MH PART 4 BEHAVIOR AND THE ENVIRONMENTCHAPTER The Annual Cycles of Birds One swallow does nor make a suamer, but one skein of geese, cleaving the murk of a March thaw, is the spring. Leopold 1966, p. 19] irds fice seasons of stress and seasons of opportunity that cor- ndar changes in day length, cli- and resources, especially food. The primary seasons are usually related to changes in temperature in the temperate zones and to changes in rainfall in the Tropics. Just to survive, much less to breed and otherwise function appropriately at different times of their year, an indi- vidual bird must change its appearance, its physiology, and its behavior. Ic must transition smoothly from one life-history stage to another. with advance notice and preparation so as to time each stage appropriately to the next set of environmental conditions (acobs and Wingfield 2000), Environmental and social cues activate internal endocrine management systems that orchestrate the sequencing of life-history stages. with con- tingencies for the unpredictable Each year, an adult bird invests time and energy above and beyond that required for dail respond to predictable ¢: mat y survival into three nuain efforts: reproduction, molt, and, in some cases. migration. The conflicting demands of these efforts combine with seasonal resources and opportunities to define a bird’s an- nual cycle (Figure 91). Tight scheduling, tradeoffs, and compromises are often required. Natural selection will favor those individual birds that schedule well and optimize the balance of their seasonal efforts. This chapter first describes the basic components of avian annual cy cles and then proceeds to the physiological clocks, called circadian thythms, that control the avian annual calendars by synchronizing a bird's with its seasonal environment. The photoperiod—the length of daylight—is an essential environmental cue for the clocks. It triggers activity in the brain and then the pituitary gland that leads to of hormonal controls of physiology and behavior. Then we more closely examine the timing, costs, and tradeoffs related to breeding, molt, and cascade246 (CHAPTER NINE Summer Solstice aa pes ves evetee, ree =! Pte es) PEE ae Se ined z ei is i \ is Foam pa fvernal ¥ enlargement ria ate ey a [rreatternate lmolt in females| [Arrival on the “SY ane ‘ontinued pair] Formation Winter Solstice FIGURE 9-1 Annual cycle of the Mallard. Most individual birds attempt to breed when they are one year old. The terms prealternate molt and prebasic molt correspond to the prenuptial molt and postnuptial mole of Owight’s (1900) system of molt and plumage nomenclature (see Chapter 4). [From Bluhm 1988] migration, including how birds handle stress, The chapter concludes with the effects of global warming on the annual cycles of birds, Basic Annual Cycles ‘The simplest type of annual cycle and the typical year of permanent res- idents—birds that live in the same place year-round—present three main sequential tasks: breed, molt. and survive until the next breeding season. Consider, tor example, the simple life of the Common Pigeon (Figure 9-2). The pigeons cycle between cwo life-cycle stages. As long as they have ample food and a mate, they nest until the young fledge (or until the mate is lost). Then they transition to the alternative, nonbreeding stage and remain in that stage until they have a mate in breeding condition and adequate food is available to initiate nesting,247 THE ANNUAL CYCLES OF BIRDS No mate or mate not in Good food, mate present: breeding condition: Remain in breeding Stay molting (nonbreeding) Mate lost or young, independent: Initiate molt Food available but not Good food, a sufficient for breeding: mate present: Stay in molt Initiate breeding. FIGURE 9-2 simple life cycle of the Common Pigeon, which alternates between a breeding stage and a nonbreeding, or molting, stage. Arrows indicate conditions (boldface type) for remaining in ane stage or switching to the other. Each condition is followed by a response to the change in environmental cues. [After Jacobs and Wingfield 2000] The annual cycles of forest birds in equatorial Borneo also are simple ones. The temperature and day length stay the same all year. Small birds start to nest when the heavy rains begin in December (Fogden 19 Adults start to molt shortly after the young have left the nest in May and continue molting until che beginning of the qvo-month “dry” season, when food starts to become scarce. When heavy rains resume and food supplies increase, gonads increase in size and the cycle repeats itself are 9-3). Similar cycles of reproduction and molt are typical of permanent res- idents of northern temperate localities. including Song Sparrows in Ohio, Black-capped Chickadees in Wisconsin, and Common Chaffinches in Jan. Apr Aug Dee. FIGURE 9-3 birds have well-defined breeding and molting seasons, which coincide with the months of greatest food availability, even in the equatorial rain forests of Borneo. [After Fogden 1972)248 (CHAPTER NINE Britain, After the quiescent winter months, sex hormones flow. gonads increase in size, and males proclaim their territories with conspicuous songs and, sometimes, brutal fights. Pair bonds are established or reaffirmed and mating takes place, Young hatch in May and June and generally reach in- dependence by late July. Molt follows in August and September, At this time, young birds leave their natal territories, and families aggregate into well-organized flocks for the winter. Social competition for territories. food, and mates—all resources essential for reproduction next spring— may start in the autumn, Migration adds a complicating challenge to the annual cycle. Major changes in physiology, body composition, and behavior take place (see Chapter 10). Afier they breed and molt, migratory birds generally gather in flocks and eat tremendous amounts of food, fueling themselves for their trips. To fuel their marathon flights, many species double their body mass with large stores of fat as fuel, As the date for departure approaches, they become restless after dark and then leave on a major trip to a distant win tering ground, Migratory preparations are repeated the following spring for the recun north, where the cycle of reproduction, molt, and prepa- ration for migration repeats. Many temperate-zone birds, especially those that migrate, molt twice a year, once after breeding and again in late win ter or early spring Annual Cycles of the White-crowned Sparrow The annual cycles of White-crowned Sparrows, including their physio~ logical controls, have been studied in depth (Chilton et al. 1996). The White-crowned Sparrow breeds throughout northem Canada and from southern Alaska to central California (Figure 9-4). The annual cycle of White-crowned Sparrows can be diagramed as a series of specific stages activated by environmental cues (Figure 9-3). The stages are activated by internal (usually hormonal) responses that, in turn, trigger the transition to the next stage in the sequence. Populations on the Pacific Coast differ in the extent of their annual migrations and in other aspects of their annual cycles. Those that breed in Alaska and in northwestern Canada (subspecies gambeli) are long- distance migrants that winter primarily in California, where they mix with winter flocks of the local nonmigracory White-crowned Sparrows (sub- species mutrall). Members of another population (subspecies pugetensi) which breed on the coasts of Washington, Oregon, and British Colum- bia, also mix with nuttalli flocks in California during the winter. ‘White-crowned Sparrows from northern localities nest later in the spring than those from southern localities. The southern resident mutalli come into breeding condition first, then the pugetensis, and, finally, the gambelii of the far north, Differences in the timing of the enlargement of the gonads and breeding activities characterize not only the three sub- species but also the geographical gradients of populations within each subspecies.FIGURE 9-4 Breeding ranges of four western sulbspecies of White-crowned Sparrows, Zonotrichia leucophirys. The most northern races, Z.. gambeli and Z 1. pugetensis, migrate to central California, where they winter with resident Z| mutalls, The Rocky Mountain race, Z. 1. oriantha ‘migrates south to Arizona and Mexico. [From Cortopass ‘and Mewaldt 1965] 30 20 0 Miles 0400 800 a 200 600 1000 kilometers Sataecal FIGURE 9-5 Annual life ‘migration cycle of a migratory population of the White- crowned Sparrow (subspecies ‘gambelii). Each seasonal stage (squares) is triggered by environmental cues (large arrows) and by the physiological changes of a > | overwintering preceding stage (thin arrows). [After Jacobs and Molt Vernal migrs [testing 249250 (CHAPTER NINE Finally, some. bue not all. of these White-crowned Sparrows molt in the spring before breeding. This extra “prenuptial” molt is known as the prealternate molt (see Chapter 4). Circadian Rhythms and the Photoperiod The annual cycle requires an orderly integration of behavior and physi ology. A nctwork of physiological controls regulate the schedules of te- production, molt, sleep, feeding. and migration. Alll plants and animals have in their cells biological clocks that release the hormones that regulate metabolism, reproduction, and behavior. Birds are no exception. Neuroendocrine systems synchronize cellular thychms so that an entire bird is organized internally and appropriately sy nized with its periodic environment. In addition to regulating the daily activity and cycles of body temperature, these internal clocks measure day length itself and calibrate the sun compass by which birds navigate (Gee Chapter 10). They govern migratory restlessness, premigratory fattening, and egg laying. Some biological clocks, called circadian rhythms, match the daily 24-hour cycle of the Earth’s rotation on its axis, Others, called circannual cycles, synchronize to the annual cycle of the Earth's revolu- tion around the sun. ‘The triangle-shaped pineal gland, which is located on top of the brain. houses the biological clock in birds (Gwinner and Hau 2000; Sassone- Corsi 1998). Most diurnal birds have a well-developed pineal gland. This gland includes photosensitive cells, each having gene-based pacemakers that direct the rhythmic production of melatonin. the chemical that reg- ulates daily rhythms in concert with daily light-dark cycles. Experimen- tal removal of the pineal gland in House Sparrows causes normal 24-hour cycles to disappear, The pineal melatonin rhythm interacts with photo sensitive cells of the hypothalamus of the lower midbrain and the retina of the eye, both of which also secrete some melatonin Circadian rhythms are a basic adaptation of cellular organisms to the 24-hour light-dark cycle of the planet (Farner 1980a), Twilight triggers a switch in physiology from diurnal to nocturnal systems. Every indi ual bird has an intrinsic chythm approximately 23 hours in length in which body temperature, rate of metabolism, and level of alertness fluctuate in predictable ways. Because they are not exactly 24 hours in length, these internal cycles tend to depart gradually from real time, starting slightly earlier each day, unless they are somehow synchronized or entrained by external cues called Zeitgebers—literally, “time givers.” ‘When Common Chaflinches are kept in constant dim light, their en= dogenous rhythms of activity and metabolic rate function in a period of about 23 hours and therefore drift about 1 hour per day (Figure 9-6). White-crowned Sparrows have a regular cycle of activity and sleep that is just under 24 hours long when they are kept in a dimly lit experimen- tal cage. Natural, external light-dark cycles then synchronize the endoge- nous rhythm with the 24-hour cycle. chro d-150. Oxygen uptake (mish) bo DT RB RBS Oe TS Time (days) FIGURE 9-6 Common Chaffinches kept in a dimly lit environment have @ daily activity cycle (measured here in milliliters of oxygen taken up per hour) of just under 24 hours. This experiment demonstrates that, under constant dim illumination (LL), the cycle drifts 1 hour of clock time unless it is synchronized by an external stimulus such as regular 24-hour light-dark cycles (LO). [After Aschoff 1980] Endogenous rhythms control the annual cycles as well as the daily cycles of some birds. Self-sustaining circannual rhythms have a period of approximately one year. When captive Common Starlings, Garden War- blers, and Eurasian Blackeaps are kept in a constant daily environment of 12 hours of light and 12 hours of dark, they continue to come into breed ing condition and molt in a predictable annual cycle (Figure 9-7) ‘The photoperiodic control system couples two kinds of information. Clock information from the internal circadian cycle enables the bird to measure day length by using time windows of photosensitivity. Environmental-light information stimulates neural receptors to translate day-length information into behavior. This two-part system allows birds co respond at the optimal time for reproduction, to synchronize repro- ductive function in mating pairs, and to terminate reproductive function— three fundamental requirements for control of the annual reproductive cycle. length, or photoperiod, plays a key role in the control system that synchronizes the physiologies of individual birds with their environment. n (1929) pioneered research on the photoperiodic control of avian gonadal cycles. He showed that increases in photoperiod of only 5 to 10 minutes per day cause the testes of Dark-eyed Juncos to increase in size, an effect that was reversible and repeatable as many as chree times between autumn and spring (Figure 9-8). The phenomenon of the photo- periodic control of gonad cycles has since been recognized in more 1 60 north temperate bird species. Molt and preparations for migration also are triggered by changes in day length and can be experimentally manipulated. Stephen Emlen (1969) for example, accelerated the annual cycle of Indigo Buntings, inducing 1920 a 2223 2a OS 251252 @ Time (years) ' 1 1 1 I I | I t + Time (years) 1305 7 9 0 135 790 ‘Time of year (months) FIGURE 9-7 Circannual chythms under constant photoperiodic conditions (A) Rhythms of testicular width (curves) and molt (bats) in a Common Starling. The tundamped oscillations in tests size and the intervals between successive molts deviate ieregulary from a 12-month cycle. (8) Rhythms of summer mole (old bers) and wincer molt (open bars) in a Garden Warbler (left) and in a Eurasian Blackcap (right), both maintained in captivity for 8 years. Both molts occur progressively earlier each year because the birds have an internal rhythm with @ mean period of about 10 ‘months. [After Gwinner 1977 and Berthold 1978] an extra molt into the year by suddenly increasing the length of the photo periods to which captive birds were exposed. ‘The circadian rhythms include a limited period of photosensitivi day. During this period, external light stimulates receptors in the brain, which in tur trigger a series of physiological reactions. As day length in- creases. so does the chance that there will be daylight during the photo- sensitive period (Figure 9-9). Not only does the chance of overlap, or coincidence, increase with day length, but the duration of the period of overlap also increases. The amount of overlap enables birds to measure day length. The “external coincidence” model was originally developed for plants, and we now have evidence of this model for many species of birds.Diameter in Mritimeters. in Pnitimelers. z { $ + Be i SUE en eh soe 1 Falent FIGURE 9-8 In the pioneer study of annual cycle contol by photoperiod, William K. Rowan demonstrated that longer day lengths cause the testes of captive Dark-eyed Juncos to increase prematurely to full size in january (lawer left) and again in April lower right), instead of in May and June, as in wild juncos (upper graph). Mean temperature is the average air temperature in that month. [From Rowan 1929] Birds monitor day length through special receptors in che hypothala- mus of the brain as well as those in the pineal gland and retina, Longer day lengths induce gonad development and migratory behavior even in sightless birds, The light receptors of the White-crowned Sparrow, for example, lie in the ventromedial hypothalamus of the lower midbrain (Figure 9-10), The receptors are structurally unspecialized elements that are sensitive to extremely low light intensities such as those thac directly penetrate brain tissues, Pinpoine illumination of the hypothalamic recep- tors by a single, thin light-conducting optical fiber induces both testicu- lar growth and migratory behavior (Yokoyama and Farner 1978). After stimulation of the photoreceptors, neurosecretory cells in the hypothalamus induce the release of neurohormones from the median em- inence, the neural part of the pituitary (wee Figure 9-10). The released neurohormones then induce the anterior pituitary gland to produce the hormones (see Table 9=1) that directly affect the activity of the gonads 253254 (CHAPTER NINE No response ato Response E # iso = Maximum response 22120 Lia 4 FIGURE 9-9 The external coincidence model suggests that day length is measured by the increased amount of time that daylight periods (open bars) coincide with the photosensitive phase of the circadian rhythm (oscillation peaks). Abbreviations: L, umber of hours of light; D, number of hours of dark. Response was measured in terms of gonadal enlargement, which was greatest for a 22-hour light-2-hour dark cycle. [From Farner 1980a] themselves. Thus, a series of neural and physiological events translate creasing day length inco sexual activity. The annual cycle of the White-crowned Sparrow outlined earlier illustrates the translation of seasonal changes in day length into appropri ate behaviors, Increasing photoperiods during late winter and early spring Cavity of third ventricle Pars tuberalis Median eminence ‘Optic chiasma Pars tuberalis Vascular bed of posterior lobe Connective tissue barrier Portal vessels: (of cephalic region of anterior lobe Portal vessels ‘of caudal region. of anterior lobe FIGURE 9-10 Avian pituitary gland and adjacent structures. Daylight stimulates special photoreceptors in the tuberal region (pars tuberslis) of the lower hypothalamus of the midbrain, Neurohormones are released in the median eminence and carried to the anterior pituitary gland through the hypophyseal portal blood vessels. They stimulate {gonadal hormone production and, as a result, gonadal activity. [From Hihn 1961)trigger events in the annual cycle. The longer days of early spring st ulate gonad development and then the spring (prealternate) molt and mi- gration. Warmer temperatures, rainfall, and the springtime display behav- ior of other sparrows stimulate the final stages of gonad development on the breeding ground and, as a result, the increased secretion of sexual hor- mones. After the birds breed, the shortened days of late summer trigger the main (prebasic) molt. The increasing day lengths of the spring also schedule, in advance, the fall light-insensitive, or photoreffactory, period of the testis. After pho= toperiodic regulation of the annual cycle evolved, some additional safe- guards and corrections were essential, Photorefiactory physiology is one of them, The gonadal cycle normally concludes with a rapid collapse and reabsorption of gonadal tissue, Then follows the photorefiactory period, during which long days do not induce gonadal regrowth, The photore- fractory physiology of adults seems to be an adapeation for scheduling molt and migratory preparations during the favorable conditions of late sum-= mer by discontinuing reproductive activity while days are still long (Farner 1980b). Finally. the very short days of early winter inhibit gonad growth and restore sensitivity to long photoperiods by terminating the refractory period. The cycle begins anew as day lengths increase in January. Short winter days are essential to the control of the annual cycle: the testes will not grow in response (0 the long days of spring unless a bird has experi- enced a prior period of short day lengths. Thus. White-crowned Sparrows stay in nonbreeding condition for several years when experimentally ex- posed only to long photoperiods. Master Hormones Much of the annual cycle, including specific behaviors in reproduction, molt, and migration. is directly controlled by hormones. Hormone pro- duction is headquartered in the lower midbrain, where the hypothalamus connects to the adjacent pituitary gland, directing it to release master hor- mones that direct the activities of specific organs (Table 9-1), The Pituitary Gland As instructed by the hypothalamus, the pituitary gland releases ewo mas- ter hormones that directly control gonadal development and function and that indirectly control many other aspects of the annual cycle. One of ing hormone (LH)—stimulates the production of the male hormone testosterone by Leydig cells in the testes. In the female, it in- duces the ovulation of mature egg follicles as well as the production of the sex hormones progesterone and testosterone. The other master hor mone—follicle-stimulating hormone (FSH)—stimulates sperm production in the testes of male birds and the initial development of egg follicles in female birds. Research on male birds has shown that increasing day lengths them—| 255 THE ANNUAL CYCLES ‘OF BIRDS[ITABLE9—1 Principal hormones that govern the annual cycles of birds ee Follicle-stimulatin, hormone Glucagon Growth hormon Luteinizing hormone Luceinizing hormone releasing hormone Melatonin Prolactin Thyroxine Testosterone Hormone Abbreviation Source Adrenocorticotropic ACTH Adrenal gland Stress management hormone Suppresses release of gonadal hormones Reduces resistance to disease nunocompetence) cory restlessness Estrogens Progesterone release by pituitary glnd Egg production in oviduct Secondary sexual morphology and brain function FSH Pituitary ghind Sperm production by testes Egg-follicle development in ovary None Pancreas Metabolism in liver and muscles Release of fatty acids to blood plasma Fasting, GH Pituitary ghnd Normal posthatching growth Fat metabolism and synthesis Scimulates immune system LH Pituitary gland Increases production of progesterone and testosterone Induces ovulation LHRH Hypothalamus Production of LH and FSH by pituitary gland None Pineal gland Circadian rhythm of cells throughout body Retina Photoreception and neural transmission Gastrointestinal Food utilization None Ovary Induces ovulation None Pituitary gland Production of crop milk in pigeons Incubation behavior and broodiness Photorefractoriness of testes Ts Thyroid gland Metabolism and thermogenesis Growth and development Onset and pace of molt None Testis, ovary Development of testes Secondary sexual morphology and. brain funetion Ovulation in females 256 ng hormone releasing hormone sts, LHRH stimulates the pi- ‘SH secretion. Pulses of plasma cause the bypothalamus to release lutein (LHRH). As its mouthful of a name sug tuitary gland to increase LH as well as LH then travel throughout the bird's body and stimulate gonadal activ- iors. ity and a host of reproductive behaIn addition to their role in reproductive behavior, endocrine hormones affect the timing and course of molt. The thyroid hormone thyroxine plays a pri 2002). Its effects, however, are subject to the presence of the gonadal hor- mones—particularly the sex steroid hormones such as testosterone, which inhibit molt by suppressing the secretion of thyroid hormones (Hahn et al, 1992), Experimental injections of gonadal hormones into molting birds slow or even stop molt. As a result, nonbreeding and reproductivel successfull birds with lower amounts of gonadal hormones begin c© molt earlier than successful breeders Other hormonal changes take place at the end of the breeding season. In addition to the gonadal hormones, thyroxin. glucagon, corticosterone, and growth hormone all play major roles at different times in the annual cycle, They are central tw depositing and using fat as fuel for migration (Tsipoura et al. 1999; Hintz 2000), Among other effects. they stimulate ravenous feeding and fat deposition through the cascade of hormonal con- trols that starts at the hypothalamus-pituitary headquarters iry role in the onset and pace of molt (enni-Biermann ct al. Managing Seasonal Stress Central to seasonal adjustments and the interplay among hormones is the need for birds co manage daily and seasonal stresses, Regular measure- ments of the amount of the hormone corticosterone in tiny samples of blood plasma from living birds allow ornithologists to monitor the pat- terns of stress that birds experience at different times of year. Cortico- steroid hormones are produced by the adrenal glands and are hus also called “adrenaline.” Corticosterones mediate tradeoffs between individual survival and breeding success. Corticosterone increases rapidly in response co acute stress events stich ing from a predator, fighting for a territory, or being hungry. A rapid rise in corticosterone—the stress response—redirects a bird's behav- ior and physiology toward basic survival efforts such as looking for food and increasing the rate of food intake (Wingfield et al. 1995). Cortico- sterone levels stay high until the bird has offset the energetic challenge, pethaps by mobilizing energy reserves or escaping the source of stress. The return to normal baseline levels as soon as possible is important be- cause continued elevation of corticosterones due to sustained or chronic stress suppresses other activities, such as reproduction, Among the effects, high levels of corticosterone suppress the release of gonadal hormones and reduce resistance to discase (mmunocompetence). Thus, breeding activ- ities, including parental care particularly, are not compatible with high levels of corticosterone in most vertebrate animals (Wingfield 2003), In- creases in corticosterone during spring storms, for example, cause birds to stop breeding. Experimental treatments with corticosterone reduce terri- torial behavior and rates of feeding young. Because of the potentially severe costs, acute stress responses affect many aspeets of a bird's annual cycle, including habitat preferences and breeding behavior. Some birds, however. live in difficult, high-stress as esca 257 THE ANNUAL CYCLES (OF BIRDS258 (CHAPTER NINE en ticosterone. Examples include desert birds, such as the Cactus Wren and Curve-billed Thrasher. which endure intense heat and aridity during the summer (Wingfield et al. 1992). At another extreme, species that breed in the Arctic, such as White-crowned Sparrows and American Tree Spar~ rows, face severe time and energy constraints imposed by the short sum- mers and unpredictable weather (Holberton and Wingfield 2003). Do such birds avoid the tradeoff costs by moderating their corticosterone responses? They seem to do so. The desert-adapted wrens and thrashers suppress the classical adrenocortical response to stress during the hot summer season but reactivate it during the winter, Similarly, the Arctic-nesting sparrows exhibit low responses to stress throughout the season, though males are more sensitive to stress before the young hatch. Then they settle down to the unchanging low levels of their mellow mates. The mechanisms of this modulation are unknown. ronments that would seem to promote debilitating, high levels of eor- Breeding Seasons Guiding the evolution of the controls of seasonal behavior eycles have been such factors as the timing of adequate food supplies for both par- ents and their young, the availability of nest sites, the locations of favor~ able climates, and areas oF times of low predation risk. These so-called ultimate factors tune the control systems to the best times for reproduc ion, However, they provide no guarantee against the vagaries of partic ular years. Drought or parasites may cause widespread nesting filure in some years, Birds, of course, cannot predict such disasters before starting o nest, but they can make last-minute adjustments, Proximate factors are the external conditions that actually induce re- production, Temperature is probably the most important modifier of an- nual gonadal cycles (Box 9-1). The correct habitat, new vegetation or abundant food, ritualized displays of aggression among neighbors. and so cial stimulation in general all help to consummate the final stages of go- nad enlargement and ovarian development. The annual cycle of Pinyon Jays in New Mexico, for example, is closely tied to the availability of the seeds of the pinyon pine, one of their primary foods. Juse the sight of green pine cones is sufficient to trigger gonadal enlargement and timely breeding by these jays (Ligon 1974). Similarly, Red Crossbills in the Rocky Mountains will nest in January and Febru: if conifer seeds. their primary food, are abundant. Tropical nesting seasons last longer than those in the temperate zones. Favorable tropical climates permit nesting for 6 to 10 months, or even in some eases, throughout the year, Although some individual birds can be found breeding in most months in the Tropics, nesting activity for most birds in lowland Costa Rica, for example, reaches a peak at the end of the dry season and early in the rainy season. Kingfishers are an excep- tion, preferring to breed during the dry season when streams run shallow surrounded by snowLocation Latitude (°N)_Jan Apr Aug Dec North Carolina 38 SS South Carolina 31-33 Ss Louisiana 29 ——— Texas 28 po Florida, East Coast 27-28 —$_$— — Pelican island 7 —— Tarpon Key I — = Alafia Banks 27 = Charlotte Harbor 26 ———— Keys 5 — Marco Island 25 a Dry Tortugas. 24 —_— Cuba 2 a US. Virgin islands 19, __ St. Martin ee Puerto Rico 5 Lesser Antilles yr oy ‘Aruba 2 a Venezuela " Trinidad and Tobago 1 Costa Rica 0 FIGURE 9-11 The time and length of the breeding season (line) of the eastern race of the Brown Pelican vary geographically as shown by the date that eggs are laid. The thicker part of the lines indicates the probable presence of eggs. [After Schreiber 1980] and clear, making fish easier to capcure. Hummingbirds, too, nest at the beginning of the dry season when flowers begin to bloom, Nestin ite latitudes usually last from three to four months or less. In the high Arctic, where only a month or so is suitable for breeding, birds must start nesting immediately times they gain a few days head start by reusing old nests. Local populations of a species respond to local conditions. Nesting by Brown Pelicans, for example, is strongly seasonal at norchem sites but is prolonged at tropical sites (Schreiber 198ila). Low water temperatures, which depress food supplies, appear to delay the onset of nesting at all sites. After food availability, the hurricane season is the factor controlling the onset of nesting in these pelicans (this observation holds true for tropical seabirds in general). Pelicans nest iregularly through out the year in the Caribbean 3 » South America, more pre: dictably after the hurricane season during the winter and spring in Florida, and from March to June in Louisiana and the Carolinas (Figure 911). seasons at tempe! alter arrival, and som econd most important id northe Timing of Migration Precise arrival and departure dates are an impressive feature of migration, Every year, after their transequatorial migration, 259 THE ANNUAL CYCLES OF BIRDSMB 0x 9-1 PRECISELY WHEN DO AMERICAN ROBINS NEST? spread and familiar species that must await the arrival of warm spring northern and western (mountain) locations. dict when robins would nest in a particular re- gion. Using dates for the nestling period in 8544 nests on file with the Cornel! Laboratory of Or- nithology’s Nest-Record Card Program, they three days later for each degree of increasing lat: itude and at progressively cooler temperatures 2 spring progressed northward. Combinations of temperature and humidity were the best predictors of the nestling period. Robins typically had nests with young in late April and early May when the relative humidity was about 50 percent and the temperatures were be- tween 45° and 65°F, These environments define either directly or indirectly the environments that allow successful nesting. The robins nested later at localities with higher or lower relative humidi- ties, The model also showed that certain locali- ties where robins do not breed, such as San Diego, California, and £1 Paso, Texas, fall outside the species-defined climate space. arrive at their breeding colonies off southern Australia within a week of the same date. The traditional return of American Cliff Swallows the week of March 19 to the San Juan Capistrano mission in California has become a symbol of the arrival of spring itself. Internal rhythms that are linked to other aspects of the annual cycle guide the timing of migration, Caged migratory passerines predictably be- come restless just before the time at which they would migrate in the wild. This phenomenon—called migratory restlessness. or Zugurinthie—has been familiar to bird fanciers for at least 200) years. Typically. a captive bird wakes shortly after dark and then jumps or flutters in the cage until at least midnight. Because the amount of activity is easily measured, it lends itself to experimental study of both the physiology of migration and orientation behavior. Nonmigratory birds do not exhibit Zuguinuhe be havior. Adrenocortical hormones are known t0 act in concert with pro- lactin in stimulating this behavior in White-crowned Sparrows. More gen- erally, however, our knowledge of the endocrine controls of the many different fieets of migratory behavior of birds is poor (Wingfield et al. 1990). We now know that increasing day length in winter stimulates early spring, restlessness, hyperphagia (eating to excess), fat deposition, and weight increases in many migratory birds, Extending Rowan's findings about the photoperiodic control of the annual eyele Gee page 251), Al- bert Wolfson showed, in another classical study, that Dark-eyed Juncos m migratory populations respond to increasing day length by adding stores. whereas sedentary juncos do not (Wolfson 1942). The spring fat deposition and migratory activity of White-crowned Sparrows are un- 260der the direct control of increasing day length, mediated by an internal clock. The average date of onset of springtime premigratory fat deposits in captive White-crowned Sparrows has been shown to remain virtually constant for a period of eight years (King 1972) The timing of preparations for fall migration is indirectly set by the spring activities. The normal fill sequence of photorefractory testes, pre- basic molt, and preparations for migration in White-crowned Sparrows, for example, depends on prior exposure to long photoperiods, but the pace is proximately influenced by shortening days (Farner and Lewis 1971). Rowan suggested some causal relations between gonadal eycles and gration, but the available evidence now indicates that sex hormones do not directly regulate migration (Wingfield et al. 1990). In one set of pi- oneering experiments, for example. castration did not prevent male Golden-crowned Sparrows from becoming restless and putting on their premigratory fat deposits at the appropriate time of the year (Morton and Mewalde 1962). ‘The timing of migration relates first to internal physiological rhy but extrinsic weather factors also play a role, primarily one of fine tun ing. Northward movements of migrants in the spring correlate with the warming of the higher latitudes, Both the American Robin and the Canada Goose move north in the eastern United States, just behind the main spring thaw, along a front of regions that have a mean daily temperature of 2°C, A line connecting these points is called the 2°C isotherm. Wil- low Warblers in Europe move north with the 9°C. isotherm. Daily weather conditions and favorable winds, in. particular, also in- fluence departure times. In spring, major northward movements in the United States coincide with a depression (lowering of barometric pres- sure) toward the southwest, followed by a strong flow of warm southern winds from the Gulf of Mexico toward the northeast. The sizes of migra- tion waves relate directly to the intensity of the depression and the strength of the favorable winds (Bagg et al. 1954), The value of favorable winds is clearly seen in records of arrivals of northbound migrants at Baton Rouge, Louisiana Gauthreaux 1971). Migrants from Central America usually reach Louisiana in midatternoon afier crossing the Gulf of Mex- ico: but, when they have strong southern tailwinds, they arrive several hours earlier, in the late morning. On rainy days with adverse winds, they arrive later in the evening, and they do not arrive at all on days when there are cold fronts or vast winds, Fall migration departures ako are stimulated by favorable weather con- ditions. Good flights of lirge numbers of raptors at Hawk Mo Pennsylvania, and of land birds ac the tips of peninsulas such as Cape May, New J are the result of strong northwest winds due to a baromet- ric depression moving east from the Great Lakes region, Departures from the New England coast are related to favorable tailwinds (Richardson 1978), and peak flights south across the Giulf of Mexico in early October coincide with improved flight conditions to the north (Buskirk 1980) Exactly how migrants forecast weather conditions is a mystery, but birds are sensitive to changes in barometric pressure and feed more intensely yehins, 261 THE ANNUAL CYCLES ‘OF BIRDS,262 CHAPTER NINE as storms approach and barometers fall. Wind directions alot, however. are not easily judged from the ground. Meteorologists track weather fronts by monitoring infrasound with a special system of microphones. Pigeons. too, seem to be sensitive to inffasound and may use this source of infor~ mation in some wa Scheduling High-Cost Efforts The correspondence beeween breeding season and food availability is cen~ tral in defining the annual energy budgets of birds. Birds can assume the costs of reproduction, molt. or migration only after they have first met the costs of self-maintenance, their highest priority. Basic social interac~ tions to obtain food or a roost site are their second-highest priority. Some seasons, such as a north temperate winter, permit only self=maintenance for most species, whereas others accommodate additional activities. Re- production and molt must be scheduled during the months when a bird's requirements for self-maintenance are lowest or when extra food is avail- able. Usually, the costs of only one extra activity can be accommodated. The energetic costs of reproduction and molt favor the segregation of these stages in the annual eycle Reproduction Peak reproductive activities increase total daily energy expenditures by as much as 50 percent, Daytime activity costs may actually double or even triple, but overnight costs remain relatively constant, At the begin= ning of the breeding season. courtship, territoriality, and nest building demand significant effort. Only minor amounts of productive energy are channeled into the growth of the gonadal tissues themselves, but subse- quent egg Formation and egg laying by females impose new demands on energy and nutrition (see Chapter 14). The large clutches of the big, richly provisioned eggs of waterfowl are especially expensive to produce. They may temporarily double a female’s total daily energy requirement. Large waterfowl, such as the Snow Goose and the Canada Goose, there- » rely on their substantial body stores of nutrients and energy t0 produce their large eggs: smaller ducks must feed to supplement their endogenous reserves (Bluhm 1988). Incubation also can create an energy: shortage because i limits the amount of time during which a bird can forage for its own maintenance. The parents then face another surge of demands on their time and energy when the hatched chicks require food and brooding fore, ¢ Molt Molt is costly effort that typically follows breeding in the warmest months of the year and precedes migration, But a bird strategically adjusts the tim- ing and sometimes the pace of its molt.The complete molt is a major undertaking. The bird sheds and then regenerates thousands of feathers. roughly from 25 to 40 percent of its lean dry mass ((.e., excluding fat and water content). Molt draws signi cantly on protein and nergy reserves to synthesize feather structure and to offset the costs of poorer insulation and flight efficiency. Thomas Ban- croft and Glen Woolfenden (1982) estimated that adult Blue Jays and Florida Scrub Jays must inerease daily metabolism trom 15 to 16 percent during peak periods of feather production. Reduced insulation while molt- ing requires increased heat production, doubling the cost of molt in Brown-headed Cowbirds at low temperatures (Lustick 1970). Molting during the warm summer months can thus be advantageous. Molt is abo a period of intense physiological change (Murphy and King 1992; Box 9-2). Accompanying the replacement of worn feathers is the synthesis of keratin by the skin, increased amino acid metabolism and increased cardiovascular activity t© supply blood to the growi feathers. The long list of changes also includes the shunting of water to 263 THE ANNUAL CYCLES OF BIRDS HB 0x 9-2 MOLT BY WHITE-CROWNED SPARROWS REQUIRES ENERGY ‘Mary Murphy and Jim King AND SPECIAL NUTRITION (1992) deciphered the costs—in both energy and nutrition—of the rapid fall (prebasic) molt in the gambelii subspecies of the White-crowned Spar- row. The complete molt of this sparrow lasts 0 about 54 days, with peak feather production and energy costs from day 18 to day 36 (see illustra- tion). The actual energy costs of molt total 605 kKilojoules to 876 kilojoules, with daily investments that are proportional to the molt intensity. The daily energy costs of peak molt (58 percent of basal metabolic rate) are higher than those asso- ciated with reproduction, Obtaining adequate nutrition for the molt is probably not a major problem for sparrows in the wild, Muscle tissues can be broken down as sparrows fast, they store extra reserves in the liver during the day, feeding selectively on foods containing such amino acids if needed; the stored cysteine is liberated for use at night. | aio needed to provide most of the amino acids required. Keratin synthesis, however, requires disproportionately high proportions of sulfur- containing amino acids, especially cysteine. To have cysteine available in amounts sufficient to continue feather growth overnight when the Molt stage Plumage, sheaths, and other epidermal structures deposited daily in the 54-day prebasic molt period of the White-crowned Sparrow (WCS). Each of the nine molt stages lasts 6 days. [From Murphy and King 1992]264 (CHAPTER NINE the developing feathers, changes in bone metabolism and calcium distri- bution, and an increased need for iron for red blood cell production. To- gether. these and other metabolic changes impose substantial hidden costs beyond the conversion of amino acids into feather proteins. Only about 7 percent of the energy used by molting birds is incorporated into the feathers themselves. Few species breed and molt at the same time. They mostly are species that live in productive, tropical environments with minimal seasonal vari~ ation. There, prolonged molts apparently minimize daily costs in the ab- sence of strong seasonal constraints. From 3 to 4 percent of the African birds examined by Robert Payne (1969) were molting while breeding. From 8 to 10 percent of the Costa Rican birds examined by Mercedes Foster (1975) bore signs of both molt and reproductive activity. Exceptions to the rule are instructive. Some female hombills molt while imprisoned in sealed nest cavities to incubate eggs and brood young. Their energy requirements for self-maintenance are minimal; as a result, the added costs of molt can be accommodated. Additionally. che dight feathers are not essential during this sedentary period. The high emper- atures that build up inside the nest cavity may favor loss of feathers and reduced insulation. In contrast, male hornbills, which feed the incubat- ing females, wait to molt until their families leave the nest. Tropical birds mole more predictably than they breed, because repro- duction may be tied co irregular periods of rain or may require several renesting attempts due co high rates of nest loss to predators, To give 1g Priority. some birds interrupt their molts. Desert birds such as Darwin’s finches of the Galipagos and the Zebra Finch of Australia stop the regular seasonal molt to nest whenever the unpredictable rains begin. ‘They resume the interrupted molt afier nesting is completed. Tropical terns such as the Angel Tern on Christmas Island eum the molt on and off to breed whenever possible (Ashmole 1968; Figure 9-12) This delicate seabird has no pigment in its flight feathers, which conse- quently wear easily and must be replaced more often than those of most other terns. Wave after wave of molt is initiated in the flight feathers. The innermost primaries often begin to molt again before the outermost pri- maries are replaced in the preceding molt. As many as three successive molts may be in progress simultaneously. When an Angel Term starts to nest (it simply lays an egg precariously on a bare branch), the molt stops suddenly, no matter which feathers may be missing—the molting equiv- alent of musical chairs. After the tern has finished nesting. mole resumes as if there had been no interruption in the complicated pattem of feather replacement. Birds adjust the pace of molt in relation to the time available (Box 9-3, pages 266-267). Gulls and sandpipers that breed in the high Arctic, where the reproductive season is short. start molting before they finish breeding to be ready for migration, The Dunlin, for example, begins to molt its primaries just before incubation and then finishes from four to five weeks later, The northernmost (pugetensis) populations of the White~ bree