Apr 2, 1986 - at 0.35 x lo9 N mP2 and spiral pre-stress was set at approximately zero ...... data are needed, this equation, equivalent to the power formula, Y= ...
Biological Journal of the Linnean Society (1987), 30: 135-162. With 6 figures
The ecological and evolutionary interdependence between web architecture and web silk spun by orb web weaving spiders CATHERINE L. CRAIG* Department of Biology, Osborn Memorial Laboratories, Tale Universily, P . 0 . Box 6666, N e w Haven, Connecticul 06511-8122, U.S.A. Received 2 April 1986, accepted for publication 23 October 1986
Spider orb webs are dynamic, energy absorbing nets whose ability to intercept prey is dependent on both the mechnical properties of web design and the material properties of web silks. Variation in web designs reflects variation in spider web spinning behaviours and variation in web silks reflects variation in spider metabolic processes. Therefore, natural selection may affect web function (or prey capture) through two independent and alternative pathways. I n this paper, I examine the ways in which architectural and material properties, singly and in concert, influence the ability of webs to absorb insect impact energy. These findings are evaluated in the context of the evolution of diverse aerial webs. O r b webs range along a continuum from high to low energy absorbing. No single feature of web architecture characterizes the amount of energy webs can absorb, but suites of characters indicate web function. I n general, webs that intercept heavy and fast flying prey (high energy absorbing webs) are large, built by large spiders, suspended under high tension and characterized by a ratio of radii to spiral turns per web greater than one. In contrast, webs that intercept light and slow flying prey (low energy absorbing webs) are suspended under low tension, are small and are characterized by radial to spiral turn ratios that are less than one. The data suggest that for spiders building high energy absorbing webs, the orb architecture contributes much to web energy absorption. I n contrast, for spiders that build low energy absorbing webs, orb architecture contributes little to enhance web energy absorption. Small or slow flying insects can be intercepted by web silks regardless of web design. Although there exists variation in the material properties of silk collected from high and low energy absorbing webs, only the diameter of web fibres varies predictably with silk energy absorption. Web fibre diameter and hence the amount of energy absorbed by web silks is an isometric function of spider size. The significance of these results lies in the apparent absence of selective advantage of orb architecture to low energy absorbing webs and the evolutionary trend to small spiders that build them. Where high energy absorption is not an exacting feature of web design, web architecture should not be tightly constrained to the orb. Assuming the primitive araneoid web design is the orb web, I propose that the evolution of alternative web building behaviours is a consequence of the general, phyletic trend to small size among araneoids. Araneoids that build webs of other than orb designs are able to use new habitats and resources not available to their ancestors.
KEY WORDS: -Araneoidea - orb web - architecture absorbing - prey capture - scale.
- silks -
high energy absorbing - low energy
CONTENTS Introduction . . . . Study Sites and Organisms.
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C. L. CRAIG Methods . . . . . . . . . . . . . . . . . Rankings of web energy absorbing capabilities . . . . . . . Artificial loading experiments . . . . . . . . . . . Contribution of web architecture to energy absorption . . . . . Contribution of web silks to energy absorption . . . . . . . Results . . . . . . . . . . . . . . . . . Rankings of web energy absorbing capabilities . . . . . . . Contribution of web architecture to energy absorption . . . . . Contribution of web silks to energy absorption . . . . . . . Discussion . . . . . . . . . . . . . . . . . Rankings of web energy absorbing capabilities . . . . . . . Contribution of web architecture to energy absorption . . . . . Contribution of web silks to energy absorption . . . . . . . Interaction between web architecture and silks in spider web function . The evolution of Araneoid foraging strategies . . . . . . . Acknowledgements . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . .
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137 137 137 140 144 147 147 149 154 157 157 157 158 158 159 160 160
INTRODUCTION
Many authors have studied the foraging ecology of orb web weaving spiders from the perspective that orb webs are adapted to sieve insects from surrounding airstreams (Kajak, 1965; Dabrowska-Prot & Luczak, 1968; Langer, 1969; Kiritani, Kawahare, Sasaba & Nakasuja, 1972; Uetz, Johnson & Schemske, 1978; Nyffeler & Benz, 1978, 1979; Eberhard, 1981; Riechert & Luczak, 1982; Wise & Barata, 1983). The assumption underlying this point of view is that the number of prey captured simply reflects the density of available insects of body lengths greater than or equal to the distance between turns of the web’s spiral fibre (Pointing, 1966; Robinson & Robinson, 1970, 1973; Uetz et al., 1978; Wise & Barata, 1983). This oversimplification of spider prey capture has led to nongeneralizable results (i.e. Robinson & Robinson, 1970; Uetz et al., 1978; Shelly, 1983), and an inability to outline the ecological differences among coexisting araneoid spiders (Wise & Barata, 1983). Prey capture at spider webs is best thought of as a three step process. From the viewpoint of an individual insect, capture probability is a product of (1) the probability of contact with the web (Chacon & Eberhard, 1980; Nentwig, 1983; Rypstra, 1982; Craig, 1986), (2) the probability that after insect and web make contact, the web is able to absorb the prey’s kinetic energy (Denny, 1976) without breaking, and (3) the probability that the insect will adhere to the web’s surface (e.g. Nentwig, 1982). Each of these probabilities depends upon prey flight behaviour and mass. The ability of a web to withstand insect impact is a function of web architecture, the material properties of web silks and the interaction between web materials and design. The more exacting the functional interdependence between the design of webs and the properties of web silks, the greater the constraint on their evolutionary diversification. While variability in web architecture reflects variation in spider web spinning behaviours, variability in the mechanical properties of web silks reflects variation in spider metabolic processes. I propose that web design and web silks can be viewed as two independent and alternative pathways through which natural selection may act to affect the kinds of insects webs intercept or the foraging ecology of coexisting araneoids. In this paper I examine the ways in which architectural and material properties, singly and in concert, influence the web’s ability to absorb insect
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impact energies. I use these data to interpret the potential for evolutionary diversification of spider foraging modes. This approach demands that the focus of the insect-web interaction be the entire web and not just the few fibres an insect may actually contact. STUDY SITES AND ORGANISMS
I collected data on the architectural and material properties of webs built by species in five different genera of orb-weaving spiders (Fig. 1). Studies on webs were done on Barro Colorado Island, Republic of Panama (9"09'N,79"5I'W). All spiders included in this research are members of the superfamily Araneoidea. Epilineutes globosus (0.Pickard-Cambridge) is a member of the family Theridiosomatidae. Leucauge globosa (0.Pickard-Cambridge) , Cyclosa caroli (Hertz), Mangora pia (Chamberline & Ivie) and Micrathena schreibersi (Perty), are members of the family Araneidae. Voucher specimens of the spiders are deposited at the Museum of Comparative Zoology, Harvard University. The forest on Barro Colorado Island is classified as tropical moist forest on the basis of the Holdridge Life Zone System (Holdridge, Grenke, Hatheway, Liant & Tosi, 1971). Within the forest, spiders and insects were investigated at two sites, in an area of mature second growth forest ( M . schreibersi, C. caroli and L. globosa) and in a steep sided ravine at the boundary between old forest and mature second growth forest ( M . pia and E. globosus) (Foster & Brokaw, 1982).
METHODS
Ranking of web energy absorbing capabilities The kinetic energy (KE = m x u 2 / 2 ) with which an insect strikes a n orb web is a function of how fast the insect is flying ( u ) and of its mass (m).Webs spun by different species of orb weavers intercept insects that differ in mass and flight behaviour. Therefore, orb webs may be classified on the basis of their energy absorbing capabilities. I used two methods to determine the ability of orb webs to absorb energy: (1) artificially loading real webs and (2) estimating the kinetic energy of prey that had been caught in the webs.
ArtiJicial loading experiments When a spider web intercepts an insect, the prey's kinetic energy is transformed into work energy in stretching the web's fibres. Work energy is measured as the product of the applied force F and the distance over which the force is applied. By loading webs artificially and determining the energies at which webs broke, I estimated the maximum energy absorbing capabilities of webs built by three coexisting orb-weaving spiders. In general, maximum energy absorption depends where on the web's surface the force is applied and angle of the application. This has important consequences for the dynamic interactions between webs and prey insects; energy absorption capability will be influenced by where the insect strikes a web and by insect angle of approach. I coated metal frames with tanglefoot and adjusted them to be slightly larger than the area of a web's orb. By gently pressing the metal frame to the web's
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C. L. CRAIG
Figure I . Webs built by spiders included in this study. A, Epilineutes globasus. B, Leucauge globosa. C, Cyclosa caroli. D, Mangora pia. E, Micrathena schreibersi.
frame, I collected unstressed webs built by M . pia, C. caroli and L. globosa for testing. Testing began immediately following web collection and only those webs estimated to be 90-100% intact were used. Pieces of metal foil of varying weights were dropped into webs from heights between 0.1 and 1.0 m and
SPIDER WEB DESIGN, ECOLOGY AND EVOLUTION
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perpendicular to the web’s surface. The largest metal weights were spherical; I was unable, however, to make minute foil spheres that I could drop on the web threads. By making the smallest metal weights flat and rectangular, all weights were large enough to be caught by the webs or break through them. The kinetic energy of the metal pieces striking the web are calculated as kg x 9.8 ms-2 x D ; kg was the weight of the metal foil and D,between 0 and 1 .O, was the fraction of one metre above the web from which the weight was dropped. I did not determine how weight shapes affected weight speed at impact. In addition, due to the radial structure and high density of threads at the web centre, a weight dropped near to the web outer edge is less likely to be retained than the same weight dropped near the web’s centre. The data gathered from this experiment were used to generate capture probabilities and estimates of the webs’ energy absorbing potentials. These estimates provide a basis for ordering different classes of webs. Direct estimation of p r y kinetic energy I collected insects from webs built by the five species. The smallest insects (minute cecidomyiids less than approximately 0.2 mm length) were mounted on glass slides and measured. I used Schoener’s (1980) regression equations of ) length-weight relationships for tropical wet forest Diptera, (w= 0.068 i 1 . 5 g to estimate the dry weights of these prey. T o correct these estimates to wet weights, I weighed, dried and re-weighed 50 mosquitoes (Aedes aegypti) and found that the average weight loss due to drying was two-thirds ( 2 = 0.63, S.D. = 0.02) of the fly’s (wet) body weight. Therefore, I multiplied all estimated dry weights for nematocerous prey by a factor of three to estimate insect wet weight. I weighed the larger insects with an electric balance; insect wings were then removed and mounted on glass slides. I projected all slides with a photographic enlarger and traced the insects’ bodies and wings. Lighthill (1977) relates insect wing loading (mass x gravityltotal wing area) to insect velocity ( V ) , coefficient of life (CL),and air density ( p ) and expresses the relationship as
Wing loading = m xg/Wing area = 0.5 C,p V 2
(1)
The coefficient of lift, C,, is a dimensionless measure and a function of wing shape, orientation and Reynolds number (Vogel, 1981). Lighthill estimates C, to be about 0.5 for an insect flying at cruising speed. Setting air density equal to g cm2 (Vogel, 1981), I solved Lighthill’s formula for V 2 1.3 x
V 2 = Wing loadingl0.5 C,p
(2) For all of my estimates of insect flight speed, p and C, do not change. Therefore, the differences in insect flight speeds that I calculated were completely determined by insect wing loading. The assumption that insect flight speed can be calculated as a function of wing loading is central to this study. Extensive data supporting the relationship between wing loading, size and speed have been gathered for both insects and birds (Greenewalt, 1962). Greenewalt (1975) shows that for birds, speed is proportional to body mass. Lighthill extrapolates these data to predict that an animal with a mass of 1 g flies at about 4 m s P 2 ,a speed characteristic of insects of that size (Lighthill, 1977). Empirical data, however, show that the
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relationship between size and flight speed is not the same for all insect taxa. For example, Diptera and Hymenoptera are fast fliers relative to their size (Greenewalt, 1962). This may be due to the fundamental difference in physiology between insects characterized by asynchronous and synchronous flight masculature. For insects characterized by synchronous flight physiology muscles attached to the thorax control both the movement and position of the wing. Among these insects, wing movement is driven by thoracic vibrations that are neurally initiated. This type of flight musculature seems to be a preadaptation for small insect size (Nachtigall & Wilson, 1967) and may result in higher insect flight speeds than would be predicted on the basis of insect size alone (for example, see the elegant studies of swarming midges by Okubo, Chiang & Ebbesmeyer, 1977; Lighthill, 1977). Therefore, the flight speeds calculated using equation (2) may not predict precise speeds for all insect taxa. Nevertheless, they provide, at the least, a reasonable estimate of the range of flight speeds expected for insects of characteristic wing loadings. I have used kinetic energy estimates to differentiate among the kinds of prey caught in webs built by the five spider species. This technique, however, is problematical because my calculations are highly derived. Kinetic energy estimates for most prey caught in webs are based on two calculations: (1) calculated insect body weights and (2) calculated insect flight speeds. A more empirical and less derived method of classifying prey caught in webs would be one based on insect weight. Therefore, I examined the distributions of the weights (measured weights and calculated weights based on size) of insects caught in the five different webs to see if they differed from the distribution of prey plotted as a function of insect kinetic energy. For captured prey, distributions of kinetic energy and weight give two different kinds of information. The estimates of prey kinetic energy, compared to estimates of the energy absorbing properties of webs, reveal the relationship between web mechanical properties and prey kinetic properties. In contrast, the distribution of captured prey plotted as a function of prey weight and compared to spider weights show how adequately the web fulfils the spider’s energetic needs. In other words, examination of web architecture and design in relation to prey kinetic energy represents a mechanistic approach to the study of spider foraging ecology. Examination of web design in relation to prey weight focuses on the results of the insect-web encounter and is a way to assess how webs function relative to fulfilling the spider’s caloric needs (see Chiang).
Contribution of web architecture to energy absorption Idealized webs Spider orb webs approximate minimum volume architectures; that is, they approximate structures which use a minimum amount of material to withstand a specified set of loads. Maxwell’s lemma for minimum volume designs states that if (1) every member of a structure is built of the same material and under uniform tension, and (2) stress (forcelarea) is the same in all members and equal to the the breaking stress of the material, then a minimum amount of material has been invested in the structure to withstand a specified set of loads (Denny, 1976). Most webs must carry a variety of load distributions, rather
SPIDER WEB DESIGN, ECOLOGY AND EVOLUTION
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than a single set of loads. For example, prey impact may occur at any point on an orb web. Since the distribution of stress in the web is different at different loading points, the conditions for Maxwell's lemma are rarely satisfied. Therefore, webs can approximately satisfy the conditions of the lemma for the distribution of forces that are likely to be encountered. Given that orb webs capture different kinds of prey, and if one accepts that all orb webs approximate minimum volume designs, webs must differ in the mechanical properties of web silks, the details of web architecture or both. It is not possible to isolate empirically the contribution of web architecture to web function from that of web silks. Therefore, I modelled idealized webs of different geometries but identical materials to interpret how architectural variations might affect real web functions. I used a computer program for the structural analyses of tensile nets (Haber, Abel & Greenberg, 1981) to generate idealized, minimum volume, webs. The results from the computer model reflect the responses of architecturally varying 'webs', composed of linear elastic materials, to static loading. This analysis focused on the effects of four aspects of web design on web function: radial prestress, number of web radials and spirals, angle of the web with respect to web loading and sliding spiral-radial intersections. I compared the effects of static loading on geometrically varying, idealized webs with the effects of static loading on a reference web. The reference web, 8 cm in diameter, was composed of 10 equally spaced concentric circles (to approximate a spiral) and 10 equally spaced radii. Each radius extended away from the web edge 4 cm (Fig. 2). The reference web radial pre-stress was set at 0.35 x lo9 N m P 2 and spiral pre-stress was set at approximately zero (0.35 x lo4 N m-*). All idealized webs were loaded perpendicularly to the web surface and midway between the web's centre and outer edge. The loading force N. (One Newton, N, is the force which gives a mass of one was 3 x kilogram an acceleration of one metre per second per second. Thus one Newton is equal to the force of an object with mass 0.102 kg due to the earth's gravity, about the weight of one apple).
ldeoltzed web
Loading angles
\
@
' 0
(In web plane)
8
45'
(Out of web plane)
I
0
90" (Out of web plane)
@ 1 3 5 O (Out of web plone) @ 180° (In web plane)
I
\
Figure 2. Diagram of idealized reference web and loading angles. A reference web of 10 radials and 10 concentric circles was constructed to explore the effects of load angle on web response. The location on the web where loads were applied is circled. The load angles are shown at the upper right.
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L. CRAIG
In order to explore the importance of web architecture to web function, free from the influence of web materials, I made several simplifying assumptions concerning the mechanical properties of web silks. First, I approximated the behaviour of web silks by treating them as linear materials or materials which stretch in direct proportion to the load applied. Second, radial fibres and viscid threads were assumed to have the same material properties. Real viscid silks are characterized by higher extensibility and flexibility than are frame silks. Therefore, the viscid threads of the idealized webs displaced less than they would if modelled with the material properties of real viscid threads. I picked a typical extension, value = 1.16 for frame silk spun by Araneus sericuatus ( = Nuctenea sclopetaria) (Denny, 1976). From Denny's graph of stress by extension, I estimated true stress, B,, equal to 0.43 GPa. Natural strain ( E , ) = lnL/L,, (where Lo is equal to initial fibre length and L is proportional to fibre length at the stress 0.43 GPa; Wainwright, Biggs, Currey & Gosline, 1976) equals 0.148. For these values, Young's modulus ( B J q ) , a measure of material stiffness, is approximately 3 GPa. Varying radial pre-stress: During web construction, spiders display stereotyped behaviour patterns that function to reduce differences in tension among the web's radii (Eberhard, 1981). Differences in fibre tensions within webs affect ( 1 ) the rate that vibrations are transmitted from prey to spiders (Masters & Markl, 1980; Eberhard, 1981; Frolich & Buskirk, 1982) as well as the (2) the ability of the web to withstand loading (Eberhard, 1981). Web radial pre-stress, or tension at which the web is suspended (in conjunction with the material properties of web silks) determines the forces a web will absorb. I doubled the radial pre-stress of one simulated web and loaded it with a N to study the effect of varying pre-tension on concentrated force of 3 x web function. Maximum stress and deformation on the idealized web were compared to the reference web loaded under a similar regime. Varying the number of spiral turns and radii: Real webs are highly variable in the number of radial and spiral turns per web. The radii function as structural members of the web while web viscid silks absorb prey impact (Denny, 1976). I estimated the role of both the radii and spiral in web function by designing two idealized webs: one with 20 radials and 10 'spirals' and a second web with 10 radials and 20 'spirals'. The stress and deformation of the experimental webs were compared to those of the reference web when loaded with a concentrated N. force of 3 x Varying angle of application of load: Orb-webs are suspended at a variety of angles that influence the probable angle of insect interception. Idealized webs were loaded at five different angles midway between the centre and outer edge of the web and at a radial-spiral intersection point: (1) in the web plane and radially outward (O"), (2) oblique to the web plane and radially outward (45"), (3) perpendicular to the web's radius (go"), (4) oblique to the web plane and radially inward (135") and (5) in the web plane and radially inward (180") (Fig. 2). Sliding junctions between radial and spiral fibres: Many radial-spiral intersection points on spider webs are not fixed but slide when loaded. When the adhesive substance that coats the spiral silk builds up at the fibre junctions, further slip is inhibited. Jackson (1971) outlined the fine structure of these junctions and Eberhard (1976) described the mechanics and the frequencies with which sliding junctions are found on a variety of orb webs.
SPIDER WEB DESIGN, ECOLOGY AND EVOLUTION
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Sliding fibres make two contributions to web function. First, sliding fibres decrease loading stress at spiral-radial intersections (Gordon, 1978) and second, the increase in fibre length due to slip enhances the web’s energy absorbing capabilities. For fibre slip to enhance web energy absorption, fibres must slide during the time an insect is intercepted. I did not attempt to measure rate of fibre slip. When loading a viscid thread, however, I observed that the thread first stretches, slides and then stretches again until failure. I observed no difference between rate of initial fibre stretch and slip. An orb web such as the idealized reference web ( 10 radials/ 10 spirals) contains 100 spiral-radial intersections. I constructed a second model to examine the effects of sliding fibre intersections on prey capture. A single fibre 20cm long was suspended across four equally spaced points. At the two outer points, the fibre was fixed and at the two inner points, the fibre was either fixed or allowed to slip. Fibre pre-stress was set at 0.35 x lo9 N m - 2 . The change in force due to friction across the N to determine the contribution of sliding intersection was specified as 1 x sliding intersections to fibre extension and reduction of stress on web threads. Real webs The number of web radii, spiral turns per web and the area of webs were measured either from photographs or in the field. The reported web areas were measured as the total web area less the area of the web’s hub. I was unable to measure the radial pre-tensions of real webs and instead estimated the relative pre-tensions of whole webs by directing a constant airflow a t webs and measuring web displacement. Webs were lightly dusted with cornstarch and the web photographed with a camera positioned in the plane of the web and focused at the web edge. A handheld, battery operated fan (10 cm in diameter) that generated a constant airsteam of about 1.2 m s-I was directed at each web’s hub and the web photographed once again. Comparison of the web’s position before and during fan treatment gives a relative estimate of web pre-stress. Measurements were made at each web’s hub in a n attempt to reduce the effect of frame size on web displacement. For all estimates of web pre-stress, the spider was removed from the web. E. globosus, however, normally sits at the centre of its web holding web radial lines under tension (in contrast to building a web hub as do the other spiders included in this study) (see Fig. 1); thus the relative pre-stress of webs built by this spider is underestimated by my experiments. In addition, web dusting, necessary for photography, may have slightly increased web displacements even though the amount of cornstarch applied to the webs was very small. Fibre slip was also estimated empirically. First, the lengths of spiral fibres of five, adjacent, radial sectors of webs were measured. The viscid thread at the centre sector was then pulled to the fibre’s breaking point. I measured and averaged the change in the lengths of fibres within the remaining adjacent sectors to estimate the contribution of slip to fibre extension. Fibre slip was estimated for webs built by all of the spiders studied except for those build by E. globosus. Epilineutes globosus normally holds web radii in tension but when disturbed the spider flees from the web leaving the radii loosely joined. When I tried to load the viscid tread, I was unable to break it without pulling the whole web apart. Therefore, I could not measure slip on webs built by E. globosus.
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C. L. CRAIG
The results on real webs are reported with the results from the web simulation studies.
Contribution of web silks to energy absorption The energy absorbing properties of materials are a function of material strength and extensibility. For linear materials, maximum energy absorption occurs when both stress and strain are maximized. Among silks of equal strength but different elasticities, the less extensible silk is more likely to break at insect impact; the more extensible the silk, the more likely it will be able to absorb insect kinetic energy through stretch. Furthermore, the greater the amount of material, the greater the total amount of energy it can absorb. Numerous investigators have studied the mechanical properties of individual silk fibres (i.e. Zemlin, 1968; Denny, 1976; Work, 1976, 1977, 1981; Gosline, Denny & Demont, 1984). The threads that make up the orb web structure, however, are composed of fibre bundles rather than single strands. This study differs from the previous studies on silks because it focuses on the mechanical properties of silks in webs (and not the material properties of different kinds of silks); I made no attempt to separate web threads into individual fibres.
Tensile strength Tensile strength is equal to the maximum force per area that a material can withstand and allows comparison of this property of silks free from dimensionality. To measure tensile strength, silks from webs built by all five spider species were collected on 2.5 x 7.5 cm cardboard cards. Each card was notched, and double-sided sticky tape was pressed to both sides of the notch. I collected unstressed samples of web threads by gently applying the tape bordered notch to the surface of a web and carefully cutting the web away from the card. A second piece of tape was applied to the sample edge to prevent the silk from separating from the card during testing. After collection, the silked cards were stored in microscope slide boxes and carried back to the lab for immediate analysis. In the laboratory, glass rods were heated, drawn into fibres of varied diameters and cut into 6 cm lengths. Securing the fibre at one end and loading it at the free end caused it to deflect in proportion to the applied load (Suter, 1977). By mounting a mirror adjusted to an arbitrary scale over which the free end of the fibre extends, one can measure the magnitude of a glass fibre’s deflection free of parallax. I used this technique to calibrate glass fibres sensitive to loads ranging from 1.0 to 0.0001 g. I estimated the breaking loads of web threads by mounting silk samples on a rack and pinion adjacent to a glass fibre and lowering a silk sample across the fibre’s free end. The magnitude of fibre deflection at silk failure is proportional to the silk’s static breaking load and I calculated the tensile strengths of frame and viscid silks from these values (Fig. 3).
Extensibility Fibre extensibility, the maximum increase in fibre length due to load before failure, was measured in the field. I collected 1 cm samples of unstressed silk on
SPIDER WEB DESIGN, ECOLOGY AND EVOLUTION Mirror scale
I45
Rack and pinion
ilk sample rotated for test
Figure 3. Diagram of apparatus used to estimate silk breaking force. Silk samples were collected on notched cards and the cards mounted in modelling clay on a rack and pinion. A plexiglass ‘T’ and a block hold a glass stoppered tube and the stopper, split in half, holds a calibrated glass fibre. The tip of the glass fibre is hooked under each silk sample and as the sample is lowered on a rack and pinion, the glass fibre deflects. A mirror mounted adjacent to an arbitrary scale allows estimation of the calibrated fibre’s deflection free from parallax.
the jaws of a pair of vernier calipers to which double-sided sticky tape had been applied. The silk fibres were gently pressed to the caliper jaws and carefully cut from the web. Silk extensibility was estimated by stretching the fibres continuously at a rate of 1.5 cm/s until the fibre broke.
Fibre diameter The diameters of viscid and frame silks were measured from SEM micrographs. Silks were collected as described above (see section on tensile strength) and mounted on metal stubs coated with double sided sticky tape. The samples were then sputter coated. Micrographs were made of frame and viscid silk samples from webs spun by all of the species studied. The best studied orb web silks are those produced by the major ampullate glands. These silks make up the web framelines as well as the spider support or drag lines. During synthesis, silk fibres produced in the major ampullate gland pass through stages of water-reduction. After emergence from the gland’s spigot, the silks may then swell to attain a moisture equilibrium relative to humidity (Work, 1985). Therefore, the diameter of dehydrated silks probably approximates the true diameter of fibres produced by the spiders. Materials placed in a high vacuum shrink due to water loss. Although the silks I examined did not appear to be affected by the SEM vacuum conditions, any water that was lost should effectively reduce variation in thread diameter due to environmental effects. This suggests that the diameter of threads viewed under vacuum conditions should approximate the true diameter of silks when they are drawn from the spider spinneretts. I have assumed that any affects of the SEM vacuum on fibre diameter are constant for frame and viscid silks. Kinetic properties of silks Work energy is equal to force x distance. If two materials are identical (i.e. have equal breaking strengths, equal extensibilities) but differ in dimension, they will differ in the absolute amount of energy they can absorb. Silks may differ in fibre length and fibre cross-sectional area and spider webs may differ in their total size. For spider orb webs dimensional differences relative to web fibre diameter (and architecture) affect the classes of prey that webs intercept (for
C. L. CRAIG
I46
Table 1. Capture probabilities for objects striking three different types of webs. The probabilities that inanimate objects falling with the estimated kinetic energy (KE = kg x 9.8 m s - x~ D, D = initial distance of weight from web surface) will be retained in webs built by Leucauge globosa, Cyclosa caroli and Micranthena schreibersi are recorded below L globosa ( N = 50) KE
__ Probability
~~
0)
~
Probability 0 0 0.56 0.59
6.7 x 10-7 5.3 x 102.5 x 102.0x 10-8
M schretbersi ( N = 29)
C. caroli ( N = 54)
~~
KE
U)
4.5 x 1 0 - 6 1.5 x 9.6 x 10- 7 5.9 x 10- 7
~~
KE
~
0)
Probability
2.3 x lo-' 8.6 x lo-' 4.9 x lo-'
0.17 0.13 0.25 0.75
0.47 0.40 0.66
example see Murakami, 1983; Spiller, 1984). The breaking energies reported here are for fibres of different cross-sectional areas but of about 5 mm in length. My estimates of silk tensile strength and extensibility do not allow for the nonlinear and visco-elastic properties of web silks. Therefore, these data are best viewed as approximations to the kinetic properties of spider silks and in relation to the silks included in this study.
-irlr 0.1
0.0 0.5
,, 0.4 -
B
0.3-
;0.23
IA
0.1
-
, ,
0.0
0.4-
0.3 -
-
0.2
I
-10
-8
-6
-4
-10 Log of impact energy ( J )
I
-8
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-4
Figure 4. Kinetic energy of insects captured in five different spider orb webs. Distributions of the kinetic energy of insects collected from orb webs varied over seven orders of magnitude. All webs intercepted prey of low kinetic energy. Webs built by Micrathena schreibersi caught insects characterized by higher kinetic energies than webs built by any other spider. Webs built by Epilineutes globosus captured prey characterized by lower kinetic energies than those collected from webs of other designs. A, Micralhena schreibersi, N = 51. B, Mangora pin, N = 47. C, Cyclosa caroli, N = 26. D, Leucauge globosa, N = 13. E, Epilineutes globasus, X = 26.
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RESULTS
Rankings of web energy absorbing capabilities The artificial loading experiments showed that webs built by M. schreibersi are able to absorb kinetic energies at least three orders of magnitude higher than webs built by C. caroli and four orders of magnitude higher than webs built by L. globosa (Table 1). O n the basis of these data, I would rank webs built by M. schreibersi as high energy absorbing, webs built by L. globosa as low energy absorbing and webs built by C. caroli as intermediate in their energy absorbing capabilities. In Fig. 4 I have plotted the kinetic energy of insects caught in webs built by all five species. I compared these distributions using a multiple comparison procedure, Turkey’s HSD test (Snedecor & Cochran, 1978). The means of the logs of prey kinetic energy caught in webs built by M. schreibersi and E. globosus differ significantly from each other (P 10-5 J 216.8 213.4 216.8 16112.4 23115.5
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captured by the different spiders (Table 2) shows that webs built by E. globosus tend to intercept more prey characterized by low kinetic energies than webs built by L. globosa, and webs built by M. schreibersi tend to intercept prey with higher kinetic energies than webs built by M. pia. I ranked webs using the artificial loading experiments, the kinetic energy of insects caught in webs and the relationship between observed and expected prey captures found in Table 2. O n the basis of these data, the order of rankings, along a gradient of low to high energy web weavers, is E. globosus, L. globosa, C. caroli, M . pia and M . schreibersi. The distributions of insects caught in each web plotted as a function of insect weight are drawn in Fig. 5. These distributions were also compared using a x 2 analysis (Table 3). Insects were grouped into three categories, 0 4 . 9 9 , 1-9.99 and 10-100 mg. The analyses showed the same statistical groupings as did comparison by insect kinetic energy; that is, the weights of prey captured by E. globosus and L. globosa differed significantly from the weights of prey caught by M. schreibersi and M . pia (P
