Differential Regulation of Adipokines May Influence Migratory Behavior in the White-Throated Sparrow (Zonotrichia albicollis)

Bartell PA (2013) Differential Regulation of Adipokines May Influence Migratory Behavior in the White-Throated Sparrow (Zonotrichia albicollis). PLoS ONE 8(6): e59097. doi:10.1371/journal.pone.0059097 Differential Regulation of Adipokines May Influence Migratory Behavior in the White-Throated Sparrow (Zonotrichia albicollis ) Erica F. Stuber 0 Jessica Verpeut 0 Maria Horvat-Gordon 0 Ramesh Ramachandran 0 Paul A. Bartell 0 Claudia Mettke-Hofmann, Liverpool John Moores University, United Kingdom 0 1 Department of Animal Science, The Pennsylvania State University, University Park, Pennsylvania, United States of America, 2 Ecology Graduate Program, The Pennsylvania State University , University Park, Pennsylvania , United States of America White-throated sparrows increase fat deposits during pre-migratory periods and rely on these fat stores to fuel migration. Adipose tissue produces hormones and signaling factors in a rhythmic fashion and may be controlled by a clock in adipose tissue or driven by a master clock in the brain. The master clock may convey photoperiodic information from the environment to adipose tissue to facilitate pre-migratory fattening, and adipose tissue may, in turn, release adipokines to indicate the extent of fat energy stores. Here, we present evidence that a change in signal from the adipokines adiponectin and visfatin may act to indicate body condition, thereby influencing an individual's decision to commence migratory flight, or to delay until adequate fat stores are acquired. We quantified plasma adiponectin and visfatin levels across the day in captive birds held under constant photoperiod. The circadian profiles of plasma adiponectin in non-migrating birds were approximately inverse the profiles from migrating birds. Adiponectin levels were positively correlated to body fat, and body fat was inversely related to the appearance of nocturnal migratory restlessness. Visfatin levels were constant across the day and did not correlate with fat deposits; however, a reduction in plasma visfatin concentration occurred during the migratory period. The data suggest that a significant change in the biological control of adipokine expression exists between the two migratory conditions and we propose a role for adiponectin, visfatin and adipose clocks in the regulation of migratory behaviors. - Funding: This project was funded by The Pennsylvania State University Dept. of Poultry Science and College of Agricultural Sciences. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Small songbirds have evolved many strategies to cope with the costly rigors of long-distance migration. During the pre-migratory period, physiological and endocrine systems change in preparation for migration; birds become hyperphagic and alter their metabolism resulting in increased fat deposition [1,2]. Fat provides more than eight times the energy per gram as protein or carbohydrates and is stored with minimal water, making it a valuable source of energy during migration [3]. The migratory programs of many small songbirds consist of segments of nocturnal flights and subsequent daytime stops to rest and refuel. Flights during successive nights under poor conditions may lower fuel reserves below critical thresholds, requiring birds to delay longer at stopover sites to replenish fat stores [4,5]. Although many small passerines commence migratory flight after peak fat deposition has been reached [1], how each individual determines whether it has enough fat accumulated to initiate migratory flight is unclear [6,7]. Pre-migratory hyperphagia and fattening may lead to changes in metabolic signals, such as adipokines, that circulate in the blood of individual birds. Consequently, changes in metabolic signals could be utilized to initiate migration once fat stores reach a critical level. Changes in food intake and dietary composition during premigration and the migratory period during stopovers can elicit changes in individuals migratory behaviors [7]. Birds are able to compensate for low diet quality by increasing food intake and decreasing migratory restlessness [7,8]. Additionally, previous work has demonstrated that physical condition is related to the initiation of spring migration, where birds in better physical condition leave the wintering site earlier than individuals in worse condition [9,10]. Birds are able to adjust their behavior in response to changing energetic conditions [11]. Recently, Cerasale et al. [12] have highlighted a potential role of fat hormones in regulating energy intake in migrating birds. However, although a relationship between body condition and migratory behavior has been highlighted in the literature, little is known of the physiological mechanisms linking endogenous information about fat stores and behavioral flexibility. Avian migrants rely heavily on circannual and circadian clocks to regulate components of migration and the processes of these clocks are shaped by changes in photoperiod [7]. Biological clocks and photoperiodic timers dictate the initiation, duration, termination, and organization of the migratory period (see reviews in [13,14,15,16,17]). Hyperphagia and pre-migratory fattening are important aspects of the physiological preparation for longdistance flight and these preparations are all under the control of biological clocks [1,18,19]. The circannual rhythm of migration is shaped by changes in photoperiod, indicating an influence of environmental cues in regulating this program. The degree to which photoperiodic cues directly regulate migratory behaviors changes among taxa and vary even within the same genus [20]. The appearance of nocturnal migratory restlessness, commonly called Zugunruhe, in otherwise diurnal animals is under the direct control of an endogenous circadian clock [21,22]. In Zonotrichia albicollis, the white-throated sparrow (WTSP), it has been demonstrated that circadian clocks and photoperiodic timers regulate the seasonal appearance of Zugunruhe [20,23,24]. Clocks are generated by molecular rhythms in the expression and activity of so called clock genes which regulate behavioral rhythms through positive and negative autoregulatory feedback loops [25]. Molecular clocks are influenced by metabolism, in particular through alterations in redox states and gas responsive elements [26,27,28]. The molecular oscillations of endogenous clocks convey rhythmic information to peripheral systems and modulate system-specific rhythmic behaviors [29]. During the course of the day, rates of lipogenesis and lipolysis vary to accommodate changes in energy demands [30]. Recent evidence demonstrates the existence of molecular circadian clocks located within adipose tissue [31,32]. Clocks in adipose tissue can be influenced by feeding regimens or central pacemakers through mul (...truncated)