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ABSTRACT Drilling and tapping behaviors in woodpeckers have long garnered significant attention, given their extreme, high-impact nature. However, how these birds integrate neuromuscular and respiratory systems to produce such high-force, high-frequency behaviors remains poorly understood. Here, we combined electromyography with measures of respiratory air-sac pressure and syringeal airflow to investigate the neuromuscular and ventilatory mechanisms of forceful pecking in downy woodpeckers. We found that both types of pecking behaviors tested engage skeletal muscles across the head, neck, hips, tail and abdomen. In-depth analysis of EMG timing and activity point to a hammer-like model associated with drilling, whereby head and neck muscles contract to create a stiffened cephalo-cervical lever arm that efficiently transfers kinetic energy from the swinging bill into the wood. Moreover, hip flexors help power protraction of the head and body for drilling, whereas tail muscles presumably help brace the bird's body against the tree. Respiratory analyses show that woodpeckers actively exhale with each bill strike of the substrate, resembling the ‘grunting’ behavior that human athletes use to stabilize their core and enhance force output. These effects persist at high tapping frequencies, indicating that individuals take mini-breaths between successive taps. Altogether, our results highlight the way motor and respiratory systems are leveraged to facilitate the production of extreme behavior, which hinges on biomechanical specializations and extraordinary performance abilities. 

Synopsis Examples of behavioral strategizing exist throughout the animal kingdom, but the quantification and analysis of these complex behavioral patterns remain a challenge. Classic research in this realm often relies either on methods that intentionally simplify complexity or that focus on a subset of abundant behaviors. Unfortunately, these approaches can sometimes eliminate informative details of behavioral strategizing. Here, we demonstrate the utility of a systems-based approach to characterize behavioral patterns in a way that captures the complexity of behavioral strategies and tactics while supporting the generation of relevant, system-specific hypotheses. We accomplish this aim by building upon classic ideas of strategy and tactic, refocusing the theory on behavioral traits, and extending the framework to make sense of patterns of behavior use. In doing so, we outline a more expansive definition of the behavioral tactic, and we provide a methodological roadmap for quantifying multi-behavior and multi-agent tactics. Our goal is to craft a framework for the study of behavioral patterns and encourage researchers to embrace the complexity in their systems. To this end, we provide a case study of territoriality in downy woodpeckers as proof of concept for a network-based systems approach to understanding behavioral strategies. 

Synopsis Sexual selection drives the evolution of a broad diversity of traits, such as the enlarged claws of fiddler crabs, the high-energy behavioral displays of hummingbirds, the bright red plumage of house finches, the elaborated antennae of moths, the wing “snapping” displays of manakins and the calculated calls of túngara frogs. A majority of work in sexual selection has aimed to measure the magnitude of these traits. Yet, we know surprisingly little about the physiology shaping such a diversity of sexually selected behavior and supportive morphology. The energetic properties underlying sexual signals are ultimately fueled by metabolic machinery at multiple scales, from mitochondrial properties and enzymatic activity to hormonal regulation and the modification of muscular and neural tissues. However, different organisms have different physiological constraints and face various ecological selection pressures; thus, selection operates and interacts at multiple scales to shape sexually selected traits and behavior. In this perspective piece, we describe illustrative case studies in different organisms to emphasize that understanding the physiological and energetic mechanisms that shape sexual traits may be critical to understanding their evolution and ramifications with ecological selection. We discuss (1) the way sexual selection shapes multiple integrated components of physiology, behavior, and morphology, (2) the way that sexually selected carotenoid pigments may reflect some aspects of cellular processes, (3) the relationship between sexually selected modalities and energetics, (4) the hormone ecdysone and its role in shaping sex-specific phenotypes in insects, (5) the way varied interaction patterns and social contexts select for signaling strategies that are responsive to social scenes, and (6) the role that sexual selection may have in the exploitation of novel thermal niches. Our major objective is to describe how sexually selected behavior, physiology, and ecology are shaped in diverse organisms so that we may develop a deeper and more integrated understanding of sexual trait evolution and its ecological consequences. 

The long‐distance migrations of thousands of bird species and their billions of individuals are feats of astounding physiological specialization and plasticity. Whereas numerous organ systems require modification to achieve successful fueling and navigation capabilities, given their overarching importance for movement and contribution to body mass, skeletal muscles are subject to exceptional performance optimization and anatomical plasticity. To express the appropriate changes throughout the complicated life history of migration, while remaining in synchrony with the environment, skeletal muscles must receive preparatory signals and express transcriptional and biochemical modifications required for full expression of the migratory phenotype. In all likelihood, these muscles must also temporally signal their state and needs to other organ systems. By considering other well‐studied avian skeletal muscle systems, this review explores how endocrine signaling likely impacts skeletal muscles involved in migration and, conversely, how those muscles might relay their condition elsewhere throughout the bird's body. Systems biology offers exceptional modeling for capturing this complex biology. 

Animal displays are often limited by the properties of the muscles that generate them. Here, using in situ muscle stimulation, we investigate the twitch properties of the longus colli ventralis (LCv), a primary muscle used protract the head and neck during territorial drumming displays in woodpeckers. Specifically, we test LCv twitch kinetics and endurance in a manner that simulates drum speed (beats s−1) and length (total beats), two signal feature that can evolve independently of each other. We identify a maximum muscle contraction rate that may represent a physiological constraint relevant to drumming speed, but no relevant constraint on the repetition of contractions that might affect drum length. This suggests twitch properties may differentially affect display components. Broadly, our findings highlight how certain display features may freely diversify independent of others due to physiological limits, while pointing to the way complex signals can evolve under partial performance constraints.