Wind speed affects prey-catching behaviour in an orb web spider

Wind has previously been shown to influence the location and orientation of spider web sites and also the geometry and material composition of constructed orb webs. We now show that wind also influences components of prey-catching behaviour within the web. A small wind tunnel was used to generate different wind speeds. Araneus diadematus ran more slowly towards entangled Drosophila melanogaster in windy conditions, which took less time to escape the web. This indicates a lower capture probability and a diminished overall predation efficiency for spiders at higher wind speeds. We conclude that spiders’ behaviour of taking down their webs as wind speed increases may therefore not be a response only to possible web damage.     

Host pollination mode and mutualist pollinator presence: net effect of internally ovipositing parasite in the fig–wasp mutualism

The Ficus–their specific pollinating fig wasps (Chalcidoidea, Agaonidae) interaction presents a striking example of mutualism. Figs also shelter numerous non-pollinating fig wasps (NPFW) that exploit the fig–pollinator mutualism. Only a few NPFW species can enter figs to oviposit, they do not belong to the pollinating lineage Agaonidae. The internally ovipositing non-agaonid fig wasps can efficiently pollinate the Ficus species that were passively pollinated. However, there is no study to focus on the net effect of these internally ovipositing non-agaonid wasps in actively pollinated Ficus species. By collecting the data of fig wasp community and conducting controlled experiments, our results showed that internally ovipositing Diaziella bizarrea cannot effectively pollinate Ficus glaberrima, an actively pollinated monoecious fig tree. Furthermore, D. bizarrea failed to reproduce if they were introduced into figs without Eupristina sp., the regular pollinator, as all the figs aborted. Furthermore, although D. bizarrea had no effect on seed production in shared figs, it significantly reduced the number of Eupristina sp. progeny emerging from them. Thus, our experimental evidence shows that reproduction in Diaziella depends on the presence of agaonid pollinators, and whether internally ovipositing parasites can act as pollinators depends on the host fig’s pollination mode (active or passive). Overall, this study and others suggest a relatively limited mutualistic role for internally ovipositing fig wasps from non-pollinator (non-Agaonidae) lineages.     

Remote monitoring of vibrational information in spider webs

Spiders are fascinating model species to study information-acquisition strategies, with the web acting as an extension of the animal’s body. Here, we compare the strategies of two orb-weaving spiders that acquire information through vibrations transmitted and filtered in the web. Whereas Araneus diadematus monitors web vibration directly on the web, Zygiella x-notata uses a signal thread to remotely monitor web vibration from a retreat, which gives added protection. We assess the implications of these two information-acquisition strategies on the quality of vibration information transfer, using laser Doppler vibrometry to measure vibrations of real webs and finite element analysis in computer models of webs. We observed that the signal thread imposed no biologically relevant time penalty for vibration propagation. However, loss of energy (attenuation) was a cost associated with remote monitoring via a signal thread. The findings have implications for the biological use of vibrations by spiders, including the mechanisms to locate and discriminate between vibration sources. We show that orb-weaver spiders are fascinating examples of organisms that modify their physical environment to shape their information-acquisition strategy.     

Infanticide by a solitary koinobiont ichneumonid ectoparasitoid of spiders

When encountering an already parasitized host, a parasitoid’s optimal choices (superparasitism, host rejection, host feeding or infanticide) seem to depend on the individual species’ life history, because the same choice may have different fitness consequences. We demonstrate infanticide under laboratory conditions by a polysphinctine, Zatypota albicoxa, which is a solitary koinobiont ectoparasitoid of spiders. The female always removed any previously attached egg or larva from the body of the host spider, Parasteatoda tepidariorum, with a rubbing behaviour. She rubbed her ovipositor back and forth toward the undersurface of the attached egg or of the saddle under the attached larva to pry it off and laid an egg after removal. When removing a larva, the infanticidal female engaged exclusively in unfastening the ‘saddle’ which fastens the larva to the body of the spider. All larvae were removed with the ‘saddle’ attached to the ventral surface of the body. The female invested more time to remove the medium second and the large penultimate instar larvae than to remove eggs and first instar larvae because of the labour involved in unfastening the saddle. Oviposition with infanticide of the medium second and the penultimate instar larvae imposed more time upon the female than that on an unparasitized host. Removal of any previous occupant in spite of the associated labour costs suggests that infanticide will always be adaptive, no matter the time costs to Z. albicoxa, because so much is invested in attacking the host and because the parasitoid cannot detect whether the spider is already parasitized until she achieves subjugation.     

Does ontogenetic change in orb web asymmetry reflect biogenetic law?

Most orb web spiders face downward on the web hub, and their webs are vertically asymmetrical, that is, the lower part of the web is larger than the upper part and the ratio of the lower part to the whole web area increases as the spider grows. This phenomenon may reflect biogenetic law such that young animals exhibit a general ancestral trait whereas adults exhibit specific and derived traits. An alternative explanation is that vertical asymmetry may arise from the difference in time required by spiders to move up or down the web to capture prey. The present study tested these two hypotheses for Eriophora sagana. Subadults of this species build their webs with reverse asymmetry in that the upper part of the web area is larger than the lower part. In both subadults and adults, the upper proportion decreased with spider weight, and adult spiders built more symmetric webs. These results support the capture time difference hypothesis.     

Optimal foraging, not biogenetic law, predicts spider orb web allometry

The biogenetic law posits that the ontogeny of an organism recapitulates the pattern of evolutionary changes. Morphological evidence has offered some support for, but also considerable evidence against, the hypothesis. However, biogenetic law in behavior remains underexplored. As physical manifestation of behavior, spider webs offer an interesting model for the study of ontogenetic behavioral changes. In orb-weaving spiders, web symmetry often gets distorted through ontogeny, and these changes have been interpreted to reflect the biogenetic law. Here, we test the biogenetic law hypothesis against the alternative, the optimal foraging hypothesis, by studying the allometry in Leucauge venusta orb webs. These webs range in inclination from vertical through tilted to horizontal; biogenetic law predicts that allometry relates to ontogenetic stage, whereas optimal foraging predicts that allometry relates to gravity. Specifically, pronounced asymmetry should only be seen in vertical webs under optimal foraging theory. We show that, through ontogeny, vertical webs in L. venusta become more asymmetrical in contrast to tilted and horizontal webs. Biogenetic law thus cannot explain L. venusta web allometry, but our results instead support optimization of foraging area in response to spider size.     

Mass predicts web asymmetry in Nephila spiders

The architecture of vertical aerial orb webs may be affected by spider size and gravity or by the available web space, in addition to phylogenetic and/or developmental factors. Vertical orb web asymmetry measured by hub displacement has been shown to increase in bigger and heavier spiders; however, previous studies have mostly focused on adult and subadult spiders or on several size classes with measured size parameters but no mass. Both estimations are suboptimal because (1) adult orb web spiders may not invest heavily in optimal web construction, whereas juveniles do; (2) size class/developmental stage is difficult to estimate in the field and is thus subjective, and (3) mass scales differently to size and is therefore more important in predicting aerial foraging success due to gravity. We studied vertical web asymmetry in a giant orb web spider, Nephila pilipes, across a wide range of size classes/developmental stages and tested the hypothesis that vertical web asymmetry (measured as hub displacement) is affected by gravity. On a sample of 100 webs, we found that hubs were more displaced in heavier and larger juveniles and that spider mass explained vertical web asymmetry better than other measures of spider size (carapace and leg lengths, developmental stage). Quantifying web shape via the ladder index suggested that, unlike in other nephilid taxa, growing Nephila orbs do not become vertically elongated. We conclude that the ontogenetic pattern of progressive vertical web asymmetry in Nephila can be explained by optimal foraging due to gravity, to which the opposing selective force may be high web-building costs in the lower orb. Recent literature finds little support for alternative explanations of ontogenetic orb web allometry such as the size limitation hypothesis and the biogenetic law.     

Effects of height and habitat type on egg parasitism by Trichogramma minutum and T. pretiosum (Hymenoptera: Trichogrammatidae)

Heliothis virescens (Fabricius) eggs were sampled to determine the effects of height and habitat type (soybean field vs. uncultivated vegetation) on rates of p arasitism by Trichogramma minutum Riley and T. pretiosum Riley. The potentially confounding effects of plant associations and host density and distribution were eliminated by sampling with laboratory-produced eggs deposited on cloths, rather than with eggs naturally deposited by endemic hosts.A 3-way contingency table analysis showed that parasitism (whether the egg cloths were parasitized or not) was significantly associated with height and habitat type in 1981, with higher rates of parasitism in the uncultivated habitat and at the greater height. Parasitism was independent of height and habitat in 1982. Rates of parasitism by the two Trichogramma species were not clearly associated with habitat type, but were associated with height. T. minutum consistently parasitized egg cloths positioned at greater heights than those parasitized by T. pretiosum. While the behavioral mechanisms responsible are unknown, this inter-specific difference could have important implications with regard to selecting the most suitable of these two Trichogramma species for a particular inundative release program.     

First evidence of regular common cuckoo, <Emphasis Type="Italic">Cuculus canorus</Emphasis>, parasitism on eastern olivaceous warblers, <Emphasis Type="Italic">Hippolais pallida elaeica</Emphasis>

Coevolution is defined as specialized relationships between species that lead to a reciprocal evolutionary change. A particularly suitable model system for studying coevolution is the interactions between obligate avian brood parasites and their hosts. The common cuckoo (Cuculus canorus, hereafter cuckoo) is a well-known brood parasite, which utilizes a range of smaller passerines as hosts. However, warblers of the genus Hippolais have rarely been reported as being victims of cuckoos, and furthermore, few data exist on the occurrence of antiparasite defenses in these hosts. In this study, we examined possible host–parasite coevolution between cuckoos and eastern olivaceous warblers (Hippolais pallida elaeica, hereafter olivaceous warblers) in three closely situated areas in northwestern Bulgaria. The olivaceous warbler has never been reported to be a regular cuckoo host. However, the present study, carried out in 2001–2003 shows that the olivaceous warbler is regularly and heavily parasitized by the cuckoo in this area. Parasitism rate was high (26.6%, 34/128) and consistent among years, with some variation between areas. The cuckoo egg mimicry was moderately good, and olivaceous warbler rejection rate of such eggs was 50%. Cuckoo eggs laid in olivaceous warbler nests had a whitish to whitish-green ground color, and the majority appeared to be distinctly different from cuckoo eggs found in other host species in the area. The olivaceous warbler proved to be a rather good host for cuckoos as 20.6% (7/34) of cuckoo eggs laid produced fledglings, a breeding success comparable to other suitable hosts in Europe. This is the first in-depth study of brood parasitism in a warbler of the genus Hippolais, and cuckoos parasitizing olivaceous warblers probably represent a previously unknown gens.     

Prey detection without successful capture affects spider’s orb-web building behaviour

Animals obtain information from past foraging experience to adjust their foraging activity according to their environment. The ability of spiders to obtain information from unsuccessful predation experiences was investigated by examining the effects on web building, a significant foraging investment, of prey detection without successful capture in the orb-web spider Cyclosa octotuberculata. Four treatments were employed: (1) successful capture and feeding: one syrphid fly was allowed to be captured and consumed by the spider on the web; (2) single prey-item detection: a syrphid fly was placed on the web to lure the spider, but was removed before capture; (3) five prey-item detection: above prey-item detection stimulus was given five times; and, (4) control: neither prey nor feeding on the web. While control spiders decreased the total thread length and capture area of their webs, prey-item detection spiders in both conditions increased them, indicating that the spider obtained information from unsuccessful predation experience to adjust their foraging investment. The fed spiders exhibited a significantly greater increase than the prey-detection-only spiders, suggesting that prey detection alone and prey detection with consumption had different informational effects. Total thread length did not differ between single and five prey-item detection spiders, but distance between two adjacent sticky spirals increased only in the former spiders, possibly because five times unsuccessful predations prevented spiders to reduce web stickiness. It suggests that the spider changed web morphology according to the number of prey detection.     

Heat-balling wasps by honeybees

Defensiveness of honeybee colonies of Apis cerana and Apis mellifera (actively balling the wasps but reduction of foraging) against predatory wasps, Vespa velutina, and false wasps was assessed. There were significantly more worker bees in balls of the former than latter. Core temperatures in a ball around a live wasp of A. cerana were significantly higher than those of A. mellifera, and also significantly more when exposed to false wasps. Core temperatures of bee balls exposed to false wasps were significantly lower than those exposed to V. velutina for both A. cerana and for A. mellifera. The lethal thermal limits for V. velutina, A. cerana and A. mellifera were significantly different, so that both species of honeybees have a thermal safety factor in heat-killing such wasp predators. During wasps attacks at the hives measured at 3, 6 and 12 min, the numbers of Apis cerana cerana and Apis cerana indica bees continuing to forage were significantly reduced with increased wasp attack time. Tropical lowland A. c. indica reduced foraging rates significantly more than the highland A. c. cerana bees; but, there was no significant effect on foraging by A. mellifera. The latency to recovery of honeybee foraging was significantly greater the longer the duration of wasp attacks. The results show remarkable thermal fine-tuning in a co-evolving predator–prey relationship.     

Recognition of foreign oviposition-marking pheromone in a multi-trophic context

Both phytophagous and parasitic insects deposit oviposition-marking pheromones (OMPs) following oviposition that function to inform conspecifics of a previously utilized host of reduced suitability. The blueberry maggot fly, Rhagoletis mendax Curran (Diptera: Tephritidae), deposits eggs individually into blueberries and then marks the fruit surface with an OMP which reduces acceptance of fruit for oviposition by conspecifics. Diachasma alloeum (Muesebeck) (Hymenoptera: Braconidae) is a parasitic wasp attacking larval R. mendax which also deposits an OMP, signaling conspecifics of a wasp-occupied host. Behavioral studies were conducted testing the hypothesis that the OMP of the parasitic wasp modifies the oviposition behavior of its host fly. In this study, we show that the OMP of D. alloeum is recognized by R. mendax, and female flies will reject wasp-marked fruit for oviposition. Thus, we present a rare demonstration of pheromonal recognition between animals occupying different taxonomic orders and trophic levels. This chemical eavesdropping may enhance the ability of the fly to avoid fruit unsuitable for larval development.     

Pre-pupation behaviour of the aphid parasitoid <Emphasis Type="Italic">Aphidius ervi</Emphasis> (Haliday) and its consequences for pre-imaginal learning

Olfactory learning may occur at different stages of insect ontogeny. In parasitoid wasps, it has been mostly shown at adult emergence, whilst it remains controversial at pre-imaginal stages. We followed larval growth of the parasitoid wasp, Aphidius ervi Haliday, inside the host aphid, Acyrthosiphom pisum Harris, and characterised in detail the behaviour of third instar larvae. We found that just before cocoon spinning begins, the third instar larva bites a hole through the ventral side of the mummified aphid exoskeleton. We then evaluated whether this period of exposure to the external environment represented a sensitive stage for olfactory learning. In our first experiment, the third instar larvae were allowed to spin their cocoon on the host plant (Vicia faba L.) surface or on a plastic plate covering the portion of the host plant exposed to the ventral opening. Recently emerged adults of the first group showed a preference for plant volatiles in a glass Y-olfactometer, whereas no preference was found in adults of the second group. In a second experiment, during the period in which the aphid carcass remains open or is being sealed by cocoon spinning, third instar larvae were exposed for 24 h to either vanilla odours or water vapours as control. In this experiment, half of the parasitoid larvae were later excised from the mummy to avoid further exposure to vanilla. Adult parasitoids exposed to vanilla during the larval ventral opening of the mummy showed a significant preference for vanilla odours in the olfactometer, regardless of excision from the mummy. The larval behaviour described and the results of the manipulations performed are discussed as evidences for the acquisition of olfactory memory during the larval stage and its persistence through metamorphosis.     

Reverse positional orientation in a neotropical orb-web spider, <Emphasis Type="Italic">Verrucosa arenata</Emphasis>

Most orb-web spiders face downwards in the web. A downward orientation has been proposed to be the optimal strategy because spiders run faster downwards and thus can catch prey quicker. Consequently, orb-web spiders also extend their web in the lower part, leading to top-down web asymmetry. Since the majority of orb-web spiders face downwards, it has been difficult to test the effect of orientation on prey capture and web asymmetry. In this study, we explored the influence of reverse orientation on foraging efficiency and web asymmetry in Verrucosa arenata, a neotropical orb-web spider that faces upwards in the web. We show that reverse orientation does not imply reverse web asymmetry in this species. V. arenata spiders captured more prey in the lower part of the web but more prey per area on the upper part. The average running speeds of spiders did not differ between upward and downward running, but heavier spiders took longer to capture prey while running upwards. We discuss these findings in the context of foraging efficiency and web asymmetry.     

The response of Trissolcus basalis to footprint contact kairomones from Nezara viridula females is mediated by leaf epicuticular waxes

Chemical footprints left behind by true bugs are perceived as contact kairomones by scelionid egg parasitoids. Female wasps encountering a contaminated artificial substrate display a characteristic arrestment posture, holding the body motionless and antennating the surface. In the system Nezara viridula (L.) and its egg parasitoid Trissolcus basalis (Wollaston), previous studies have shown that the kairomone mediating such behavior is part of N. viridula’s cuticular hydrocarbons (CHC) and furthermore that the wasp’s ability to discriminate host male and female footprints is mainly based on the presence/absence of nonadecane (nC₁₉). In this study, the effect of epicuticular waxes of leaves of broad bean, Vicia faba, on wasp responses to footprints of N. viridula females were investigated. Approximately 20% of T. basalis females displayed an arrestment posture when released on the adaxial leaf surfaces of broad bean plants with intact wax layer and without host chemical contamination; whereas ∼70% of wasps displayed the arrestment posture when intact leaves were contaminated by host female footprints. Adaxial leaf surfaces of broad bean plants dewaxed with an aqueous solution of gum arabic and afterwards contaminated by N. viridula females induced arrestment responses in about 10% of female wasps; the same percentage of arrestment (10%) was observed when the wasps were released on leaves contaminated by host females and subsequently dewaxed. The side of the polymer film that was appressed to the leaf surface, peeled from the contaminated leaves, induced an arrestment posture in about 95% of observed wasps. Scanning electron microscopy (SEM) revealed that the epicuticular waxes occurred as a film densely crystallized as irregularly shaped platelets with spherical granules randomly distributed. These findings demonstrated that epicuticular waxes of broad bean leaves can mediate the foraging behavior of T. basalis females by absorbing contact kairomones of the host.     

Bee-hawking by the wasp, <Emphasis Type="BoldItalic">Vespa velutina</Emphasis>, on the honeybees <Emphasis Type="BoldItalic">Apis cerana</Emphasis> and <Emphasis Type="BoldItalic">A</Emphasis>. <Emphasis Type="BoldItalic">mellifera</Emphasis>

The vespine wasps, Vespa velutina, specialise in hawking honeybee foragers returning to their nests. We studied their behaviour in China using native Apis cerana and introduced A. mellifera colonies. When the wasps are hawking, A. cerana recruits threefold more guard bees to stave off predation than A. mellifera. The former also utilises wing shimmering as a visual pattern disruption mechanism, which is not shown by A. mellifera. A. cerana foragers halve the time of normal flight needed to dart into the nest entrance, while A. mellifera actually slows down in sashaying flight manoeuvres. V. velutina preferentially hawks A. mellifera foragers when both A. mellifera and A. cerana occur in the same apiary. The pace of wasp-hawking was highest in mid-summer but the frequency of hawking wasps was three times higher at A. mellifera colonies than at the A. cerana colonies. The wasps were taking A. mellifera foragers at a frequency eightfold greater than A. cerana foragers. The final hawking success rates of the wasps were about three times higher for A. mellifera foragers than for A. cerana. The relative success of native A. cerana over European A. mellifera in thwarting predation by the wasp V. velutina is interpreted as the result of co-evolution between the Asian wasp and honeybee, respectively.     

An epicuticular multilayer reflector generates the iridescent coloration in chrysidid wasps (Hymenoptera, Chrysididae)

Chrysidid wasps in the subfamily Chrysidinae are brood parasitoids or cleptoparasites of other insects and famous for their cuticular iridescence. In this study, we examine the dorsal abdominal cuticle of the chrysidid wasp Hedychrum rutilans to identify the underlying color mechanism. Using scanning electron microscopy, reflectance spectral analysis, and theoretical calculations, we demonstrate the presence of an epicuticular multilayer reflector consisting of six lamellae with a thickness of 185 nm each. The lamellae exhibit a rough surface probably functioning as spacers between the individual layers. The reflector has a measured reflectance maximum at λ = 630 nm, i.e., in the red part of the visible spectrum of light at normal incidence and the reflectance maximum shifts to green as the angle of incidence increases. Complementary theoretical modeling corroborates the view that the epicuticular multilayer generates the iridescent color of the chrysidid cuticle. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Homing in the wolf spider Lycosa tarantula (Araneae, Lycosidae): the role of active locomotion and visual landmarks

Previous studies on the homing of the wolf spider Lycosa tarantula have shown that it is carried out by path integration. Animals using this mechanism must measure the distance walked and the angles turned. This study aims to understand if wolf spider L. tarantula is able to estimate the walked distance in an outward path. As this information is more likely obtained by proprioceptive mechanisms, active or passive displacements have been performed. An active locomotion was found essential to estimate distances. During passive locomotion, spiders searched for their burrows near the release point while when displaced actively the inbound journey was longer than the outbound one. The possible use of visual landmarks near the burrow was also tested as a cue to complete the inbound journey. Our results did not show that L. tarantula used these visual landmarks to find the burrow. L. tarantula seems to use only proprioceptive information obtained during the outbound path to estimate the distance traveled.     

An acanthocephalan parasite increases the salinity tolerance of the freshwater amphipod <Emphasis Type="Italic">Gammarus roeseli</Emphasis> (Crustacea: Gammaridae)

Studies of the influence of parasites on host fitness generally conclude that parasites have a strong negative effect on their hosts. In this study, we have investigated experimentally the role of Polymorphus minutus, an acanthocephalan parasite, on the salinity tolerance of the freshwater amphipod Gammarus roeseli, one of its intermediate hosts. Unexpectedly, P. minutus-infected gammarids were more tolerant to salinity stress than uninfected ones. The mean lethal salt concentrations for 50% mortality of hosts tested were 17.3 (infected) and 9.7 g/L (uninfected). The parasitic load (one or two parasites per host) did not affect the result. The size of hosts had no significant influence on the salinity tolerance of either infected or uninfected gammarids. The mobility of all types of gammarid decreased when the salinity exceeded 9.0 g/L, but there was no significant difference between infected and uninfected gammarids. We discuss the higher salinity tolerance of infected amphipods in relation to O₂ consumption and osmoregulation. Finally, we demonstrate that the salinity tolerance is enhanced in the parasitized amphipod but without a significant change in behavior or an osmoregulatory adjustment.     

Optimal Area Use in Orb Webs of the Spider Araneus diadematus

 We studied the abilities of the garden cross spider Araneus diadematus regarding adaptation of web geometry to spatial constraints. Spiders reacted to a spatial reduction in their building site from a square-shaped frame to a slimmer, rectangular frame (side ratio 1 : 2) by maintaining overall web geometry while reducing the web area covered by the sticky capture spiral. However, when the frames were changed further to a rectangular side ratio of 1 : 3, the spiders changed specific web properties in such a way that a further reduction in the capture spiral area was prevented. Construction of the threads making up the web frame and the auxiliary spiral requires that the spider explores the spatial constraints of its building site. The geometry of both frame and auxiliary spiral threads in turn determine the geometry of the capture threads. Since in very narrow frames the spider adjusted the auxiliary to suit the subsequent capture spiral, we suggest that an initial spatial survey led to the final adaptation of overall web geometry to a web site. Received: 26 April 1999 / Accepted in revised form: 26 November 1999