Pisauridae Research Articles

Taxonomic notes on the nursery-web spider genus Dendrolycosa Doleschall, 1859 (Araneae: Pisauridae) from India, with the description of a new species.

A new species of the nursery-web spider genus Dendrolycosa Doleschall, 1859, D. sahyadriensis spec. nov. () is described from the Mookambika Wildlife Sanctuary, Karnataka, India. Detailed morphological descriptions, diagnoses and illustrations of the copulatory organs of both sexes are provided. The status of the Dendrolycosa species in India is also given, along with a distribution map.

Dragline silk reveals female developmental stage and mediates male vibratory courtship in the nuptial gift‐giving spider Pisaura mirabilis

AbstractMale mate choice likely occurs when costs are associated with courtship or mating. For example, when males produce continuous vibrational signals, provide nutritious nuptial gifts, or are likely killed during mating, they should assess female developmental and reproductive state. Substrate‐borne vibratory courtship signals are very common in spiders serving species recognition, suppressing the female's aggression towards the male, or signalling individual quality. Males of the nursery web spider, Pisaura mirabilis, usually offer a prey item wrapped in silk as a nuptial gift to the female; the gift is commonly produced prior to female contact. When touching dragline silk deposited by a female, males tremulate their opisthosoma presumably reacting to chemical cues. Courtship energy expenditure and resource transfer should select for selective male mating decisions in this species. We hypothesized that male P. mirabilis differentiate between developmental stages of the female (sub‐adult vs. adult). Differential courtship towards virgin and mated females was not expected since females forage for nuptial gifts and might continuously signal receptivity. To test this, vibrational courtship signals of male spiders towards draglines of sub‐adult, adult unmated and mated females were recorded with a Laser Doppler Vibrometer. We found that males were less likely to perform vibrational courtship and produced less pulses when contacting silk of sub‐adult females, compared to silk produced by adult females, while their reaction towards silk of unmated and mated adult females did not differ. Reduced courtship in response to sub‐adult female silk seems beneficial since it reduces energy expenditure in the face of a not yet reproductive female. When vibratory courtship occurred, the temporal patterns and dominant frequencies of the males' vibratory signals were similar, regardless of female developmental stage or mating status. Such stable patterns suggest a role in species recognition already at a distance without direct physical contact and in reducing female aggression.

Condition-dependent differences in male vibratory pre-copulatory and copulatory courtship in a nuptial gift-giving spider

Condition-dependent secondary sexual traits and signals are often crucial for mate choice decisions. Nuptial gifts, provided by the male to the female during mating, may represent an indicator of male condition, especially if production of the gift is energetically costly. Additionally, other signalling modalities may well play a role in mate choice in such systems. Females of the nursery web spider Pisaura mirabilis preferably mate with males that provide a prey item wrapped in silk. Apart from the nuptial gift, vibrational signals employed during courtship and mating may reveal additional information about male condition. We tested condition-dependence of male vibrational signals of well-fed versus starved males, when in contact with female dragline silk and during mating trials. Our results show that vibrational signals are produced in P. mirabilis, both during pre-copulatory courtship and during copulation. Male courtship signals were condition-dependent: males in good condition initiated signalling earlier and emitted more vibrational pulses than poor-condition males. They were also more likely to be accepted by the female for copulation. We additionally identified vibrational signals during copulation. These signals were different from pre-copulatory courtship vibrations but did not differ between the treatment groups. This study shows that vibrational communication plays an important role before and during copulation in P. mirabilis. It sets the stage for further experiments on spider biotremology associated with nuptial gift giving behaviour.Significance statementMale courtship behaviour can indicate a male’s condition and quality and be subject to female mate choice. Vibrational communication during mating plays a crucial role in many animal species. Spiders are known to be extremely sensitive towards vibrations, and there is evidence that vibratory signals are also used during courtship. Here, we study the nuptial gift-giving spider Pisaura mirabilis in which courtship entails providing a nuptial gift by the male to the female. The gift quality determines on the probability and duration of mating. We investigated the role of vibrational behaviour in this species by standardizing nuptial gifts. Our study demonstrates that vibratory signals comprise information about the male’s condition, that signals are also produced during mating and that courtship and copulatory signals are strikingly different. We suggest that vibrational communication provides important condition-dependent traits for female mate choice in addition to the nuptial gift.

Woodlice change the habitat use of spiders in a different food chain.

BackgroundIn old field systems, the common woodlouse may have an indirect effect on a nursery web spider. Woodlice and nursery web spiders feed in different food chains, yet previous work demonstrated that the presence of woodlice is correlated with higher predation success by nursery web spiders upon their grasshopper prey. This finding suggested a new hypothesis which links two seemingly disparate food chains: when woodlice are present, the spider predator or the grasshopper prey changes their location in the vegetative canopy in a way that increases their spatial overlap and therefore predation rate. However, warming temperatures may complicate this phenomenon. The spider cannot tolerate thermal stress, meaning warming temperatures may cause the spider to move downwards in the vegetative canopy or otherwise alter its response to woodlice. Therefore, we would expect warming and woodlice presence to have an interactive effect on predation rate.MethodsWe conducted behavioral experiments in 2015, 2017, and 2018 to track habitat domains—the use of the vegetative canopy space by grasshoppers and spiders—in experimental cages. Then, we used three models of spider movement to try to explain the response of spiders to woodlice: expected net energy gain, signal detection theory, and individual-based modelling.ResultsHabitat domain observations revealed that spiders shift upward in the canopy when woodlice are present, but the corresponding effect on grasshopper prey survival was variable over the different years of study. Under warming conditions, spiders remained lower in the canopy regardless of the presence of woodlice, suggesting that thermal stress is more important than the effect of woodlice. Our modelling results suggest that spiders do not need to move away from woodlice to maximize net energy gain (expected net energy gain and signal detection theory models). Instead spider behavior is consistent with the null hypothesis that they move away from unsuccessful encounters with woodlice (individual-based simulation). We conclude that mapping how predator behavior changes across biotic (e.g. woodlouse presence) and abiotic conditions (e.g. temperature) may be critical to anticipate changes in ecosystem dynamics.

The complete mitochondrial genome of a nursery-web spider Dolomedes angustivirgatus (Araneae: Pisauridae)

The complete mitochondrial genome of a nursery-web spider Dolomedes angustivirgatus is 14,783 bp in length and contains a standard set of 37 genes including 13 protein-coding genes, 22 transfer RNAs, 2 ribosomal RNAs and a putative control region. The A + T content of the major strand is 77.0%. All the protein-coding genes are initiated by typical ATN codons, except for COII and COIII, which use a special start codon TTG. The truncated stop codon (T) occurs in ND4L, whereas the rest 12 genes end with the canonical stop codon (TAA and TAG). 15 tRNAs cannot be folded into typical cloverleaf-shaped secondary structure. The control region is 1084 bp in length and contains a long tandem repeat region. The result of phylogenetic analysis show that D. angustivirgatus is nested within Lycosoidea and recovered as sister to the cluster of three wolf spiders (Lycosidae).

NMR assignments of a dynamically perturbed and dimerization inhibited N-terminal domain variant of a spider silk protein from E. australis.

Web spiders use specialized glands to produce silk proteins, so-called spidroins, which assemble into extraordinarily tough silk fibers through tightly regulated phase and structural transitions. A crucial step in the polymerization of spidroins is the pH-triggered assembly of their N-terminal domains (NTDs) into tight dimers. Major ampullate spidroin NTDs contain an unusually high content of the amino acid methionine. We previously showed that the simultaneous mutation of the six hydrophobic core methionine residues to leucine in the NTD of the major ampullate spidroin 1 from Euprosthenops australis, a nursery web spider, yields a protein (L6-NTD) retaining a three-dimensional fold identical to the wildtype (WT) domain, yet with a significantly increased stability. Further, the dynamics of the L6-NTD are significantly reduced and the ability to dimerize is severely impaired compared to the WT domain. These properties lead to significant changes in the NMR spectra between WT and L6-NTD so that the previously available WT-NTD assignments cannot be transferred to the mutant protein. Here, we thus report the de novo NMR backbone and side chain assignments of the major ampullate spidroin 1 L6-NTD variant from E. australis as a prerequisite for obtaining further insights into protein structure and dynamics.

Methionine in a protein hydrophobic core drives tight interactions required for assembly of spider silk

Web spiders connect silk proteins, so-called spidroins, into fibers of extraordinary toughness. The spidroin N-terminal domain (NTD) plays a pivotal role in this process: it polymerizes spidroins through a complex mechanism of dimerization. Here we analyze sequences of spidroin NTDs and find an unusually high content of the amino acid methionine. We simultaneously mutate all methionines present in the hydrophobic core of a spidroin NTD from a nursery web spider’s dragline silk to leucine. The mutated NTD is strongly stabilized and folds at the theoretical speed limit. The structure of the mutant is preserved, yet its ability to dimerize is substantially impaired. We find that side chains of core methionines serve to mobilize the fold, which can thereby access various conformations and adapt the association interface for tight binding. Methionine in a hydrophobic core equips a protein with the capacity to dynamically change shape and thus to optimize its function.

Male preferences for nuptial gifts and gift weight loss amongst the nursery web spider, Pisaura mirabilis

Sexual signals produced by males are costly. Thus, sexual selection may favour males who are able to minimise these costs, but are still reproductively successful. I investigated male preferences for large and small prey used to produce nuptial gifts, which serve as sexual signals in the nursery web spider, Pisaura mirabilis. Males showed strong preferences for large prey compared to small prey for gift production, which is likely to be more attractive for females and provide males with longer copulation. These preferences were strongest in the presence of female pheromonal cues. Unexpectedly, carrying nuptial gifts did not influence male mobility measured in a 5-min-long behavioural test. Both gifts carried by males and the intact gifts showed similar decreases in mass, suggesting that males did not actively suck the content of the gift. Wrapping the gift with silk did not effectively reduce the gift’s dehydration, meaning that the function of the silk is not to protect the gift’s contents. Males in poor body condition were more likely to feed on the prey before wrapping it. This is consistent with condition dependent signalling, as males in low condition are predicted to feed on the prey as they are not able to pay the cost of gift production. Males preferred large-sized prey for gift production and males in poor body condition reduced the cost of gift production by feeding on the prey, supporting the idea that nuptial feeding is condition dependent.

Two-step self-assembly of a spider silk molecular clamp

Web spiders synthesize silk fibers of unique strength and extensibility through the controlled self-assembly of protein building blocks, so-called spidroins. The spidroin C-terminal domain is highly conserved and connects two polypeptide chains through formation of an all-helical, intertwined dimer. Here we use contact-induced fluorescence self-quenching and resonance energy transfer in combination with far-UV circular dichroism spectroscopy as three orthogonal structural probes to dissect the mechanism of folding and dimerization of a spidroin C-terminal domain from the major ampullate gland of the nursery web spider Euprosthenops australis. We show that helices forming the dimer core assemble very rapidly and fold on association. Subsequently, peripheral helices fold and dock slowly onto the preformed core. Lability of outer helices facilitates formation of a highly expanded, partially folded dimer. The high end-to-end distance of chain termini in the partially folded dimer suggests an extensibility module that contributes to elasticity of spider silk.

Female nursery web spiders (Pisaurina mira) benefit from consuming their mate

AbstractThe often coincidental involvement of cooperation and conflict in animal reproduction is epitomized by sexual cannibalism, which can lead to obvious male costs while simultaneously providing direct benefits to developing offspring. Male nursery web spiders (Pisaurina mira) avoid postcopulatory sexual cannibalism by wrapping females with silk. Here, we test the hypothesis that this silk wrapping results in a loss of consumption cost for females. In specific, we hypothesize that females lose out on potential fitness benefits associated with cannibalizing their mating partners. To test this, we paired females with males that were experimentally manipulated to prevent the silk wrapping of females, thereby increasing the likelihood of sexual cannibalism. Females either did not kill their mate, and thus consumed nothing, or did kill their mate. If females killed their mating partner, we allowed them to consume the male, consume nothing, or consume a cricket. We found no effect of female or male body sizes on the likelihood of females killing their mate. While our treatments did not affect the number of offspring females produced, females that consumed either a male or a cricket produced egg sacs faster than females that consumed nothing, suggesting a benefit of increased postcopulatory food consumption. Further, only females that ate a male had heavier and longer lived offspring, suggesting a benefit of sexual cannibalism specifically. Our results support the hypothesis that females can receive fitness benefits associated with sexual cannibalism.

Males mate with multiple females to increase offspring numbers in a nursery web spider

Male spiders wrap female’s legs in silk before mating to increase their likelihood of surviving a female’s cannibalistic attack. We demonstrate that surviving such an attack allows males to acquire future matings. Mating with multiple females in the laboratory increased males’ offspring production. Using demographic data, we constructed a mathematical model that suggests that males have the opportunity to mate with multiple partners in our population given that female encounter rates are sufficiently high.

Increased insertion number leads to increased sperm transfer and fertilization success in a nursery web spider

Across animals, a male's fitness is largely dictated by his ability to fertilize eggs; and there exists a plethora of male adaptations associated with increasing fertilization success. In the nursery web spider, Pisaurina mira, males restrain females prior to and during copulation by wrapping them with silk. Previous research demonstrates that copulatory silk wrapping reduces a male's chance of being sexually cannibalized and increases the number of sperm transfer opportunities (termed insertions) that a male can achieve within a mating. While avoiding cannibalism provides an obvious survival benefit to males, the impact of insertion number on male fitness remains unknown. This study tested the hypothesis that increased insertion number realized through copulatory silk wrapping increases (1) the quantity of sperm transferred and (2) fertilization success. To accomplish this, we directly quantified the amount of sperm in male pedipalps (i.e. the male sperm storage organ) before mating and after obtaining one or two insertions. We also, indirectly quantified fertilization success by measuring the number of hatched offspring when males were capable of achieving one versus two insertions within a mating. In support of our hypotheses, we found that males transfer roughly twice the amount of sperm when achieving two insertions compared to one. We additionally found that the amount of sperm transferred is negatively related to female size. In terms of offspring number, females obtaining two insertions had more offspring compared to females obtaining only one insertion. These results show that males achieve a fertilization benefit from increased insertion number, which is obtained through the male behaviour of copulatory silk wrapping.

Natural enemies partially compensate for warming induced excess herbivory in an organic growth system

Predators can limit prey abundance and/or levels of activity. The magnitudes of these effects are contingent on predator and prey traits that may change with environmental conditions. Aberrant thermal regimes could disrupt pest suppression through asymmetric effects, e.g. heat-sensitive predator vs. heat-tolerant prey. To explore potential effects of warming on suppressing pests and controlling herbivory in a vegetable crop, we performed laboratory experiments exposing an important pest species to two spider predator species at different temperatures. Heat tolerance was characterised by the critical thermal maxima parameter (CTM50) of the cucumber beetle (Diabrotica undecimpunctata), wolf spider (Tigrosa helluo), and nursery web spider (Pisaurina mira). Cucumber beetles and wolf spiders were equally heat tolerant (CTM50 > 40 °C), but nursery web spiders had limited heat tolerance (CTM50 = 34 °C). Inside mesocosms, beetle feeding increased with temperature, wolf spiders were always effective predators, nursery web spiders were less lethal at high temperature (38 °C). Neither spider species reduced herbivory at ambient temperature (22 °C), however, at warm temperature both species reduced herbivory with evidence of a dominant non-consumptive effect. Our experiments highlight the contingent nature of predator-prey interactions and suggest that non-consumptive effects should not be ignored when assessing the impact of temperature change.

Benefits of size dimorphism and copulatory silk wrapping in the sexually cannibalistic nursery web spider, Pisaurina mira.

In sexually cannibalistic animals, male fitness is influenced not only by successful mate acquisition and egg fertilization, but also by avoiding being eaten. In the cannibalistic nursery web spider, Pisaurina mira, the legs of mature males are longer in relation to their body size than those of females, and males use these legs to aid in wrapping a female's legs with silk prior to and during copulation. We hypothesized that elongated male legs and silk wrapping provide benefits to males, in part through a reduced likelihood of sexual cannibalism. To test this, we paired females of random size with males from one of two treatment groups-those capable of silk wrapping versus those incapable of silk wrapping. We found that males with relatively longer legs and larger body size were more likely to mate and were less likely to be cannibalized prior to copulation. Regardless of relative size, males capable of silk wrapping were less likely to be cannibalized during or following copulation and had more opportunities for sperm transfer (i.e. pedipalpal insertions). Our results suggest that male size and copulatory silk wrapping are sexually selected traits benefiting male reproductive success.

Intraspecific differences in plant chemotype determine the structure of arthropod food webs.

It is becoming increasingly appreciated that the structure and functioning of ecological food webs are controlled by the nature and level of plant chemicals. It is hypothesized that intraspecific variation in plant chemical resistance, in which individuals of a host-plant population exhibit genetic differences in their chemical contents (called 'plant chemotypes'), may be an important determinant of variation in food web structure and functioning. We evaluated this hypothesis using field assessments and plant chemical assays in the tansy plant Tanacetum vulgare L. (Asteraceae). We examined food webs in which chemotypes of tansy plants are the resource for two specialized aphids, their predators and mutualistic ants. The density of the ant-tended aphid Metopeurum fuscoviride was significantly higher on particular chemotypes (borneol) than others. Clear chemotype preferences between predators were also detected. Aphid specialist seven-spotted ladybird beetles (Coccinella septempunctata) were more often found on camphor plants, while significantly higher numbers of the polyphagous nursery web spider (Pisaura mirabilis) were observed on borneol plants. The analysis of plant chemotype effects on the arthropod community clearly demonstrates a range of possible outcomes between plant-aphid-predator networks. The findings help to offer a deeper insight into how one important factor--plant chemical content--influences which species coexist within a food web on a particular host plant and the nature of their trophic linkages.

Nukuhiva Berland, 1935 is a troglobitic wolf spider (Araneae: Lycosidae), not a nursery-web spider (Pisauridae).

The monotypic genus Nukuhiva Berland, 1935 with N. adamsoni (Berland, 1933) as type species, is re-described and transferred from the Pisauridae Simon, 1890 (fishing or nursery-web spiders) to the Lycosidae Sundevall, 1833 (wolf spiders) based on genitalic and somatic characters. Nukuhiva adamsoni, originally described from French Polynesia, appears to inhabit mountainous habitats of volcanic origin. Its troglobitic morphology--comparatively small eyes and pale, uniform coloration--suggest it to be associated with subterranean habitats such as caves or lava tubes, similar to the Hawaiian troglobitic species Lycosa howarthi Gertsch, 1973 and Adelocosa anops Gertsch, 1973.

Sublethal effects of imidacloprid on interactions in a tritrophic system of non-target species

Imidacloprid is one of the most used insecticides worldwide, but is highly toxic to non-target arthropods. Effects of sublethal imidacloprid intoxication can potentially propagate in food webs, yet little is known about the impact on non-target populations and communities. We investigated short-term sublethal toxicity of imidacloprid in a tritrophic model system of wild strawberry Fragaria vesca, wood cricket Nemobius sylvestris and nursery web spider Pisaura mirabilis. Strawberries were treated two times with 0mg (control), 1mg (low rate) and 10mg (high rate) of Confidor® WG 70 and crickets were allowed to feed on them. In four lab experiments, we quantified the impact of imidacloprid on leaf damage, growth, behaviour and survival of crickets. The high imidacloprid rate reduced feeding, mass gain, thorax growth and mobility in crickets compared to the control, while mortality was similarly low in all treatments. The low rate reduced mass gain only. Cricket survival of spider predation was higher in the low rate treatment than in the control.Overall, herbivory and predation were reduced at sublethal imidacloprid rates in a non-target organism, three-level food chain, which demonstrates possible propagation of sublethal effects through trophic interactions.

Plant choice, herbivory and weight gain of wood crickets under the risk of predation

Predators can indirectly reduce herbivory by killing herbivores. In addition, predation risk can influence the feeding rate and feeding location of herbivores. Herbivores are expected to avoid plants currently occupied by a predator. Consequently, less herbivory is expected on plants bearing fresh predator cues. We examined whether wood crickets, Nemobius sylvestris Bosc (Orthoptera: Gryllidae), avoided plants bearing the chemical cues of nursery web spiders, Pisaura mirabilis Clerck (Araneae: Pisauridae), or red wood ants, Formica rufa L. (Hymenoptera: Formicidae). We conducted a series of behavioural experiments, in which crickets had the choice between a plant with spider or ant cues vs. a control plant, a plant with spider cues vs. a plant with ant cues, or two control plants. For all plants, we quantified leaf damage and the position and weight change in the crickets. Crickets avoided plants with spider cues. In contrast, ant cues did not significantly deter crickets. The herbivory pattern among the plants reflected the plant choice of the crickets. However, net herbivory was not affected by the presence of predator cues. Thus, our results suggest that spider cues affect feeding location rather than the total amount of herbivory.

Chemotype of tansy (Tanacetum vulgareL.) determines aphid genotype and its associated predator system

Field assessments and genetic analyses on tansy aphid, Metopeurum fuscoviride Stroyan were made aiming to investigate whether a specialist aphid species and its associated predator density differ between chemotypes of the plant host, tansy, and whether the essential oil composition of the plant host determines the genetic differences observed between colonies of M. fuscoviride inhabiting these different chemotypes. Tansy plants were defined after volatile extractions as Camphor Pure and Borneol Pure, respectively, with hybrid chemotypes defined as Camphor Hybrid, Borneol Hybrid, and Thujone Hybrid, respectively. Ladybird beetles, Coccinella septempunctata (L.), clearly dominated Pure Camphor plants, whereas significantly higher numbers of the nursery web spider, Pisaura mirabilis (Clerck), were detected on Borneol Pure and Borneol Hybrid plants. Genetic analyses using five polymorphic microsatellite markers revealed that higher genetic similarity existed between M. fuscoviride aphids from Borneol Pure and Borneol Hybrid plants and between Camphor Pure and Camphor Hybrid plants, respectively, whereas a lower level of genetic similarity was seen between these aphids from Thujone Hybrid plants. Accordingly, it is possible that host plant-adapted species can create much context-dependency in the nature and strength of predation effects, which may in turn alter costs and benefits of host plant chemical differentiations, or even the prey genotype variations. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 114, 709–719.

Microsecond folding and domain motions of a spider silk protein structural switch.

Web spiders rapidly assemble protein monomers, so-called spidroins, into extraordinarily tough silk fibers. The process involves the pH-triggered self-association of the spidroin N-terminal domain (NTD), which contains a structural switch connecting spidroins to supermolecules. Single-molecule spectroscopy can detect conformational heterogeneity that is hidden to conventional methods, but motions of the NTD are beyond the resolution limit. Here, we engineered probes for 1 nm conformational changes based on the phenomenon of fluorescence quenching by photoinduced electron transfer into the isolated NTD of a spidroin from the nursery web spider Euprosthenops australis. Correlation analysis of single-molecule fluorescence fluctuations uncovered site-dependent nanosecond-to-microsecond movement of secondary and tertiary structure. Kinetic amplitudes were most pronounced for helices that are part of the association interface and where structural studies show large displacements between monomeric and dimeric conformations. A single tryptophan at the center of the five-helix bundle toggled conformations in ∼100 μs and in a pH-dependent manner. Equilibrium denaturation and temperature-jump relaxation experiments revealed cooperative and ultrafast folding in only 60 μs. We deduced a free-energy surface that exhibits native-state ruggedness with apparently similar barrier heights to folding and native motions. Observed equilibrium dynamics within the domain suggest a conformational selection mechanism in the rapid association of spidroins through their NTDs during silk synthesis by web spiders.