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Influence of Web-Monitoring Tactics on the Density of Mitochondria

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Influence of Web-Monitoring Tactics on the Density of Mitochondria JOURNAL OF MORPHOLOGY2t3:34t-347 (1992) Influenceof Web-MonitoringTactics on the Densityof Mitochondriain LegMuscles of theSpider Family Uloboridae BRENT D. OPELL ANo DAVID C, KONUR ni a Po t v t ec h n i c I ns t i t ut e qn d s tat e (rn iu e r si tv, Er:ff:w, {,i;: l:y; [; ;ri ABSTRACT From electron micrographs we determined the ratio of mitochon- drial to myofibril cross sectional area in cells of the first leg anterior depressor muscles of adult females of four spider species, each from a different genus. Specieswith more active web-monitoring tactics and greater tracheal supplies to their first legs have muscle cells that are better supplied with mitochondria than those with less active tactics and less well-developed tracheal systems. These results demonstrate that, even in homologous tissues of closely related species,mitochondrial supply can change to accommodate changesin metabolic activity. o 1992Wiley-Liss, Inc. Mitochondria are the sites of oxidative single monitoring line and shake the web '87a).In phosphorylation and are found in greater when a prey strikes it (Opell, both numbers in more active tissues.For example, orb-web and reduced-web spiders, the first in insects mitochondrial densitv is low in legs play an important role in web monitor- small visceral muscles and inactive fat cells ing and manipulation. (Dean '85; '68; 'ZB) et al., Smith, Sohal, and As summarized in Table 1, previous stud- high in metabolically active tissues such as ies show that these differences in web-moni- flight muscles (Chapman,'54; Edwards and toring tactics are reflected in both the web- Ruska, '55; Levenbook '56; and Williams, monitoring force expressed by a species and Smith, '62), (Smith, '68; Malpighian tubules the degree of its tracheal development (Opell, Wigglesworth and Salpeter, '62), '87a,b). and anal Hyptiotes cauatus has the greatest papillae (Copeland,'64). The purpose of this absolute and relative resting forces (force study is to determine if changes in mitochon- exerted on a single, resting thread) and also drial density accompany diverging activity the greatest tracheal supply to its first legs levels in homologous arthropod muscles. We (i.e., the smallest volume of tissue served do this by comparing the mitochondrial sup- by each pm2 of tracheal cross plies of the leg muscles of spiders that have section). Uloboru,s glomosus has the next greatest different web-monitoring tactics. resting force and the next greatest The orb-web is the primitive web form in first leg tracheal sup- the family Uloboridae (Coddington, '86, 'g0; ply, followed by Miagrammopes animotus. '79). Opell, Members of orb-weaving genera The tracheal spiracle of uloborids is near the such as Uloborus and Octonoba hang be- abdomen's posterior tip and the long abdo- neath the hubs of their horizontal webs while men of M. animolzs reduces the first leg's '86; waiting for prey (Lubin, Cushing and oxygen supply by increasing tracheal length '90; '88). Opell, Peaslee and Peck, In con- and, thereby, the distance over which oxygen trast, species that construct reduced webs must diffuse. The resting force expressed by more actively monitor and manipulate them Octonoba sinensis has not been measured during prey capture. Members of the genus and attempts to do so for this study proved Hyptiotes spin taut, vertical triangle-webs unsuccessful, as spiders hung for only a few wtrich they monitor from the anchoring point secondson resting threads and failed to estab- of the web's apex thread (Lubin, '86; lish stable resting forces. However, as '82). Opell, this Members of the genus MiagratnnLopes species' tracheal system is restricted to its '90b) construct irregular webs that have one to abdomen (Opell, and its prosomal and eight prey capture lines that diverge at vary- legmuscles are supplied solelyby '86;Lubin hemolymph ingangles(Lubin, et al., '78; '90a). Opell, borne oxygen, it probably exerts less monitor- Like Hyptiotes, these spiders uJe a ing force than the other three species. o 1992 WILEY-LISS, INC. 342 B.D. OPELL AND D.C. KONUR TABLE 1. Comparison of the mean leg uolumes, messes,tracheal areas, and resting forces of adult female uloborids Hyptiotes Uloborus Miagrammopes Octonoba cavatus glomosus animotus sinensis Leg I volume x 104pm3 1 27,438 48,822 104,188 Prosomal and leg weight mg3 L.49 1.91 2.38 g.as RestingforceN x 10-52 13.42 r0.72 7.09 Resting forcelleg I volume x 10 a/mm3 4.89 2.02 0.68 Resting force/prosomal and leg weight 9.01 5.61 2.89 Tracheal area serving leg I pm2 t 387 289 891 n Leg I volume/leg I tracheal arealsquare root distance 3,239 8,565 7,180 0 from spiracle to leg I1 rOpell,'87b. 2Opell,'87a. 3Opell,'90. Becausethe first legs are important in web make them easy to identify, isolate, and han- monitoring, the activity level of their mus- dle and because their role as flexors of the cles, as predicted by a species' resting force patella is important for the leg movements and tracheal supply, should be reflected in associatedwith web monitoring and manipu- their mitochondrial supply. This study will lation. test the hypothesis that the density of mito- The ADDM were post-fixed for 30 min in chondria in first leg muscles is ordered, from 17oosmium tetroxide, washed with sodium gTeatest to least, as follows: Hyptiotes caua- cacodylate buffer for 5 min, and dehydrated tus, Uloborus glomosus, Miagrammopes ani- through a series of ethanol dilutions. Mus- motus, Octonobasinensis. cles were then infiltrated with Spurr's epoxy resin (hard formula) and polymerized for 24 MATERIAISAND METHODS hr at 65'C. Thin cross and longitudinal sec- Adult females of the following specieswere tions were stained with lead citrate and ura- used in this investigation: the introduced nyl acetate and examined and photographed Asian orb-weaver, Octonoba sinensis (Si- at x 1,600-3,300 with a transmission elec- mon), collected from free ranging popula- tron microscope. tions in greenhouses at Virginia Polytechnic Enlarged cross sectional photographs of Institute and State University (VPISU); the individual muscle cells (Fig. 1) were mea- eastern North American orb-weaver, Ul- sured with a digitizing tablet connected to a oborusglomosus (Walckenaer),collected from computer. We first determined the cell's total shrubbery on the VPISU campus; the east- surface area (TA), the combined surface ar- ern North American triangle-web-weaver, eas of its mitochondria (MA), the surface Hyptiotes cauatus (Hentz), collected in the area of its central clear region where a nu- forests of Montgomery and Craig Counties of cleus was often found (CA), and the com- Virginia; and the Puerto Rican "single-line- bined surface areas of the mitochondria found weaver," Miagramm,opes animotus Chicker- within the central clear region (CMA). '68, We ing, collected at the Center for Energy used the following formula to determine the and Environment Research's El Verde field area occupied by a cell's contractile elements station in the Luquillo National Forest. These (CEA): species were identified by reference to the CEA: TA - CA- (MA- taxonomic revisions of Chickering ('68), CMA) Muma and Gertsch ('64), Opell ('79), and However, in addition to myofibril bundles, Yoshida('80). this cortex region (: CEA) also contains sar- Specimens were anesthetized with carbon coplasmicreticula, T-system tubules, and in- dioxide, fixed at 20-26"C for 12-18 hr in 3Vo tracellular space(Figs. L, 2). We determined glutaraldehydel}o/o formaldehyde in 0.1 M the density of myofibrils within the CEA sodium cacodylatebuffer (pH 7.3), and rinsed (NIYD) by dividingthe total area of a represen- in 0.1 M sodium cacodylate buffer. First legs tative cortex region into the total area occu- were removed at the trochanter and their pied by this region's myofibril bundles. We retrolateral and prolateral anterior dorsal de- then multiplied each cell's CEA by its NIYD pressor muscles (ADDM; Whitehead and to determine its corrected total myofibril sur- '59) Rempel, were exposed.We chose these face area (CMYA). When CMYA is divided by muscles becausetheir large size and position MA it yields an index of how densely a cell's MITOCHONDRIAL DENSITY IN SPIDER LEG MUSCLES 343 -w.# ''i:t& i*F',; Fig. 1. Cross section of the first leg anterior dorsal Fig. 2. Longitudinal section of the first leg anterior depressormuscle of Uloborus glomosus. CA, central clear dorsal depressor muscle of Uloborus glomosus. M, mito- area; M, mitochondria; MYO, myofibrils; N, nucleus; T, chondria; MYO, myofibrils. tracheole. 344 B.D. OPELL AND D.C. KONUR myofibrils are supplied by mitochondria. The M : Miagrammopes, lJ : Uloborus, and O : larger this index, the greater the cell's mito- Octonoba: chondrial supply. Hr : (H + M) + (H + (U + Ol2))+ (M + (U + o^12))16 This method assumes that the mitochon- Hz: (U + O)+ (U + (H + Mlz))+ (O+ (H +Ml2))16 dria of all species have similar shapes. If a species' mitochondria are greatly elongated He:Hr +Hrl2 in the longitudinal dimension (Fig. 2) this We inferred the resting force and tracheal method might underestimate that species' supply of the common ancestor of Hyptiotes mitochondrial surface area. We evaluated andMiagrarllrnopes from the mean values of each species'mitochondrial shapeby measur- Waitkera waitakerensis, an orb-weaver that ing the maximum and minimum dimensions is a primitive member of the outgroup of the of mitochondria in cross and longitudinal four species included in this study, and Ul- sectionsof muscle cells (Figs. 1, 2). We mea- oborus glornosus, the most primitive member sured either all of the mitochondria in a cell of the outgroup of the Hyptiotes-Miagram- (or, in the caseof longitudinal sections, all of nxopesclade (Coddington, '90).
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