The influence of web monitoring tactics on the tracheal systems of spiders in the family Uloboridae (Arachnida,Araneida)

Summary Uloborids that spin reduced webs more actively monitor them than those that construct orb webs. Hyptiotes use both their first and fourth legs to tense their triangle-webs, whereas Miagrammopes rely principally on their first legs to monitor and jerk the threads of their irregular webs. The respiratory systems of these spiders include tracheae that extend into the prosoma, bifurcate, and enter the legs. To determine if the legs responsible for active web-monitoring tactics have more extensive tracheal supplies, the total cross sectional area has been computed of the tracheae entering the legs of mature female orb web and reduced web uloborids. Each leg's value has been divided by the cross sectional area of the tracheal trunks that enter the prosoma. These indexes reveal no significant differences between the relative tracheal supplies of the orb weavers investigated (Waitkera waitkerensis, Tangaroa beattyi, Uloborus glomosus). But the first, third, and fourth legs of H. cavatus and the first legs of M. animotus and M. pinopus have greater relative tracheal supplies than those of the three orb weaving species. Relative to leg volume, the first and fourth legs of H. cavatus have the greatest and the first legs of Miagrammopes species the next greatest tracheal supplies. When tracheal lengths are considered, these differences in potential oxygen supplies remain, showing that area differences do not simply compensate for differences in the distances over which oxygen must diffuse. These differences are leg-specific and not species-specific, and uloborids with the most extensive tracheal supplies are found in moist habitats. Thus the observed differences are best explained as adaptations to meet the greater oxygen demands of legs responsible for active web-monitoring tactics and not as adaptations to reduce respiratory water loss.     

Factors governing the stickiness of cribellar prey capture threads in the spider family Uloboridae

The surface of a cribellar prey capture thread is formed of thousands of fine, looped fibrils, each issuing from one of the spigots on an oval spinning plate termed the cribellum. This plesiomorphic capture thread is retained by members of the family Uloboridae, in which its stickiness differs among genera. An examination of five cribellar thread features in nine uloborid species shows that only the number of fibrils that form a thread explains these differences in thread stickiness. Neither the physical features of these fibrils, nor the manner in which they are combined to form threads differs among species. Threads produced by orb-weaving species contain fewer fibrils than those produced by species that build reduced webs. Relative to spider weight, the number of fibrils that form a cribellar thread is greatest in simple-web species of the genus Miagrammopes, less in triangle-web species of the genus Hyptiotes, and least in orb-weaving species representing five genera. A transformational analysis shows that change in the number of cribellum spigots is directly related to change in the stickiness of cribellar thread. This direct relationship between the material invested in a cribellar thread and its stickiness may have been a limiting factor that favored the switch from the dry cribellar threads of uloborids to the adhesive capture threads produced by other orb-weaving families. © 1994 Wiley-Liss, Inc.     

Respiratory organs in wolf spiders: morphometric analysis of lungs and tracheae in Pardosa lugubris (L.) (Arachnida, Araneae, Lycosidae)

The respiratory system of the wolf spider Pardosa lugubris consists of a pair of well-developed lungs and four unbranched tube tracheae. We used stereological morphometric methods to investigate the morphological diffusing capacity of the lungs and of the walls of the tracheae ('lateral diffusing capacity'). We examined three groups of female P. lugubris with different mean body masses. The barrier thickness of the gas-exchange epithelium of the lungs was 0.17 microm for the total diffusion barrier and the calculated oxygen diffusing capacity (D(O2)) for the lungs was between 12.9 and 13.4 microl min(-1)g(-1)kPa(-1). Measured metabolic rates compared with the D(O2) of the lungs result in necessary oxygen partial pressure differences of 0.2 kPa during rest and 2.1 kPa during maximum measured activity. The diffusion barrier of the entire tracheal walls was 0.31-0.50 microm and the calculated lateral D(O2) was 0.05-0.2 microl min(-1)g(-1)kPa(-1). Therefore, tracheae are of no importance for the overall oxygen exchange. However, they might be of some importance in local oxygen supply or in overall carbon dioxide release. The comparison with the respiratory system of the jumping spider Salticus scenicus reveals that the lungs have very similar mass-specific D(O2) in both species, and that, in addition, jumping spiders possess a much better developed tracheal system.     

Book lung development in the embryo,postembryo and first instar of the cobweb spider,Parasteatoda tepidariorum C. L Koch, 1841 (Araneomorphae,Theridiidae)

Light and electron microscopy were used to compare spider book lung development with earlier studies of the development of horseshoe crab book gills and scorpion book lungs. Histological studies at the beginning of the 20th century provided evidence that spider and scorpion book lungs begin with outgrowth of a few primary lamellae (respiratory furrows, saccules) from the posterior surface of opisthosomal limb buds, reminiscent of the formation of book gills in the horseshoe crab. In spider embryos, light micrographs herein also show small primary lamellae formed at the posterior surface of opisthosomal limb buds. Later, more prominent primary lamellae extend into each book lung sinus from the inner wall of the book lung operculum formed from the limb bud. It appears most primary lamellae continue developing and become part of later book lungs, but there is variation in the rate and sequence of development. Electron micrographs show the process of air channel formation from parallel rows of precursor cells: mode I (cord hollowing), release of secretory vesicles into the extracellular space and mode II (cell hollowing), alignment and fusion of intracellular vesicles. Cell death (cavitation) is much less common but occurs in some places. Results herein support the early 20th century hypotheses that 1) book lungs are derived from book gills and 2) book lungs are an early step in the evolution of spider tracheae.     

Changes in spinning anatomy and thread stickiness associated with the origin of orb-weaving spiders

The cribellum is an oval spinning field whose spigots produce silk fibrils that form the outer surfaces of the primitive prey capture threads found in aerial spider webs. A comparison of the cribella and cribellar capture threads of 13 species of spiders representing seven families (Amaurobiidae, Desidae, Dictynidae, Filistatidae, Neolanidae, Oecobiidae, and Uloboridae) confirms that the stickness of a cribellar thread is directly related to the number of spigots on a spider's cribellum. This comparison also demonstrates that the origin of orb-weaving spiders from ancestors that constructed less highly organized webs was associated with increases in both the weight-specific number of cribellum spigots and the weight-specific stickiness of cribellar prey capture threads. In contrast to other cribellate spiders, the number of cribellum spigots of orb-weaving species of the family Uloboridae scales to spider mass. Thus, the origin of orb-weaving spiders involved not only behavioural changes that stylized and restricted the placement of cribellar threads, but also included morphological changes that increased the stickiness of these capture threads by endowing them with more cribellar fibrils.     

Impact of predation by spiders on a territorial damselfly (Odonata: Calopterygidae)

Summary Predation by orb-weaving spiders and crab spiders on the damselfly Calopteryx haemorrhoidalis was studied at a small stream in Southern France. One species of orb-weaving spider, Larinioides folium, caught 76% of the damselflies which fell prey to spiders. Displacement experiments on spiders on sections of bank and the positioning of webs in male territories show that the density and distribution of damselflies is not influenced by orbweb density or by the position of webs. Predation rates corresponded to orb-web density, but neither for sex nor for stage was there a relationship with damselfly density. Mean daily predation rates ranged between 0.9% for females and 4.1% for adult males. Predation risk to adult damselflies by orb-weaving spiders was male biased, whereas among tenerals there was no bias. Males were captured more frequently at territories near the water. Captures show a maximum at noon when territorial disputes of adult males were most frequent. After orbwebs were placed within territories predation rate of males was strongly increased. Predation risk to adult females in the direct vicinity of the stream was less than in the bank vegetation where they perch close to orbwebs. The risk of predation by crab spiders, which catch damselflies at their perching sites, was not sex-biased.     

Diverse adaptations of an ancestral gill: a common evolutionary origin for wings,breathing organs,and spinnerets

Changing conditions of life impose new requirements on the morphology and physiology of an organism. One of these changes is the evolutionary transition from aquatic to terrestrial life, leading to adaptations in locomotion, breathing, reproduction, and mechanisms for food capture. We have shown previously that insects' wings most likely originated from one of the gills of ancestral aquatic arthropods during their transition to life on land. Here we investigate the fate of these ancestral gills during the evolution of another major arthropod group, the chelicerates. We examine the expression of two developmental genes, pdm/nubbin and apterous, that participate in the specification of insects' wings and are expressed in particular crustacean epipods/gills. In the horseshoe crab, a primitively aquatic chelicerate, pdm/nubbin is specifically expressed in opisthosomal appendages that give rise to respiratory organs called book gills. In spiders (terrestrial chelicerates), pdm/nubbin and apterous are expressed in successive segmental primordia that give rise to book lungs, lateral tubular tracheae, and spinnerets, novel structures that are used by spiders to breathe on land and to spin their webs. Combined with morphological and palaeontological evidence, these observations suggest that fundamentally different new organs (wings, air-breathing organs, and spinnerets) evolved from the same ancestral structure (gills) in parallel instances of terrestrialization.     

Same same but different: a stunning analogy between tracheal and vascular supply in the CNS of different arachnids

Described herein is an as yet unprecedented structural and functional analogy of both the tracheal supply of the prosomal ganglion in opilionids and the arterial supply of the prosomal ganglion in pulmonate arachnids. Within Arachnida, two different modes of respiration can be observed: the so-called book lungs, and the tube-like tracheae. These different respiratory modes always correlate with a specific setup concerning the complexity of the circulatory system. This fact has a particular influence on the supply of certain organ systems, such as the central nervous system. It has recently been shown that pulmonate arachnids possess a highly complex pattern of intraganglionic arteries. Here, we show that Opiliones (harvestmen) possess a complex tracheal system (which supplies the different organ systems with oxygen) and only a relatively simple vascular system, comprising a short heart and an anterior aorta that runs directly to the prosomal ganglion. Using a variety of modern and classical morphological methods, we studied the vascular, tracheal and nervous systems of different representatives from all higher taxa of Opiliones. We show that the prosomal ganglion is extensively supplied with intraganglionic tracheae. What is especially surprising is the high degree of correspondence between the pattern of these ganglionic tracheae in harvestmen and the pattern of arteries in the prosomal ganglion of pulmonate arachnids. We aim to provide mechanistic causal explanations of these analogous patterns by applying the concepts of role analogy and constructional analogy. We also aim to establish the circulatory system as a model organ system and hope that this may, in turn, provide a starting point for future research programmes.     

Damping capacity is evolutionarily conserved in the radial silk of orb-weaving spiders

Orb-weaving spiders depend upon their two-dimensional silk traps to stop insects in mid flight. While the silks used to construct orb webs must be extremely tough to absorb the tremendous kinetic energy of insect prey, webs must also minimize the return of that energy to prey to prevent insects from bouncing out of oscillating webs. We therefore predict that the damping capacity of major ampullate spider silk, which forms the supporting frames and radial threads of orb webs, should be evolutionarily conserved among orb-weaving spiders. We test this prediction by comparing silk from six diverse species of orb spiders. Silk was taken directly from the radii of orb webs and a Nano Bionix test system was used either to sequentially extend the silk to 25% strain in 5% increments while relaxing it fully between each cycle, or to pull virgin silk samples to 15% strain. Damping capacity was then calculated as the percent difference in loading and unloading energies. Damping capacity increased after yield for all species and typically ranged from 40 to 50% within each cycle for sequentially pulled silk and from 50 to 70% for virgin samples. Lower damping at smaller strains may allow orb webs to withstand minor perturbations from wind and small prey while still retaining the ability to capture large insects. The similarity in damping capacity of silk from the radii spun by diverse spiders highlights the importance of energy absorption by silk for orb-weaving spiders.     

Behavior of Colonial Orb-weaving Spiders during a Solar Eclipse

The behavior of colonial orb-weaving spiders (Metepeira incrassata) in tropical Veracruz, Mexico was studied during the total solar eclipse on July 11, 1991. Spiders behaved in a manner typical of daily activity until totality, when many began taking down webs. After solar reappearance, most spiders that had begun taking down webs rebuilt them. There was no significant difference in the overall activity patterns of spiders during totality across a range of colony sizes. Experimental illumination of part of a colony during totality altered web takedown behavior. While spiders in the darkness of totality began to take down webs, those spiders which were artificially illuminated did not. These observations suggest that the primary environmental cue responsible for the daily rhythm of web building behavior in this species is light level.     

Developmental changes in barrier web structure under different levels of predation risk inNephila clavipes (Araneae: Tetragnathidae)

Individuals of the orb-weaving spider Nephila clavipesbuild complex webs with a region used for prey capture, the orb, and tangle webs opposite either face, the barrier webs. Barrier webs have been hypothesized to serve a variety of functions, including predator defense, and the primary function of the barrier web should be reflected in the relative size of the barrier to the orb under varying conditions of foraging success and predation risk. To investigate the effects of predation pressure and foraging success on barrier web structure, I conducted a comparative study in three disjunct populations that differed in predation risk and foraging success. Although both the orb web and the barrier webs are silk, there was no indication of a foraging-defense trade-off. Barrier web structure did not change during seasonal shifts in orb web size related to changes in preycapture rate, and barrier web silk density and orb radius were positively correlated. The hypothesis that the construction of barrier webs is in part a response to predation pressure was supported. Barrier webs do deflect attacks by some predators, and barrier webs built by small spiders, suffering frequent predation attempts, had a higher silk density than barrier webs built by larger individuals. Additionally, barrier web complexity decreased at a later age in areas with higher predation risk.     

Kleptoparasites or commensals? Effects of Argyrodes antipodianus (Araneae: Theridiidae) on Nephila plumipes (Araneae: Tetragnathidae)

Argyrodes antipodianus is a small kleptobiotic spider that steals prey from webs of the large orb-weaving spider Nephila plumipes, and sometimes removes the web itself. We used experiments in a greenhouse to test how the presence of the kleptobiont, differences in food availability, and web damage affected fitness of the web owner. After 49 days, N. plumipes with four A. antipodianus on their webs gained 55% less weight and relocated their webs 4.5 times as often as spiders with no kleptobionts. Increased web relocation and decreased weight gain may have resulted from reduced prey levels or from web damage by A. antipodianus. A second experiment demonstrated that hosts gained weight at the feeding rate used in the first experiment, but not at lower rates. Web relocation rate also varied with feeding rate, but in a non-linear manner. Web loss was evaluated in a separate experiment, by manually removing one-quarter of the web every 5 days for 30 days; however, neither weight gain nor rate of web relocation were affected. We conclude that A. antipodianus is a true kleptoparasite that can reduce the growth rate of its host N. plumipes, but that neither food theft nor web damage alone explain increased web relocation rates. Received: 28 November 1996 / Accepted: 3 April 1997     

Quantitative food webs of lepidopteran leafminers and their parasitoids in a Japanese deciduous forest

Quantitative food webs were constructed to explore the community structure of leaf-mining moths in the family Gracillariidae and their parasitoid wasps in a deciduous forest in Hokkaido, Japan. A whole food web was constructed from data collected from June to October 2001. In the web, 16 leafminer species on seven tree species were attacked by 58 species of hymenopteran parasitoid; 376 links between leafminers and parasitoids were observed. Leafminers were specialist herbivores, but most parasitoids were generalists. Five webs were constructed for the seasonal prevalence of leafminers over the one-year period to reveal the temporal dynamics in community structure. Among the seasonal webs, the first web in June was distinctive because two tree species, Japanese umbrella tree Magnolia obovata and Japanese magnolia M. kobus, supported the community. Second to fourth webs from July to September were dominated by the leafminer species on Japanese oak Quercus crispula, and the fifth web was marked by that on Carpinus cordata. The extent of potential apparent competition among leafminers was evaluated using quantitative parasitoid overlap diagrams. These diagrams suggested that abundant host species are likely to have large indirect effects on less abundant species. Moreover, the potential for apparent competition between leafminer species inhabiting different host tree species can occur, although leafminers sharing the same tree species are prone to interact via shared parasitoids. In this system, particular leafminer species, acting as potential sources of apparent competition, can affect other species as sinks, and control whole-community dynamics. Directed apparent competition may potentially occur around oak trees.     

Spiders that decorate their webs at higher frequency intercept more prey and grow faster

Many orb-weaving spiders decorate their webs with extra, bright white, ultraviolet light reflecting silk. Previous studies suggest that these decorations increase a spider's foraging efficiency by improving web attractiveness, which is known as the prey-attraction hypothesis. One assumption of this hypothesis is that individuals which decorate their webs at a higher frequency are expected to have a higher growth rate. Using a decoration-building orb-weaving spider, Argiope versicolor, I show a strong positive relationship between the growth rate in terms of weight gain and the frequency of decoration-building, as well as the rate of insect interception. This is the first study to reveal a fitness consequence of decorating behaviour in spiders.     

Stereological determination of tracheal volume and diffusing capacity of the tracheal walls in the stick insect Carausius morosus (Phasmatodea, Lonchodidae)

First instars of Carausius morosus provide a good model for morphometric evaluation of the diffusing capacity between the tracheal system and hemolymph: air sacs are lacking, tracheoles do not penetrate the organs and muscles, and entire animals can be evaluated electron microscopically without subsampling. The tracheal volume makes up 1.3% of the volume of the whole insect excluding appendages. We calculated the lateral diffusing capacity for oxygen and carbon dioxide for five classes of tracheae according to their diameters, from 0.2 microm to 35 microm. The harmonic mean thickness of the tracheal epithelium is lowest in smallest tracheae and increases with increasing tracheal diameter. Although the smallest tracheae make up 70% (O2) and 60% (CO2) of the total diffusing capacity, the proximal four classes may also be significant in diffusion of oxygen and particularly of carbon dioxide. The suppression of the development of respiratory pigments in the evolution of terrestrial insects may have increased the relative importance of small tracheal elements for local oxygen consumption.     

Effects of an experimental increase in prey abundance upon the reproductive rates of two orb-weaving spider species (Araneae: Araneidae)

Summary A field experiment was performed to determine if food is a limited resource for adult females of two species of orb-weaving spiders, Mecynogea lemniscata and Metepeira labyrinthea. Spiders built webs after being added to open experimental units located in a mixed deciduous-pine forest in Maryland, USA. Each unit was a frame supporting dead branches of the type used by both species for anchoring webs. Spiders on half the units were exposed to natural prey densities only, while each spider on the other units was given laboratory-reared flies in order to increase prey availability above natural levels. Supplemental feeding continued for 2.5 months. At the end of the experiment all egg sacs were removed from the units.Providing additional prey did not increase the survival rate on the units (net effect of mortality, emigration and immigration). However, both species responded to additional prey by significantly increasing the number of eggs produced per female, indicating that food was a limited resource for these species. Median egg production per female increased from 34 to 62 for Mecynogea lemniscata and from 65 to 145 for Metepeira labyrinthea. Egg weight was not affected.Feeding rates and nearest neighbor distances were determined for spiders in non-experimental populations, which permitted evaluation of the experiment's naturalness. The effects of food supply upon the reproductive rates of the two species are discussed in relation to their numerical response and population dynamics.     

Foraging strategies of Eriophora transmarina and Nephila plumipes (Araneae: Araneoidea): Nocturnal and diurnal orb-weaving spiders

Abstract The foraging behaviour, web characteristics and prey availability of two sympatric orb-weaving spiders, Nephila plumipes and Eriophora transmarina (Araneae: Araneoidea), are compared. The spiders are similarly sized but have different temporal foraging patterns. Nephila plumipes spins a relatively permanent web and captures most of its prey during the day. Eriophora transmarina only forages at night, spinning a new web every night and usually dismantling it at dawn. These different foraging activities are most likely to be responsible for the observed differences in the types and rates of prey capture: E. transmarina captured mostly Lepidoptera that were more abundant at night than during the day, while N. plumipes captured mostly Hymenoptera that were more abundant during the day than at night. While nocturnal E. transmarina have less time available for foraging than the diurnal N. plumipes, the former has a substantially higher nocturnal prey capture rate. We argue that the difference between the species in their prey capture rates are likely to be due to differences in the architecture of their webs.     

Immunocytochemical survey of the neuropeithelial endocrine system in the respiratory tract of the Tokyo salamander,Hynobius neubulosus tokyoensis Tago

The epithelial lining of the respiratory tract of urodeles has been shown to harbor an innervated system of neuroepithelial endocrine (NEE) cells. Even between phylogenetically closely related species, large differences have been reported in the appearance and chemical coding of the NEE system. Although urodeles are well suited for the purpose, none of the prior studies have provided an immunocytochemical survey of the NEE system in all parts of the respiratory tract. In the present study, many bioactive substances and a general marker were immunocytochemically demonstrated in serial sections of the entire respiratory tract of the Tokyo salamander, Hynobius nebulosus tokyoensis, a species in which neuroepithelial bodies (NEBs) were previously characterized at the electron microscopic level. In the current study, serotonin-immunoreactive solitary NEE cells were observed in variable numbers in the larynx, in all parts of the trachea, and in areas of the lungs covered with ciliomucous epithelium. Serotonin-containing NEBs, however, were detected in small cranial areas of the lung only. Solitary NEE cells were seen in the trachea and lungs of H. nebulosus tokyoensis by immunocytochemical staining for somatostatin, calcitonin, calcitonin gene-related peptide, and bombesin, but the number, localization, and appearance of the labeled NEE cells differed considerably. Only calcitonin-like immunoreactivity was also noted in some NEB-like cell clusters in the cranial parts of the lungs. Unlike many other vertebrates, neuron specific enolase was found to be a poor marker for the NEE system in the salamander species used in this investigation. It may be concluded that the NEE system of H. nebulosus tokyoensis contains at least five different bioactive substances. The different markers, however, demonstrate the presence of NEE cells with obvious differences in respect to appearance and topographical distribution. The necessity is emphasized of reliable methods for adequate sampling of all regions of the respiratory tract in comparative histological studies of the NEE system.     

The tracheal supply and muscle metabolism during muscle growth in the puparium of Calliphora vomitoria

Thirty hours after puparium formation in Calliphora, the larval tracheal system is replaced by an air-filled pupal system. This is characterized initially by many tufts of tracheae and coiled tracheoles lying in the blood. Between the third and fourth day, the sixth dorsal longitudinal flight muscles are practically without attached tracheae and their longitudinal growth can partially occur when oxygen uptake is inhibited with potassium cyanide. Sodium iodoacetate prevents muscle growth. After the fifth day of development the pupal tracheoles spread out over the surface of the developing adult muscles. Between the seventh and ninth day, longitudinal growth and increases in the diameter of the myofibrils are halted by cyanide and iodoacetate. Some longitudinal growth and an increase in the total protein content of the muscles can occur in 1% oxygen. Air filling of the adult tracheae takes place 2–3 hr before the emergence of the adult and is accompanied by an increase in oxygen consumption of the thorax. The metabolism and growth of the muscles is discussed with respect to their changing oxygen supply.     

Co-adapted foraging traits in a guild of orb-weaving spiders

Summary From a previous two-species comparison, specific suites of morphological and web design traits are predicted to characterize foraging specializations in old-field orb-weaving spiders. Species with stout legs, large fangs, open mesh webs, high webs, and retreats should specialize on innocuous, rapidly escaping prey types. Species with long legs, small fangs, dense mesh webs, and low webs that rest in the hub should specialize on dangerous, clumsy prey that escape from webs slowly. Factor and discriminant analyses are used to test for these association patterns in eight co-occurring species of old-field orb-weavers. The association between most of the characters is supported, but the appearance of a new combination suggests that another dimension needs to be added to the model. Habitat use and diet predicted by the model are tested for species where data are available.