The allometry of CNS size and consequences of miniaturization in orb-weaving and cleptoparasitic spiders

Allometric studies of the gross neuroanatomy of adults from nine species of spiders from six web-weaving families (Orbicularia), and nymphs from six of these species, show that very small spiders resemble other small animals in having disproportionately larger central nervous systems (CNSs) relative to body mass when compared with large-bodied forms. Small spiderlings and minute adult spiders have similar relative CNS volumes. The relatively large CNS of a very small spider occupies up to 78% of the cephalothorax volume. The CNSs of very small spiders extend into their coxae, occupying as much as 26% of the profile area of the coxae of an Anapisona simoni spiderling (body mass < 0.005 mg). Such modifications occur both in species with minute adults, and in tiny spiderlings of species with large-bodied adults. In at least one such species, Leucauge mariana, the CNS of the spiderling extends into a prominent ventral bulge of the sternum. Tiny spiders also have reduced neuronal cell body diameters. The adults of nearly all orbicularian spiders weave prey capture webs, as do the spiderlings, beginning with second instar nymphs. Comparable allometric relations occur in adults of both orb-weaving and cleptoparasitic species, indicating that this behavioral difference is not reflected in differences in gross CNS allometry.     

Behavioural and biomaterial coevolution in spider orb webs

Mechanical performance of biological structures, such as tendons, byssal threads, muscles, and spider webs, is determined by a complex interplay between material quality (intrinsic material properties, larger scale morphology) and proximate behaviour. Spider orb webs are a system in which fibrous biomaterials—silks—are arranged in a complex design resulting from stereotypical behavioural patterns, to produce effective energy absorbing traps for flying prey. Orb webs show an impressive range of designs, some effective at capturing tiny insects such as midges, others that can occasionally stop even small birds. Here, we test whether material quality and behaviour (web design) co‐evolve to fine‐tune web function. We quantify the intrinsic material properties of the sticky capture silk and radial support threads, as well as their architectural arrangement in webs, across diverse species of orb‐weaving spiders to estimate the maximum potential performance of orb webs as energy absorbing traps. We find a dominant pattern of material and behavioural coevolution where evolutionary shifts to larger body sizes, a common result of fecundity selection in spiders, is repeatedly accompanied by improved web performance because of changes in both silk material and web spinning behaviours. Large spiders produce silk with improved material properties, and also use more silk, to make webs with superior stopping potential. After controlling for spider size, spiders spinning higher quality silk used it more sparsely in webs. This implies that improvements in silk quality enable ‘sparser’ architectural designs, or alternatively that spiders spinning lower quality silk compensate architecturally for the inferior material quality of their silk. In summary, spider silk material properties are fine‐tuned to the architectures of webs across millions of years of diversification, a coevolutionary pattern not yet clearly demonstrated for other important biomaterials such as tendon, mollusc byssal threads, and keratin.     

Ballooning propensity of canopy and understorey spiders in a mature temperate hardwood forest

1. Spiders frequently disperse and colonise habitats through ballooning, a passive aerial dispersal process. Ballooning is pre‐eminent in open habitat spider communities and its propensity can be modulated by habitat conditions and availability, and by life‐history traits such as body size, degree of specialisation, and feeding behaviour. 2. Using spiders from the canopy and understorey of a north‐temperate hardwood forest as a model system, our main objectives were to detect if foliage spiders of a mature forest disperse through ballooning, and identify life‐history traits that influence ballooning propensity. 3. Our results demonstrate that foliage spiders living in the canopy and understorey of a mature forest do balloon, and in some cases have very high ballooning propensities similarly to open field spiders. Species level models showed that small body size had a strong positive effect on ballooning for juveniles of species with large‐bodied adults, while individuals of small‐bodied species initiated ballooning regardless of size, habitat or development stage. A generalised linear mixed model indicated that small size web‐building spiders from the Retro Tibial Apophysis (RTA) and Orbicularia clades had the highest propensity for foliage spiders of this north‐temperate hardwood forest. 4. In conclusion, we provide the first demonstration that forest spiders can have high ballooning propensities and that ballooning propensity is negatively affected by body size and positively affected by the prominent use of silk to catch prey. However, spiders originating from the canopy and understorey of a north‐temperate hardwood forest did not differ in their ballooning propensities.     

Task specialization in two social spiders,Stegodyphus sarasinorum (Eresidae) and Anelosimus eximius (Theridiidae)

Understanding the social organization of group‐living organisms is crucial for the comprehension of the underlying selective mechanisms involved in the evolution of cooperation. Division of labour and caste formation is restricted to eusocial organisms, but behavioural asymmetries and reproductive skew is common in other group‐living animals. Permanently, social spiders form highly related groups with reproductive skew and communal brood care. We investigated task differentiation in nonreproductive tasks in two permanently and independently derived social spider species asking the following questions: Do individual spiders vary consistently in their propensity to engage in prey attack? Are individual spiders' propensities to engage in web maintenance behaviour influenced by their previous engagement in prey attack? Interestingly, we found that both species showed some degree of task specialization, but in distinctly different ways: Stegodyphus sarasinorum showed behavioural asymmetries at the individual level, that is, individual spiders that had attacked prey once were more likely to attack prey again, independent of their body size or hunger level. In contrast, Anelosimus eximius showed no individual specialization, but showed differentiation according to instar, where adult and subadult females were more likely to engage in prey attack than were juveniles. We found no evidence for division of labour between prey attack and web maintenance. Different solutions to achieve task differentiation in prey attack for the two species studied here suggest an adaptive value of task specialization in foraging for social spiders.     

Sexual Selection in the Water Spider: Female Choice and Male–Male Competition

The water spider Argyroneta aquatica is the only spider spending its whole life under water, and one of the few spider species in which males are larger than females. Previous studies indicated that males can cannibalize females, which is uncommon among spiders. Here we aimed to further test for a potential influence of sexual selection on male body size. We examined the importance of female choice by testing whether females prefer the larger of two simultaneously presented males as mating partners. Further, we examined the influence of male–male competition by comparing the fighting behaviour between large and small males when alone or when together with a female, and we determined the outcome of fights. We found that females approach and choose large males as mating partners, despite the risk of male cannibalism. Additionally, males intensively compete for females, and large males clearly win against smaller ones. Hence sexual selection seems to be important for the evolution of the peculiar sexual size dimorphism of water spiders, as large size is beneficial for males in both the intra‐ and intersexual context. Previous studies have suggested an important role of natural selection in the sex‐specific body size of water spiders, but natural and sexual selection mechanisms apparently work in the same direction, favouring large male size.     

Rearing environment affects behaviour of jumping spiders

We tested the effect of rearing conditions on the behaviour of jumping spiders, Phidippus audax. Spiders were assigned randomly to either small or large cages that either were empty or contained a painted dowel. Laboratory-reared spiders were raised from second instar to adult in these environments. Field-caught adults also were randomly assigned to these containers and were held for approximately 4 months prior to testing. We presented spiders with three tests designed to examine a range of behaviours. Field-caught spiders were more likely than laboratory-reared spiders to (1) react to videotaped prey, (2) progress further on a detour test, and (3) be less stereotactic and more active in an open field. Larger cage size and the presence of the dowel also improved performance in several tests. Our results suggest that the rearing conditions we used, which are commonly employed by behavioural researchers, may profoundly influence the behaviour of adult spiders. Copyright 2000 The Association for the Study of Animal Behaviour.     

Maternal care and subsocial behaviour in spiders

While most spiders are solitary and opportunistically cannibalistic, a variety of social organisations has evolved in a minority of spider species. One form of social organisation is subsociality, in which siblings remain together with their parent for some period of time but disperse prior to independent reproduction. We review the literature on subsocial and maternal behaviour in spiders to highlight areas in which subsocial spiders have informed our understanding of social evolution and to identify promising areas of future research. We show that subsocial behaviour has evolved independently at least 18 times in spiders, across a wide phylogenetic distribution. Subsocial behaviour is diverse in terms of the form of care provided by the mother, the duration of care and sibling association, the degree of interaction and cooperation among siblings, and the use of vibratory and chemical communication. Subsocial spiders are useful model organisms to study various topics in ecology, such as kin recognition and the evolution of cheating and its impact on societies. Further, why social behaviour evolved in some lineages and not others is currently a topic of debate in behavioural ecology, and we argue that spiders offer an opportunity to untangle the ecological causes of parental care, which forms the basis of many other animal societies.     

Does body size influence thermal biology and diet of a python (Morelia spilota imbricata)?

Current theory predicts that larger‐bodied snakes not only consume larger prey (compared with smaller individuals), but may also have a different range of prey available to them due to their thermal biology. It has been argued that smaller individuals, with lower thermal inertia (i.e. faster cooling rates at nightfall when air temperature falls and basking opportunities are limited), may be thermally restricted to foraging and hunting during the day on diurnally active prey, and have reduced capacity to hunt crepuscular and nocturnal prey species. This predictive theory was investigated by way of dietary analysis, assessment of thermal biology and thermoregulation behaviour in an ambush forager, the south‐west carpet python (Morelia spilota imbricata, Pythonidae). Eighty‐seven scats were collected from 34 individual pythons over a 3‐year radiotelemetry monitoring study. As predicted by gape size limitation, larger pythons took larger prey; however, 65% of prey items of small pythons were represented by nocturnally active, small mammals, a larger proportion than present in larger snakes. Several measures of thermal biology (absolute body temperature, thermal differential of body temperature to air temperature, maximum hourly heating and cooling rates) were not strongly affected by python body mass. Additionally, body temperature was only influenced by the behavioural choice of microhabitat selection and was not affected by python body size or position, suggesting that these behavioural choices do not allow smaller pythons to vastly increase their temporal foraging window. By coupling dietary analysis, measures of body temperature and behavioural observations of free‐ranging animals, we conclude that, contrary to theoretical predictions, a small body size does not thermally restrict the temporal window for ambush foraging in M. s. imbricata. An ontogenetic or size‐determined switch from ambush feeding to actively foraging on slower prey would account for the differences in prey taken by these animals. The concept of altered foraging behaviour warrants further investigation in this species.     

Mating‐Associated Changes in the Behaviour of Leptothorax gredleri Ant Queens

Throughout their lives, animals adapt their behaviour to environmental fluctuations and to their own requirements. In social insects, behavioural changes are often particularly conspicuous. For example, in many ant species, reproductive sexuals leave their maternal nests and engage in risky mating and dispersal activities. Female sexuals experience, during a short period of time, dramatic changes in terms of behaviour and environmental conditions. But because sexual activities of ants are not easily observed, few studies have quantified in detail how behaviour alters with maturation and mating. We studied how various behavioural traits of Leptothorax gredleri female sexuals, a species in which female sexuals attract males by ‘female calling’, change before and after mating. We tested the hypothesis that behavioural variation reflects the altered requirements of queens to adapt to a particular situation. To this end, we compared geotactic, phototactic and locomotor behaviour across a wide range of life stages from lightly coloured, unmated female sexuals to old, mated queens. The results showed that female sexuals of L. gredleri change conspicuously their geotactic, phototactic and locomotor behavioural traits over their life stages. Three different behavioural states were evident (1) from light to dark female sexuals, individuals have negative phototaxis and reduced locomotor activity; (2) mature female sexuals during the daily period of sexual activity have strong phototaxis, negative geotaxis and an important locomotor activity; and (3) freshly mated and old mated queens avoid light and decrease their locomotor activity. These sharp differences in behaviour between stages match the transition from the relative safety of the nest chamber to the adversary world outside the nest , and back.     

The adaptive value of sociality in mammalian groups

According to behavioural ecology theory, sociality evolves when the net benefits of close association with conspecifics exceed the costs. The nature and relative magnitude of the benefits and costs of sociality are expected to vary across species and habitats. When sociality is favoured, animals may form groups that range from small pair-bonded units to huge aggregations. The size and composition of social groups have diverse effects on morphology and behaviour, ranging from the extent of sexual dimorphism to brain size, and the structure of social relationships. This general argument implies that sociality has fitness consequences for individuals. However, for most mammalian species, especially long-lived animals like primates, there are sizable gaps in the chain of evidence that links sociality and social bonds to fitness outcomes. These gaps reflect the difficulty of quantifying the cumulative effects of behavioural interactions on fitness and the lack of information about the nature of social relationships among individuals in most taxa. Here, I review what is known about the reproductive consequences of sociality for mammals.     

Salticid predation as one potential driving force of ant mimicry in jumping spiders

Many spiders possess myrmecomorphy, and species of the jumping spider genus Myrmarachne exhibit nearly perfect ant mimicry. Most salticids are diurnal predators with unusually high visual acuity that prey on various arthropods, including conspecifics. In this study, we tested whether predation pressure from large jumping spiders is one possible driving force of perfect ant mimicry in jumping spiders. The results showed that small non-ant-mimicking jumping spiders were readily treated as prey by large ones (no matter whether heterospecific or conspecific) and suffered high attack and mortality rates. The size difference between small and large jumping spiders significantly affected the outcomes of predatory interactions between them: the smaller the juvenile jumping spiders, the higher the predation risk from large ones. The attack and mortality rates of ant-mimicking jumping spiders were significantly lower than those of non-ant-mimicking jumping spiders, indicating that a resemblance to ants could provide protection against salticid predation. However, results of multivariate behavioural analyses showed that the responses of large jumping spiders to ants and ant-mimicking salticids differed significantly. Results of this study indicate that predation pressure from large jumping spiders might be one selection force driving the evolution of nearly perfect myrmecomorphy in spiders and other arthropods.     

Consequences of sexual size dimorphism on energetics and locomotor performance of Grammostola rosea (Araneae; Teraphosidae)

Most male spiders are smaller than females; during sexual maturity, males change their behaviour, abandoning their web or nest to seek out receptive females actively, whereas females stalk prey near their web or nest and tend not to move away from it. Considering this behavioural difference to be associated with increased locomotor activity at maturity, it may be hypothesized that males will have traits that increase locomotor performance. The present study examines the kinetics and energetics of the movements of the mygalomorph spider Grammostola rosea Walckenaer, a large spider with sexual size dimorphism. It is found that males have a higher maximum aerobic speed, average speed, distance travelled and critical angle of climbing than females, indicating better performance. Males also have lower costs of transport than females. These results support the hypothesis that sexual dimorphism in wandering spiders with active males, which are characterized by smaller body size and longer legs than the larger and more static females, is associated with low transport cost, high velocity and better locomotor performance.     

The feeding behaviour of New Zealand Dolomedes species (Araneae: Pisauridae)

Abstract

The prey spectrum and predatory behaviour of Dolomedes sp. (‘D. III’), D. aquaticus, and D. minor are described from a series of field and laboratory investigations, the former made around Nelson and on Banks Peninsula, Canterbury, during summer months. All species are large, robust spiders that capture prey by directly seizing it in their mouthparts, not using silk at any stage of predation. Adult aquatic insects are their main prey, but these are available only irregularly during their activity period (night-time), and the spiders are opportunistic in their feeding habits. They will eat virtually any available small animal, and at least the largest species, D. III, is able to capture and ingest small fishes. Dead as well as live organisms are taken. Furthermore, the spiders are capable of feeding infrequently; when feeding on small prey organisms they may capture several sequentially, to increase the size of the meal. Live prey is caught while it is in flight, or on the ground, or at the water surface (rarely submerged), and is detected primarily by touch and airborne sound; vision is unnecessary for normal predation. Prey is captured very rapidly, even though this may initially involve a dash of up to 40 cm across the water surface to locate the organism. Stages in the behaviour of an active spider, from waiting for prey to grooming after ingestion, are described.     

Personality composition is more important than group size in determining collective foraging behaviour in the wild

Describing the factors that shape collective behaviour is central to our understanding of animal societies. Countless studies have demonstrated an effect of group size in the emergence of collective behaviours, but comparatively few have accounted for the composition/diversity of behavioural phenotypes, which is often conflated with group size. Here, we simultaneously examine the effect of personality composition and group size on nest architecture and collective foraging aggressiveness in the social spider Stegodyphus dumicola. We created colonies of two different sizes (10 or 30 individuals) and four compositions of boldness (all bold, all shy, mixed bold and shy, or average individuals) in the field and then measured their collective behaviour. Larger colonies produced bigger capture webs, while colonies containing a higher proportion of bold individuals responded to and attacked prey more rapidly. The number of attackers during collective foraging was determined jointly by composition and size, although composition had an effect size more than twice that of colony size: our results suggest that colonies of just 10 bold spiders would attack prey with as many attackers as colonies of 110 ‘average’ spiders. Thus, personality composition is a more potent (albeit more cryptic) determinant of collective foraging in these societies.     

Age-related sequential web building in the colonial spider Metepeira incrassata (Araneidae): an adaptive spacing strategy

Colonial orb-weaving spiders provide insight into the proximate mechanisms by which social animals space themselves within a group. We examined mechanisms for the temporal patterns of web building that determine individual positions in Metepeira incrassata (Araneidae) colonies. The spiders display a characteristic age-related sequence of daily web building, with larger spiders completing their webs significantly earlier than smaller ones. We used data on behavioural interactions, web building, prey capture and predator attacks to evaluate four hypotheses. (1) Larger spiders are better competitors and pre-empt optimal spatial positions. (2) Smaller spiders reduce competition with larger individuals by building webs later. (3) Prey captured by different size classes is available at different times. (4) Differential predation risk determines web-building times. Large individuals dominated behavioural interactions. Disturbances by larger spiders during web construction significantly delayed the completion of smaller individuals' webs and precipitated movements to new web sites. One prediction of the first hypothesis, that spatial needs translate into earlier building, was confirmed by significantly earlier web building by mature females with egg sacs (which are unable to move their egg sacs) compared with same-sized females without eggs (which can change locations freely). Experiments to determine whether the presence of large spiders inhibited the web building of smaller individuals were equivocal. Prey availability and risk of predation are not factors affecting web-building patterns. Sequential web building appears to be a result of both larger spiders competing to pre-empt space from one another and smaller individuals attempting to reduce conflict during web construction. Sequential web building is a proximate mechanism that influences spacing among colonial orb-weaving spiders and helps shape the typical hierarchical size distribution of spiders within the colony. Similar spacing mechanisms may be seen in colonial birds and marine invertebrates. Copyright 2000 The Association for the Study of Animal Behaviour.     

Investment in higher order central processing regions is not constrained by brain size in social insects

The extent to which size constrains the evolution of brain organization and the genesis of complex behaviour is a central, unanswered question in evolutionary neuroscience. Advanced cognition has long been linked to the expansion of specific brain compartments, such as the neocortex in vertebrates and the mushroom bodies in insects. Scaling constraints that limit the size of these brain regions in small animals may therefore be particularly significant to behavioural evolution. Recent findings from studies of paper wasps suggest miniaturization constrains the size of central sensory processing brain centres (mushroom body calyces) in favour of peripheral, sensory input centres (antennal and optic lobes). We tested the generality of this hypothesis in diverse eusocial hymenopteran species (ants, bees and wasps) exhibiting striking variation in body size and thus brain size. Combining multiple neuroanatomical datasets from these three taxa, we found no universal size constraint on brain organization within or among species. In fact, small-bodied ants with miniscule brains had mushroom body calyces proportionally as large as or larger than those of wasps and bees with brains orders of magnitude larger. Our comparative analyses suggest that brain organization in ants is shaped more by natural selection imposed by visual demands than intrinsic design limitations.     

Individual decisions and group dynamics: why pholcid spiders join and leave groups

To examine the role of individual variation in the dynamics of group formation, I conducted a mark-recapture study and a series of laboratory and field experiments with Holocnemus pluchei spiders (Araneae: Pholcidae). These spiders can either share webs or live alone, and individuals shift frequently between these strategies. Spiders' decisions were influenced by size and recent feeding success. In the laboratory, small hungry spiders introduced into a web that held a larger conspecific resident were more likely than small well-fed spiders to abandon the web and build their own web. This behaviour pattern gradually reversed as spiders grew: large hungry spiders were more likely than large well-fed spiders to stay in the shared web. When I introduced spiders into empty webs, they were more likely to stay compared with spiders tested with conspecifics. However, hunger level also influenced behaviour even when conspecifics were not present. Food-deprived spiders were more likely to abandon webs and build their own, consistent with the idea that spiders were following a win-stay/lose-shift strategy. In the field, spiders were more likely to stay in webs overnight when they were given supplemental food. In another experiment, spiders that were found building webs in cleared areas were smaller and thinner than average. Finally, I tested whether the size of the intruder or the resident affected whether spiders joined webs. Large intruders were more successful at remaining in webs than smaller intruders, although spiders of all sizes had some success in joining groups. Additional synthetic theoretical work is needed to integrate the complex processes underlying the formation and persistence of groups.     

Inhibitory motoneurons in arthropod motor control: organisation,function, evolution

Miniaturisation of somatic cells in animals is limited, for reasons ranging from the accommodation of organelles to surface-to-volume ratio. Consequently, muscle and nerve cells vary in diameters by about two orders of magnitude, in animals covering 12 orders of magnitude in body mass. Small animals thus have to control their behaviour with few muscle fibres and neurons. Hexapod leg muscles, for instance, may consist of a single to a few 100 fibres, and they are controlled by one to, rarely, 19 motoneurons. A typical mammal has thousands of fibres per muscle supplied by hundreds of motoneurons for comparable behavioural performances. Arthopods—crustaceans, hexapods, spiders, and their kin—are on average much smaller than vertebrates, and they possess inhibitory motoneurons for a motor control strategy that allows a broad performance spectrum despite necessarily small cell numbers. This arthropod motor control strategy is reviewed from functional and evolutionary perspectives and its components are described with a focus on inhibitory motoneurons. Inhibitory motoneurons are particularly interesting for a number of reasons: evolutionary and phylogenetic comparison of functional specialisations, evolutionary and developmental origin and diversification, and muscle fibre recruitment strategies.     

The biocontrol potential of Philodromus (Araneae,Philodromidae) spiders for the suppression of pome fruit orchard pests

A number of different generalist (polyphagous) predators occur in agroecosystems. Yet their biocontrol potential has been little investigated in detail. Philodromus species (Philodromidae) belong to the dominant spider species occurring in commercial orchards. We studied in detail the trophic functional traits of Philodromus albidus, Philodromus aureolus, and Philodromus cespitum (Philodromidae) by means of (1) the analysis of natural prey; and (2) experiments on acceptance of a variety of prey taxa. We found that the three philodromids are euryphagous. We classified prey species into three categories according to their function in the orchard: beneficial species, indifferent species, and pests. Philodromid spiders captured mostly other spiders in the field because spiders were most available. As concerns pests, the philodromids preyed mostly on Brachycera and Sternorrhyncha. They selected Acari and Brachycera. Indifferent species, such as Collembola and Nematocera, were also highly selected. In the laboratory, philodromids accepted mostly pests, such as lepidopterans, brachycerans, and aphids, while other spiders were accepted the least. The three philodromids have differentiated trophic niches with respect to prey size not only in the adult stage but throughout their ontogenetic development: P. albidus utilized smaller prey than the other two species. We conclude that the philodromids have a potential as biocontrol agents because they prey mostly on pests but their predation pressure is reduced due to higher selectivity for the indifferent fauna.