ventana Specimens of M. thorelli were collected at (Gertsch & Platnick 1979)) and Uruguay Sierra de las Animas, Maldonado, Uruguay, in

317 318 THE JOURNAL OF ARACHNOLOGY

the streamside forest of Pedregoso Stream (34°45'S, 55°15'W) . The cryptozoic arachno- of this site has been intensely studied (Capocasale et al. 1989; Costa et al . 1991 ; Pe- rez-Miles et al. 1993 ; Capocasale & Gudynas 1993; Costa & Perez-Miles 1994) . Voucher specimens were deposited in the arachnolog- ical collection of the Museo National de His- toria Natural, Montevideo . Six field collections were made : 1) 4 fe- males, 2 males and 5 juveniles on 29 June 1989 ; 2) 1 female and 9 juveniles on 16 Au- 1 gust 1989 ; 3) 3 juveniles on 20 November 1989; 4) 3 females, 1 male, 5 juveniles on 18/ 19 1990 ; 5) 33 juveniles on 9 September 1994; and 6) 36 juveniles on 21 September 1995 . Individuals from the last collection were measured and released, except six which were raised. constructions were observed in the field. On 30 June 1993, measurements were made of 17 webs of M. thorelli, the stones that covered them, and the distances to the stream (spiders were not collected) . Seventy-two individuals were kept in the laboratory from June 1989-April 1996 . Most individuals were placed in glass vials of 80 mm X 15 mm, with damp cotton wool at the bottom end and dry cotton wool closing the open end, leaving 5 cm of free in the vial for the spider. Vials were maintained slightly inclined with the open end upward . For specific observations and for short periods spiders were maintained in : a) glass jars of 9 cm diameter, with soil, water provision and a microslide covered with a plumb bob . Under the micro slide we made a small to fa- cilitate spider excavation . Plumb bob removal allowed us to observe the spider. b) Arena A. Petri dishes of 9 cm diameter with a damp cotton wool placed centrally and a small vial (30 mm X 7 mm ) with both ends open, placed against the dish wall . c) Arena B . Cy- lindrical glass jars of 14 cm diameter, with soil, water and a piece of wood of 3 cm di- ameter placed on the soil . We made a small burrow under the wood to facilitate spider ex- cavation . Figures 1-3 .Mecicobothrium thorelli. 1, Adult male; 2, Adult female ; 3, Sheet and entrances of M. The temperature in the laboratory varied thorelli web in the laboratory . (Photos by M . Lal- with the outdoor temperature, except in winter inde). when it was maintained around 20 °C (range : 15-23 °C) . Natural light was provided by win- dows facing west; artificial light was on from Monday to Friday from 0830 to 1700 h . Spi- ders were fed mainly with Tenebrio sp. larvae COSTA & PEREZ-MILES-BIOLOGY OF MECICOBOTHIUM THORELLI 3 19

(alive or in pieces), sometimes complemented webs measured 225 ± 101 mm long, 168 ±59 by , mosquitoes, small , , mm wide and 103 ±33 mm high. The mean etc. major axis of the silk tubes was 64 ±20 mm Thirty male-female encounters were set up and their diameter varied from 4-8 mm. A with 32 of the spiders collected on 9 Septem- web constructed in the laboratory by an adult ber 1994. Twenty observations of these en- female consisted of two more-or-less parallel counters occurred in a female breeding vial tubes fused medially (H-shaped web) : its total connected to an open petri dish (9 cm diam- length was 23 mm, the exposed portion lying eter), containing sand and surrounded with a on the soil was 14 mm, and the underground plastic band 45 mm high (Arena C) . The en- portion was 9 mm . This web was constructed trance (2 cm) of the female's glass tube had under a small section of a branch placed on no silk because the cotton wool plug was re- the soil . moved before the encounter . Arena C was el- Females which copulated in the laboratory evated in such a way that observations could and lived in glass vials exhibited reduced web be made from below using a 5 X lens and fo- construction in winter. Eight females placed in cused light. Six observations were done in containers with soil each occupied a burrow Arena A and the other four in Arena B . All made for it under a piece of glass . These fe- available males and females were used . Ob- males did not make webs but excavated and servations were carried out between 9 May-3 closed the burrow entrance with soil and silk . July 1995 (fall/winter) . Laboratory tempera- Usually males made a silk mat in the glass ture varied between 16 and 24 °C ; observa- vials during winter, but only one male made tions were conducted at 22 .2 ±1 .1 °C (range : a rudimentary retreat. Males placed in con- 19-23 .5 °C) . Other male-female encounters, tainers with soil similar to those used for fe- including a copulation, were recorded on Su- males rarely occupied pre-existing . per-8 movie film . Prey capture .-When a prey is offered, the spider detects vibrations through the web and RESULTS suddenly approaches the prey, biting it and Webs and retreats .-The spiders construct pulling it back to the retreat, entangling the dense funnel-and-sheet webs (see Coyle's prey with silk threads while it is being carried . 1986a nomenclature) . The web, after experi- Adult males also fed actively . mental wetting, appeared to be hydrophobic . Daily activity pattern .-Spiders in the lab- The distance from the web to stream edge for oratory showed little diurnal activity . When a seven individuals was 5 .28 ±4 .55 m (range light was turned on in the dark winter morn- 0.57-10 m) . The web nearest the stream was ings, spiders ran back into their retreats . The found at 25 cm above the water level . Presum- dense draglines observed around the inner pe- ably the spiders remain in the retreats during riphery of the containers suggested they were short-term rain-caused flooding . In the labo- very active during night. ratory, we observed that they easily drown in Development and reproduction .-Thirty- a fine water film if webs are lacking. Two of three large juveniles were captured on 9 Sep- 17 webs observed in the field were not oc- tember 1994. No subadult individuals were cupied ; no male was observed occupying a found then . The spiders constructed the retreat complete web . in the damp end of the glass vial ; each retreat The funnel (tubular retreat) of the web ex- had two lateral entrances . One died 29 tends under the stone (or similar object) and days after capture. The 32 remaining individ- emerges with one or more entrances onto a uals matured in the laboratory (19313?) . small, irregular prey capture sheet (Fig . 3). In Seasonal distribution of the molts is given in the field, this sheet lies on the soil, extends to Fig. 4. These spiders molted synchronously at both sides of the entrances, and continues be- the beginning of October. Between October neath the leaf litter, moss or grass. Retreat and December they molted an average of 1 .5 tubes were more or less curved, some of them ±0.6 times. Smaller molted more fre- branched . Seven webs had only one entrance, quently than larger ones . In the warm period two webs had three entrances, and one had (last three weeks of January and first two of four entrances . Eight webs were found under February) no molting occurred. Molting re- stones and one was under a log . Stones with sumed at the end of February and continued

320 THE JOURNAL OF ARACHNOLOGY

0 0 0 b r reached maturity in a very limited period (last o week of March and first two weeks of April) o0 0 0 ~~ (Fig . 4). The time of maturation molts of both r sexes overlapped only in the last week of 00 00 0 March. Laboratory rearing showed that males o o r molted (2 .79 ±0 .63 times) more times than 0 -0 a rrr did the females (2 .38 -*0.51 times), with sig- 00 0 0 r nificant differences in the Mann-Whitney's U- 0 test (U = 77 .5, P < 0.05) . 0 0 0 r Adults mated in the laboratory from 9 o May-3 July 1995 . Two males died acciden- o ! tally (bad manipulation) after the copulation o Sr r . 0 0 0 Males lived 118-206 days (X = 166 .5 ±22.9 fir 0 r days, n = 16) and females lived 161-298 days 0 0 0 r (t = 215.5 ±41 0 0 r .4 days, n = 12) after reaching adulthood o . The male and female adult life- o ! !r -o spans were significantly different (Student's t- ! test ; t = 3 .84; P < 0.001) . Complementary results were obtained from Sep. Oct. Nov . Dec. Jan . Feb . Mar. Apr. five other groups that were reared between Figure 4-Development of 32 juveniles collect- 1989-1996 and kept under conditions similar ed on September 9, 1994 . Empty circles (0) indicate to the previous described group . Molts started ordinary molts and dark circles (•) indicate the mat- in August and were especially frequent in uration molt and sex . September-December and March-April (Fig . 5). Molts were very rare or absent in June- July and January-February . Maturity molts to April, when all individuals had reached ma- were frequent in March and April . Two ex- turity . The spiders carried the far ceptional maturity molts were observed, an away from the retreat. early male (February) and a late male (May, Male palpal tarsi were incrassate in the pen- dead when molting) . Six males raised in the ultimate instar. No evidence of spermathecae laboratory lived 172 .2 ±19.7 days after ma- was observed in the last exuviae of females . turity. Another male captured as adult lived Females molted over a longer period (Decem- 160 days. Two females molted in March and ber-March) and earlier than the males . Males lived as adults 206 and 393 days, respectively .

0 0 0 0 00 ~;r 0 0 r 0 0 0 0 0 ~ 00 0 -0 0 0 r 0 0 0 0~ -00 0 0 0 O . 0 0 0 0

May. Jun . Jul . Aug . Sep . Oct. Nov. Dec . Jan . Feb. Mar. Apr . May .

Figure 5-Development of five groups of M. thorelli from five collections. Empty circles (0) indicate ordinary molts and dark circles (0) indicate the maturation molt and sex . Some of these juveniles did not reach maturity due to natural or accidental death, or were sacrificed .

COSTA & PEREZ-MILES-BIOLOGY OF MECICOBOTHIUM THORELLI 321

eaten immediately by the female, the other 10- contained 26 eggs (all of which were dead and decomposed) when the female died . Courtship .-In Arena C, males were placed on clean sand and they walked to enter the female's glass vial . A rim of female silk N was observed when the cotton plug was re- 5 moved. Thirteen of 20 males stopped on the silk rim, remained immobile between 4-128 see, and then started sexual activity. The other seven males began sexual activity just inside the female's web . In Arena B, males walked around the periphery of the arena (on female 1 draglines) but initiated their sexual behavior 3 6 only very close to the female's retreat. Finally, body length in Arena A, sexual behavior started close to Figure 6 .-Body length (in mm) distribution of the small glass vial where the female resided, a sample of 36 individuals of M. thorelli collected or after female contact. on 21 September 1995 in Sierra de las Animas, Male sexual behavioral units elicited by the Maldonado . Class intervals : 0.5 mm, N : absolute female web were : 1) Body vibrations, which frequencies . are brief, rapid, sagittally orientated body movements, and are apparently caused by leg- III movements . 2) Palpal drumming, which On 21 September 1995, 36 individuals (no are alternate movements of palps against the adults or subadults) were captured, and most substratum; these movements turn into steps of them were released after being measured . when the male walks . 3) Leg tapping, in Six were reared in the laboratory . Measure- which the forelegs touch the female's silk mat, ments of these six were made from successive pulling the silk and sometimes penetrating it . molts. Body size distribution is shown in Fig . These units took place alone or during slow 6 . length increased between 9 .4 and locomotion movements and were interrupted 22.0% during the molt (z = 15 .5 ±3.4%, n = by brief motionless periods. The main behav- 14). The relative size increase was not related ioral sequence was locomotion with body vi- to the size of the individual. Small spiders brations at the beginning, with leg tapping and (less than 3 mm body length) are very light palpal drumming added later. Similar behavior brown while large juveniles are darker. The was observed in eight males which contacted of some adult females becomes the silk of females which had been removed lighter when swollen . from their breeding containers . This first In the laboratory males had their maturation searching phase lasted from 17 seconds to 22 molt between February and May, with a clear minutes, until the female was contacted . Fe- peak between March and April (Figs . 4, 5). males did not attack or approach the males but Adult males lived from February to October . remained immobile or retreated. After making An egg-clutch was observed in the laboratory direct contact, the male increased his tapping on 27 September 1989, from a female col- movements on the female body and legs . The lected on 16 August . In the retreat, the eggs male penetrated the silk and oriented toward were agglomerated in a sphere without a well- the female chelicerae . Then the male pushed developed silk cover, resembling the egg-sac the female with his chelicerae. His cephalic of phalangioides (Fuesslin 1775) . region was directed downward while pushing The egg-sac, slightly larger than the carapace her and his legs I and II held the female, pre- of the female, contained 33 yellow, translu- venting upward biting (Fig . 7). The male ex- cent eggs . The female kept the egg-sac until erted a great effort to maintain this frontal po- the emergence of the spiderlings, 27 days after sition with respect to the female . Females oviposition. The female died on 9 January were passive and generally flexed their legs 1990. Two other egg-sacs were observed in against their bodies . the laboratory on 31 August : one of them was Males pursued females sometimes with ap-

322 THE JOURNAL OF ARACHNOLOGY

7

Figures 7-10 .-Copulation in Mecicobothriu,n thorelli. 7, Initial stage of copulation . Male (at left) pushing female with his chelicerae while legs I and II prevent upward biting ; 8, Schematic representation of the cheliceral clasping, prolateral view . Female fang (to the right) penetrates into the male cheliceral groove delimited by two apophyses and several cusps ; 9, Copulation and palpal insertion . Cheliceral clasping and legs I and II of the male (at left) firmly maintain this position . The long palps of the male are able to reach the female genital zone without extreme elevation of the couple ; 10, Embolus position during insertion attempt of male right palp, reproduced from a preserved specimen . (Photos M . Lalinde)

parent violence . The male usually spread apart beginning contact with the female to the com- his chelicerae when pushing the female, but pletion of clasping varied from 10 sec to 8 .5 he never attempted to bite her. This sequence minutes . was repeated until the female finally opened Copulation .-Twenty-six copulations were her chelicerae and bit into the male's cheli- observed. Copulation can occur completely ceral groove lying between the two cheliceral inside the retreat. Cheliceral clasping and the apophyses . Her fangs remained firmly be- long male palps allowed a non-elevated cop- tween these cheliceral apophyses (Fig . 8) . ulation position, which took place in the nar- During cheliceral clasping, the male per- row silk tube. The ventral angle between lon- formed rough up-and- down movements . gitudinal body axes was 90° (if male is small) Hinge-like body movements were performed or more . Also, the and abdo- 3-7 times, while pulling the female back- men can adopt a small dorsal angle to facili- wards . If the female was small or showed low tate in small . Females were ex- resistence, the male pulled the female out of tremely passive during copulation . However, the retreat and copulation took place on the when one copulating male was intentionally sheet-web . Otherwise, the male pulled the fe- disturbed for photographic purposes, the fe- male to near the entrance . The duration from male attacked and killed him . Later the same COSTA & PEREZ-MILES-BIOLOGY OF MECICOBOTHIUM THORELLI 323 day, the same female copulated normally with corkscrew-shaped portion of the embolus pen- another male . In another encounter, the couple etrated during insertion, the straight basal por- had difficulty in uncoupling : the male re- tion remained visible . We attempted to recon- mained entangled in the web after being re- struct the insertion with dead specimens and leased. The female then attacked and killed observed that only the right embolus can enter him. the right receptacle (and the same for left or- During copulation (Fig . 9), the male-female gans) according to the complementary spiral ventral body angle varied (according to spider orientation. During the insertion of one palp size) between 90-130°. The female's legs I the other remained extended, either moving or and II were flexed against her body . The male being immobile against the female abdomen. placed his forelegs dorsally on the female, The embolus extraction was similar to inser- legs 11 more laterally, with legs III and IV on tion-withdrawal movements, pivoting on ti- the floor, maintaining the equilibrium . Male bio-palpal joint . Despite the difficult obser- palps were extended to the female venter dur- vation of small spiders through the dense ing copulation (Fig . 9). That the male palpal webs, the insertion pattern was clearly seen in femora and tibiae are bent dorsally was evi- 12 copulations and partially observed in an- dent during insertion . other 4 . The palpal insertion pattern was complex . During early palpal insertions, the in-out The embolus reached a perpendicular position movements were frequent . Males performed with respect to the dorsum of the palp, but three, four, five or more insertion-withdrawal turned slightly back to be inserted (Fig . 10) . movements during a period of 1-6 min . The Embolus movement was reconstructed in dead palps did not always alternate ; two-four suc- specimens under the stereo-microscope . The cessive insertions with the same palp were rotated around an approximately common, especially following a failed inser- dorso-ventral axis of the palpal tarsus . The tion attempt. palpal embolus emerged retrolaterally, mov- Males performed 2-22 (x = 10.3 ±6.5, n ing along the glabrous notch and stopping in = 10) palpal insertions during a period of 5 .7- a small retrolateral lobe (see Gertsch & Plat- 30.0 min (x = 18.4 ±8 .6 min) . Late insertions nick 1979, figs . 46, 47, 50) . Palpal bulb ro- were brief (10-40 sec) and involve in-out tation was complex . Initially the tip of the em- movements only during palpal extraction . bolus turned retrolaterally and later went Other behaviors present in the periods be- upward ; it is possible that the whole palp also tween insertion attempts increased in frequen- rotates . When manipulated in preserved spec- cy during the later stages of copulation . These imens, the embolus is flexible . In resting po- behaviors were : pulling of male and female, sition the palpal embolus is prolateral and par- moving outside and inside the retreat ; rear- allel to the longitudinal axis of the palpal rangement of legs ; hinge-like movements tarsus, its tip points forward, and it is pro- (when the angle between the bodies changes) ; tected by a wide notch and a prolateral para- leg push from male to female, etc. cymbium-like lobe . During the 26 copulations observed, only During copulation the palpal tarsus ap- two pairs reclasped after unclasping . Unclasp- proached the epigastric furrow, which ap- ing had complications . The male pulled and/ peared swollen . The embolus was inserted or pushed the female, forcing her outside the and, in this position, insertion/withdrawal retreat and pulling her with his legs . The most movements were repeated numerous times . conspicuous maneuvers of the male were These movements were generated by the ti- cheliceral outspreading as well as series of vi- bio-tarsal joint of the palp. Withdrawal move- olent hinge-like movements . The female al- ments were discontinuous, suggesting that lowed unclasping and determined the end of they must overcome a mechanical resistence . the copulation . When females did not release Discontinuous female abdominal movements the male chelicerae, additional insertions were also observed synchronously . During could occur. An extreme case was a male withdrawal movements the palpal tarsus which attempted to unclasp after 35 min of reached a dorsal angle of nearly 90 ° with re- copulation but the female kept him in the cop- spect to the tibia. Finally, the palp remained ulation position for 21 .5 min more . In another immobile in the insertion position . Only the remarkable case the female dragged along the 324 THE JOURNAL OF ARACHNOLOGY male (for 32 min) because one fang remained encounter the female killed the male after a clasped. This long interaction ended when the difficult uncoupling . male unclasped (at 120 min) and the female In four encounters carried out in Arena B, killed him . Cheliceral anomalies were not with a more complex web, the female retreat- found in these specimens . ed to the bottom of the funnel . Although the Copulation duration from the start of clasp- males persisted, only one female left the web . ing to complete unclasping was 11-56 .5 min In the other three encounters the male stayed (x = 24.7 ± 10.0, n = 23) . Three other cop- together with the female for at least 30 min . ulations were unusual. Two of these pairs un- These males placed themselves at the entrance clasped and clasped again : one unclasped at of the funnel web and sporadically contacted 19 min, clasped again after 3 min and contin- the female ; but no attacks were observed . Lat- ued copulating for 18 min ; the other unclasped er, another male (intruder) was placed in each at 14.5 min, clasped again after 3 min and of these three webs which the males were then definitively unclasped without inserting, guarding . These intruders began to court as after 2 min . The third case was described soon as they touched the web near the en- above and involved the most difficult unclasp- trance. Then the guarding male vigorously at- ing, which lasted 88 min. tacked the intruder. In one case the intruder All available individuals in the laboratory won; the guarding males won the other two copulated (18d, 13?) . In some cases copu- contests . In one of these last two encounters lation did not occur during the first encounter, the fight was long; the males fought in a rit- but only after a second (two cases) or third ualized manner, pushing themselves with out- attempt (one case). Failed attempts were one spread chelicerae, which resemble a rhomboid with a virgin female and three with once-mat- from the dorsal view . With legs I and II firmly ed females . Eight males recopulated between interlaced, the males bit the web several times . 8-47 days after first copulation . Twelve fe- After a separation, one male caught the other males (one female died after first copulation) from behind but did not bite him ; when the recopulated between 5-44 days after first cop- first turned around they re-initiated the frontal ulation ; one female made a third copulation embrace. Guarding winners touched the fe- 12 days after the second copulation . males and returned to guarding . The intruder Postcopulatory activities .-Thirteen males winner unsuccessfully courted the female . No were very active after copulation . These ac- spiders were damaged . Males were removed tivities included leg tapping, violent pushes between 30-60 min after copulation . with outspread chelicerae, and conspicuous Two other copulations, one partially record- body vibrations when males pursued females . ed in a Super-8 movie-film, were observed in Females hid in the retreat and remained very 1990, using Arena A. and copu- passive. In response to these male behaviors, lations were similar to those previously de- females flexed their legs against the body and scribed and copulation durations were 24 .5 remained immobile (with venter up in two and 55 min . cases). These males continued pursuing the fe- male until the female abandoned her web . If DISCUSSION the female returned, the male pursued her and webs.-The high sensivity of again until she remained outside the web. M. thorelli to variations seems to be These males then took over the female webs, critical in understanding its biology and ecol- occupying the retreat . In other cases the males ogy. In the laboratory, individuals not provid- touched the female, made palpal drumming ed with abundant water quickly died, but a and slightly pushed her. In four encounters the minimal excess of water also caused the male remained peacefully in the retreat with death . This sensivity clearly suggest a high the female for 30 min, at which time he was dependence on the funnel-and-sheet web . The removed . In three encounters the female left need for hygro-thermo stability is also em- the web and came back several times, without phasized by reinforced by their habit of living being disturbed by the male. In another three under stones, roots and trunks, in hilly areas encounters, males ran away from the web after in streamside forests. Probably the web gives copulation . Finally, in two encounters both protection from and occasional partners ran away after copulation and in one flooding . Although this species lives near the COSTA & PEREZ-MILES-BIOLOGY OF MECICOBOTHIUM THORELLI 325 water it does not invade the stones of the dry termine the time when the spider will molt to stream bed (Costa et al . 1991 ; Perez-Miles et maturity : biorhythm and seasonal environ- al. 1993) . Then, M. thorelli seems to be very mental factors . Females reach maturity before restrictive in its habitat selection . Collection males, which explains why males molt more data from Argentina, Provincia de Buenos Ai- times than females during September-April. res, generally agree with our findings (Holm- Females of pococki Platnick 1987 berg 1882 ; Goloboff & Ramirez 1991 ; Maury (Hypochilidae) also reach maturity earlier in list.). Also, North American Mecicobothi- than males (Catley 1993). idae live under stones or other objects in the The results suggest that maturity molting soil, in crevices, and deep in organic ground and sexual activity occur at the beginning of litter (Gertsch & Platnick 1979). These spe- the cool period, which is also supported by cies are frequently found in the shade of co- the collection dates of Holmberg (1882), niferous and oak woods from Washington and Gertsch & Platnick (1979) and Perez-Miles et Oregon to California (western USA) . al. (1993) . In the field Perez-Miles et al . Our observations indicate that adult males (1993) found adult males from May to Sep- do not construct funnel-and-sheet webs, but tember, with a peak of activity in July . These Holmberg (1882) found the holotype male in authors interpreted the fall/winter activity as a a funnel web of 2 cm length which opened way to avoid . We also interpreted onto a sheet of 2 cm2. Holmberg was not sure the synchronized male maturity in the same if the male was occupying its own web be- way, satiating the scarce winter predators . A cause he found several individuals of "Tege- capture of a male in October in Sierra de la neria" in coexistence . M. thorelli found in Si- Ventana, Argentina (Gertsch & Platnick 1979) erra de las Animas were syntopic with seems to be extremely late . However, several hydrophilic spiders of the captive males remained alive during Septem- (Lycosidae), the webs of which could corre- ber and a few in October, suggesting a longer spond to Holmberg's "" . However, lifespan in the laboratory . The male activity it is more likely that the male collected by period of M. thorelli resembles a "stenoch- Holmberg was occupying a conspecific female ronous, winter-mature species" of Schaefer web; this would fit our observations of post- (1987), a category mainly occupied by Liny- copulatory female expulsion . Or perhaps this phiidae in . However, this species has male had recently molted to adulthood in his a longer lifespan - at least three . Indi- juvenile web . viduals molt more than expected for their size Apart from the role of webs in water reg- and have two periods without molting (winter ulation, they also play a key role in prey cap- and summer). The wide range of sizes found ture. M. thorelli has long posterior spinnerets in field samples and laboratory developmental well suited for sheet-web construction and re- data suggest the coexistence of at least three pair. Biting and pulling back behavior in prey generations . capture is widely distributed among spider Reproduction .-As far as we know, our taxa, suggesting a primitive condition . This observations of the sexual behavior of M. tho- technique is simple and safe because entan- relli are the first ever published for any spe- gled threads effectively prevent the defensive cies of Mecicobothiidae . Females of M. tho- movements of the prey . North American Me- relli may release a sex , which has cicobothriidae also live in funnel-and-sheet previously been reported for webs and show similar prey capture tactics (Haupt 1977) and several families of Myga- (Gertsch & Platnick 1979) . lomorphae : (Coyle & Icenogle Life cycle.-Most spiders collected in Sep- 1994), Atypidae (Coyle & Shear 1981), Di- tember 1994 molted in October 1994 (Fig . 4). pluridae (Coyle 1985, 1986b), This synchronized development would reflect (Buchli 1962 ; Costa 1982) and Theraphosidae the influence of uniform breeding conditions, (Baerg 1958; Minch 1979 ; Perez-Miles & mainly feeding . These juveniles molted 2, 3 Costa 1992). This wide distribution indicates or 4 times to reach maturity . Therefore, ma- that tactochemical sexual communication is an turity molting seems to occur in a fixed period early aquisition in spiders . The effect of a sex- of the year, independent of the initial devel- ual pheromone of M. thorelli should be of opmental stage . Two main factors seem to de- short duration and/or it would only be released 326 THE JOURNAL OF ARACHNOLOGY near the retreat, considering that males started Kaston 1972 and Hexura Simon 1884, males the courtship in the sheet web . have a series of short spines above the chelic- Courtship characteristics suggest that vibra- erae, distally stronger (Gertsch & Platnick tions transmitted through the silk threads are 1979), suggesting their use in copulation . the primary means of communication before These structures may perform a similar to that direct contact. Male sexual behavior strongly found in riversi (Antrodiadetidae) . inhibited female attacks . The extreme passiv- Coyle (1971) observed that in this species the ity of females during courtship, copulation males used their long cheliceral apophyses to and postcopulation is remarkable, although it hold the outspread female chelicerae during is common in mygalomorphs (Jackson & Pol- copulation . Clasping of M. thorelli might have lard 1990) . Only if we manipulated a couple evolved from a frontal fight with full contact during copulation was the male attacked and of chelicerae, common in agonistic encoun- cannibalized . ters . In successive steps male chelicerae Cheliceral sexual clasping has been report- would be modified to neutralize female biting ed in Mygalomorphae only for Atypoides riv- and increase male security during copulation . ersi O.P.-Cambridge 1883 (Antrodiaetidae ; Clasping also serves in communication and Coyle 1971) but not involving fang clasping epigamic , as well as to hold as in M. thorelli. However, it resembles that female in position (Coyle 1985, 1986b ; Eber- of some . For example, in hard 1985 ; Jackson & Pollard 1990) . some species of Sundevall 1923 In its initial stages cheliceral clasping re- and Latreille 1804 (Tetragnathi- quires very complex movements . Positional dae) males immobilize female chelicerae with reconstruction with dead specimens helped us their own modified chelicerae (Bristowe understand the mechanics of clasping . We 1941). Also males of bitubercula- were able to verify that: 1) Both male and tum (Wider 1834) () (Bristowe female must separate the basal segments of 1931, 1941) and antipodiana (O .E- the chelicerae laterally ; 2) Females must fully Cambridge 1880) () (Whitehouse open the cheliceral fangs obliquely; 3) The in- 1987) immobilize female chelicerae by stim- troduction of the female fangs is initially di- ulating female biting on male frontal tuber- vergent and finally convergent ; 4) Female cles. In Theraphosidae, precopulatory and fangs enter the male cheliceral channels up to copulatory female clasping on tibial spurs of the basal incrassate region . Male hinge-like male forelegs is a well-known mechanism movements facilitate this rigid clasping posi- (Baerg 1928, 1958 ; Minch 1979 ; Perez-Miles tion; 5) In copula, the basal chelicerae of fe- & Costa 1992) . The sexual embrace, behavior male and male remain closed ; 6) Two simul- and reproduction of Mygalomorphae were re- taneous procedures are necessary for viewed by Coyle (1985, 1986b), Coyle & unclasping: male cheliceral opening with O'Shields (1990), Jackson & Pollard (1990) hinge-like movements, and female cheliceral and Costa & Perez-Miles (1992) . opening with fangs relaxed ; 7) Males must The male of M. thorelli elicits female clasp- move downward and the female upward . ing by pushing her with his chelicerae repeat- Male safety during copulation is reinforced edly. The cheliceral embrace is a sine qua non by positioning the forelegs on the female, condition for a successful copulation. Female which probably prevents the female from bit- biting appears to cancel the aggressive and/or ing the male prosoma . The long palps of the predatory impulse and consequently inhibit male allow him to copulate more horizontally further attacks. In cuneata (Clerck than other mygalomorphs. Consequently, mat- 1757) (Lycosidae), where males offer their in- ing can take place safely inside the retreat . crassate foreleg tibiae for female biting Also, male backward movements probably (Kronestedt 1979, 1990) a similar explanation improve clasping . could be applied . The release of aphrodisiac Copulation of M. thorelli is very complex from these male structures was and long in comparison with other mygalo- also suggested (Kronestedt 1986 ; Whitehouse morph spiders . The insertion/withdrawal pal- 1987). pal movements deserve special attention . The In Mecicobothriidae, cheliceral clasping is palpal embolus is rigid and spiral-shaped and only present in M, thorelli. In Megahexura cannot enter by rotation as in other araneo- COSTA & PEREZ-MILES-BIOLOGY OF MECICOBOTHIUM THORELLI 327 morphs or (Abalos & Baez 1967 ; webs constructed by females in the laboratory ; Grasshoff 1973) . The palpal embolus must en- these would facilitate female expulsion . In the ter forcibly, spiral by spiral, in a discontinuous laboratory, females with deep retreats were jerky movement which would explain the fe- less likely to be expelled than were those with male's sudden movements . This penetration shallow retreats ; in the field deep retreats were appears to be made possible by the elasticity the only type observed . However, high female of the embolus, as well as the spermathecae . tolerance to males seems to be a species-spe- The number of embolus spirals and sperma- cific tactic which could be understood if com- thecae spirals are the same - four. This close bined with cryptic female location . correspondence suggests that the whole em- In the laboratory, copulated females did not bolus enters the inner spiral-shaped receptacle spin intensely in winter and they dug deeply but not in the outer round receptacles (see fig . into the soil. Usually they did not make an 38 in Gertsch & Platnick 1979) . This unique exterior sheet for prey capture, and therefore penetration pattern probably causes intense would riot be found by males (nor collectors) . genitalic stimulation which would determine This cryptic postcopulatory female behavior, sexual selection by female choice, following together with female expulsion by the male, Eberhard's theory (Eberhard 1985) . This stim- could protect the paternity of the copulating ulation might also have an inhibitory function male . Our hypothesis agrees with the high on non-sexual female behaviors . competition expected among males of M. tho- The characteristics of both embolus and re- relli which reach maturity synchronously and ceptacle spirals require that the palpal inser- have an activity peak in July (Perez-Miles et tions must be crossed (right palp in right re- al. 1993) . ceptacle, and left palp in left receptacle) . This At first, our hypothesis fails to explain the crossed insertion is the norm in araneomorphs benefits from the female perspective because but has not been indicated yet for the myga- she loses her web and, consequently, the pos- lomorphs . Although the insertion mode is not sibility of other copulations . New copulations evident from direct observation, it was con- would increase the variation of her offspring firmed from the study of helicoidal orientation and avoid the risk of a single copulation with complementarity between male and female an sterile male. (See Austad 1984 for a review genitalia. The orientation of both embolus tips of remating advantages for females) . Howev- and receptacle basis would also suggest that er, some female benefits could be suggested . only crossed palpal insertion is possible . The If prey were scarce in winter, it would be wide separation between receptacle bases more economical for a female to suspend pre- would facilitate a correct insertion . dation and thereby avoid the cost of web Male postcopulatory behavior in M. thorelli maintenance, predation and risks, is remarkable . Some males seemed to practice considering the low metabolic rates of the spi- postcopulatory mate guarding, which would der in this season. The risk to the female dur- be predicted on the basis of this species sper- ing expulsion from the retreat would be min- mathecal morphology (cul-de-sac type of Aus- imal if a low predation level in winter is tad 1984). Mate guarding prevents later cop- assumed (Perez-Miles et al . 1993) . Webs ulations with other males and consequently could elicit persistent courting males which competition, but can be only main- make prey capture difficult and also attract tained for a brief time . Although the mor- predators. This would help to explain the phology of the receptacle stalk is adequate for "complicity" of the female in allowing the mating plugs, males recopulated normally, weak male to expel her. Two field observa- which suggests the absence of mate plugs in tions are consistent with the hypothesis : 1) we M. thorelli . did not find adult females in September, when Unlike mate guarding, female expulsion is intense collections were carried on, and 2) a an uncommon male postcopulatory behavior male found by Holmberg in 1881 was prob- in spiders, and without a clear interpretation ably occupying a web of an expelled female. in M. thorelli. Isolated males may have an ex- M. thorelli make eggsacs earlier (at the end cessive aggressive motivation due to the ab- of winter and end of spring) than North Amer- sence of fights in natural male-male encoun- ican Mecicobothriidae (spring and summer) ters . Another factor would be the fragmentary (Gertsch & Platnick 1979) . The eggsacs of 328 THE JOURNAL OF ARACHNOLOGY these species are round as in M. thorelli, ex- of the male . Quart . Rev . Biol., 3 :109- cept in Hexura rothi Gertsch & Platnick 1979 116. (lenticular) . The number of eggs is related to Baerg, W.J . 1958 . The Tarantula. Univ . Kansas Press, Lawrence, Kansas . spider size : M. thorelli (body length approxi- Barrowclough, G .E 1992 . Systematics, biodiversi- mately 7 mm) laid between 23-33 eggs ; Hex- ty, and conservation biology . Pp . 121-143 . In ura rothi (body length approximately 11 mm) Systematics, Ecology, and the Cri- laid 80 eggs, Hexurella Gerstch & Platnick sis . (N . Eldredge, ed.), Columbia Univ . Press, 1979 species (body length between mm) 3-4 New York . laid only 4-7 eggs (Gertsch & Platnick 1979) . Bristowe, W.S . 1931 . The mating habits of spiders : Phylogeny and biogeography .-The a second supplement, with the description of a monophyly of Mecicobothriidae, supported by new thomisid from Krakatau . Proc . Zool . Soc. Gertsch & Platnick (1979), Raven (1985) and London, 27 :395-413 . Goloboff (1993), is considered as a starting Bristowe, W.S . 1941. The Comity of Spiders . 2, point to discuss some biogeographical aspects . Ray Society, London . The amphitropical distribution of the Meci- Buchli, H. 1962 . Note preliminaire sur cobothriidae is similar to that reported to some 1'accouplement des araignees mygalomorphes caementaria, Nemesia dubia et Pachy- coleopterans, fishes and (Humphries & lomerus piceus () . Vie Milieu, 13 :167- Parenti, 1986) . According to Gertsch & Plat- 178. nick (1979) and Raven (1985), Hexurella Capocasale, R .M ., F Perez-Miles, EG . Costa, E . seems to be the sister genus of the rest of Me- Gudynas & L . Prandi . 1989 . Comunicacion pre- cicobothriidae and consequently Mecicoboth- liminar sobre la aracnofauna criptozoica de Si- rium is more closely related to the mecico- erra de las Animas, Uruguay. Bol . Soc . Zool . bothriid genera Megahexura and Hexura than Uruguay, 5 :31-32. to Hexurella . Considering the present geo- Capocasale, R .M . & E . Gudynas . 1993 . La fauna graphic distribution of these taxa, only an an- de (Arachnida) del criptozoos de Sierra cient generic cladogenesis (pangeic) could be de las Animas (Uruguay) . Aracnologfa, 19/20 :1- hypothesized, prior to the separation of the 15 . Catley, K .M . 1993 . Courtship, mating and post- Americas . Avoiding dispersalist interpreta- oviposition behaviour of tions, a post-pangeic cladogenesis of North Platnick (Araneae, Hypochilidae) . Mem. Queens- American genera could only be proposed if land Mus . 33 :469-474 . Mecicobothriurn was the sister genus of the Costa, FG . 1982 . Etologia . In E Perez-Miles & rest of Mecicobothriidae . R.M . Capocasale. Hallazgo de una tercera espe- cie del genero Pvcnothelopsis : Pycnothelopsis ACKNOWLEDGMENTS tacuariensis sp . nov . (Araneae, ) . We thank E . Gudynas, A . Mignone and J .C . Com. Zool . Mus. Hist . Nat . Montevideo, 11 :1 7 . Larriera for their help in the field work. We Costa, EG . & E Perez-Miles . 1992 . Notes on mat- ing and reproductive success of Ceropelina lon- are particularly grateful to EA . Coyle for his gisternalis (Araneae, Theraphosidae) in captivity . suggestions and the careful review of an early J . Arachnol ., 20 :129-133 . version of the manuscript . We also thank J . Costa, F.G. & F Perez-Miles . 1994 . Ecologia de Berry, N . Platnick, P. Sierwald and an anon- los escorpiones Bothriuridae de Sierra de las An- ymous reviewer for conceptual and style re- imas, Maldonado, Uruguay . Aracnologfa, 21 : views of the manuscript. 1-5. Costa, EG ., E Perez-Miles, E . Gudynas, L . Prandi LITERATURE CITED & R .M . Capocasale . 1991 . Ecologia de los ar- Abalos, J .W. & E .C . Baez . 1967. The spider genus acnidos criptozoicos, excepto acaros, de Sierra Latrodectus in Santiago del Estero, Argentina . de las Animas (Uruguay) . Ordenes y familias . Animal , Pergamon Press, Oxford & New Aracnologfa, 13/15 :1-41 . York . Coyle, EA . 1971 . Systematics and natural history Austad, S .N. 1984 . Evolution of sperm priority of the mygalomorph spider genus patterns in spiders . Pp . 223-249. In Sperm Com- and related genera (Araneae: Antrodiaetidae) . petition and the Evolution of Animal Mating Bull . Mus . comp . Zool ., 141 :269-402 . Systems . (R .L . Smith, ed.) . Academic Press, San Coyle, EA. 1985 . Observations on the mating be- Diego, California . havior of the tiny mygalomorph spider, Micro- Baerg, W.J . 1928 . The life cycle and mating habits hexura montivaga Crosby & Bishop (Araneae, Di- COSTA & PEREZ-MILES-BIOLOGY OF MECICOBOTHIUM THORELLI 329

pluridae) . Bull . British Arachnol . Soc ., 6 :328- sous-ordre des araignees territelaires (Territelar- 330 . iae) specialement du genre Nord-Americain Ca- Coyle, EA . 1986a. The role of silk in prey capture tadysas, Hentz et de la nouvelle famillie Meci- by nonaraneomorph spiders . Pp. 269-305 . In cobothrioidae, Holmb., Bol . Acad . Argentino, 4: Spiders : Webs, Behavior, and Evolution ..A. ( 153-174 . Shear, ed.). Stanford Univ . Press, Stanford, Cal- Humphries, C .J. & L.R. Parenti. 1986 . Cladistic ifornia. biogeography . Clarendon Press, Oxford . Coyle, EA . 1986b. Courtship, mating, and the Jackson, R .R. & S.D. Pollard . 1990 . Intraspecific function of male-specific leg structures in the interactions and the function of courtship in my- mygalomorph spider genus (Araneae, galomorph spiders : a study of Porrhothele anti- ) . Proc . Ninth Internat . Congr. Arach- podiana (Araneae : ) and a literature nol ., Pp . 33-38 . review . New Zealand J . Zool ., 17 :499-526 . Coyle, FA . & W.R. Icenogle . 1994. Natural history Kronestedt, T. 1979 . Etologiska karaktarer vid tax- of the Californian trapdoor spider genus Aliaty- onomiska studier av vargspindlar . Entomol. pus (Araneae, Antrodiaetidae) . J. Arachnol ., 22 : Tidskr., 100 :194-199 . 225-255 . Kronestedt, T. 1986 . A presumptive pheromone- Coyle, EA . & T.C. O'Shields . 1990 . Courtship and emitting structure in wolf spiders (Araneae, Ly- mating behavior of Thelechoris karschi (Arane- cosidae) . Psyche, 93 :127-131 . ae, Dipluridae), an African funnelweb spider . J. Kronestedt, T. 1990 . Separation of two species Arachnol., 18 :281-296 . standing as (Clerck) by mor- Coyle, EA . & Shear, W.A. 1981 . Observations on phological, behavioural and ecological charac- the natural history of abboti and ters, with remarks on related species in the pul- (Araneae, Atypidae), with evi- verulenta group (Araneae, Lycosidae) . Zool . dence for a contact sex pheromone . J . Arachnol ., Scripta, 19 :203-225 . 9 :317-326 . Minch, E .W. 1979 . Reproductive behaviour of the Eberhard, W.E. 1985 . Sexual selection and animal tarantula chalcodes Chamberlin genitalia . Harvard Univ. Press, Harvard, Massa- (Araneae : Theraphosidae) . Bull . British Arach- chusetts . nol . Soc ., 4 :416-420 . Grasshoff, M. 1973 . Konstruktions-und Funklion- Perez-Miles, E & FG . Costa . 1992. Interacciones sanalyse an Kopulationsorganen einiger Radnetz- intra e intersexuales en mollicoma spinnen . Aufs . u . Red . Senckenberg naturf . Ges ., (Araneae, Theraphosidae) en condiciones exper- 24 :129-151 . imentales . Bol . Soc . Zool . Uruguay, 7:71-72 . Gertsch, WJ . & N.I. Platnick. 1979 . A revision of Perez-Miles, F, EG . Costa & E . Gudynas . 1993 . the spider family Mecicobothriidae (Araneae, Ecologia de una comunidad de Mygalomorphae Mygalomorphae) . American Mus . Nov ., 2687 :1- criptozoicas de Sierra de las Animas, Uruguay 32. (Arachnida, Araneae) . Aracnologia, 17/18 :1-22 . Goloboff, PA . 1993. A reanalysis of mygalomorph Raven, R .J. 1985 . The spider infraorder Mygalo- spider families (Araneae) . American Mus. Nov ., morphae (Araneae): Cladistics and systematics . 3056:1-32 . Bull . American Mus. Nat. Hist ., 182 :1-180 . Goloboff, PA . & Ramirez, M .J . 1991 . A new spe- Schaefer, M . 1987 . Life cycle and diapause . Pp. cies of (Araneae: Scytodoidea) from 331-347, In Ecophysiology of spiders . (W. Nen- twig, . Argentina . J. New York Entomol . Soc ., 99 :691- ed.). Springer Verlag, Berlin 695 . Whitehouse, M .E.A. 1987 . The external structural Haupt, J . 1977 . Preliminary report on the mating detail of the protrusions on the cephalothorax of male Argyrodes antipodiana (Theridiidae) . Bull . behaviour of the primitive spider Heptathela ki- British Arachnol . Soc ., 7 :142-144 . murai (Kishida) (Araneae, Liphistiomorphae) . Z . Naturforsch ., 32 :312-314 . Manuscript received 1 August 1996, revised 20 July Holmberg, E .L. 1882 . Observations a propos du 1998.