2003. The Journal of Arachnology 31:90±104

EGGSAC RECOGNITION IN LOXOSCELES GAUCHO (ARANEAE, SICARIIDAE) AND THE EVOLUTION OF MATERNAL CARE IN

Hilton Ferreira JapyassuÂ, CaÂtia Regina Macagnan and Irene Knysak: Laboratory of , Butantan Institute, Av. Vital Brazil 1500, SaÄo PauloÐSP, 05503-900, BRAZIL

ABSTRACT. We report for the ®rst time the existence of eggsac recognition and maternal care in Loxosceles gaucho. Spiders confronted simultaneously with their own and foreign eggsacs stay closer to their own eggsacs. This is unexpected since eggsac recognition should evolve among with clumped distributions, high maternal investments and few breeding opportunities, features not present in this spe- cies. Despite this recognition, spiders with a single eggsac make no distinction between their own and foreign eggsacs: they adopt eggsacs from sympatric, conspeci®c females, and take care of them as their own. It seems that there is a readiness to perform maternal care that overrules the recognition system. We describe oviposition behavior and compare it with other descriptions in the literature. Seven behavioral characters related to eggsac building and/or guarding are mapped onto available phylogenies. Maternal care behaviors are quite conservative among spiders, useful for the grouping not only of families, but also of higher order ranks. Keywords: Maternal care, offspring recognition, oviposition, evolution, Sicariidae, Loxosceles gaucho

Spiders show varying degrees of maternal ditions are a high probability of encountering care, from the building of an eggsac to ovi- other conspeci®cs brood, and a low probabil- position at suitable sites (Suter et al. 1987; ity of future breeding opportunities. Christenson & Wenzl 1980), eggsac guarding Loxosceles gaucho Gertsch 1967 is a (Pollard 1984; Richman & Jackson 1992; Cas- of medical importance whose bites cause ne- tanho & Oliveira 1997), extended maternal crotic lesions in humans (Jorge et al. 1991). care during the spiderlings' communal life Due to this medical importance, much of its (Morse 1992) including prey supply and re- biology is well documented (Rinaldi et al. gurgitation for feeding the young (Ito & Shin- 1997; Rinaldi & Stropa 1998). Loxosceles kai 1993; Evans 1998a; Li et al. 1999) and spp. are active at night, build simple or com- even extreme suicidal care (Evans et al. 1995; plex white silk sheet webs covering the sub- Schneider & Lubin 1997; Kim et al. 2000). strate (BuÈcherl 1964), usually in small natural Maternal care has positive ®tness consequenc- cavities (BuÈcherl 1962). Species in the es, reducing on eggs (Fink 1987) do not ful®ll any of the requirements for the and offspring (Fink 1986; Willey & Adler evolution of kin recognition: they lay up to 1989; Morse 1992), or providing nutrition and eight egg clutches from a single mating (Ga- liano 1967), and are solitary (Delgado 1966), consequently enhancing spiderling survival showing a low probability of encountering un- (Kullmann & Zimmermann 1974; Kim et al. related offspring. In this paper we describe as- 2000). pects of L. gaucho behavior, including ovi- Spiders with extended maternal care should position, maternal care, and kin recognition. evolve offspring recognition systems to avoid We also review the literature concerning these exploitation by non-relatives. However, there characters and discuss the results from a phy- is little evidence of kin recognition among spi- logenetic perspective. ders (Clark & Jackson 1994), perhaps because other conditions are necessary for the evolu- METHODS tion of offspring discriminating systems. Sixty-three females (voucher specimens de- Evans (1998b) suggests that two of these con- posited at Butantan Institute, numbers 30064±

90 JAPYASSUÂ ET AL.ÐEVOLUTION OF MATERNAL CARE 91

30069) were observed from mating to the group), leaving the eggsac alone (ncare, n ϭ emergence of the spiderlings (April±Decem- 12). ber 1999). Each spider was kept in a 30 ϫ 15 Observational scheme.ÐIn all the exper- ϫ 20 cm glass terrarium, under an external imental treatments, the terraria were scanned light±dark cycle, in the laboratory. Prey was three times a day (morning, afternoon and offered three times/week, alternating between night), in three alternate days for each week, Gryllus sp. (Orthoptera), Tenebrio molitor lar- from mating to 15 days after the emergence vae (Coleoptera), Pycnocellus surinamensis of the offspring. We observed the relative po- (Blattodea) and Alphitobius pisceus larvae sition between spiders and eggsacs, and also (Coleoptera). Newborn Gryllus sp. and Gryl- the number of appendages touching the egg- lodes sigilattus (Orthoptera) were offered sac. If the spiders and/or offspring were in ac- twice to the spiderlings ®ve and ten days after tivity (ovipositing, foraging) the observational their emergence from the eggsac. The obser- scheme changed to focal and ad libitum, that vation period was terminated 15 days after the is, we focused on the active spider(s) until the spiderlings emerged from the eggsac. end of the behavioral bout. Experimental design.ÐTwo experiments Comparative data.ÐThe comparative in- were conducted, one to test the existence of formation available in the literature allowed eggsac recognition by the mother (n ϭ 24), the description of 7 behavioral characters (Ap- and the other to evaluate the existence of ma- pendix 1). We mapped these characters onto ternal care and its ®tness consequences (n ϭ the family cladogram proposed by Codding- 39). In both cases, the mother was left ®ve ton & Levi (1991), modi®ed at the araneid days with her own eggsac before it was re- node by means of the cladogram proposed by moved for the beginning of the experimental Scharff & Coddington (1997); only unambig- treatment. The spiders spun a delicate cover- uous optimizations were discussed. We split the family Sicariidae in order to better analyze ing sheet on the ¯oor of the terraria, and at- the genus Loxosceles; we also split the family tached the eggsacs into available folded pieces Salticidae in order to distinguish the proposed of cardboard paper, which served as retreats. primitive spartaeines (Jackson & Pollard In order to exchange eggsacs between spiders 1996) from the other salticids. we removed these cardboard retreats from the terraria. RESULTS Eggsac recognition: Twenty-four females Eggsac building.ÐEggsac building oc- with eggsacs were divided into pairs, each curred in four phases. First, the spider con- pair with eggsacs built on the same day. In structed a silken basal plate on the substrate. each pair, one female received back her own A few days later, she layed a gelatinous mass eggsac plus the one of the other female (here- with the eggs on the basal plate, dried this in considered the ``foreign'' eggsac). The sec- mass by moving her palps and , and ond female in each pair was merely an eggsac ®nally layed a cover plate, composed of two donor. superimposed silken layers. The observed Maternal care: The females were assigned time intervals within the whole reproductive to one of three experimental treatments, de- period are presented in Table 1. The time in- signed to evaluate the effect of maternal care terval from mating to eggsac building varies on spiderling survival. Spiders in the ``- much more than the time of egg maturation. er-with-own-offspring'' group (own, n ϭ 14) Basal plate: The spider ®xed dry threads received back their own eggsac; this allowed onto the substrate with swinging movements the description of maternal care, and also of the abdomen. During the ®rst part of the functioned as a control for the other treat- movement the spinnerets continuously ments. In the two remaining treatments, the touched the substrate; then they were lifted, females were divided into pairs, and each in- describing an arch, just to touch the substrate dividual received the eggsac from the other in again, then the movement was re-started in the the pair; one female in the pair (adoption opposite direction (Fig. 1a). This was repeated group) took care of the eggsac from her paired many times (Fig. 1b, c, d) until the spider conspeci®c (adopt, n ϭ 13) while the other made a small pause, changed the orientation was removed from the terraria (no-care of her body, and performed this whole pro- 92 THE JOURNAL OF ARACHNOLOGY

Table 1.ÐMean time lag (in days) between distinct behaviors performed by the mothers, from mating to the hatching of the spiderlings. Sample size, standard deviation and range are also shown.

First/Second event n Mean (days) SD Range Mating/basal plate 19 47.4 18.0 24±82 Mating/egg mass (and cover plate) 70 59.6 28.1 21±120 Basal plate/egg mass (and cover plate) 19 1.7 1.4 0±5 Egg mass (and cover plate)/hatching 36 56.7 6.5 45±68 cedure over and over (Fig. 1d) to the comple- Desiccation: The spider handled the egg tion of a circular sheet with a diameter of ap- mass with the palps and paused with the che- proximately 2 cm. licerae on the eggs for some minutes. Then Egg mass: The spider stayed close to the she rotated and performed this same sequence basal plate for approximately two days, at until a full 360Њ rotation was completed. In the which time she layed the egg mass onto it meantime, the gelatinous mass disappeared, (Table 1). Initially, she layed a brownish ge- exposing the conically arranged eggs. latinous mass on the basal plate. This was Cover plate: Three distinct sequences of done with the cephalotorax directed upwards. movements compose this last eggsac building The spider repeatedly touched this mass with phase (Fig. 2). First the spider attached silk at the palps, then with the chelicerae, ventral ce- two points near the boundary of the basal phalotorax and ventral abdomen, always in plate (open dots, Fig. 2a) and at one point over this sequence. Next she layed the eggs in the the egg mass (closed dot, Fig. 2a); this small mass, with a series of rhythmic leg I and II three-attachments cycle was repeated as the ¯exions (in one episode we counted 55 ¯ex- spider rotated on the eggsac (Fig. 2b, c, d); at ions); then she paused, rotated the body axis, the end of each cycle the spider paused and and repeated this procedure several times touched the egg mass with her palps. After a (never more than ten times), gradually reduc- 360Њ rotation the spider sometimes repeated ing the frequency of the rhythmic ¯exions and the whole procedure in the opposite direction. enlarging the pauses. At the end of this phase, In the next sequence of movements, the spider the eggs were clearly visible through the ge- ®xed several times at opposite sides of the latinous mass. boundary of the basal plate (Fig. 3a, b); she

Figure 1.ÐBuilding of the basal plate. The spider lays threads (continuous and interrupted black lines) onto the vertical substrate (dark gray). These threads will eventually compose the basal plate (light gray). The spider touches the substrate continuously with the spinnerets during the ®rst part of each movement (1) and then raises the abdomen (2) to touch the substrate again only at the end of the movement (a). These movements are shown in the remaining diagrams without perspective; threads laid in previous movements are depicted as dotted lines; threads currently being laid are shown as in b. After various back and forth movements (c, d) the spider changes the orientation of her body and begins a new back and forth series. JAPYASSUÂ ET AL.ÐEVOLUTION OF MATERNAL CARE 93

Figure 2.ÐBuilding of the ®rst cover plate sheet. The spider lays threads over the basal plate (light gray) and egg mass (dark gray). The large dotted arrow represents the spider body axis (the arrow head is the cephalothorax). The building of this sheet involves the repetition of one same series of movements (1,2,&3ina,b,&c)while rotating the body axis around the whole structure (d); at each movement the spider attaches the current thread in three points, two at the periphery of the basal plate (open dots in a and b), and one over the egg mass (black dot). Dotted lines indicate previous series of movements, and continuous lines indicate current series of movements. then rotated to initiate a new bout of lateral structure. She sometimes repositioned it and, ®xations (Fig. 3c). Small variations in these in one case, even brought back the egg mass movements are depicted at Fig. 3d. The spider (which had fallen on the terrarium ¯oor) to its then increased the amplitude of these lateral original place, adding a new cover plate. A ®xations, and occasionally scraped the ventral few days before the emergence of the spider- side of her cephalothorax and abdomen with lings the mother made an aperture in the egg- her hind legs, possibly leaving hairs on the sac and began to knock persistently at the cov- silken tissue. Sometimes the spider added er plate, hitting at it with the tip of her small pieces of debris to the cover plate. forelegs (as if signaling to the spiderlings the Mother-offspring interactions.ÐThe fe- appropriate moment to emerge); in one case male interacted in various ways with her egg- we witnessed the mother holding the aperture sac. She repaired it, adding lines to the whole while the spiderlings abandoned the eggsac.

Figure 3.ÐBuilding of the second cover plate sheet. The spider makes various back and forth move- ments (a & b) before changing the body axis to restart this same series in another position (c). These back and forth movements may vary as to the ®xation points (d), which can occur near the egg mass (1) or outside the basal plate (2); sometimes the spider slows down the movement while passing over the egg mass and attaches variously onto it (3). 94 THE JOURNAL OF ARACHNOLOGY

Figure 4.ÐMaternal displacement and eggsac recognition. Spiders without eggsacs move for larger distances than spiders with eggsacs (cm, mean Ϯ 2SE; 4a). Spiders with eggsacs stay nearer to their own than to foreign eggsacs (cm, mean Ϯ 2SE; 4b).

The female appeared to compete with her or in the frequency (Z ϭϪ1.165, P ϭ 0.244, offspring for food. Jerking the web repeatedly n ϭ 27) or amplitude (Z ϭϪ.437, P ϭ 0.662, with her front legs, she appeared to signal to n ϭ 27) of their movements in the terrarium. the spiderlings her precedence over a prey There was no signi®cant in¯uence of the item; she also actively pushed nearby spider- presence and kind of maternal care on the fre- lings, or even departed carrying the prey item. quency of successful eggsacs (␹2 ϭ .559, P ϭ Despite that, some spiderlings fed along with 0.756, n ϭ 39). Spiderlings in all treatments the mother. (own, adopt and ncare) did not differ, on the Offspring-offspring con¯icts over prey usu- time of emergence from the eggsac (␹2 ϭ ally resulted in a behavioral arms race: ®rst .991, P ϭ 0.609, n ϭ 28) or on their total they elevated their forelegs, next they beat weight (␹2 ϭ .941, P ϭ 0.625, n ϭ 27) or each others cephalothorax with these legs, and survival rate (␹2 ϭ 1.260, P ϭ 0.533, n ϭ 33). ®nally they bit each other until one of them This may be due to the absence of enemies in ¯ed. Notwithstanding this aggressiveness, the laboratory conditions, and experiments under winner often accepted the approach of its sib- natural environments are necessary to com- lings after he/she had consumed part of the plement these results. prey, so that collective feeding among siblings Eggsac recognition.ÐAlthough L. gaucho was frequent. treated her own and foreign eggsacs similarly Maternal investment and ®tness conse- (as shown above), she discriminated between quences: After building their eggsac the spi- them. When simultaneously offered two egg- ders became much more sedentary, moving sacs the spider stayed closer to her own than only a few centimeters between observations to the foreign eggsac (Fig. 4b; t2,22 ϭϪ1.911, (Fig. 4a, U ϭ 21, P Ͻ 0.001, n ϭ 37). It made P ϭ 0.034). no difference whether the spider took care of Choosing between her own and foreign her own or an adoptive eggsac: in either case eggsacs is not an all-or-nothing process: the she stayed equally near it (Z ϭϪ.679, P ϭ spider frequently oscillated between the egg- 0.497, n ϭ 27). Furthermore, the females in sacs for a variable period before settling for the own group did not differ in any aspect of one or the other (Fig. 5a, c). Many factors maternal care from the ones in the adopt seem to interfere in this process. The spider group, either in the number of legs touching is able to detect eggsac viability: if one of the the eggsac (Z ϭϪ.776, P ϭ 0.438, n ϭ 27) eggsacs is not viable (n ϭ 4), the spider usu- JAPYASSUÂ ET AL.ÐEVOLUTION OF MATERNAL CARE 95

Figure 5.ÐOscillations between own and foreign eggsacs. Exposed to her own and a foreign eggsac, the mother frequently oscillated between them, staying sometimes nearer to her own eggsac, and some- times nearer to the foreign eggsac. The ®gure depicts the displacement of four spiders (a, b, c, d) in the eggsac recognition experiment. The distance between the spider and each of the eggsacs in the terrarium is shown throughout the experimental period. Continuous line ϭ distance to own eggsac; dotted line ϭ distance to foreign eggsac. Light gray triangles point to the moment of the oviposition of a second eggsac by the mother (from this moment on there are three eggsacs into the terraria); if the triangle is placed onto the dotted line, the new eggsac is close to the foreign eggsac, and vice versa. ally chooses the other (n ϭ 3), even if the this recognition is more likely to appear with- other is the foreign eggsac (Fig. 5d). When in species that show high levels of maternal the spider lays a new eggsac, she preferen- investment, breed only once and present high tially attends this new eggsac, regardless of probability of encountering unrelated off- where she placed it: near her own old eggsac spring (Evans 1998b). Although these condi- or near the foreign eggsac. In some cases the tions may enhance the probability of the evo- spider may visit the foreign eggsac just to lution of recognition systems, they are not open it, helping the spiderlings to emerge, re- necessary conditions for it, since we have turning afterwards to the original one (Fig. found eggsac recognition in L. gaucho (Fig. 5b). 4b), a species that does not meet these re- DISCUSSION quirements. L. gaucho does not show high There are few reports of kin recognition levels of maternal investment: the female among spiders, and it has been suggested that maintains foraging activities throughout the 96 THE JOURNAL OF ARACHNOLOGY entire egg-guarding phase, and does not ac- own brood. Conversely, if web characteristics tively feed the young. She breeds many times were predominant, both eggsacs would seem during her lifetime (in the present study, some rather similar, so that the spider could oscillate spiders laid up to three eggsacs in a 9 month between them (Fig. 5). period). Also, this spider has a reduced prob- We have also observed that L. gaucho fe- ability of encountering conspeci®c offspring males add threads to the eggsac. Thread ad- during the egg-guarding phase, since a female dition could render foreign eggsacs progres- reduces activity level after building her eggsac sively more familiar, and this familiarity could (Fig. 4a) and, at least in the Butantan Institute explain the otherwise aberrant behavior of woods, L. gaucho specimens are solitary. some females (Fig. 5b) that go to the foreign They are found mainly under dead fallen palm eggsac just to open it, facilitating the emer- tree leaves, usually one per 1.5m long leaves, gence of the spiderlings. sparsely distributed in the forest litter (Kash- If eggsac recognition is based on chemical imata, pers.com.). cues in the silk, there may be no speci®c Detailed studies of the structure and dy- brood recognition system. The female could namics of natural populations of L. gaucho are only discriminate between familiar and for- necessary in order to evaluate the probability eign silk, whatever the location of the silk. of encountering conspeci®c offspring, since This could explain the existence of eggsac inter-individual distances may vary as a func- recognition in a spider that does not present tion of environmental factors and previous ex- the ecological features usually related to the perience (Cangialosi & Uetz 1987), so that evolution of kin recognition systems. spatial strategies may change from one pop- Comparative data on the building of ulation to another. eggsacs.ÐSpiders within the genus Loxosce- Readiness for maternal care and cues to les build their eggsacs in a very similar way. eggsac recognition.ÐIf female L. gaucho Loxosceles intermedia Mello-LeitaÄo 1934 and recognize their own eggsac, why should the L. laeta Nicolet 1849 all follow the basal- females adopt conspeci®c eggsacs? Roland et plate/egg-mass/cover-plate sequence, present- al. (1996) show that adult, virgin Coelotes ter- ing a conical egg mass and a cover plate with restris Wider 1834 females () may two silken layers (Fischer 1996; Galiano adopt conspeci®c offspring in the presence of 1967). newborn spiderlings, demonstrating the exis- Despite these similarities, there are some tence of a readiness to provide maternal care. differences between species. For example, this This readiness could explain adoption by L. gaucho females of a single foreign eggsac is the ®rst report of a Loxosceles species that (adopt group). scrapes her ventral abdomen and cephalotho- Nevertheless, this readiness could not ex- rax while building the last layer of the cover plain adoption in the group of females with plate. Also, L. ru®pes Lucas 1834 stays inside two eggsacs: they should always prefer their an eggsac nest during the egg-guarding phase own brood. They should not oscillate between (Delgado 1966); a similar structure has been their own and foreign eggsacs (cf. Fig. 5). observed in some L. intermedia (Fischer Clark & Jackson (1994) showed that 1996), but not in L. laeta or L. gaucho. The labiata Thorell 1887 (Salticidae) recognizes building of eggsacs by L. intermedia has been her offspring based not only on cues from the described in some detail, and it differs from eggsac (possibly chemical cues in the silk), L. gaucho in two additional aspects: she but also on cues from the web itself: spiders builds the basal plate with movements similar in foreign webs destroy foreign eggsacs more to the building of the ®rst cover plate layer in frequently than spiders in their own webs. It L. gaucho (Fig. 2); besides this, L. intermedia seems from our data that web characteristics lays the egg mass right after the building of are not only important factors in the recogni- the basal plate (cf. Table 1). tion system, but that they are more important Eggsac building has been described for than eggsac factors. If eggsac characteristics many spider species, but the descriptions vary were predominant factors in maternal care de- strongly as to the details included. Despite this cisions, L. gaucho, confronted with her own variation, the literature reveals a consistent be- and foreign eggsacs, should always prefer her havioral sequence pattern: most spiders spin a JAPYASSUÂ ET AL.ÐEVOLUTION OF MATERNAL CARE 97 basal plate, deposit the egg mass over it, and usually spun between leaves (Montgomery ®nally spin a cover plate. 1909; Holm 1940; Jackson 1986, 1990a; Hal- Although this sequence might seem a log- las & Jackson 1986). The apomorphic pres- ical one, there are exceptions to the rule which ence of eggsac nests among non-spartaeine show that this is not a necessary sequence. salticids gives support to the idea that spar- Ariadna bicolor Hentz 1842 does not build teaineae are basal salticids as suggested by either a base or a cover sheet over her eggs; Jackson & Pollard (1996). instead this spider builds a closed, silken nest; The sequence base/eggs/cover (character 2) inside this nest, she secretes a mucous ¯uid is basal to the whole clade, and disappeared from the oral region, which gradually turns once (A. bicolor, Segestriidae, Montgomery into a gelatinous sheet adhered to the ventral 1909). As discussed above, P. viridans (Ox- surface of her body; she then deposit her eggs yopidae) shows a singular base/cover/eggs/ onto this sheet, and stays close to it in the sealing eggsac building sequence (Randall nest, until the emergence of the spiderlings 1977); nevertheless, her ``cover'' should be (Montgomery 1909). Peucetia viridans Hentz considered a remarkable, large marginal wall. 1832 (Oxyopidae) builds the basal plate and There is a striking similarity between the the cover plate (this last one with an opening building of Peucetia' ``cover'' (Whitcomb in the bottom), and only then lays the egg 1962; Whitcomb et al. 1966) and the building mass into the empty space, sealing the aper- of marginal walls in other spiders (for exam- ture afterwards (Randall 1977; Whitcomb ple, Rabidosa punctulata Hentz 1844, Mont- 1962; Whitcomb et al. 1966). Some spiders, gomery 1903 or Castianeira longipalpa Hentz like Pholcus opilionoides Schrank 1781 1847, Montgomery 1909), all of them per- (Pholcidae) and the Helio- formed with the same up and down looped phanus cupreus Walckenaer 1802 cover the strokes of the tip of the abdomen, applied to eggs with only a few threads, holding the ex- the circular edge of the basal plate in a clock- posed egg mass with their chelicerae (Pok- wise or counter-clockwise direction (while the rowsky 1899; Holm 1940). tips of the palps are pressed against the op- A thorough review of the literature shows posite margin of the basal plate). Therefore that eggsac building information is available the comparative analysis shows, on the basis for at least 60 spider species, scattered of this special similarity of movements (Wen- through 18 families (Appendix 2). This infor- zel 1992), that these supposedly distinct struc- mation was mapped onto available clado- tures are indeed the same, homologous struc- grams (Coddington & Levi 1991; Scharff & tures, distinct only in size. Coddington 1997) to evaluate the evolution of The use of a silken sheet as a base for the the behavioral characters. cocoon (character 3) is the plesiomorphic state Evolution of maternal behavior.ÐThe se- of this character among Opisthothelae. On this lected behavioral characters (Appendix 1) are silken sheet there can sometimes exist a cu- quite conservative. Most of them are plesio- shionlike mat of silk, which can be more or morphic within Opisthothelae spiders (Fig. 6), less pronounced in different species. Theri- and were subsequently lost or modi®ed in diids have discarded the sheet to oviposit di- some groups (see discussion below). To our rectly onto this cushionlike mat of silk (Mont- knowledge, there is no information on mater- gomery 1903), a putative synapomorphy to nal behavior of liphistiids (Mesothelae), the the family. Unfortunately the available de- outgroup of Opisthothelae, which prevents scriptions do not allow a clear distinction be- any generalization of the present analysis to tween a single-sheet basal plate and one with Araneae. both the single-sheet and the mat of silk. De- Eggsac nests (character 1) have appeared tailed observations are necessary to split this independently at least three times (Ariadna bi- state and further analyze the evolution of this colorÐSegestriidae, gnaphosids, and among character. non-spartaeineae salticids, Fig. 6). Structural- The presence of a marginal wall surround- ly, gnaphosid nests are similar to the ones of ing the basal plate (character 4) is also ple- A. bicolor (a silken tube closed all around) siomorphic for Opisthothelae, but this char- and different from salticid nests, which are acter disappeared independently at least 5 composed of two interconnected silken sheets, times (Fig. 6). The marginal wall is extremely 98 THE JOURNAL OF ARACHNOLOGY

Figure 6.ÐProbable evolution of maternal behavioral characters among Opisthothelae. Data on Appen- dix 2 were mapped onto the family cladogram proposed by Coddington & Levi (1991), modi®ed at the araneid node by means of the cladogram proposed by Scharff & Coddington (1997). Ⅵ ϭ synapomorphy; ᮄ Ⅺ ϭ plesiomorphy or reversion; ϭ polymorphism; ``?'' ϭ unknown; ``*'' ϭ nonapplicable.

variable in size, ranging from 1.5 cm high in acters have appeared simultaneously and in- P. viridans (Randall 1977) to a subtle, almost dependently in three taxa: among mygalo- imperceptible ridge in Schizocosa crassipes morph spiders [they also occur in Vitalius Walckenaer 1837 (Montgomery 1903). In this sorocabae Mello-LeitaÄo 1923 (HFJ, last case, some authors may have simply over- pers.obs.)], in Cyrtophora moluccencis Doles- looked this delicate feature, and it is possible chall 1857, and at the node Pisauridae plus that more careful observations will reveal its Lycosidae (BuÈcherl 1951; Berry 1983; Mont- existence in many more taxa, thus reducing gomery 1903, 1909). If a spider detaches the the level of homoplasy in this character. eggsac from the substrate, she will also wrap After covering the eggsac, some spiders de- it afterwards, but the reverse is not true: ther- tach it from the substrate (character 5) and idiids and liocranids (Agroeca brunnea Black- wrap it all around (character 6). These char- wall 1833) wrap the eggsac while it is still JAPYASSU ET AL.ÐEVOLUTION OF MATERNAL CARE 99 hanging from the upper substrate (Montgom- LITERATURE CITED ery 1903; Ewing 1918; Bonnet 1935; Holm Atz, J.W. 1970. The application of the idea of ho- 1940). mology to behavior. Pp.53±74. In Development Although egg guarding (character 7) is a and Evolution of Behavior: Essays in the Mem- plesiomorphic behavior for Opisthothelae, it ory of T.C. Schneirla. Aronson, L.; E. Tobach; has been lost at least three times, and its ab- D. Lehrman & E.H. Rosenblatt (Eds.). Freeman, sense is a putative synapomorphy for a large San Francisco. group of families, the araneoids. These web Austin, A.D. & D.T. Anderson. 1978. Reproduction building spiders may place the eggsac either and development of the spider Nephila edulis (Araneae: Araneidae). Australian Journal of Zo- far from or near their web, sometimes even at ology 26:501±518. the periphery of the trap, but usually do not Berry, J.W. 1983. The egg laying process in the maintain close, persistent contact with it as micronesian orb-weaving spider, Cyrtophora other spiders do (Montgomery 1903; Bonnet moluccensis (Araneae, Araneidae). Proceedings 1925, 1935; Austin & Anderson 1978; Gobbi of the Indiana Academy of Science 93:149. et al. 1979). Since uloborids, the outgroup of Bonnet, P. 1925. Sur la ponte des oefs chez Argiope araneoids (Griswold et al. 1998), still preserve bruennichi Scl. (AraneÂide). Bulletin de la SocieÂteÁ the plesiomorphic egg guarding behavior entomologique de France:51±54. [Miagrammopes animotus Chickering 1968 Bonnet, P. 1935. Theridion tepidariorum C.L. guards her eggsac until the emergence of the Kock: araigneÂe cosmopolite: reÂpartition, cycle vital, moeurs. Bulletin de la Societe d'Histoire spiderlings (Opell 2001)], it is possible that Naturelle de Toulouse 68(4):335±386. this behavior has been lost at the araneoid Brown, J.H. 1975. The Evolution of Behavior. W.W. node. Norton, New York. This analysis reveals that maternal behav- BuÈcherl, W. 1951. Sobre o geÃnero Grammostola Si- ioral characters are conservative among Op- mon (1892). Monogra®as do Instituto Butantan isthothelae, useful for the grouping not only 1:1±203. of families, but also of higher order ranks, BuÈcherl, W. 1962. Aranhas do geÃnero Loxosceles e such as araneoids and Pisauridae plus Lycos- Loxoscelismo na AmeÂrica do Sul. MemoÂrias do idae. It is surprising that behavioral characters, Instituto Butantan 30:167±186. frequently considered labile features to be BuÈcherl, W. 1964. Biologia de artroÂpodos pecËon- hentos. MemoÂrias do Instituto Butantan 31:85± avoided in phylogenetic contexts (Atz 1970; 94. Brown 1975), present such a conservative Cangialosi, K.R. & G.W. Uetz. 1987. Spacing in evolutionary pattern. Nevertheless, the hy- colonial spiders: effect of environment and ex- potheses herein discussed about the evolution perience. Ethology 76:236±246. of behavioral characters are based on a still Castanho, L.M. & P.S. Oliveira. 1997. Biology and scattered database: many families are not in- behavior of the neotropical ant-mimicking spider cluded in the analysis, or are represented by Aphantochilus rogersi (Araneae, Aphantochili- just a few species. Furthermore, it must be dae): nesting, maternal care and ontogeny of ant- clear that such hypotheses are always just as hunting techniques. Journal of Zoology (London) good as the phylogenies they rely on, because 242(4):643±650. Christenson, T.E. & P.A. Wenzl. 1980. Egg-laying changes in the cladistic structure entail chang- of the golden silk spider, Nephila clavipes L. es in the evolutionary hypotheses (Ryan (Aranea, Araneidae): functional analysis of the 1995). Maternal behaviors have proved to be eggsac. Behaviour 28:1110±1118. useful at the phylogenetic level, but much Clark, R.J. & R.R. Jackson. 1994. ,a work is necessary to gather enough informa- cannibalistic jumping spider, discriminates be- tion for a comprehensive analysis within Ar- tween own and foreign eggsacs. International aneae. Journal of Comparative Psychology 7(1):38±43. Coddington, J.A. & H.W. Levi. 1991. Systematics ACKNOWLEDGMENTS and evolution of spiders (Araneae). Annual Re- We thank Petra Sierwald, Robert Suter, Ro- view of Ecology and Systematics 22:565±592. Crome, W. 1956. Kokonbau und Eiablage einiger geÂrio Bertani and an anonymous reviewer for Kreuzspinnenarten des Genus Araneus (Araneae, helpful commentaries. The senior author re- Araneidae). Deutsche entomologische Zeitschrift ceived ®nancial support from ``FundacËaÄo de 3:28±40. Amparo aÁ Pesquisa do Estado de SaÄo Paulo'' Delgado, A. 1966. InvestigacioÂn ecoloÂgica sobre (FAPESP No. 1999/04442-9). Loxosceles ru®pes (Lucas), 1834 en la regioÂn 100 THE JOURNAL OF ARACHNOLOGY

costera del PeruÂ. MemoÂrias do Instituto Butantan Jackson, R.R. 1986. Silk utilisation and defensive 33(3):683±688. behavior of Thiania, an iridescent jumping spider Eason, R.R. 1969. Life history and behavior of Par- (Araneae: Salticidae) from Malaysia. New Zea- dosa lapidicina Emerton. Journal of the Kansas land Journal of Zoology 13:553±561. Entomological Society 42:339±360. Jackson, R.R. 1990a. Comparative study of lysso- Emerton, J.H. 1877. Cocoon-making and egg-lay- manine jumping spiders (Araneae: Salticidae): ing of spiders. Psyche 2:33±34. silk use and predatory behavior of Asemonea, Evans, T.A. 1998a. Factors in¯uencing the evolu- Goleba, Lyssomanes, and Onomatus. New Zea- tion of social behavior in Australian crab spiders land Journal of Zoology 17:1±6. (Araneae: Thomisidae). Biological Journal of the Jackson, R.R. 1990b. Predatory and nesting behav- Linnean Society 63:205±219. ior of Cocalus gibbosus, a spartaeine jumping Evans, T.A. 1998b. Offspring recognition by moth- spider (Araneae: Salticidae) from Queensland. er crab spiders with extreme maternal care. Pro- New Zealand Journal of Zoology 17:483±490. ceedings of the Royal Society (London) B 265: Jackson, R.R. 1990c. Predatory and silk utilisation 129±134. behavior of Gelotia sp. indet. (Araneae: Saltici- Evans, T.A., E.J. Wallis, & M.A. Elgar. 1995. Mak- dae: ), a web-invading aggressive ing a meal of mother. Nature 376:299. mimic from . New Zealand Journal of Ewing, H.E. 1918. The life and behavior of the Zoology 17:475±482. house spider. Proceedings of the Iowa Academy Jackson, R.R. & S.E.A. Hallas. 1986a. Predatory of Science 25:177±204. versatility and intraspeci®c interactions of spar- Fink, L.S. 1986. Costs and bene®ts of maternal be- taeine jumping spiders (Araneae: Salticidae): havior in the green lynx spider (Oxyopidae, Peu- Brettus adonis, B. cingulatus, Cyrba algerina, cetia viridans). Animal Behaviour 34:1051± and Phaeacius sp. indet. New Zealand Journal of 1060. Zoology 13:491±520. Fink, L.S. 1987. Green lynx spider eggsacs: sources Jackson, R.R. & S.E.A. Hallas. 1986b. Comparative of mortality and the function of female guarding biology of Portia africana, P.albimana, P. ®m- (Araneae, Oxyopidae). Journal of Arachnology briata, P. labiata, and P. shultzi, araneophagic, 15:231±239. web-building jumping spiders (Araneae: Saltici- Fischer, M.L. 1996. Biologia e ecologia de Loxos- dae): utilisation of webs, predatory versatility, celes intermedia Mello-LeitaÄo, 1934 (Araneae, and intraspeci®c interactions. New Zealand Jour- Sicariidae), no municõÂpio de Curitiba, PR. Dis- nal of Zoology 13:423±489. sertacËaÄo de MestradoÐZoologia, Universidade Jackson, R.R. & D. Pollard. 1996. Predatory be- Ferderal do ParanaÂ. havior of jumping spiders. Annual Review of En- Galiano, M.E. 1967. Ciclo biologico e desarollo de tomology 41:287±308. Loxosceles laeta (Nicolet 1849). Acta Zoologica Jorge, M.T., V.R.D. Eickstedt, I. Knysak, L.F.Z. Fis- Lilloana 23:431±464. man, & L.A. Ribeiro. 1991. Acidentes por picada Gobbi, N., R. Zucchi, & S.F. Sakagami. 1979. Gen- de aranha. Arquivos Brasileiros de Medicina eral behavioral patterns and life-cycle of the co- 65(5):457±468. lonial spider, Eriophora bistriata (Araneida: Ar- Kim, K.W., C. Roland, & A. Horel. 2000. Func- giopidae). Boletim de Zoologia (Universidade de tional value of matriphagy in the spider Amau- SaÄo Paulo) 4:65±74. robius ferox. Ethology 106:729±742. Griswold, C.E., J.A. Coddington, G. Hormiga, & Krafft, B., A. Horel, & J.M. Julita. 1986. In¯uence N. Sharff. 1998. Phylogeny of the orb-web build- of food supply on the duration of the gregarious ing spiders (Araneae, Orbiculariae: Deinopoidea, phase of a maternal-social spider, Coelotes ter- Araneoidea). Zoological Journal of the Linnean restris (Araneae, Agelenidae). Journal of Arach- Society 123:1±99. nology 14:219±226. Hallas, S.E.A. & R.R. Jackson. 1986. A compara- Kullmann, E.J. & W. Zimmermann. 1974. Regur- tive study of Old and New World Lyssomanines gitationsfuÈtterung als Bestandteil der BrutfuÈrsor- (Araneae: Salticidae): utilisation of silk and pred- ge bei Haubennetz und RoÈhrenspinnen (Araneae, atory behavior of Asemonea tenuipes and Lys- Theridiidae und Eresidae). Proceedings of the In- somanes viridis. New Zealand Journal of Zool- ternational Arachnological Congress 6:1125± ogy 13:543±551. 1146. Holm, A. 1940. Studien uÈber die Entwicklung und Levi, H.W. & L.R. Levi. 1969. Eggcase construc- Entwicklungsbiologie der Spinnen. Zoologiska tion and further observations on the sexual be- Bidrag fran Uppsala 19:1±213. havior of the spider Sicarius (Araneae: Sicari- Ito, C. & A. Shinkai. 1993. Mother young interac- idae). Psyche 76:29±40. tions during the brood-care period in Anelosimus Li, D., R.R. Jackson, & A.T. Barrion. 1999. Parental crassipes (Araneae, Theridiidae). Acta Arach- and predatory behavior of Scytodes sp., an ara- nologica 42(1):73±81. neophagic spitting spider (Araneae: Scytodidae) JAPYASSUÂ ET AL.ÐEVOLUTION OF MATERNAL CARE 101

from the . Journal of Zoology (Lon- Stegodyphus lineatus (Eresidae). Animal Behav- don) 247:293±310. iour 54:305±312. Montgomery, T.H. 1903. Studies on the habits of Suter, R.B., G. Doyle, & C.M. Shane. 1987. Ovi- spiders, particularly those of the mating period. position site selection by Frontinella pyramitela Proceedings of the Academy of Natural Sciences (Araneae, Linyphiidae). Journal of Arachnology of Philadelphia:59±149. 15:349±357. Montgomery, T.H. 1907. The sex ratio and cocoon- Warburton, C. 1891. The oviposition and cocoon- ing habits of an aranead and the genesis of sex weaving of labyrinthica. The Annals ratios. Journal of experimental Zoology 5:429± and Magazine of Natural History 6(8):113±117. 452. Wenzel, J.W. 1992. Behavioral homology and phy- Montgomery, T.H. 1909. Further studies on the ac- logeny. Annual Review of Ecology and System- tivities of araneads, II. Proceedings of the Acad- atics 23:361±381. emy of Natural Sciences of Philadelphia:458± Whitcomb, W.H. 1962. Eggsac construction and 569. oviposition of the green lynx spider, Peucetia Morse, D.H. 1992. Predation on dispersing Misu- viridans (Oxyopidae). Southwestern Naturalist 7: mena vatia spiderlings and its relationship to ma- 198±201. ternal foraging decisions. Ecology 73(5):1814± Whitcomb, W.H., M. Hite, & R. Eason. 1966. Life 1819. history of the green lynx spider, Peucetia viri- Opell, B.D. 2001. Eggsac recognition by female dans. Journal of the Kansas Entomological So- Miagrammopes animotus. Journal of Arachnol- ciety 39:259±267. ogy 29:244±248. Willey, M.B. & P.H. Adler. 1989. Biology of Peu- Pokrowsky, V.S. 1899. Beobchtungen uÈber das cetia viridans (Araneae, Oxyopidae) in South Carolina, with special reference to predation and Eierablegen bie Pholcus. Zoologischer Anzeiger maternal care. Journal of Arachnology 17:275± 22:270. 284. Pollard, S.D. 1984. Egg guarding by Clubiona cam- bridgei (Araneae, Clubionidae) against conspe- ci®c predators. Journal of Arachnology 11:323± 326. APPENDIX 1. Randall, J.B. 1977. New observations of maternal Description of behavioral characters and de®nition care exhibited by the green lynx spider, Peucetia of character states. viridans Hentz (Araneidae, Oxyopidae). Psyche 84:286±291. Character 1. Nest for the eggsac: (0) absent; (1) Richman, D.B. & R.R. Jackson. 1992. A review of present. There is considerable structural variation the ethology of jumping spiders (Araneae, Sal- among nests; as a rule they are built before eggsac ticidae). Bulletin of the British Arachnological construction, and they are larger than the female. Society 9(2):33±37. Salticids usually present open nests, with one to Rinaldi, I.M.P., L.C. Forti, & A.A. Stropa. 1997. On many ways out; gnaphosids and segestriids build the development of the brown spider Loxosceles closed nests, and stay in them until the emergence of the spiderlings. Despite the variations in nest gaucho (Araneae, Sicariidae): the nympho-ima- structure, all of them had at least an upper and a ginal period. Revista Brasileira de Zoologia 14: lower substrate, usually made up of silken sheets 697±706. [but see Jackson (1986) for a nest almost without Rinaldi, I.M.P. & A.A. Stropa. 1998. Sexual behav- silk, between two leaves, built by the spider Thiana ior in Loxosceles gaucho. Bulletin of the British demissa Thorell 1892]. Arachnological Society 11(2):57±61. Character 2. General eggsac building sequence: Roland, C., J.L. Gundermann, & A. Horel. 1996. base/oviposition/cover; (0) absent; (1) present. This Maternal state induction in female spiders by the is a widespread character: the spider starts building young. Behavior 133:1125±1131. a base silken sheet, deposits the eggs onto it and Ryan, M.J. 1995. Phylogenetics in behavior: some builds a silken cover sheet onto the egg mass. This cautions and expectations. Pp.1±21. In Phyloge- character was scored as present if these three steps nies and the comparative method in animal be- were all present, and were performed in this order, havior. E.P. Martins (ed.). Oxford University notwithstanding the existence of intermediate steps, Press, Oxford. like the building of a silken wall (see below) onto Scharff, N. & J.A. Coddington. 1997. A phyloge- the base, before egg-laying. netic analysis of the orb-weaving spider family Character 3. Shape of the base: (0) silken sheet, Araneidae (Arachnida, Araneae). Zoological sometimes with a cushionlike mat of curled strands Journal of the Linnean Society 120:355±434. of silk; (1) cushionlike mat of curled strands of silk. Schneider, J.M. & Y. Lubin. 1997. Infanticide by Most spiders present the single sheet state of the males in a spider with suicidal maternal care, character. 102 THE JOURNAL OF ARACHNOLOGY

Character 4. Marginal wall: (0) absent; (1) pres- Character 7. Eggsac guarding: (0) absent; (1) ent. After building the basal plate, some spiders present. This behavior varies strongly, for the spider spin at its perimeter a wall of curled loops of silk. may carry the eggsac on the chelicerae (like phol- This is built with up and down movements of the cids), on the spinnerets (like lycosids) or may not abdomen, while the spider slowly rotates her body carry it at all, in which case she may stay contin- and touches the opposite side of the basal plate with uously in touch with it until the emergence of the the tip of the palpi. This silken wall can be a clearly spiderlings, or even make foraging trips and then visible structure (as in Sicarius sp., Levi & Levi return to the eggsac. For the sake of simplicity, and 1969), but it is sometimes rather dif®cult to see. We due to the incompleteness of many descriptions, we only scored this character as present when explicitly decided to score all these instances merely as the described by the author or clearly distinguishable in presence of eggsac guarding behavior. pictures or photographs. Character 5. Free eggsac from substrate: (0) no; (1) yes. After building the cover plate, some spiders APPENDIX 2. remove the whole structure from the substrate with Matrix of spider species versus characters for legs I and/or chelicerae. Species that have the egg- maternal behaviors. sac ®rmly adhered to the substrate pull the basal plate from the substrate with legs I. Species that If the species name has changed, the old name is hang the eggsac from the web merely cut the sus- also cited. Only species for which there is infor- pension threads with the chelicerae. Once the egg- mation on at least 2 characters were included. Data sac has been removed from the substrate, the spider were compiled based mainly on original descrip- handles it freely with legs II, III and IV. tions and, in a few cases on informative illustra- Character 6. Final eggsac wrapping: (0) absent; tions. Character 1 ϭ eggsac nest; character 2 ϭ (1) present. After covering the eggmass with a sheet base/eggs/cover building sequence; character 3 ϭ of threads (cover plate), some spiders envelop the base shape; character 4 ϭ marginal wall; character whole structure (basal plate included) with a ®nal 5 ϭ free eggsac from substrate; character 6 ϭ ®nal silken protection. Note that the cover plate never wrapping; character 7 ϭ eggsac guarding. See Ap- enwraps the whole structure, but is built over the pendix 1 for character descriptions and de®nitions basal plate and eggmass. This behavior may be of states. ``?'' ϭ unknown; ``*'' ϭ nonapplicable; somewhat simpli®ed in some taxa, as is the case for ``v'' ϭ polymorphism. Pardosa lapidicina Emerton 1885, which wraps only the junction between the cover and the basal Manuscript received 10 March 2001, revised 11 plate (Eason 1969). February 2002. JAPYASSUÂ ET AL.ÐEVOLUTION OF MATERNAL CARE 103 es marginal wall; ϭ Reference Whitcomb et al. 1966 Montgomery 1909) Emerton 1877 Montgomery 1903 Gobbi et al 1979 Montgomery 1909 Montgomery 1903 Montgomery 1909 Montgomery 1909 Emerton 1877 Holm 1940 Montgomery 1903 Warburton 1891 Montgomery 1903 Crome 1956 Bonnet 1925 Berry 1983 Whitcomb 1962; Eason 1969 Montgomery 1903 Montgomery 1903 Montgomery 1903 Montgomery 1903 Montgomery 1903 Montgomery 1903 Pokrowsky 1899 Pappenheim 1903 (apud Montgomery 1909 Holm 1940 Holm 1940 Montgomery 1909 Jackson 1986 ? ? ? ? ? ? 0 1 0 1 1 1 1 1 0 0 1 1 1 1 1 1 1 1 1 1 1 1 ? ? ? ? ? ? ? ? ? 0 0 1 1 0 0 1 0 1 1 1 1 1 1 0 1 1 0 0 base shape; character 4 ϭ ? ? ? ? ? ? ? 0 0 0 0 0 0 1 1 0 0 1 1 1 1 1 1 0 1 0 0 0 ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? 1 0 1 1 1 1 1 0 1 1 1 1 ? ? ? ? ? ? ? ? 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ? 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 ? 1234567 0 0 0 0 1 0 0 0 0 1 1 1 0 0 0 0 0 0 0 0101001 0 0 1 0101111 v 1 1 1 1 eggsac guarding. See Appendix 1 for character descriptions and ϭ Araneidae Araneidae Araneidae Corinnidae Dictynidae Agelenidea Agelenidae Araneidae Araneidae Araneidae Gnaphosidae Gnaphosidae Gnaphosidae Liocranidae Lycosidae Lycosidae Lycosidae Lycosidae Lycosidae Lycosidae Philodromidae Pholcidae Pisauridae Pisauridae Salticidae Salticidae Salticidae Salticidae polymorphism. base/eggs/cover building sequence; character 3 ϭ ϭ ) ®nal wrapping; character 7 ϭ ) ) ) ) ) nonapplicable; ``v'' ) ) ) Lycosidae ϭ ) ) ) eggsac nest; character 2 Poecilochroa variegata ) ϭ Geotrecha pinnata ) Epeira labyrinthea T. derhami Epeira strix L. punctulata Eriophora bistriata L. ocreata M. rump®i Lycosa stonei Dyctina volupis unknown; ``*'' L. lepida Herpyllus ater ϭ Doleschall 1857 P. nigropalpis Hentz 1847 ( Hentz 1847 ( Clerck 1757 Clerck 1757 Keyserling 1885 Walckenaer 1802 Schrank 1781 Clerck 1757 Clerck 1757 ( Clerck 1757 ( Hentz 1844 ( Keyserling 1887 Walckenaer 1837 ( Scopoli 1772 Hentz 1844 ( Clerck 1757 Clerck 1757 ( Clerck 1757 Rengger 1836 ( Hentz 1832 Oxyopidae Blackwall 1833 Hentz 1850 ( Thorell 1892 Walckenaer 1837 free eggsac from substrate; character 6 Emerton 1885 Species (previous name, if changed) Family Hentz 1832 ( Walckenaer 1837 ( ϭ Hentz 1844 ( Walckenaer 1837 ( Appendix 2.ÐMatrix of spider species versus characters for maternal behaviors. If the species name has changed, the old name is also cited. Only speci character 5 for which thereinformative is illustrations. Character information 1 on at least 2 characters were included. Data were compiled based mainly on original descriptions and, in a few cases on de®nitions of states. ``?'' Agelena labyrinthica Tegenaria domestica Pardosa amentata Agroeca burnnea Zelotes ater Araneus quadratus Argiope bruennichi Cyrtophora moluccensis Prawixia bistriata Emblyna sublata Castianeira longipalpa Sergiolus capulatus Drassodes neglectus Rabidosa punctulata P. milvina P. lapidicina Larinioides cornutus Metepeira labyrinthea Schizocosa ocreata S. avida Dolomedes ®mbriatus Philodromus aureolus Pholcus opilionoides Phidippus purpuratus Thiania demissa Heliophanus cupreus Marpissa muscosa S. crassipes Peucetia viridans Pisaurina mira 104 THE JOURNAL OF ARACHNOLOGY Reference 1918; Bonnet 1935 Ècherl 1951 Ècherl 1951 Jackson 1986 Jackson & Hallas 1986a Jackson 190b Jackson & Hallas 1986a Jackson 1990c Jackson & Hallas 1986b Jackson & Hallas 1986b Jackson 1990a Hallas & Jackson 1986 Jackson 1990a Jackson 1990a Jackson 1990a Jackson 1990a Hallas & Jackson 1986 Jackson 1990a Jackson 1990a Montgomery 1909 Present paper Fischer 1996 Galiano 1967 Delgado 1966 Levi & Levi 1969 Austin & Anderson 1978 Bu Bu Montgomery 1903; Ewing Montgomery 1903 Montgomery 1907 Montgomery 1903 Fabre 1823 Montgomery 1903 ? ? ? 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 1 1 0 0 1 1 ? ? ? ? ? 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 ? ? 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 * 0 0 0 0 0 1 1 0 0 0 1 0 ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? 0 0 0 0 0 0 0 0 0 1 1 1 0 0 1 ? ? ? ? 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 * 0 0 0 0 0 0 0 1 1 0 ? ? 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1 1 1 1 1 1 ? 1234567 1 0 0 0 0 0 1 1 1 1 1 1 1 1 1 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 Salticidae Salticidae Salticidae Salticidae Salticidae Salticidae Salticidae Salticidae Salticidae Salticidae Salticidae Salticidae Salticidae Salticidae Salticidae Salticidae Segestriidae Sicariidae Sicariidae Sicariidae Sicariidae Sicariidae Tetragnathidae Theraphosidae Theraphosidae Theridiidae Theridiidae Theridiidae Theridiidae Thomisidae Thomisidae Appendix 2.ÐContinued. ) ) ) ) ) ) ) ) Onomastus holmi G. longimana Theridion tepidariorum Teutana triangulosa Steatoda marmorata O. nigricauda A. murphyi Koch 1841 ( Xysticus stomachosus Hentz 1850 ( Ausserer 1875 ( Áre 1799 Äo 1934 Simon 1900 ( Pocock 1903 Walckenaer 1802 ( Fabricius 1775 Wanless 1980 ( Âszynski & Zabka 1983 ( Cambridge 1869 Peckham & Peckham 1896 Walckenaer 1837 Gertsch 1967 Thorell 1895 Walckenaer 1805 Wanless 1981 Pro Doleschall 1859 Hentz 1842 Lucas 1846 Labillardie Simon 1885 Thorell 1887 Hentz 1847 ( Mello-Leita sp. 2 Species (previous name, if changed) Family sp. 1 Lucas 1834 sp. 1 Nicolet 1849 sp. sp. Thiania Brettus cingulatus Cocalus gibbosus Cyrba algerina Gelotia Asemonea murphyae Portia ®mbriata Portia labiata Goleba puella Asemonea tenuipes Lyssomanes patens Lyssomanes Tomocyrba holmi Lyssomanes viridis Onomastus nigricaudus Lysssomanes Ariadna bicolor Loxosceles gaucho L. intermedia L. laeta L. ru®pes Sicarius Nephila edulis Grammostola actaeon Grammostola mollicoma Achaeraranea tepidariorum Thomisus onustus Xysticus ferox Enoplognatha marmorata Latrodectus mactans Steatoda triangulosa