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Family Uloboridae the Refationship of Book Lung and Tracheal Systems in the Spider

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Family Uloboridae the Refationship of Book Lung and Tracheal Systems in the Spider JOURNAL OF MORPHOLOGY 206:211-216(1990) The Refationshipof Book Lungand Tracheal Systems in the Spider FamilyUloboridae BRENT D. OPELL nia Po lv t ec hni c l rx t i t ute and s t at e u niue r s it v Bf::I r,i;,', ltt#;Y l ;#F ABSTRACT The book lung surface areas of representatives of six genera were measured and divided by spider prosomal and leg mass and by the product of prosomal length and width to obtain two indexes of book lung area. Both indexesare greatest in speciesthat have the simplest tracheal systemsand smallest in those with the most extensivetracheal systems.When speciesare ordered phylogenetically and the lung area indexes of their hypothetical ancestorscomputed, a transformational increasein lung area is indicated. Neither the lung area of a speciesnor its phyloge- netic position is significantly related to the generalmoisture regime of its habitat. The number of leavesin a book lung is positively correlated with both spider sizeand total lung area. However, leaf number is not correlated with tracheal development and showsno transformational change. The Tracheospira (seruu, Platnick, '77) con- branch to enter the legs. Tracheae entering the tains spiders that have two respiratory compo- prosomaeof Hyptiotes and Miagrammopes have nents: a pair of book lungs that oxygenate the diameters that are, relative to combined proso- hemolymph and a tracheal system that carries mal and leg masses,nearly twice those of Waitk- oxygen directly to tissues. A variety of spider era artd Uloborus (Table 1). This difference is tracheal patterns have been documented and attributed to the fact that they more actively '87; their adaptiveness discussed (Bromhall, monitor and manipulate their reduced prey cap- Opell,'87a). However,the relationship between ture webs(Opell'87a,b). Orb-weavers of the gen- these patterns and book lung development has era Octonoba and Philoponella have tracheae not beenstudied. that are restricted to the opisthosoma (Opell, Spider book lungs residein the anterior, ven- '79). Opell ('79) reported that the tracheolesin tral region of the opisthosoma. Each lung is Octonoba extend into the prosoma, but none formed of a stack of elongate,flattened, cuticle- appeared in cross sections through the pedicels lined leaves,between which hemolymph circu- of North American Octonoba sinensis used in lates.The air spacebetween the two lamellae of this study (unpublished observations). each leaf is maintained by cuticular struts and Comparisons of the relative book lung surface communicateswith a common atrium that opens areasin these taxa make it possibleto determine '67; to the outside via a spiracular slit (Levi, how tracheal development,activity patterns, and '76; '80; Moore, Anderson and Prestwich, Hex- phylogenetic position influence book lung devel- ter,'82). The width of the interlamellar air space opment. If spiders with more extensive tracheal within eachleaf showsa negativeallometric rela- systems have greater book lung surface areas tionship with spider mass, €Lnapparent adapta- than those with more weakly developed tra- tion to reduce the distance over which oxygen cheae,this would suggestthat both systems act must diffuse to reach the hemolymph (Anderson in consort to supply a spider's increasedoxygen and Prestwich,'80). demands.If more extensivetracheal systemsare Members of the family Uloboridae exhibit the associatedwith smaller book lung surface areas, full range of tracheal development found in spi- this would indicate that the tracheae meet more '87). ders (Opell,'79,'87a; Bromhall, The orb- acute or more specific oxygen demands (such as weavinggenera Waitkera and Uloborus, the tri- those imposed by web-monitoring behaviors) angle-weaving genus Hyptiotes, and the and, therefore have assumed a greater role in irregr.rlar-web-weavinggenus Mi agranxnxopesre- meeting a spider's total oxygen demands. Any tain the family's plesiomorphic pattern, charac- transformational changesin book lungs of these terized by two stout tracheal trunks that extend speciesshould be apparent when their relative through the pedicel, into the prosoma, and surface areasare ordered phylogenetically. o 1990WILEY-LISS. INC. TABLE 1. Comparbonof tracheal d.etelnpneat,spider size, booh lungsurface areas,and. interhmellar ah apaNewidth.s (nean t standarddcoiatiaa [sampla size]) Do not enter prosoma Enter prosoma Tracheae, Orb-web Orb-web Reduced-web web type, species P. tingerw O. sinensis W. waitakeriensis U. glomosus M. animotus H. cauatus Pedicle tracheal area'/ prosomal and leg mass 0 0 410 448 76t 840 Carapacelength (pm) 1,460t 158(10) 1,484* 126(10) 1,252r 88 (5) 1,364t 49 (9) 1,507t 112(10) 1,017t 69 (7) Carapacewidth (pm) 1,358t 145(10) 1,394t 134(10) 1,168t 70 (5) 1,171t 45 (9) 1,0?3t 57 (10) 1,151t 32 (7) Prosomal and leg mass (mg) 2.84t 0.95(10) 3.43t 1.25(10) 2.L7t 0.26(7) 1.91t 0.30(9) 2.38t 0.53(10) 1.49t 0.26(7) Book lung leaves 29.4r 6.3(10) 30.9 t 6.7 (9) t7.2x2.8(5) 229 t 2.0(7) 22.4 x3.8(9\ r5.7 t 7.7 (7) Number of lung leaves/ prosomal and leg mass (mg) r0.4x.2.4 (r0) 9.2 r 2.2(9) 8.2t 2.5(5) tr.9 t 2.2 (7) 9.9t 1.0(9) 10.0t 1.9(7) Book lung area (mm') 6.97t 2.55(10) 7.47+ 2.76(9) 2.53 t0.47 (7) 3.77t 0.61(8) 2.98t 0.91(10) 2.08t 0.31(7) Lung area (mm')/ prosomal and leg mass (mg) 2.35r 0.51(10) 2.13r 0.33(9) 1.19r 0.31(5) 1.92t 0.31(8) 1.26t 0.19(10) 1.43x 0.29(7) Lung area Atm')/ ctuapacelength x width 0.83* 0.20(10) 0.87t 0.17(9) 0.4a t 0.08(5) 0.59 t 0.09(8) 0.46t 0.10(10) 0.45 t 0.07(7) Live spider mass (mg) L4.52t 3.63(20) 9.93 r 4.65(45)'z 6.39 t 3.36(37)'? 6.76 t 3.06(42)2 Predicted interlamellar air space width (rrm) 1.6 1.5 1.3 1.3 Measured interlamellar air space width (rrm) 1.5r 0.1(5) 1.3t 0.1(5) 1.2t 0.1(5) 1.5t 0.3(5) 1.5t 0.2(5) r.2 t 0.2(5) '87a. 'Mean valuesfrom Opell, '87b. 'Mean valuesfrom Opell, SPIDER BOOK LUNG SURFACE AREAS 2L3 METHODSAND MATERIALS ment leacheslittle material from tissue.has little Adult females, representing 6 of the 18 de- effect on mass,and coagulateshemolymph, pre- scribed uloborid genera were studied: the orb- venting its loss when a specimen's pedicel is weavers Waitkera waitakeriensis (Chamber- severed.Prior to weighing, specimenswere blot- lain, '46) from northern New Zealand, Uloborus ted and air dried for 30 seconds.The massesof glomosus(Walckenaer, 1841) from Virginia, Oc- eight Miagramnxopes animotus so treated aver- (range tonoba sinensis (Simon, 1880) an introduced aged103 % 95-t05 % ) of their live weights. Asian speciescollected in Virginia, and Philo- Specieswere assignedto one of three groups of increasingtracheal phy- ponella tingena (Chamberlinand Ivie, '36) from development,one of four groups, Panama and Colombia;the irregular-web weaver logenetic and one of three habitatgroups (Fig. M iagrammop es animotus (Chickering,'68)from of increasingmoistureavailability 1). Within limited Hyptiotes Puerto Rico; and the triangle-web weaver Hyp- the context of this study, and Miagrammop es Philoponella Oct onoba tiotes cauatus(Hentz, 1847)from Virginia. These arrd artd are sister taxa, making it inappropriate to assign specieswere identified using the following revi- one member of the pair a more advanced status sions (Muma and Gertsch,'64; Chickering, '68; than the other. One factor analysis of variance Opell,'79;and Yoshida,'80). (ANOVA) and Kruskal-Wallis K-sample rank- The anterior region of the opisthosoma con- ing (K-W) tests were used to determine if tra- taining the book lungs was removed, cleared in cheal type and habitat explained the differences hot l0 (weight/volume) NaOH to remove non- % in relative book lung surface area. chitinous tissue, rinsed in water, and stained to Phylogenetic tracts were evaluated using make the thin book lung leavesvisible. One book ANOVA tests, K-W tests, and transformational lung from in eachspecimen was dissected a drop analysis.The latter approach infers from termi- its isolated leavesflat- of mounting medium and nal (living) taxathe states of hypothetical Ernces- tened under a coverslip. tral taxa and determines if these states exhibit leaves lung The surface areasof the of a book directional changesindicative of an evolutionary were measuredwith a digitizing tablet, summed, trend (Lauder, '81; Huey, '87; Huey and Ben- and this value multiplied by four to obtain a nett,'87). Hypothetical ancestorsare used in an spider's total book lung surface area. The width attempt to neutralizethe unique selectiveforces of the air spaceseparating a leafs lamellae was that have operated on each terminal taxa since photo- measured from compound microscope its origin. I used the following schemeof iterative graphsof a folded leaf (Anderson and Prestwich, '80). averaging to determine the states of hypotheti- The shapeof a species'booklung leaveswas cal ancestorsHr-Hn. reconstructed from outline drawings of one of the three largest leavesof five specimensof each H1: Hyptiotes + Miagrammopes/2. species.A midline was drawn from a leafs tip to Hz: (Ht + Waitkera) + (Hr + Uloborw) the center of a line connecting the corners of its + (Waitkera + Uloborus)/6. base.The perpendicular distance from this mid- He: (Hr + Uloborus) + (Uloborus + Octonoba) line to the leafs left and right margins was mea- + (Hr + Octonoba)/6. sured at 15 equidistant points (Fig.
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