Eileen Hebets Publications

Seismic signal dominance in the multimodal courtship display of the wolf spider Schizocosa stridulans Stratton 1991

Eileen Hebets — Wed, 14 Sep 2011 10:56:57 PDT

Unraveling the function and evolutionary history of multimodal signaling is a difficult, yet common task of much research in animal communication. Here, I investigated multimodal signal function in the visual and seismic courtship display of the wolf spider Schizocosa stridulans and found that only the seismic courtship signal was important for mating success. First, copulation frequency was assessed in the presence/ absence of both visual and seismic courtship signals. The seismic signal was sufficient for successful copulation, whereas the visual signal was neither necessary nor sufficient, suggesting that the signals are not redundant and do not function as backups. Next, female receptivity to video courtship sequences with altered male ornamentation was assessed in the presence of a live male’s seismic signal. Female receptivity did not depend on male foreleg ornamentation. Instead, females performed receptivity displays equally to all video stimuli, demonstrating that in the presence of seismic signaling, receptivity is independent of visual signaling—indicating seismic signal dominance. Finally, female responses to isolated seismic cues from crickets and courting males suggest that seismic courtship signals carry both location and identification information. Schizocosa stridulans represents one of the few examples in which a single component likely dominates a multimodal signal.

Includes Supplemental Video of male courtship display, attached as "Related File" (below).

Condition-dependent alternative mating tactics in a sexually cannibalistic wolf spider

Dustin J. Wilgers et al. — Wed, 14 Sep 2011 08:32:15 PDT

Condition-dependent male mating tactics often involve high-quality males capitalizing on the outcome of intersexual selection, whereas low-quality males use behaviors that circumvent female choice to achieve copulation. In the wolf spider Rabidosa punctulata, males display 2 distinct mating tactics: 1) “courtship”—consisting of visual and seismic components or 2) “direct mount”—consisting of males grappling/holding females until they assume a copulatory posture. We tested for condition-dependent tactic expression using both field-collected individuals (representing natural variation in body mass and condition) and individuals whose diet we manipulated in the laboratory (representing extreme divergences in body size and condition). Across both natural and diet manipulated individuals, mating tactic was found to be condition dependent; however, the pattern of tactic expression was initially unexpected. Larger males with better body condition primarily adopted a direct mount tactic, whereas smaller males with poorer body condition primarily utilized courtship. Across all males, copulation success tended to be greatest for the direct mount tactic. We suggest that small, poor condition males predominantly utilize the less-successful mating tactic (courtship) in part due to their increased susceptibility to female cannibalism when attempting a direct mount.

Includes Supplemental Video of mating interaction.

Courtship effort is a better predictor of mating success than ornamentation for male wolf spiders

Paul S. Shamble et al. — Thu, 01 Sep 2011 08:28:45 PDT

Female mate choice decisions are often based on a variety of male characteristics, some of which may reflect male quality via condition-dependent trait expression. Here, we explore the condition dependence of a male secondary sexual trait in a wolf spider and examine its influence on female mate choice. In the wolf spider Schizocosa uetzi, mature males possess a multimodal courtship display (visual + seismic) in which they slowly raise and lower their dark colored forelegs. Foreleg color is highly variable among S. uetzi males with respect to both total amount and darkness. Using diet manipulations in conjunction with color quantifications, we demonstrate condition-dependent foreleg color. High-nutrient diet males had significantly higher body condition indices and possessed more and darker foreleg color than low-nutrient diet males. However, using multiple mate choice designs, we were unable to demonstrate a female preference for male foreleg color. Using both single and 2-choice mating designs as well as using females from a range of ages, we found that copulation success was consistently independent of male foreleg color. Instead, we found courtship intensity to be the only aspect of male courtship that influenced copulation success—males that copulated displayed more leg raises per second than those that did not copulate.

Tactile learning by a whip spider, Phrynus marginemaculatus C. L. Koch (Arachnida, Amblypygi)

Roger D. Santer et al. — Thu, 01 Sep 2011 07:39:04 PDT

The ability of animals to learn and remember underpins many behavioral actions and can be crucial for survival in certain contexts, for example in finding and recognizing a habitual refuge. The sensory cues that an animal learns in such situations are to an extent determined by its own sensory specializations. Whip spiders (Arachnida, Amblypygi) are nocturnal and possess uniquely specialized sensory systems that include elongated “antenniform” forelegs specialized for use as chemo- and mechanosensory feelers. We tested the tactile learning abilities of the whip spider Phrynus marginemaculatus in a maze learning task with two tactile cues of different texture—one associated with an accessible refuge, and the other with an inaccessible refuge. Over ten training trials, whip spiders got faster and more accurate at finding the accessible refuge. During a subsequent test trial where both refuges were inaccessible, whip spiders searched for significantly longer at the tactile cue previously associated with the accessible refuge. Using high-speed cinematography, we describe three distinct antenniform leg movements used by whip spiders during tactile examination. We discuss the potential importance of tactile learning in whip spider behavior and a possible role for their unique giant sensory neurons in accessing tactile information.

Mate Choice and Learning

Eileen Hebets et al. — Wed, 31 Aug 2011 06:52:47 PDT

While an individual’s genetic framework is a major contributor in determining its eventual mate choice, the role of the environment in further influencing mating decisions has long been recognized. Animals gather information from the environment throughout life, and in some cases, may apply this information to increase their odds of obtaining a high-quality mate. In short, these individuals learn. Moreover, such learning can have a social component. “Social learning” is a general term that describes any learning based on observing, interacting with, and/or imitating others in a social context. Social learning can transmit information vertically, generation to generation (e.g., parent to offspring) and/or horizontally, within a generation (as individual to individual). This form of information transfer is generally referred to as “cultural transmission.” This entry will focus on social learning that relates to mate choice – mate-choice learning.

Female mate choice based upon male motor performance

John Byers et al. — Tue, 30 Aug 2011 09:11:11 PDT

Our goal in this essay is to review the hypothesis that females choose mates by the evaluation of male motor performance. We define motor performance as vigor, the ability to perform energetically expensive acts repeatedly, or as skill, the ability to perform difficult motor tasks well. Motor performance reflects most aspects of whole-organism performance that relate to survival, and thus should indicate, more reliably than ornaments do, individual male genetic quality and/or developmental history. Male sexual displays in many animal taxa contain elements of vigor and/or skill, and accumulating evidence suggests that females choose mates in nature based upon their evaluations of male motor performance. We note that male ornaments in many species are accompanied by conspicuous motor display, and we propose that ornaments often arise secondarily as a way to enhance the apparent skill or vigor of male motor performance. More and better methods to measure male vigor and skill are needed, as well as additional studies on the abilities of females to make discriminations of this type.

Costs and benefits of freezing behavior in the harvestman Eumesosoma roeweri (Arachnida, Opiliones)

Marie-Claire Chelini et al. — Mon, 22 Aug 2011 13:28:22 PDT

Animals present an enormous variety of behavioral defensive mechanisms, which increase their survival, but often at a cost. Several animal taxa reduce their chances of being detected and/or recognized as prey items by freezing (remaining completely motionless) in the presence of a predator. We studied costs and benefits of freezing in immature Eumesosoma roeweri (Opiliones, Sclerosomatidae). Preliminary observations showed that these individuals often freeze in the presence of the syntopic predatory spider Schizocosa ocreata (Araneae, Lycosidae). We verified that harvestmen paired with predators spent more time freezing than when alone or when paired with a conspecific. Then, we determined that predator chemical cues alone did not elicit freezing behavior. Next, we examined predator behavior towards moving/non-moving prey and found that spiders attacked moving prey significantly more, suggesting an advantage of freezing in the presence of a predator. Finally, as measure of the foraging costs of freezing, we found that individuals paired with a predator for 2 h gained significantly less weight than individuals paired with a conspecific or left alone. Taken together, our results suggest that freezing may protect E. roeweri harvestmen from predatory attacks by wolf spiders, but at the cost of reduced food and/or water intake.

Multimodal courtship efficacy of Schizocosa retrorsa wolf spiders: Implications of an additional signal modality

Aaron S. Rundus et al. — Wed, 27 Jul 2011 14:07:22 PDT

Here, we simultaneously examine both content and efficacy-based sources of selection on the visual and seismic multimodal courtship display of the wolf spider Schizocosa retrorsa. Immature field-collected S. retrorsa were reared in the laboratory on either high-quantity diet (HD) or low-quantity diet (LD) treatments. On maturation, females of each diet treatment were run in simultaneous mate choice trials with both a HD and an LD male (content-based selection). Simultaneous mate choice trials were conducted across different signaling environments (efficacy-based selection) in a fully crossed 2 × 2 design with visual treatments of light/dark (visual signal present/absent) and seismic treatments of filter paper substratum/granite substratum (seismic signal present/absent). Male copulation success did not differ across either signaling environment or diet treatment. However, copulation success was related to male leg waving displays as males who engaged in more bouts of leg waving were more likely to copulate regardless of experimental manipulations. The observation that copulation success was independent of signaling environment suggests the use of an additional courtship signal modality.

The degree of response to increased predation risk corresponds to male secondary sexual traits

Kasey Fowler-Finn et al. — Mon, 25 Jul 2011 13:59:22 PDT

Secondary sexual traits are expected to reflect a balance between sexual selection and natural selection. We test the hypothesis that plasticity in sexual advertisement behaviors can influence this trade-off, allowing showier traits than expected for a given level of predation risk. Specifically, we tested whether the degree of behavioral plasticity exhibited in response to chemical cues of a co-occurring predatory wolf spider corresponds to courtship rate and the degree of ornamentation in male wolf spiders. Both ornamented (brush-legged) males and non-ornamented males decreased locomotion, decreased their likelihood to court, and increased their time to initiate courtship in response to predator cues. However, brush-legged males increased their time to initiate courtship more than did non-ornamented males, demonstrating a greater response to the risk of predation for the more ornamented males. Similarly, within brush-legged males, individuals with the highest courtship rates also showed the greatest degree of plasticity in time to initiate courtship across predation contexts, whereas behavioral plasticity was independent of courtship rate for non-ornamented males. We found no correlation between ornament size and plasticity in response to predator cues within brush-legged males. Ultimately, we suggest that our data provide support for the hypothesis that behavioral plasticity in response to predator cues may alter the trade-off between predation risk and sexual advertisement and may be more important for males with higher degrees of conspicuousness in ornamentation and courtship.

Chemical Communication in a Multimodal Context

Eileen A. Hebets et al. — Tue, 19 Jul 2011 11:47:12 PDT

All animals are equipped with multiple sensory systems (e.g., visual, chemical, acoustic, tactile, electrical, thermal), and signals perceived via these sensory systems facilitate communication. Such communication often involves displays that incorporate more than one signal from more than one sensory modality, resulting in multimodal signaling. The number of empirical and theoretical studies addressing issues of multimodal signaling is ever-increasing and this chapter highlights why crustaceans, as a taxonomic group, are ideal for advancing such studies. Early classifications of multimodal signaling sought to categorize signal components as either redundant or nonredundant, while more recent classifications lay out specific hypotheses relating to multimodal signal function. Two common empirical approaches used in studying multimodal signaling involve signal isolation and signal playback designs—both of which are extremely amenable to crustaceans.

Chemical communication is considered the oldest and most widespread channel for communication, and as such, it is not surprising that numerous crustaceans incorporate chemical signals into multimodal displays. In this chapter, we review multimodal signaling in crustaceans with a focus on those displays that incorporate a chemical component. Specifically, we highlight examples of taxa that combine chemical and hydrodynamic as well as chemical and visual cues. We conclude that despite the plethora of excellent studies examining crustacean responses to isolated signal components, relatively few studies are couched in a communication framework—ultimately limiting the conclusions that can currently be drawn with respect to multimodal signal evolution and function in crustaceans. We suggest that future studies using a hypothesis-testing framework of multimodal signal function could greatly advance our understanding of multimodal signaling in this group. Furthermore, studies involving signal manipulations and correlations between signaler attributes and variation in signal form could be extremely informative. These avenues are wide open for crustacean biologists. We argue that several aspects of crustacean biology (e.g., their abundance, the ease with which they can be manipulated, the ease with which their environment can be manipulated, their morphological diversity, the diversity of habitats in which they live, etc.) make them ideal for studying multimodal signaling.

Enigmatic Ornamentation Eases Male Reliance on Courtship Performance for Mating Success

Eileen Hebets et al. — Tue, 12 Jul 2011 10:51:46 PDT

Female preferences are frequently invoked to explain the widespread occurrence of elaborate male ornaments, yet empirical data demonstrating such preferences are sometimes equivocal or even contradictory. In the wolf spider Schizocosa stridulans, despite evidence of strong female choice, prior research has been unable to link the conspicuous sexually dimorphic foreleg ornamentation of males to their mating success. We conducted three experiments aimed at determining the function of this previously enigmatic ornamentation. Our first two experiments used males with phenotypically modified foreleg phenotypes in simple and complex mating environments in order to examine the relationship between the presence/absence of ornamentation and male mating success. In both experiments, we found no relationship: courtship rate was the sole predictor of mating success. In a third experiment, we used males with naturally varying foreleg ornamentation in mating trials. Ornamentation was subsequently quantified and we again examined the factors influencing male mating success. As in our first two experiments, we found courtship rate to be a good predictor of mating success. Additionally, we discovered that foreleg ornamentation and courtship rate interact to influence male mating success. At low courtship rates, males with more foreleg ornamentation have a mating advantage, whereas at high courtship rates, males with less foreleg ornamentation have a mating advantage. We discuss several potential explanations for these results. In summary, we provide the first evidence of a benefit of foreleg ornamentation in male S. stridulans and suggest that this benefit is realized by the interaction between ornamentation and courtship rate.

A sticky situation: Solifugids (Arachnida, Solifugae) use adhesive organs on their pedipalps for prey capture

Rodrigo H. Willemart et al. — Tue, 12 Jul 2011 10:51:43 PDT

Solifugids (Arachnida, Solifugae) have unique evertable adhesive organs on the tips of their pedipalps, named ‘suctorial’ or ‘palpal’ organs. Previous studies have shown that these organs enable solifugids to climb smooth glass-like surfaces and have hypothesized that these structures facilitate prey capture. Here, we use high-speed videography to demonstrate that the suctorial organs of Eremochelis bilobatus are its primary means of capturing insect prey. We also present calculations of the adhesive pressure exerted by these suctorial organs during real prey capture events.

Females Are Choosier in the Dark: Environment-Dependent Reliance on Courtship Components and Its Impact on Fitness

Aaron S. Rundus et al. — Wed, 06 Jul 2011 10:39:44 PDT

A broad understanding of multimodal courtship function necessitates knowledge of the potential information content of signal components, the efficacy of signal components in eliciting the appropriate receiver response, and the fitness consequences of mating decisions based upon various signal components. We present data addressing each of these requirements for the multimodal-signaling wolf spider, Schizocosa floridana Bryant. Using diet manipulations, we first demonstrate that both visual and seismic courtship signals are condition-dependent. Next, using high- and low-quantity diet individuals in mate choice trials across manipulated signaling environments, we demonstrate that the seismic signal is crucial for mating success and further show that female choosiness is environment-dependent. Females mated more with high diet males only in the absence of visual signals, showing no discrimination in the presence of visual signals. Finally, by quantifying the number of offspring produced by our mated females, we reveal that a female’s mating environment, in conjunction with her potential resource availability, influences her fitness—in environments in which females exerted choice, heavier females produced more offspring. Together, this comprehensive set of experiments demonstrates that female choosiness varies across environments, leading to direct fitness consequences.

More Ornamented Males Exhibit Increased Predation Risk and Antipredatory Escapes, but not Greater Mortality

Kasey D. Fowler-Finn et al. — Tue, 28 Jun 2011 11:28:00 PDT

Secondary sexual traits not only confer benefits to their bearer through increased mate acquisition, but may also have inherent costs, including the attraction of predators. Here, we examined the relationship between conspicuous secondary sexual traits and predation costs using two male morphs of Schizocosa wolf spiders: brushlegged and non-ornamented. In the field, we ran two predation experiments using artificial enclosures to directly test mortality costs of predation on the two male morphs. Using a natural predator, a larger wolf spider in the genus Hogna, we found no difference in predation on brush-legged vs. non-ornamented males. However, predation was depends on environmental conditions. More individuals were preyed upon at night (vs. during the day) and on rock litter (vs. leaf litter), but the two male morphs were preyed upon equally to each other across environmental treatments. A laboratory experiment incorporated staged interactions between a single predator (Hogna) and each male morph to examine finer details of predation events. Again, we found no differential mortality between brush-legged and non-ornamented males. However, brush-legged males were attacked sooner and were more likely to escape the attack. Our results show an association between sexual ornamentation and predation risk as well as escape behavior.

A signal-substrate match in the substrate-borne component of a multimodal courtship display

Damian O. Elias et al. — Mon, 27 Jun 2011 14:52:10 PDT

The environment can impose strong limitations on the efficacy of signal transmission. In particular, for vibratory communication, the signaling environment is often extremely heterogeneous at small scales. Nevertheless, natural selection is expected to select for signals well-suited for effective transmission. Here, we test for substrate-dependent signal efficacy in the wolf spider Schizocosa stridulans Stratton 1991. We first explore the transmission characteristics of this important signaling modality by playing recorded substrate-borne signals through three different substrates (leaf litter, pine litter, and red clay) and measuring the propagated signal. We found that the substrate-borne signal of S. stridulans attenuates the least on leaf litter, the substrate upon which the species is naturally found. Next, by assessing mating success with artificially muted and non-muted males across different signaling substrates (leaf litter, pine litter, and sand), we explored the relationship between substrate-borne signaling and signaling substrate for mating success. We found that muted males were unsuccessful in obtaining copulations regardless of substrate, while mating success was dependent on the signaling substrate for non-muted males. For non-muted males, more males copulated on leaf litter than any other substrate. Taken together, these results confirm the importance of substrate- borne signaling in S. stridulans and suggest a match between signal properties and signal efficacy – leaf litter transmits the signal most effectively and males are most successful in obtaining copulations on leaf litter.

Complex courtship displays facilitate male reproductive success and plasticity in signaling across variable environments

Dustin Wilgers et al. — Mon, 27 Jun 2011 14:49:18 PDT

Effective signal transmission is essential for communication. In environments where signal transmission is highly variable, signalers may utilize complex signals, which incorporate multiple components and modalities, to maintain effective communication. Male Rabidosa rabida wolf spiders produce complex courtship signals, consisting of both visual and seismic components. We test the hypothesis that the complex signaling of R. rabida contributes to male reproductive success in variable signaling environments. We first examine the condition-dependence of foreleg ornamentation (a presumed visual signal) and seismic signal components and find that both may provide potentially redundant information on foraging history. Next, we assessed reproductive success across manipulated signaling environments that varied in the effectiveness of visual and/or seismic signal transmission. In environments where only one signal could be successfully transmitted (e.g., visual or seismic), pairs were still able to successfully copulate. Additionally, we found that males altered their courtship display depending on the current signaling environment. Specifically, males reduced their use of a visual display component in signaling environments where visual signal transmission was ablated. Incorporating signals in multiple modalities not only enables R. rabida males to maintain copulation success across variable signaling environments, but it also enables males to adjust their composite courtship display to current signaling conditions.

Current Status and Future Directions of Research in Complex Signaling

Eileen Hebets — Mon, 27 Jun 2011 14:46:31 PDT

The term ‘complex signaling’ reflects a recent scientific focus on the multiple elements frequently incorporated into animal signals (reviewed in Candolin, 2003; Hebets and Papaj, 2005; Partan and Marler, 2005; Bro-Jorgensen, 2010). It embodies a new appreciation that signals used in communication are regularly composed of numerous components and that each component may individually vary in a number of ways. For example, signal components may vary in their time or mechanism of production, in the efficacy of their transmission, and/or in their mechanism of reception, among others. Employing the term ‘complex signaling’ reminds us of the need to maintain a broad, inclusive view of the dynamic, interactive nature of communication when trying to understand its evolutionary history and current function.

Prey capture by the whip spider Phrynus marginemaculatus C.L. Koch

Roger D. Santer et al. — Tue, 06 Oct 2009 11:02:37 PDT

Whip spiders (Arachnida, Amblypygi) are little-studied arachnids with enlarged spiny pedipalps and elongated ‘‘antenniform’’ forelegs. These antenniform legs contain at least seven giant sensory neurons with no known behavioral function. Here we use high-speed cinematography to describe the prey capture behavior of the whip spider Phrynus marginemaculatus C.L. Koch 1840, in order to examine how these giant neurons might be involved. When presented with a prey item (a cricket), a whip spider first accurately aims one of its antenniform legs in the prey’s direction. Next, the whip spider orients its body to the prey item and approaches, placing one antenniform leg tip on either side of the prey. The whip spider may remain relatively still in this position for some time, before opening its pedipalps in preparation for a strike and then rapidly swinging its antenniform legs away from the prey item and striking at it with its pedipalps. In common with previous studies, our results show that giant neuron activity is not necessary to trigger any of the stages of normal prey capture behavior, but they also suggest that these neurons could still provide information important in this context.

Sensory Biology of Whip Spiders (Arachnida, Amblypygi)

Ranier Foelix et al. — Tue, 10 Feb 2009 10:46:16 PST

Whip spiders belong to a small arachnid order (Amblypygi) that is not well known. Their most conspicuous feature are the elongated, extremely thin front legs (“whips”, or antenniform legs). These are no longer used for walking but are modified extremities carrying various sense organs – very much like the antennae of insects. Whereas hundreds of olfactory hairs are concentrated near the tip of each antenniform leg, large bristles (contact chemo-receptors) are evenly distributed over the entire antenniform leg. The sensory hairs of each antenniform leg contribute about 30,000 small sensory axons which proceed toward the Central Nervous System (CNS). The sensory fibers originating from the mechano-receptive bristles make chemical synapses with a few giant interneurons in the periphery. The giant axons (10-20 μm in diameter) of these large interneurons transmit nerve impulses with a high velocity (6 m/s) to the CNS. The purpose of this fast pathway still needs to be determined. Originally it was thought that the fast giant axons would trigger quick escape reactions, but this was not confirmed in physiological experiments. However, other possible behaviors that may be aided by the giant interneurons are prey capture, fighting, and orientation.

What makes whip spiders unique is that both synapses and giant neurons are located far out in the peripheral nervous system. In all other arthropods – except for some arachnids – synapses and giant fiber systems are always found inside the CNS, never the in the periphery.

Supplementary Material: Agonistic signals received by an arthropod filiform hair allude to the prevalence of near-field sound communication

Roger D. Santer et al. — Thu, 20 Nov 2008 08:07:35 PST

SUPPLEMENTARY METHODS
(i) Analysis of behaviour
(ii) Stimulator design

SUPPLEMENTARY RESULTS
(i) Typical contest behaviour
(ii) Additional data on ALV positioning relative to the receiver
(iii) Electrophysiological control experiments
(iv) Analysis of phase-locking

SUPPLEMENTARY REFERENCES

Includes 3 figures and 1 table.