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Biomimetics, the transfer of functional principles from living systems into product designs, is increasingly being utilized by engineers. Nevertheless, recurring problems must be overcome if it is to avoid becoming a short-lived fad. Here we assess the efficiency and suitability of methods typically employed by examining three flagship examples of biomimetic design approaches from different disciplines: (1) the creation of gecko-inspired adhesives; (2) the synthesis of spider silk, and (3) the derivation of computer algorithms from natural self-organizing systems. We find that identification of the elemental working principles is the most crucial step in the biomimetic design process. It bears the highest risk of failure (e.g. losing the target function) due to false assumptions about the working principle. Common problems that hamper successful implementation are: (i) a discrepancy between biological functions and the desired properties of the product, (ii) uncertainty about objectives and applications, (iii) inherent limits in methodologies, and (iv) false assumptions about the biology of the models. Projects that aim for multi-functional products are particularly challenging to accomplish. We suggest a simplification, modularisation and specification of objectives, and a critical assessment of the suitability of the model. Comparative analyses, experimental manipulation, and numerical simulations followed by tests of artificial models have led to the successful extraction of working principles. A searchable database of biological systems would optimize the choice of a model system in top-down approaches that start at an engineering problem. Only when biomimetic projects become more predictable will there be wider acceptance of biomimetics as an innovative problem-solving tool among engineers and industry.

Building behaviour in animals extends biological functions beyond bodies. Many studies have emphasized the role of behavioural programmes, physiology and extrinsic factors for the structure and function of buildings. Structure attachments associated with animal constructions offer yet unrealized research opportunities. Spiders build a variety of one- to three-dimensional structures from silk fibres. The evolution of economic web shapes as a key for ecological success in spiders has been related to the emergence of high performance silks and thread coating glues. However, the role of thread anchorages has been widely neglected in those models. Here, we show that orb-web (Araneidae) and hunting spiders (Sparassidae) use different silk application patterns that determine the structure and robustness of the joint in silk thread anchorages. Silk anchorages of orb-web spiders show a greater robustness against different loading situations, whereas the silk anchorages of hunting spiders have their highest pull-off resistance when loaded parallel to the substrate along the direction of dragline spinning. This suggests that the behavioural 'printing' of silk into attachment discs along with spinneret morphology was a prerequisite for the evolution of extended silk use in a three-dimensional space. This highlights the ecological role of attachments in the evolution of animal architectures., (© 2017 The Author(s).)

Foraging is one of the main evolutionary driving forces shaping the phenotype of organisms. In predators, a significant, though understudied, cost of foraging is the risk of being injured by struggling prey. Hunting spiders that feed on dangerous prey like ants or other spiders are an extreme example of dangerous feeding, risking their own life over a meal. Here, we describe an intriguing example of the use of attachment silk (piriform silk) for prey immobilization that comes with the costs of reduced silk anchorage function, increased piriform silk production and additional modifications of the extrusion structures (spigots) to prevent their clogging. We show that the piriform silk of gnaphosids is very stretchy and tough, which is an outstanding feat for a functional glue. This is gained by the combination of an elastic central fibre and a bi-layered glue coat consisting of aligned nanofibrils. This represents the first tensile test data on the ubiquitous piriform gland silk, adding an important puzzle piece to the mechanical catalogue of silken products in spiders., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2017. Published by The Company of Biologists Ltd.)

Silks play an important role in the life of various arthropods. A highly neglected prerequisite to make versatile use of silks is sufficient attachment to substrates. Although there have been some studies on the structure and mechanics of silk anchorages of spiders, for insects only anecdotal reports on attachment-associated spinning behaviour exist. Here, we experimentally studied the silk attachment of the pupae and last instar caterpillars of the tea bagworm Eumeta minuscula (Butler 1881) (Lepidoptera, Psychidae) to the leaves of its host plant Ilex chinensis We found that the bagworms spin attachment discs, which share some structural features with those of spiders, like a plaque consisting of numerous overlaid, looped glue-coated silk fibres and the medially attaching suspension thread. Although the glue, which coats the fibres, cannot spread and adhere very well to the leaf surface, high pull-off forces were measured, yielding a mean safety factor (force divided by the animal weight) of 385.6. Presumably, the bagworms achieve this by removal of the leaf epidermis prior to silk attachment, which exposes the underlying tissue that represents a much better bonding site. This ensures a reliable attachment during the immobile, vulnerable pupal stage. This is the first study on the biomechanics and structure of silk attachments to substrates in insects., (© 2017 The Author(s).)

Here Stygophrynus orientalis sp. nov. is described, a new charontid whip spider from Banggai Island, Indonesia, representing the most eastern record of the genus exceeding the formerly postulated restriction of its distribution western of the Wallace Line. In addition, the third known spermatophore of a Stygophrynus species is presented, which differs remarkably from those previously described from the genus. Finally, the cerotegument structure of the new species is depicted and compared with that of other Charontidae and Charinidae.

The anchorage of structures is a crucial element of construction, both for humans and animals. Spiders use adhesive plaques to attach silk threads to substrates. Both biological and artificial adhesive structures usually have an optimal loading angle, and are prone to varying loading situations. Silk anchorages, however, must cope with loading in highly variable directions. Here we show that the detachment forces of thread anchorages of orb-web spiders are highly robust against pulling in different directions. This is gained by a two-step back-and-forth spinning pattern during the rapid production of the adhesive plaque, which shifts the thread insertion point towards the plaque centre and forms a flexible tree root-like network of branching fibres around the loading point. Using a morphometric approach and a tape-and-thread model we show that neither area, nor width of the plaque, but the shift of the loading point towards the plaque centre has the highest effect on pull-off resistance. This is explained by a circular propagation of the delamination crack with a low peeling angle. We further show that silken attachment discs are highly directional and adjusted to provide maximal performance in the upstream dragline. These results show that the way the glue is applied, crucially enhances the toughness of the anchorage without the need of additional material intake. This work is a starting point to study the evolution of tough and universal thread anchorages among spiders, and to develop bioinspired 'instant' anchorages of thread- and cable-like structures to a broad bandwidth of substrates., (© 2017 The Author(s).)

The cuticle of arthropods is usually composed of layers of a chitin-protein-microcomposite, a proteinaceous epicuticle and a thin lipid coating. However, in some instances a thick cement layer (cerotegument) covers the cuticle and may produce elaborate microstructures. This has previously been described for millipedes and mites. Here we report the previously unknown presence of a superhydrophobic cerotegument in whip-spiders (Ambypygi) and reveal its variation in ultrastructure and water-repellence between species. We discuss the relevance of found micro-morphological and physical characters for taxonomy and phylogenetics of this group, and the potential biological functions., (Copyright © 2016 Elsevier Ltd. All rights reserved.)

Background: Among both plants and arthropods, super-hydrophobic surfaces have evolved that enable self-cleaning, locomotion on water surfaces, or plastron respiration. Super-hydrophobicity is achieved by a combination of non-polar substances and complex micro- and nano-structures, usually acquired by growing processes or the deposition of powder-like materials., Results: Here we report on a multi-phasic secretion in whip spiders (Arachnida, Amblypygi), which externally forms durable, hierarchical microstructures on the basically smooth cuticle. The solidified secretion crust makes the previously highly wettable cuticle super-hydrophobic. We describe the ultrastructure of secretory cells, and the maturation and secretion of the different products involved., Conclusion: Whip spiders represent intriguing objects of study for revealing the mechanisms of the formation of complex microstructures in non-living systems. Understanding the physical and chemical processes involved may, further, be of interest for bio-inspired design of functional surface coatings.

Many insects possess adhesive foot pads, which enable them to scale smooth vertical surfaces. The function of these organs may be highly affected by environmental conditions. Ladybird beetles (Coccinellidae) possess dense tarsal soles of tenent setae, supplemented with an adhesive fluid. We studied the attachment ability of the seven-spotted ladybird beetle ( Coccinella septempunctata ) at different humidities by horizontal traction experiments. We found that both low (15%) and high (99%) relative humidities lead to a decrease of attachment ability. The significantly highest attachment forces were revealed at 60% humidity. This relationship was found both in female and male beetles, despite of a deviating structure of adhesive setae and a significant difference in forces between sexes. These findings demonstrate that not only dry adhesive setae are affected by ambient humidity, but also setae that stick due to the capillarity of an oily secretion.

Whip spiders (Amblypygi) are a small, cryptic order of arachnids mainly distributed in the tropics. Some basal lineages (families Charinidae and Charontidae) have adhesive pads on the tips of their six walking legs. The present study describes the macro- and ultrastructure of these pads and investigates their contact mechanics and adhesive strength on smooth and rough substrates. Furthermore, the structure of the pretarsus and its kinematics are compared in Charon cf. grayi (with an adhesive pad) and Phrynus longipes (without an adhesive pad). The adhesive pads exhibit an elaborate structure with a unique combination of structural features of smooth and hairy foot pads including a long transversal contact zone performing lateral detachment, a thick internally-branched cuticle with longitudinal ribs and hexagonal surface microstructures with spatulate keels. The contact area of the pads on smooth glass is discontinuous due to the spatulate microstructures with a discontinuous detachment, which could be observed in vivo by high speed videography at a rate of up to 10,000 fps. Adhesive strength was measured with vertical whole animal pull-off tests, obtaining mean values between 55 and 200 kPa. The occurrence of viscous lipid secretions between microstructures was occasionally observed, which, however, seems not to be a necessity for good foothold. The results are discussed in relation to the whip spider's ecology and evolution. Structure-function relationships of the adhesive pads are compared to those of insects and vertebrates., (Copyright © 2015 Elsevier Ltd. All rights reserved.)

A specific type of maternal care occurs in several groups of Arachnida: mothers carry their offspring on their back (pulli-carrying behaviour). In scorpions, whip scorpions and whip spiders it is the prenymphal stage that settles on the mother. The prenymph is not yet fully developed for a free life and very limited in its mobility, but its feet are equipped with special adhesive organs (arolia) that become lost at the nymphal stage. Here we study the morphology, ultrastructure and mechanical function of the arolia. In scorpions (Scorpiones) the contact area between arolia and substrate and thus adhesion of the pad is controlled by the antagonistic work of hydrostatic pressure and muscular retraction. Arolia of whip scorpions (Thelyphonida) do not require muscular action for strong attachment. Arrays of long, branching fibres in the mesocuticle lead to high compliancy of the pad. In whip spiders (Amblypygi) the prenymphal pretarsus is already equipped with sclerites and claws. Its arolium is retained in nymphs and adults in some taxa, but acquires a more complex structure. These results contribute to our knowledge on the postembryonic development of arachnids and to the understanding of attachment pad evolution among arthropods. Some of the described developmental, structural, and mechanical phenomena are not known from other animals and might be of potential interest for further biomimetic developments., (Copyright © 2015 Elsevier Ltd. All rights reserved.)

Silk is a key innovation in spiders, fascinating both biologists and material scientists. However, to fulfil their biological function silken threads must be strongly fastened to substrates or other threads. The majority of modern spiders produce a unique and rather unexplored bio-adhesive: the two-compound pyriform secretion, which is spun into elaborate patterns (so called attachment discs) and used to anchor silken threads to substrates. Strong adhesion is achieved on a high variety of surfaces with a minimum of material consumption. Pyriform threads polymerize under ambient conditions, become functional within less than a second and can remain stable for years. They are biodegradable, biocompatible and highly versatile - the adhesion and the overall toughness of the attachment disc can be controlled by spinneret movements on a macroscopic level (ref. 1: V. Sahni et al., Nat. Commun., 2012, 3, 1106, DOI: 10.1038/ncomms2099). We found that the pyriform thread is a silk fibre that is coated with glue-like cement consisting of aligned nanofibrils, lipid enclosures and a dense, isotropic boundary layer. The threads are spun in a meshwork pattern that promotes stress distribution and crack arresting. Our results demonstrate, that hierarchical organization and fibre embedding may explain the high adhesive strength and flaw tolerance of a structure made by the same, rather simple type of silk glands.

Hairy pads relying on dry adhesion are fascinating structures that convergently evolved among spiders and lizards. Numerous studies underline the functional aspects leading to their strong adhesion to smooth surfaces, but rarely has their role been studied in the context of natural habitats and surfaces that animals are faced with. In hunting spiders, the hairy foot pads (claw tufts) underneath the paired claws are assumed to be an adaptation to a climbing lifestyle, particularly on smooth plant surfaces. However, surfaces that are too smooth for claws to generate a sufficient grip are rather rare in natural habitats and above-ground habitats are occupied by hunting spiders both with and without claw tufts. In this study we estimated the proportion of claw tuft-bearing hunting spiders (ct+ ratio) among microhabitat-specific assemblages by conducting both a field study and a meta-analysis approach. The effect of surface characteristics, structure fragmentation and altitude of the microhabitat niche on the ct+ ratio was analyzed. We hypothesized that the ct+ ratio will be higher in (i) hunting spider assemblages obtained from microhabitats above the ground than from those at the ground and (ii) in hunting spider assemblages obtained from microhabitats with smoother surfaces (tree foliage) than those with rougher surfaces (barks, stones), and lower in (iii) hunting spider assemblages obtained from microhabitats with more fragmented structures (small leaves) than in those with comparable but less fragmented structures (large leaves). We found the ct+ ratio to be significantly affected by the microhabitat's distance from the ground, whereas surface characteristics and fragmentation of the substrates were of minor importance. This suggests that claw tufts are highly beneficial when the microhabitat's height exceeds a value where the additional pad-related costs are exceeded by the costs of dropping. We assume the benefit to be mainly due to gaining a high safety factor at a lower energy demand if compared to alternative attachment devices (claws, silk). The previously presumed enhanced access to new microhabitat sites may play only a minor role as hunting spiders without claw tufts are present in most microhabitats., (Copyright © 2014 Elsevier GmbH. All rights reserved.)

Gluing can be a highly efficient mechanism of prey capture, as it should require less complex sensory-muscular feedback. Whereas it is well known in insects, this mechanism is much less studied in arachnids, except spiders. Soil-dwelling harvestmen (Opiliones, Nemastomatidae) bear drumstick-like glandular hairs (clavate setae) at their pedipalps, which were previously hypothesized to be sticky and used in prey capture. However, clear evidence for this was lacking to date. Using high-speed videography, we found that the harvestman Mitostoma chrysomelas was able to capture fast-moving springtails (Collembola) just by a slight touch of the pedipalp. Adhesion of single clavate setae increased proportionally with pull-off velocity, from 1 μN at 1 μm s(-1) up to 7 μN at 1 mm s(-1), which corresponds to the typical weight of springtails. Stretched glue droplets exhibited characteristics of a viscoelastic fluid forming beads-on-a-string morphology over time, similar to spider capture threads and the sticky tentacles of carnivorous plants. These analogies indicate that viscoelasticity is a highly efficient mechanism for prey capture, as it holds stronger the faster the struggling prey moves. Cryo-scanning electron microscopy of snap-frozen harvestmen with glued springtails revealed that the gluey secretions have a high affinity to wet the microstructured cuticle of collembolans, which was previously reported to be barely wettable for both polar and non-polar liquids. Glue droplets can be contaminated with the detached scaly setae of collembolans, which may represent a counter-adaptation against entrapment by the glue, similar to the scaly surfaces of Lepidoptera and Trichoptera (Insecta) facilitating escape from spider webs., (© 2014. Published by The Company of Biologists Ltd.)

Araneomorph spiders have evolved different silks with dissimilar material properties, serving different purposes. The two-compound pyriform secretion is used to glue silk threads to substrates or to other threads. It is applied in distinct patterns, called attachment discs. Although ubiquitously found in spider silk applications and hypothesized to be strong and versatile at low material consumption, the performance of attachment discs on different substrates remains unknown. Here, we analyse the detachment forces and fracture mechanics of the attachment discs spun by five different species on three different substrates, by pulling on the upstream part of the attached thread. Results show that although the adhesion of the pyriform glue is heavily affected by the substrate, even on Teflon it is frequently strong enough to hold the spider's weight. As plant surfaces are often difficult to wet, they are hypothesized to be the major driving force for evolution of the pyriform secretion., (© 2014 The Author(s) Published by the Royal Society. All rights reserved.)

Dynamic attachment is the key to moving safely and fast in a three-dimensional environment. Among lizards, hexapods and arachnids, several lineages have evolved hairy foot pads that can generate strong friction and adhesion on both smooth and rough surfaces. A strongly expressed directionality of attachment structures results in an anisotropy of frictional properties, which might be crucial for attachment control. In a natural situation, more than one leg is usually in contact with the substrate. In order to understand the collective effect of hairy foot pads in the hunting spider Cupiennius salei (Arachnida, Ctenidae), we performed vertical pulling experiments combined with stepwise disabling of the pads. We found the attachment force of the spider to be not simply the sum of single leg forces because with leg pair deactivation a much greater decrease in attachment forces was found than was predicted by just the loss of available adhesive pad area. This indicates that overall adhesion ability of the spider is strongly dependent on the antagonistic work of opposing legs, and the apparent contact area plays only a minor role. It is concluded that the coordinated action of the legs is crucial for adhesion control and for fast and easy detachment. The cumulative effect of anisotropic fibrillar adhesive structures could be potentially interesting for biomimetic applications, such as novel gripping devices.

Spiders are the most important terrestrial predators among arthropods. Their ecological success is reflected by a high biodiversity and the conquest of nearly every terrestrial habitat. Spiders are closely associated with silk, a material, often seen to be responsible for their great ecological success and gaining high attention in life sciences. However, it is often overlooked that more than half of all Recent spider species have abandoned web building or never developed such an adaptation. These species must have found other, more economic solutions for prey capture and retention, compensating the higher energy costs of increased locomotion activity. Here we show that hairy adhesive pads (scopulae) are closely associated with the convergent evolution of a vagrant life style, resulting in highly diversified lineages of at least, equal importance as the derived web building taxa. Previous studies often highlighted the idea that scopulae have the primary function of assisting locomotion, neglecting the fact that only the distal most pads (claw tufts) are suitable for those purposes. The former observations, that scopulae are used in prey capture, are largely overlooked. Our results suggest the scopulae evolved as a substitute for silk in controlling prey and that the claw tufts are, in most cases, a secondary development. Evolutionary trends towards specialized claw tufts and their composition from a low number of enlarged setae to a dense array of slender ones, as well as the secondary loss of those pads are discussed further. Hypotheses about the origin of the adhesive setae and their diversification throughout evolution are provided.

Dynamic attachment is the key to move on steep surfaces, with mechanisms being still not well understood. The hunting spider Cupiennius salei (Arachnida, Ctenidae) possesses hairy attachment pads (claw tufts) at its distal legs, consisting of directional branched setae. The morphological investigation revealed that adhesive setae are arranged in a radial manner within the distal tarsus. Friction of claw tufts on smooth glass was measured to reveal the functional effect of seta arrangement within the pad. Measurements revealed frictional anisotropy in both longitudinal and transversal directions. Contact behaviour of adhesive setae was investigated in a reflection interference contrast microscope (RICM). Observations on living spiders showed, that only a small part of the hairy pads is in contact at the same time. Thus the direction of frictional forces is depending on leg placement and rotation. This may aid controlling the attachment to the substrate.

Many wandering spiders bear attachment pads (scopulae) on their tarsi, consisting of hierarchically-branching adhesive setae. Amongst spider families and even species, these show remarkable differences in morphology. Using scanning electron microscopy, the scopula microstructure of sixteen spider species was described, with the focus on pretarsal scopulae (claw tufts). Area and shape of the claw tuft, seta and setule density, as well as seta and spatula dimensions were analysed and compared. Claw tufts of the majority of species studied show a similar gradient in size and shape from anterior to posterior legs: the dimension of pads increases, while setal density decreases. Commonly, there is also a gradient of both the seta and spatula size within the claw tuft: Setae become larger from the proximal to the distal part of the pad, and spatulae size increases in the same direction at the level of individual seta. Often, different hierarchical levels of claw tuft organisation are differently expressed in different species: Species with lower setal density usually have broader setae. Smaller spatula size often implicates higher setule density. Evolutionary and ecological aspects of the scopula origin are discussed., (Copyright © 2012 Elsevier Ltd. All rights reserved.)

Hairy attachment devices that are not supplemented with fluid secretion have evolved independently in lizards and spiders. van der Waals forces have previously been shown to be responsible for excellent adhesive properties of these structures, but it has recently been reported that wetting phenomena also play an important role in such 'dry adhesives'. To investigate the effect of ambient humidity on the attachment of the living spider Philodromus dispar, traction force was measured on a smooth epoxy resin surface at relative humidities (RHs) of 15, 50, 70, 80 and 99 per cent. The results show that attachment ability is significantly higher at an intermediate humidity compared with that in a dry atmosphere and at high humidity. Water condensation on the substrate surface almost completely abolishes adhesion. Experimental results obtained may be explained by an increase in capillarity or changes in mechanical properties of setae and spatulae owing to water absorption by the cuticle at an intermediate RH. The results obtained show dry adhesion limits under different environmental conditions and are important for understanding spider biology.

The morphology of the tarsal attachment system of the running spider Philodromus dispar Walckenaer 1826 (Araneae, Philodomidae) was studied using scanning electron microscopy and its performance was experimentally tested in traction force measurements. Each pretarsus bears a hierarchically built hairy adhesive pad that consists of a dense array of flattened setae covered with numerous microtrichia on the substrate-facing side. Microtrichia carry spatulate end tips that allow close contact with the substrate. Forces were estimated on tethered living specimens on rough epoxy resin surfaces (asperity size 0.3, 1, 3, 9 and 12 μm) and on a smooth surface as a control. A strong reduction in adhesion was observed for substrates with an asperity size of 0.3 and 1 μm. Comparison of the present data with previous results of different organisms demonstrates that the difference in force reduction on rough substrata depends on the dimensions of terminal contact elements (spatulae).

Mating system and philopatry influence the genetic structure of a social group in mammals. Brandt's vole (Lasiopodomys brandtii) lives in social groups year-round and has male biased dispersal, which makes the vole a model system for studies of genetic consequences of mating system and philopatry. This study aimed to test the hypotheses that: (1) multiple paternity (MP) would exist in Brandt's voles, enhance offspring genetic diversity and reduce genetic relatedness between littermates; (2) promiscuity would occur in this species in that males and females mate with multiple partners; and (3) plural breeders of a social group would be genetically related because of philopatry of female juveniles in Brandt's voles. Paternity analysis indicated that MP occurred in 11 (46%) of 24 social groups examined and that promiscuity existed in this species. Multiple paternity litters had twice the offspring genetic diversity and half the average within-litter genetic relatedness of single paternity litters. We also found plural breeding females in six social groups. Average pairwise genetic relatedness of plural breeders ranged from 0.41 to 0.72 in four social groups, suggesting first-order kinship. Future studies need to investigate effects of reproductive skew and MP on population genetic structure of Brandt's voles., (Copyright (c) 2010 Elsevier B.V. All rights reserved.)

Although prairie voles (Microtus ochrogaster) are socially monogamous, males vary in both sexual and spatial fidelity. Most males form pairbonds, cohabit with one female, and defend territories. Wandering males, in contrast, have expansive home ranges that overlap many males and females. In the laboratory, pairing is regulated by arginine vasopressin and its predominant CNS receptor, vasopressin 1a receptor (V1aR). We investigated individual differences in forebrain V1aR expression of male prairie voles in mixed-sex seminatural enclosures. Individual differences in V1aR were compared with space use measured by radio telemetry and paternity determined with microsatellite markers. Animals engaging in extra-pair fertilizations (EPFs) as either wanderers or paired residents overlapped significantly more in same- and opposite-sex home ranges. Surprisingly, neither social fidelity measured by space use nor sexual fidelity measured by paternity was associated with V1aR expression in the ventral pallidum (VPall) or lateral septum, areas causally related to pairbond formation. In contrast, V1aR expression in the posterior cingulate/retrosplenial cortex (PCing) and laterodorsal thalamus (LDThal), areas implicated in spatial memory, strongly covaried with space use and paternity. Animals engaging in EPFs either as wanderers or paired residents exhibited low levels of LDThal and PCing V1aR expression. Individual differences in brain and behavior parallel differences between prairie voles and promiscuous congeners. The concordance among space use, paternity, and V1aR in spatial circuits suggests a common link between the mechanisms of spatial behaviors and success at EPF. The combined data demonstrate how organismal biology can inform our understanding of individual and species differences in behavioral mechanisms.

In the socially monogamous prairie vole, Microtus ochrogaster, male affiliation and parental care are influenced by the neuropeptide arginine vasopressin and expression of its receptor V1aR. If parental care and adult affiliation can be considered a behavioral syndrome, females might use male affiliative behavior as a cue to choose a good father. We investigated three questions: (1) do females prefer affiliative males; (2) do males that are affiliative with females demonstrate paternal behavior with pups; and (3) is male V1aR expression related to male behavior or female preference? We evaluated paternal behavior of individual males, then offered sexually receptive females a choice between paternal and non-paternal males and measured the proportion of time each male spent engaging in affiliative behavior with the choosing female. Females showed a preference for more affiliative males, but affiliation was not predictive of paternal care. Thus females did not discriminate between paternal and non-paternal males. Perhaps surprisingly, paternal behavior was correlated with the relative amount of aggression males directed toward females. Finally, females did not discriminate between males with high or low V1aR expression and V1aR expression did not predict male affiliative behavior or parental care. These data suggest that male affiliative behavior, but not paternal care, is associated with female mate choice., ((c) 2007 S. Karger AG, Basel.)

Herein, I summarize some basic components of rodent social biology. The material in this paper is summarized and condensed from a recent book "Rodent Societies: An Ecological and Evolutionary Perspective" edited by J. O. Wolff and P. W. Sherman (2007). I describe the four basic spacing patterns and illustrate how female territoriality is a function of offspring defense and male mating tactics are a function of female defensibility. The vulnerability of young to infanticide shapes female spacing and mating behavior. Food does not appear to be a defensible resource for rodents, except for those species that larder hoard nonperishable items such as seeds. Philopatry and the formation of kin groups result in genetic sub-structuring of the population, which in turn affects effective population size and genetic diversity. Dispersal is male biased and typically involves emigration from the maternal site to avoid female relatives and to seek unrelated mates. Scent marking is a major form of communication and is used in reproductive competition and to assess prospective mates, but it is also eavesdropped by predators to locate prey. Females do not appear to alter the sex ratio of litters in response to maternal condition but among arvicoline rodents daughters appear to be favored in spring and sons in autumn. Rodents are relatively monomorphic; however, females tend to be larger than males in the smallest species and smaller in the larger species. Predation risk results from an interaction among foraging time and vulnerability and in turn affects behavioral and life history characteristics.

We conducted field and laboratory experiments with the well-studied monogamous prairie vole, Microtus ochrogaster, to distinguish among three hypotheses for the failure of females that lose their mates to bond with a new male ("the widow effect"). The reproductive value hypothesis predicts that males prefer young to older females because they potentially have a longer reproductive lifespan. The mate rejection hypothesis predicts that females will prevent repairing by aggressively deterring males that might harm their current offspring. The misdirected paternal care hypothesis assumes that females will mate during postpartum estrus and thus will be pregnant and/or nursing young throughout the breeding season; males will avoid pairing with older females to avoid providing care to unrelated offspring and/or because of a delay to the next breeding opportunity. Males associated and bred more with older than young females, allowing us to reject the reproductive value hypothesis. Our results were consistent with the male rejection hypothesis in that females were aggressive toward unfamiliar males. Our results were most consistent with the misdirected paternal care hypothesis in that once females started breeding, they continued to become pregnant and nurse young throughout the study period. Thus, our findings suggest that the potential of misdirected paternal care and delayed mating opportunity in conjunction with the aggressive behavior of females toward unfamiliar males are likely explanations for the lack of repairing for widow females.

Multi-male mating (MMM) by females is relatively common among mammals, occurring in at least 133 species and several evolutionary benefits of MMM have been proposed. The most convincing explanation is that MMM confuses paternity, thereby deterring infanticide by males. A second explanation for females that are unlikely to experience infanticide is that MMM is a consequence of sexual harassment. Mate guarding and, perhaps even in some cases, behavioral monogamy, might have evolved in response to the threat of infanticide and the subsequent tendency for females to mate multiply. Benefits relating to improved genetic fitness of offspring do occur in some species, but do not provide a widespread explanation for the evolutionary origin of MMM; if cryptic female choice through sperm competition is adaptive to females it probably evolved as a consequence of, rather than a precursor to, female promiscuity. Here, we provide support for the original hypothesis of paternity confusion for MMM, rather than for the more popular good genes or sperm competition hypotheses.

We conducted an experiment to test three alternative hypotheses for the function of frequency of scent marking in male prairie voles, MICROTUS OCHROGASTER: (1) sexual attraction (to advertise male quality for mating); (2) reproductive competition; and (3) self-advertisement or individual identity. In laboratory experiments, males deposited scent on all areas of a bare substrate, and more in an area next to a stimulus animal than other areas, regardless of the stimulus animal's sex. Females did not choose mates based on their frequency of scent marking and scent marking did not antagonize or stimulate aggression between males. The frequency of scent marking by males supports the individual identity hypothesis, and is less consistent with the sexual attraction or reproductive competition hypotheses. Mate choice is likely based on a complex suite of characters, but at least in prairie voles, the frequency of scent marking by males does not appear to be one of them.

We conducted a mating experiment in the laboratory using prairie voles, Microtus ochrogaster, to document that multi-male mating (MMM) can occur in this supposedly monogamous species and to test two hypotheses for the advantages of MMM in female mammals. The two hypotheses are that MMM (1) increases the probability of pregnancy and (2) increases litter size. We also tested the hypothesis that multiple copulations, rather than multiple partners, increases litter size and/or probability of pregnancy. Females were given a choice of mating with any of three males, each of which was tethered in a separate compartment. The mate choice bouts were recorded on videotape. We recorded the number of copulations and number of males with which females mated over a 24 h period. Litter size and probability of pregnancy were not significantly different for females that mated with one, two or three males. Increasing numbers of copulations, independent from the number of males, also did not increase litter size but did significantly increase the probability of pregnancy. MMM, at least in prairie voles, must serve some function other than increasing litter size and probability of conception.

Reproductive suppression of young females by conspecific females has been reported from laboratory studies on several species of rodents, including the prairie vole, Microtus ochrogaster, but not meadow voles, M. pennsylvanicus. We exposed female prairie voles and meadow voles to two treatments: a mother and one 23-26-day-old daughter paired with a strange male and a 23-26-day-old daughter paired with a different strange male. We found no differences in the proportion of daughters breeding or the time to sexual maturation for daughters raised in the two treatments for either species. Thus, we have no indication that mothers had any adverse effect on reproductive efforts of their daughters. These results differ from previous studies that concluded young female prairie voles were reproductively suppressed by female relatives. The difference between our and previous studies on reproductive suppression is that we examined breeding in young females rather than proximate measures of growth and reproductive development. We question the evolutionary significance of reproductive suppression among related female microtine rodents, especially in that it has not been documented from field populations.

Risk of exposure to Lyme disease is a function of the local abundance of nymphal Ixodes ticks that are infected with the etiological agent, the spirochete Borrelia burgdorferi. We monitored abundance of white-footed mice (the principal B. burgdorferi reservoir in the eastern and central United States) and acorns (a critical food resource for mice), and Ixodes scapularis ticks, as well as ambient temperature (cumulative growing degree days) and growing season precipitation, in a forested landscape of southeastern New York State from 1994 to 2000. We found that acorn production in autumn strongly influenced abundance of white-footed mice the following summer and that abundance of mice in summer, when larval ticks are active, influenced the abundance of infected nymphs the following year. Consequently, the abundance of infected nymphal ticks can be predicted from acorn production 1.75 years earlier. Monitoring of natural fluctuations in acorn production thus supports results of prior acorn addition experiments that were conducted at small spatial scales. Growing degree days and precipitation either had no significant effect on density of nymphs or marginally increased the explanatory power of models that included acorns or mouse density as independent variables. We conclude that, at our study site in New York, the risk of human exposure to Lyme disease is affected by mouse density in the prior year and by acorn production 2 years previously.

We used gray-tailed voles (Microtus canicaudus) and northern bobwhite quail (Colinus virginianus) as experimental model species to field test whether small mammals and birds respond differently to equivalent concentrations of a pesticide applied in granular and flowable formulations. In mid-May 1998, we placed voles into 15, 0.2-ha enclosures planted with a mixture of pasture grasses. In mid-July, we placed quail into the same enclosures with the voles. In late July, we applied the organophosphorus insecticide diazinon in five treatments; a control (all habitats sprayed with water), liquid formulation of diazinon at 0.55 kg/ha, liquid formulation of diazinon at 1.11 kg/ha, broadcast of granular diazinon at 1.11 kg/ha, and broadcast of granular diazinon at 2.22 kg/ha. The diazinon treatment in liquid and granular formulations did not depress population size or growth rate, or survival rate of voles. We found a significant difference in the survival rate of the quail between the controls and treatments; granular diazinon caused a measurable decline of quail survival, whereas the liquid application at an equivalent rate did not significantly affect quail survival. Analysis of our results suggests that ground-feeding birds are more susceptible to granular insecticides than flowable applications, but voles were not susceptible to either formulation at the rate we used.

We used gray-tailed voles, Microtus canicaudus, as an experimental model species to field test a prediction of the Quotient Method (QM) for risk to small mammals of an insecticide in grasslands. In May 1997, we placed voles into 12 0.2-ha enclosures planted with a mixture of pasture grasses. In late July, we applied 1.55 kg/ha of the insecticide Guthion(R) 2S (azinphos-methyl) in three treatments: a control (all habitat sprayed with water), full spray (all of the habitat sprayed with Guthion 2S), and half-spray (one-half of the habitat sprayed with Guthion 2S and one half with water). Five replicates were used for the half-spray and control, and two replicates for the full-spray. The Guthion 2S treatment did not depress population size, growth rate, or survival of voles in half-spray or full-spray enclosures. Our results were inconsistent with the QM prediction for use of Guthion 2S in grass habitats. These results also differed from our previous studies in alfalfa habitats in which measurable responses were detected at the same application rate. The differences probably are due to the different types of vegetation between current and previous studies. The grass habitat in our enclosures was an average of 60 cm high and was very thick from ground level to about 40 cm. Much of the residue likely accumulated in the upper strata of vegetation and did not reach ground level at this application rate. Under the conditions of this study, voles were less affected in grassland habitat than they were in alfalfa habitat.

In eastern U.S. oak forests, defoliation by gypsy moths and the risk of Lyme disease are determined by interactions among acorns, white-footed mice, moths, deer, and ticks. Experimental removal of mice, which eat moth pupae, demonstrated that moth outbreaks are caused by reductions in mouse density that occur when there are no acorns. Experimental acorn addition increased mouse density. Acorn addition also increased densities of black-legged ticks, evidently by attracting deer, which are key tick hosts. Mice are primarily responsible for infecting ticks with the Lyme disease agent. The results have important implications for predicting and managing forest health and human health.

White-footed mice, Peromyscus leucopus noveboracensis, and deer mice, P. maniculatus nubiterrae, occur sympatically throughout much of the Appalachian Mountains of the eastern United States. Previous studies have shown that these two species are behaviorally and ecologically similar and do not partition food or microhabitat. In this paper I use a 14-year data set to demonstrate that the two species have differential population growth and survival rates in response to food abundance and season, which may mediate their coexistence. The ratio of white-footed mice to deer mice ranged from 0.5:1 to 6:1. During summer and times of tood abundance, white-footed mice gained a numerical advantage over deer mice in 10 of 14 years, whereas following winter and poor food production, deer mice had higher survival in 9 of 13 years. The major decline in white-foote mice, but not deer mice, was associated with poor mast (acorn) production in autumn. Differential survival of deer mice may be due to their physiological adaptations to cold temperature and efficient use of torpor during food shortage. Inter-year variance in food production and climatic conditions appear to change the competitive advantage of each species often enough to permit coexistence. Coexistence of these two ecologically similar species may be maintained by different physiological limitations in a fluctuating environment.

A laboratory toxicity study on house mice and laboratory mice (Mus musculus), gray-tailed voles (Microtus canicaudus), and deer mice (Peromyscus maniculatus) was conducted as part of a comprehensive laboratory and field study to field validate laboratory-based risk assessment of pesticides. The single dose oral LD50 for the organophosphorus insecticide azinphos-methyl (Guthion) was 10, 11, 32, and 48 mg/kg body weight in wild house mice, laboratory mice, gray-tailed voles, and deer mice, respectively. Ten-day dietary LC50s were 277 ppm for laboratory mice, 297 ppm for gray-tailed voles, and 1,180 ppm for deer mice. All treated animals lost more weight, consumed less food, and had depressed brain cholinesterase (ChE) activity compared to controls. Five-day LC50s were significantly higher than 10-day LC50s for laboratory mice and deer mice. For all three species, animals that died during dietary LC50 tests had mean ChE activity of 50-55% while survivors had 56-70% of controls. The conclusions were that: (1) Laboratory mice were not representative of deer mice or gray-tailed voles with respect to sensitivity to azinphos-methyl, but provided a conservative estimate for risk assessment; (2) 10-day dietary LC50 tests indicate substantially greater estimates of toxicity of azinphos-methyl to rodents than do 5-day tests; and (3) brain ChE depression of 45-50% was lethal in these species.

Juvenile dispersal is sex-biased in many mammals and birds: one sex often disperses more often or farther than the other. Two hypotheses are generally presented for sex-biased dispersal. The first holds that juvenile dispersal reduces reproductive and/or resource competition between parents and same-sexed offspring. If so, presence of a parent on the natal home range should both promote dispersal of same-sex offspring and suppress reproduction of those that remain. The second is that juvenile dispersal reduces matings between parents and offspring, thus decreasing the likelihood of inbreeding depression. If so, presence of a parent should favour dispersal and reproductive suppression of offspring of the opposite sex. Here I present evidence that juvenile dispersal in white-footed mice, Peromyscus leucopus, is due to inbreeding avoidance. When population density was high, experimental removal of one parent delayed dispersal of opposite-sexed offspring and only the presence of the parents of opposite sex suppressed juvenile reproduction.