André Walter

The evolution of novel animal signals: silk decorations as a model system.

Contemporary animal signals may derive from an elaboration of existing forms or novel non‐signalling traits. Unravelling the evolution of the latter is challenging because experiments investigating the maintenance of the signal may provide little insight into its early evolution. The web decorations, or stabilimenta of some orb web spiders represent an intriguing model system to investigate novel animal signals. For over 100 years, biologists have struggled to explain why spiders decorate their webs with additional threads of silk, producing a conspicuous signal on a construction whose function is to entangle unsuspecting prey. The numerous explanations for the maintenance of this behaviour starkly contrast with the absence of a plausible explanation for its evolutionary origin. Our review highlights the difficulties in resolving both the evolution and maintenance of animal signalling, and inferring the causative arrow—even from experimental studies. Drawing on recent research that focuses on physiological processes, we provide a model of the evolutionary progression of web‐decorating behaviour.

THE WASP SPIDER ARGIOPE BRUENNICHI (ARACHNIDA, ARANEIDAE): BALLOONING IS NOT AN OBLIGATE LIFE HISTORY PHASE

Abstract Aerial dispersal (“ballooning”) of Argiope bruennichi spiderlings has been claimed to be an obligate life history trait and a prerequisite for spinning prey-capture webs. If this were true, a ballooning phase would be essential for any laboratory rearing of A. bruennichi making rearing protocols particularly elaborate. We tested the significance of ballooning for second-instar spiderlings in the laboratory and showed that the ballooning behavior is not essential for building prey-capture orb webs. Our results also give no evidence for the hypothesis that recent natural selection has changed ballooning behavior in newly founded field populations.

Signals for damage control: web decorations in Argiope keyserlingi (Araneae: Araneidae)

Orb web spiders of the genus Argiope are permanently located at the hub of the orb web and are thus vulnerable to changing environmental conditions. Severe damage to the web by non-prey animals can have a significant impact on survival, through the cost of producing expensive silk and the loss of foraging opportunities. Thus, selection should favor web protection mechanisms, and the conspicuous web decorations, typical of Argiope spiders, may play a role. Decorated webs suffer less damage than undecorated webs, consistent with the view that they advertise the presence of the web to non-prey animals that may damage the web. However, whether spiders respond to web damage by increasing investment in web decorations has not been investigated. We subjected adult St. Andrews Cross spider (Argiope keyserlingi) females to three levels of web damage and recorded their subsequent web-decorating behavior. Mild damage, similar to that caused by impacting prey, did not affect either web building or decorating behavior. However, spiders subjected to substantial web damage both reduced the size of subsequent webs and increased investment in web decoration size. These data are consistent with an advertising role of web decorations.

Argiope bruennichi shows a drinking-like behaviour in web hub decorations (Araneae, Araneidae)

As stationary predators, araneid spiders that lack protective retreats are especially vulnerable to abiotic influences. Species of the genus Argiope permanently remain at the hub of their orb webs and are thereby exposed to desiccating circumstances. Like other land arthropods, spiders must balance their hygric status. Beside desiccation avoidance behaviours, they can manage this balance by water gain through either liquefied prey items or direct ingestions of free water. Drinking-like behaviours are sparely documented for Araneids. We observed Argiope bruennichi ingesting accumulated water droplets from the silk-overstitched web hub, a part of the web decoration, and subsequently tested whether this behaviour is a regular feature of this species. In 50% of our observations, spiders that had been sprayed with water actively searched the hub decoration for water droplets and ingested them. The behavioural elements were very stereotypic among the tested individuals. Significantly, A. bruennichi females only searched the covered web hubs for water, even though the entire web was moistened. These data suggest that hub decorations of A. bruennichi might have an adaptive significance by helping to maintain a balance of water metabolism, adding yet another element to the spirited debate about the functional significance of web decorations.

Diet influences female signal reliability for male mate choice

Pheromones, arguably the most ubiquitous mode of animal communication, are determined by both genetic and environmental factors. Recent evidence suggests that diet may be an important determinant of pheromone variation, which may both enhance and reduce the reliability of the chemical signal. We investigated experimentally the impact of population origin and diet on chemical signals used in mate assessment by monogynous males of the golden-banded orb web spider, Argiope trifasciata. Initial mate preference experiments revealed environmentally determined fine scaling of male mate choice: shortly after their introduction into the laboratory, male spiders preferred females from either their own or a nearby population rather than females from a distant population, suggesting that male choice is driven by phenotype matching, ensuring correct species identity. However, when diet was controlled, males preferred females originating from a distant rather than the same population, allowing males to choose a mate with the most potential genetic benefits. A second set of experiments clearly demonstrated that diet affected the chemical compounds on the surface of the silk threads produced by females, and that males preferred females that had experienced a similar diet. We suggest that phenotype matching strongly influences broad-scale male mating preferences, but it remains to be seen how a combination of genetic and environmental (e.g. dietary) factors influence the relative abundance of these, and perhaps other, mate choice-relevant, silk-bound chemical cues.

Molting interferes with web decorating behavior in Argiope keyserlingi (Araneae, Araneidae)

Abstract Various orb weaving spiders decorate their webs with extra silk structures. In the araneid genus Argiope, these web decorations consist of flimsy aciniform silk threads arranged in zig zag shaped bands. The adaptive value of these structures is still unclear and controversy over a suite of possible functional explanations persists: the high variation of web decoration adds further uncertainty. Web decorations can differ in shape, size, and frequency across species and even within species. Physiological processes may influence individual variation in web decorating behavior. Molting events are major physiological transitions combined with fundamental alterations of the metabolic state of the spiders. For gaining new insights into possible proximate mechanisms driving web decorating behavior, we observed subadult Argiope keyserlingi Karsch 1878 females in the laboratory and registered the individual variation of web decorations associated with the maturity molt under laboratory conditions. We found substantial individual variation of web decorations of A. keyserlingi. The most striking result was that subadult spiders built dramatically oversized decorations prior to the last molt. Since aciniform silk is used for both constructing web decorations and immobilizing prey we suggest that these extensive decorations might provide a store for the swift replenishment of aciniform silk after the molt. High silk recycling rates make temporary outsourcing less costly and facilitate a rapid resumption of prey capture following lost foraging opportunities during the molting phase. Thus, we argue that the solution of the riddle of web decorations might reside in the physiology of molting spiders.

Characterisation of protein families in spider digestive fluids and their role in extra-oral digestion

BackgroundSpiders are predaceous arthropods that are capable of subduing and consuming relatively large prey items compared to their own body size. For this purpose, spiders have evolved potent venoms to immobilise prey and digestive fluids that break down nutrients inside the prey’s body by means of extra-oral digestion (EOD). Both secretions contain an array of active proteins, and an overlap of some components has been anecdotally reported, but not quantified. We systematically investigated the extent of such protein overlap. As venom injection and EOD succeed each other, we further infer functional explanations, and, by comparing two spider species belonging to different clades, assess its adaptive significance for spider EOD in general.ResultsWe describe the protein composition of the digestive fluids of the mygalomorph Acanthoscurria geniculata and the araneomorph Stegodyphus mimosarum, in comparison with previously published data on a third spider species. We found a number of similar hydrolases being highly abundant in all three species. Among them, members of the family of astacin-like metalloproteases were particularly abundant. While the importance of these proteases in spider venom and digestive fluid was previously noted, we now highlight their widespread use across different spider taxa. Finally, we found species specific differences in the protein overlap between venom and digestive fluid, with the difference being significantly greater in S. mimosarum compared to A. geniculata.ConclusionsThe injection of venom precedes the injection with digestive fluid, and the overlap of proteins between venom and digestive fluid suggests an early involvement in EOD. Species specific differences in the overlap may reflect differences in ecology between our two study species. The protein composition of the digestive fluid of all the three species we compared is highly similar, suggesting that the cocktail of enzymes is highly conserved and adapted to spider EOD.

Signal polymorphism under a constant environment: the odd cross in a web decorating spider

The quality of many animal signals varies, perhaps through their use in different contexts or by representing an adaptive response to reduce the risk of exploitation. Spiders of the orb weaver genus Argiope add linear, cruciate or circular silk structures to their orb webs, creating inter- and intra-specific polymorphic visual signals. Different decoration patterns are frequently attributed to different signal effects, but this view is contradicted by commonly observed intraspecific variation in decorating behaviour. Adults of Argiope mascordi are bimodal web decorators, building two distinct patterns, circular and cruciate silk structures. We investigated the variation of patterns under controlled, invariant laboratory conditions. Circular decorations were most frequent, but individuals often switch to the other pattern. This variation neither increased nor decreased over time, suggesting that pattern variability is primarily intrinsic rather than an exclusive response to environmental changes. Accordingly, we discuss the evolutionary implications in the light of the conservation of a single signal function through maintaining the variation of its quality and the alternative view that silk decorations may not represent adaptive signals at all.

Drinking behaviour of the orb web spider Argiope bruennichi (Araneae; Araneidae)

Water is essential for survival in terrestrial animals. Balancing the water budget can be achieved by avoiding water loss and gaining water. In arthropods drinking as a process of water gain is well investigated in insects. In spiders drinking has only been shown to be present in cursorial spiders but not revealed for web builders. However, some orb web spiders were observed to occasionally ingest water droplets in the web. We here tested whether this reflects drinking. We subjected individual Argiope bruennichi spiders to two different treatments — water deprivation vs. water saturation. We conducted drinking tests by recording the spiders behavioural response to spraying the web with defined amounts of water. After spraying A. bruennichi searched the silk-overstitched web hub for water droplets and ingested them. Individuals that experienced the water deprivation treatment showed significantly more water ingesting behaviours, revealing that this response represents a true drinking mode. All individuals exclusively searched the covered web hubs. We further demonstrated that this structure can retain water for up to 40 min providing an effective substrate for the spiders to drink from. Hence, without the need of leaving the web the silk-covered hubs may help A. bruennichi spiders to balance their water budget.

Tracing the evolutionary origin of a visual signal: the coincidence of wrap attack and web decorating behaviours in orb web spiders (Araneidae)

The silk decorations that adorn the webs of many orb-web spiders are thought to have a signal function, but the evolution of the decorating behaviour remains unresolved. The decoration signal is maintained apparently because it improves foraging efficiency, through either increased encounter rates with prey or reduced damage to the web. Recent investigations suggest that the decorations may originate in a regulation of the activity of the aciniform silk glands, which produce silk for both decorating the web and wrapping prey. This view predicts a link between decorating behaviour and a preference for restraining prey by wrapping with silk, which is evident among species of Argiope spiders. Here I compare the frequency of the wrap attack behaviour in four species of orb-web spiders that occupy the same habitat, but differ in their silk decorating behaviour: two species, Plebs bradleyi and Gea theridioides, build silk decorations, while the other two, Araneus hamiltoni and Backobourkia brounii do not. Spiders were presented with prey items that varied in the ease with which they could be captured, with houseflies being more easily subdued than house crickets. As predicted, the silk decorating species used wrap attacks significantly more often than non-decorating spiders, irrespective of the prey species. These data support the view that both behaviours are evolutionary linked. I propose that silk decorating originated from the evolution of wrap attacking, and that silken web decorations have later evolved into a signal and are now maintained for that function.