Environmental regulation of annual schedules in opportunistically-breeding songbirds: Adaptive specializations or variations on a theme of white-crowned sparrow?

General and Comparative Endocrinology 157 (2008) 217–226

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Environmental regulation of annual schedules in opportunistically-breeding songbirds: Adaptive specializations or variations on a theme of white-crowned sparrow? Thomas P. Hahn a,*, Jamie M. Cornelius a, Kendra B. Sewall a, T. Rodd Kelsey a, Michaela Hau b, Nicole Perfito c a b c

Section of Neurobiology, Physiology and Behavior, and Animal Behavior Graduate Group, University of California, Davis, CA 95616, USA Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08540, USA Department of Integrative Biology, University of California, Berkeley, CA 94720, USA

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Article history: Received 14 February 2008 Revised 14 May 2008 Accepted 20 May 2008 Available online 27 May 2008 Keywords: Photoperiod Opportunism Crossbill Zebra finch Darwin’s finch Taeniopygia Loxia Geospiza Photorefractoriness Annual cycles Non-photic cues GnRH

a b s t r a c t How birds use environmental cues to time breeding, migration and molt has been the subject of intensive study for nearly 90 years. Most work has focused on seasonal breeders; opportunistic breeders have been presumed to differ fundamentally from seasonal taxa in ways that facilitate coping with unpredictable environments. Understanding patterns and mechanisms of opportunists’ responses to environmental cues can reveal the extent to which different environments require specialized adaptations of cue response systems. In this review we will present our perspective on how patterns and mechanisms of environmental cue response of three groups of opportunists—zebra finches, crossbills and Darwin’s finches—compare with seasonal breeders. Long-standing predictions regarding tonic activity of the hypothalamic gonadotropin-releasing hormone system have been confirmed in at least some opportunists. However, opportunists resemble seasonal breeders in some surprising ways, illustrating basic similarity among taxa facing very different timing challenges. For instance, many opportunists completely regress the gonads outside breeding times, rely on initial predictive cues (both photic and non-photic) to regulate timing and rate of reproductive development, and in some cases even appear to display internal changes in responsiveness to environmental cues (i.e., cycles of reproductive refractoriness and sensitivity). Although advantages of unrestricted temporal flexibility are intuitively clear for animals coping with unpredictable habitats, the available data on these opportunists indicate that in all but the most extremely capricious situations the advantages of flexibility may be at least partly outweighed by contrasting advantages of following a reliable temporal schedule. Ó 2008 Elsevier Inc. All rights reserved.

1. Introduction It has now been roughly 80 years since the original discovery that the reproductive and migratory physiology of juncos (Junco hyemalis) responds to the seasonal changes in photoperiod (Rowan 1925, 1926). Many studies have since confirmed that this phenomenon is widespread in taxa from virtually all latitudes (e.g., Lofts and Murton, 1968; Dawson et al., 2001). Subsequent studies have also explored the patterns of response to different types of environmental cues and their integration with photoperiod (e.g., Wingfield et al., 1992; Hahn et al., 1997; Dawson and Sharp, 2007), the role of endogenous changes in responsiveness to those cues (Gwinner, 1986; Farner et al., 1983; Nicholls et al., 1988; Dawson and Sharp, 2007), and details of the mechanisms of cue detection and integration to time changes in physiology, morphology and behav-

* Corresponding author. Fax: +1 530 752 8391. E-mail address: [email protected] (T.P. Hahn). 0016-6480/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.ygcen.2008.05.007

ior (Wingfield et al., 1992, 1993; Wingfield and Farner, 1993; Wingfield and Kenagy, 1991). The objective of this review is not to duplicate any of the recent reviews of these topics, but to return to a question that arose not long after Rowan’s original pioneering studies, and that remains only partially answered: Is the annual cycle organization of birds that deal with unpredictable environmental variation—the opportunists—similar to that of seasonal temperate zone species that experience predictable resources and conditions? Information on opportunists, when combined with that from seasonal breeders, permits us to determine whether species in different environments have evolved adaptively specialized environmental cue response patterns and mechanisms that facilitate flexible timing of annual cycle events, or are best viewed simply as ‘‘variations on a theme” of the response patterns and mechanisms of familiar seasonal breeders (Lofts and Murton, 1968; Hahn et al., 1997; Hau et al., 2008; Hahn and MacDougall-Shackleton, 2008; Adkins-Regan, 2008). In this review, we will present a perspective based on our collective field and laboratory studies of three different opportu-

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nists: zebra finches (Taeniopygia guttata), crossbills (Loxia spp.), and Darwin’s finches (Geospiza spp.).

3. Hypotheses and predictions regarding environmental regulation of reproduction in opportunists

2. Environmental challenges, seasonal patterns, and mechanisms of response to environmental cues in opportunists

Seasonal breeders are well known to cycle through stages of being responsive but not yet stimulated by environmental cues (‘‘photosensitive”), stimulated and reproductively active (‘‘photostimulated”), and reproductively refractory to environmental cues (‘‘absolutely refractory”; Fig. 1A; see, e.g., Nicholls et al., 1988; Dawson et al., 2001; Dawson and Sharp, 2007). The general hypothesis regarding opportunists is that they will display characteristics that facilitate rapid onset of reproductive activity at any time primarily in response to short-term cues (e.g., food, social factors, and rainfall), and lack any period of absolute reproductive refractoriness to environmental cues (Fig. 1B and C). Several predictions based on this hypothesis follow.

Most of the early discussion of opportunists and nomads centered on birds living in the arid interior of Australia, where unpredictable rainfall presents the primary environmental timing challenge (Immelmann, 1963, 1971; Serventy, 1971). Rainfall leads to growth of grass and production of seeds required for breeding by granivorous birds, flushes of insects and in some cases flowering of shrubs and trees for insectivorous and nectarivorous species, and the appearance of temporary lakes and ponds used by water birds (Serventy, 1971; Nix, 1976). However, rain in these regions is sporadic. This pattern would seem to preclude birds anticipating when and where to be prepared to breed using long-term initial predictive cues (cf. Wingfield, 1980, 1983). Hence, many species were suspected to begin reproductive activity practically instantly upon the onset of drought-breaking rain so as not to miss infrequent breeding opportunities. Field observations lend support to these suppositions: ‘‘In several pairs of Wood-Swallow, courtship started several minutes after the beginning of the rain. The first copulation occurred about 2 h later. The Zebra Finches, too, started to copulate before the end of the heavy downpour, which lasted about 4 h.” (Immelmann, 1963) Likewise ‘‘. . .this almost instantaneous response in arid areas is not at all unusual. It was a common saying among bird observers in these areas, long before Immelmann published his striking data, that if a cloud passes over the sky Artamus cinereus [black-faced woodswallow] will start picking up nesting sticks!” (Serventy, 1971). Several researchers have been struck by the apparent similarity of the challenges faced by Australian desert birds and crossbills (Loxia spp.). Crossbills reside in climatically seasonal north-temperate conifer forests, where they feed primarily on conifer seeds. Owing to the boom-bust cone production patterns over large spatial scales displayed by many conifers (e.g., Koenig and Knops, 2000), many authors have presumed that crossbills cannot anticipate when they will locate a seed supply sufficient to support nesting any better than zebra finches can anticipate when or where rain will permit nesting. For instance: ‘‘. . .we are impressed by the parallel between the situations facing nomadic desert finches of Australia. . .and crossbills. In each case, the birds move in flocks through vast areas of fairly uniform and generally unproductive habitat, until their wanderings, or the passing of time, bring them to an area suitable for breeding. With the desert birds, rainfall or its immediate consequences serves as the proximate stimulus, and hatching of young is well synchronized with maturation of seeds and build-up of insect populations following the rain. In crossbills, on the other hand, food probably is both the proximate and ultimate factor producing breeding” (Tordoff and Dawson, 1965). Consequently, crossbills have been presumed to be capable of initiating breeding opportunistically whenever and wherever they encounter an abundant seed crop (Newton, 1972). As will become apparent below, we have become skeptical both of the degree to which ‘‘unpredictable” environmental conditions require an ability to initiate nesting immediately at any time, and of the near-mythical temporal flexibility that many authors have conferred on opportunists like zebra finches and crossbills. We will return to these issues below, and begin by summarizing the specific predictions—some stated explicitly in the literature, but some only implicit—regarding opportunists’ expected patterns of response to proximate environmental cues as well as mechanisms underlying these responses (see especially Serventy, 1971, but also Hahn et al., 1997; Dawson et al., 2001; Perfito et al., 2006).

1. Predictions regarding patterns of response to environmental cues Prediction 1.1: Initial predictive cues such as photoperiod or endogenous rhythms should be ignored even if they are present because they provide no useful information about when conditions suitable for successful breeding are likely to occur. Prediction 1.2: Short-term cues, such as food supply itself or rainfall immediately preceding a surge of productivity, will be the primary cues used to time breeding. Prediction 1.3: Extended, continuous breeding will be possible, with no period of reproductive absolute refractoriness to environmental cues (see Hahn et al., 1997; Ball and Hahn, 1997). 2. Predictions regarding regulation of reproductive state Prediction 2.1: Gonads will remain in a near-ready state, eliminating the time required by a ‘‘growth and development” phase of the breeding life cycle stage (see Wingfield, 2008), permitting immediate onset of nesting when good conditions commence. Prediction 2.2: The hypothalamo-pituitary axis will remain in a state of tonic activity as a means of maintaining gonads in a near-ready state (Farner and Serventy, 1960), and facilitating rapid onset of nesting. 3. Prediction regarding sexual maturity Prediction 3.1: Reproductive maturity will be possible at a very young age, facilitating exploitation of continuing favorable conditions by young produced early during a breeding event. A corollary of this is that the juvenile refractory period common in temperatezone seasonal breeders will be absent.

4. Case studies 4.1. Zebra finches 4.1.1. Temporal patterns of reproduction, and responses to environmental conditions Zebra finches have long been viewed as the archetypal opportunists (see Serventy, 1971; Zann, 1996), allegedly capable of initiating nesting activity literally within hours of the onset of droughtbreaking rain. However, the most comprehensive analysis of the relationship between environmental conditions (rainfall, temperature, time of year) and zebra finch breeding in the wild casts some doubt on this long-standing belief. During a 7-year study at Alice

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Fig. 1. Schematic comparisons of hypothesized cue response patterns and neuroendocrine (GnRH system) correlates in strictly seasonal species (A), seasonally opportunistic species (B), and purely opportunistic species (C). (A) Individuals cycle repeatedly through stages of responsiveness, stimulation, and refractoriness. During responsiveness, the brain (GnRH system) is ready to respond but gonads remain small because cues are not yet stimulatory and GnRH, LH, and FSH secretion are all low. When cues (especially photoperiod) become stimulatory, hypothalamo-pituitary activity increases and gonads enlarge. The transition to a reproductively refractory state then occurs spontaneously, with no further environmental input (e.g., declining stimulation through reduced photoperiod, temperature, etc.) required. GnRH secretion and eventually production cease, and the gonads collapse. The transition back to a responsive state then also occurs spontaneously, although in some cases exposure to short days is required. (B) Individuals would also cycle through responsive but not stimulated, stimulated, and ‘‘refractory” states, but refractoriness would only be relative, and the transition to refractoriness would require declining environmental stimulation rather than occurring spontaneously, as in (A). Further, the GnRH system is never down-regulated. Under this scenario, persistence or re-acquisition of reproductive competence should be possible but much less likely during the refractory period than at other times of year. Crossbills and possibly Darwin’s finches may fit this model. In (C), the default state is to remain reproductively competent, and only when a variety of external environmental cues cease to be stimulatory—and possibly only when some, such as water availability, become actively inhibitory—would any decline in reproductive competence occur. Only peripheral reproductive physiology would be down-regulated; the GnRH system would remain tonically active. Zebra finches, and possibly Darwin’s finches, are proposed to fit this model.

Springs (Zann et al., 1995), zebra finches did breed when rain fell, and the response was greater the more rain fell. Strikingly, however, the effect of rainfall on nesting was not immediate, as suggested by Immelmann (1963), but followed a lag time of 2 months in summer or 3 months in winter. Zann and colleagues (1995) used historical rainfall records and their empirically-derived rainfall-nesting relationship to show that what Immelmann observed was almost certainly a continuation of breeding activity following several months of repeated breeding (Zann et al., 1995,

see also Hahn et al., 1997). This revised interpretation of Immelmann’s observations is appealing because new grass seed used by zebra finches for breeding would not be available soon enough for pairs that start nesting immediately when drought-breaking rain falls (see Zann et al., 1995). Zann’s interpretation also would account for other observations that even three weeks after drought-breaking rain fell, ‘‘most species” showed ‘‘some degree of enlargement” of the gonads (Serventy, 1971; see Keast, 1959; Serventy and Marshall, 1957), rather than universal full gonadal

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development, as would be expected if the opportunistic response was immediate. Zann and colleagues’ findings suggest that either zebra finches do not remain constantly near-ready to initiate breeding as previously supposed, or that under certain circumstances they delay the response to rainfall even if they could respond more quickly. Consistent with either of these possibilities are studies by Davies (1977), Frith and Tilt (1959), Kikkawa (1980), and Zann and Straw (1984), which reveal little or no zebra finch breeding during late autumn and/or early winter—when photoperiod and ambient temperature are at annual minima—even if rainfall occurs or if irrigation maintains lush vegetation and high food availability (see Hahn et al., 1997, for review; Fig. 2). In fact, zebra finches nest predominantly seasonally in many parts of their range, and even in the arid interior around Alice Springs there is a pronounced peak of nesting in October (spring) and dearth in autumn (April; Zann et al., 1995; Zann, 1996; see also Hahn et al., 1997; Fig. 2). 4.1.2. Gonad cycles and neuroendocrine mechanisms As might be expected from an opportunistic breeder, free-living zebra finches sampled in an arid and climatically unpredictable area around Alice Springs did not collapse the gonads even during periods of non-breeding (Perfito et al., 2007). This finding is consistent with the idea that these birds maintain increased readiness to initiate breeding in relatively unpredictable areas despite failing to respond to drought-breaking rain with immediate onset of nesting (Zann et al., 1995, see above). By contrast, finches from a relatively mesic and climatically predictable location in southern Australia (Numurkah) displayed pronounced seasonal cycles of gonadal regression and development (Perfito et al., 2007). These data document great variability among pop-

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ulations in the regulation of gonadal development, but at the same time document that certain populations of zebra finches can regress their gonads. It is likely that the population differences reflect plastic responses to environmental conditions, and not evolutionary changes in gonadal regulation, though this still needs to be tested. Consistent with the above, environmental cues can affect gonadal state in captive zebra finches. Eleven weeks of water restriction led captive zebra finches that were initially in breeding condition to reduce testis length and circulating luteinizing hormone (LH) levels significantly (Perfito et al., 2006; see also Vleck and Priedkalns, 1985). Notably, this treatment had no detectable effect on the reproductive neuroendocrine system: number or size of cGnRH-I immunoreactive cells in the preoptic area and septum were not affected by the treatment despite the changes in peripheral reproductive function (gonad size and hormone concentrations). Interestingly, the reduction in testis size in laboratory birds also did not coincide with significant reduction in spermatogenic activity (though there was a trend for fewer birds’ testes to be fully spermatogenic during water restriction than in controls). Together, these findings are consistent with the long-standing prediction that opportunists should maintain the hypothalamo-pituitary component of the reproductive axis in a state of tonic readiness to respond to environmental cues, so as to facilitate a rapid response to favorable conditions should they be encountered (Farner and Serventy, 1960; Farner, 1967; Perfito et al., 2006). However, under certain environmental conditions peripheral reproductive activity can be suppressed/reduced (see Fig. 1C). It is noteworthy that zebra finches maintain at least partial spermatogenic activity in mostly-regressed gonads and display very modest overall changes in gonad size from non-breeding to

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Fig. 2. Schematic diagrams of natural reproductive schedules of crossbills, Darwin’s finches and zebra finches. More southerly zebra finch populations that occupy relatively temperate and seasonal environments are presented separately from those in the arid interior, where rainfall patterns are extremely erratic.

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8 7 Testis Length (mm)

breeding condition in the wild (roughly from 4 to 20 mg; Perfito et al., 2007). In contrast, in north-temperate-zone seasonal breeders such as emberizine sparrows, non-breeding testes collapse to the point of only the earliest stages of the spermatogenic sequence (Marshall, 1961), and wintering adult males have testes similar in size to those of the non-breeding zebra finches but they increase to 250–500 mg in breeding birds (e.g., Wingfield and Farner, 1978; Wingfield, 1985). Although maximal testis size probably depends more on mating system and sperm competition than on reproductive schedule (see Birkhead and Moller, 1992), breeding with relatively small gonads would also help minimize time delay to full reproductive competence (see Perfito et al., 2006, 2007; Priedkalns et al., 1984).

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4.2. Crossbills 4.2.1. Temporal patterns of reproduction Crossbills (Loxia spp.) are highly specialized morphologically and behaviorally to feed on seeds of conifers (Newton, 1972; Benkman, 1992, 1993; Adkisson, 1996). Many conifers are boom-bust seed producers over very large spatial scales (e.g., Fowells, 1965; Koenig and Knops, 2000). Consequently, most crossbill populations tend to be nomadic (Newton, 1972; Benkman, 1992; Adkisson, 1996). Further, despite living in climatically seasonal north-temperate environments, crossbills are widely reputed to breed in any month of the year (e.g., Brehm, 1924; Griscom, 1937; Bailey et al., 1953; Jewett et al., 1953; Tordoff and Dawson, 1965; Newton, 1972; Burleigh, 1972; Berthold and Gwinner, 1978; Benkman, 1990; Cramp and Perrins, 1994). Food supply itself is supposed to be the primary or even sole proximate cue because of the presumed unpredictability of when crossbills may happen to wander into a region with abundant seeds (e.g, Griscom, 1937; Tordoff and Dawson, 1965; Newton, 1972). The references to crossbill flexibility are sometimes colorful: ‘‘Those who would fondly believe that the ‘‘riddle of migration” has been largely explained by the effects of increased exposure to light and heat on the secretion of the sex hormones will find the crossbill a tough nut to crack!” (Griscom, 1937). New data and careful examination of the literature both suggest that reports of year-round breeding by crossbills are largely a myth. There is an autumn hiatus in nesting activity and in physiological reproductive condition that appears to be universal in both Eurasia and North America (Fig. 2 and 3; see also Berthold and Gwinner, 1978; Hahn, 1998). This contradicts the implication that crossbills will breed continuously as long as seed supplies remain high. We are reviewing this conflict in detail elsewhere, but briefly, the references generally held up as providing the best evidence of continuous breeding for many months beginning in summer (e.g., Newton’s reference to Formasov, 1960, and to unpublished data for Scotland), either do not support this interpretation at all (e.g., Formasov, 1960 does not describe nesting in October or November at all in northern Russia) or are equivocal owing to imprecision regarding timing of nesting when only fledglings were observed (Newton, 1972). November nesting in the Pyrenees (Clouet, 2000) probably represents early onset of ‘‘winter” nesting when no summer breeding (which delays molt) has occurred, and does not disprove a general autumn breeding hiatus. 4.2.2. Responses to environmental cues, and neuroendocrine mechanisms Crossbills respond strongly both to long-term (e.g., photoperiod) cues and to short-term non-photic cues (Hahn, 1995, 1998; Hahn et al., 1995, 1997). Gonadal development to full breeding condition can occur in winter, and is most rapid if birds are mated, even if food supply is unlimited, suggesting a strong role of social

Fig. 3. Seasonal changes in testis length estimated by laparotomy in free-living adult male red crossbills. Box and Whisker plots show range (statistical outliers excluded), first and third quartiles, and overall median. Trend lines connect means with standard errors shown. Diamonds show means (horizontal line) and 95% confidence limits. Sample sizes for each 2-month bin are shown above each plot. Individual data points also shown, but multiple estimates overlap, so the total number of data points visible is fewer than the total sample size. Data for all time intervals were collected during multiple years between 1987 and 2007, at multiple locations in Washington, Oregon, California and Wyoming. Testis lengths above about 4 mm are likely to be spermatogenic (Tordoff and Dawson, 1965).

factors in addition to food (Hahn et al., 1995). Further, preferred foods (sunflower seeds and seed-filled cones) can accelerate winter reproductive development (Hahn et al., 2005). In the absence of strong social or food stimulation, increased photoperiod induces rapid gonadotropin secretion and development of the gonads to near-breeding size (Hahn, 1995). Completion of gonadal development follows if preferred food (sunflower seeds) is subsequently provided ad libitum (Hahn, 1995). These observations can explain the flexible development of breeding condition in winter, apparently contingent on local food and social conditions (see Fig. 3 and note variability of gonadal condition during winter and spring), as well as seasonal acquisition of near-competent gonads by early summer even if birds have not yet located a suitable place to settle and nest (Hahn, 1998). Termination of reproductive competence in late summer/early autumn occurs without any decline in food supply (Hahn, 1995, 1998), and yet male crossbills do not become absolutely photorefractory by either standard criterion (see Hahn and MacDougall-Shackleton, 2008; Hahn, 1995; Hahn et al., 2004; MacDougall-Shackleton et al., 2006). However, when held on a natural seasonal photocycle they collapse the gonads and begin to molt by early autumn (Hahn, 1995; MacDougall-Shackleton et al., 2001, 2006; see also Deviche, 2000; Deviche and Sharp, 2001). Thus, gonadal development begins on short days of winter, but reverses on relatively long days before the autumn equinox in September (Hahn, 1995). These data are consistent with crossbills becoming reproductively relatively refractory to the stimulatory effects of long days. Relative refractoriness reduces, but does not eliminate, the reproductive response to normallystimulatory cues (see Hamner, 1968; Robinson and Follett, 1982; Nicholls et al., 1988; Hahn et al., 1997; Dawson et al., 2001; Dawson and Sharp, 2007). The result is reduced probability of initiating or maintaining reproductive competence at some times of year. Relative refractoriness is a logical mechanism for maintaining a fundamentally seasonal reproductive cycle without strictly prohibiting breeding at some times, the way absolute refractoriness does (Hahn et al., 1997; Ball and Hahn, 1997; Hahn and MacDougall-Shackleton, 2008). Though different in details, this phenomenon resembles the graded effects of photoperiodic history on seasonal breeding, as well as on onset of puberty, in some rodents (see Gorman and Zucker, 1997; Park et al., 2006; Butler et al., 2007).

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The neuroendocrine correlates of changing reproductive competence of crossbills are consistent with predictions for opportunists, as for zebra finches. White-winged crossbills allowed to regress their gonads on declining photoperiod in captivity, and those held for an extended period on constant long days (20L:4D), maintain immunoreactivity of the hypothalamic GnRH system, unlike other temperate-zone songbirds (MacDougallShackleton et al., 2001, 2005; Pereyra et al., 2005; see also Dawson et al., 2001; Dawson and Sharp, 2007). This is similar to the neuroendocrine condition of relatively refractory Japanese quail (Foster et al., 1988; Follett and Pearce-Kelly, 1990). 4.3. Darwin’s finches Darwin’s ground finches (Geospiza spp.) from the arid, equatorial Galapagos Islands are mainly granivorous, but they rely on insects for breeding (although Cactus finches, Geospiza scandens, can begin breeding foraging on cactus pollen alone; Grant, 1996). Ground finches typically breed between December and May during the semi-seasonal rains (Grant and Boag, 1980; Boag and Grant, 1984; Grant et al., 2000). These rains can lead to rapid (within about 10 days) flushes of insect availability (Grant and Grant, 1989). Large inter-annual variation in the amount and duration of rainfall evidently favors retention of pronounced temporal reproductive flexibility in these birds. Frequent ENSO (El Nino–Southern Oscillation) events bring exceptional rainfall, beginning early and continuing longer than usual, spectacularly prolonging reproductive activity in these birds, from December through August, and involving as many as 10 consecutive clutches by individual females (Gibbs and Grant, 1987; Grant et al., 2000; see Hahn et al., 1997 for review). Despite the fact that clutch initiations had not been observed in Darwin’s finches during September, October, or most of November (Fig. 2), the possibility remained open that the opportunistic capabilities of these birds may be based on maintenance of near-readiness to initiate reproductive activity immediately upon exposure to rain, vis a vis the tonic HPG-axis activity hypothesis (Farner and Serventy, 1960; Farner, 1967). It turns out, however, that populations of small ground finches (Geospiza fuliginosa) undergo complete collapse of the gonads during nonbreeding periods, similar in magnitude to many temperate-zone seasonal breeders (Hau et al., 2004; other species of Darwin’s finch show similar patterns, Hau, Gwinner and Gwinner, unpublished data). It remains possible that these birds maintain central (i.e., GnRH system) activity, retaining releasable stores of GnRH that would facilitate a rapid activation of the pituitary–gonad axis when conditions favorable for nesting commence. However, the magnitude of the change in gonadal state suggest that even if this was true, the time lag before breeding could occur would be on the order of weeks, not the hours to days reported historically for other opportunists such as zebra finches (discussed above). These fascinating data on small ground finches provide further evidence that even species with pronounced opportunistic capabilities nevertheless collapse the reproductive system during times of reduced probability of breeding, probably to conserve energy (Hau et al., 2004).

5. A revised view of opportunists How do the current data on zebra finches, crossbills and Darwin’s finches affect how we should be thinking about the environmental regulation of reproductive patterns opportunists? At this point it is fruitful to revisit the predictions summarized at the beginning of this review, and discuss them in light of current data.

5.1. Prediction 1.1 Initial predictive cues clearly do affect at least some opportunists. This is particularly clear for crossbills, which grow their gonads in response to increased photoperiod (Tordoff and Dawson, 1965; Hahn, 1995) even if food intake is not allowed to increase (Hahn, 1995). Although zebra finches have also been shown to display some response to photoperiod (e.g., Bentley et al., 2000), recent evidence on the Lesser Sundas subspecies of Zebra finch (Taeniopygia g. guttata) suggests that food or social factors may actually mediate this effect (Perfito et al., 2008). Thus, whether zebra finches respond directly to the specific initial predictive cue of photoperiod remains doubtful. However, zebra finches might be making use of drought-breaking rainfall as an initial predictive cue regulating the early stages of reproductive development leading up to the subsequent onset of nesting (although this still needs to be tested directly). The temporal scale on which drought-breaking rain influences the timing of onset of zebra finch reproduction (i.e., with a 2- to 3-month lag) is very similar to the time scale on which increasing photoperiod affects gonadal development in seasonal breeders (e.g., Farner and Wilson, 1957; Farner and Lewis, 1971; Farner and Wingfield, 1980). Still, the fact that zebra finches show only low-amplitude gonad cycles both in terms of size and gametogenic activity (see below) indicates that they may not always require initial predictive cues to the same degree as typical temperate-zone seasonal breeders. Whether Darwin’s finches make use of any initial predictive information, either in the form of an anticipatory endogenouslycontrolled change or through responsiveness to external environmental cues, remains unclear. Reproductive activation in small ground finch populations matched seasonal rainfall patterns but not annual variations in photoperiod or temperature, indicating that these birds do not time breeding according to initial predictive cues (Hau et al., 2004). Furthermore, finches studied in 1 year about 2 weeks before the onset of the rainy season did not have enlarged gonads, suggesting that they have no means to predict the coming rainy season. Finally, reproductive activation occurred in different months in two study years, making endogenous seasonal control mechanisms unlikely (Hau et al., 2004). However, laboratory experiments in constant conditions would be needed to rule out a seasonal susceptibility to environmental cues. Some pairs of Geospiza scandens do initiate nesting in advance of actual rainfall during normal, seasonal breeding years, but this could result from a direct response to the seasonal increase in cactus pollen that forms part of these cactus finches’ diet (Grant, 1996; see also Grant and Grant, 1989; Boag and Grant, 1984; Millington and Grant, 1984). In any case, whatever stimuli the birds use to time recrudescence of the gonads must be acting in a way more similar to the effects of photoperiod initiating gonadal development in seasonal breeders than to the instantaneous stimulation of nesting in birds with already-functional gonads supposed by Immelmann (1963) for zebra finches. 5.2. Prediction 1.2 Short-term cues are critical environmental cues for opportunists. Continuing rainfall once a breeding event has begun for zebra finches, or the discovery (or persistence) of cones with abundant seeds for crossbills, undoubtedly affect the timing of nesting dramatically in these opportunists. However it appears likely that social interactions are at least permissive and possibly even more potent direct stimulators of reproductive physiology, rather than the external environmental cues (rain and food) themselves (Hahn et al., 1995; Perfito et al., 2007, 2008). Further, something (relative reproductive refractoriness?) at least attenuates crossbills’ response to these types of cues in autumn, leading to the autumn

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reproductive hiatus, even if these non-photic cues remain favorable. If winter gonadal recrudescence in crossbills is primarily food-dependent, food is acting more like an initial predictive cue stimulating the early stages of reproductive development, just as drought-breaking rainfall may do in some populations of zebra finches. Likewise, in small ground finches, factors associated with rainfall probably provide direct proximate information to stimulate gonad growth, although the collapse of small ground finch gonads often precedes any decline in rainfall or deterioration of vegetation conditions (Hau et al., 2004; but see Grant et al., 2000). Given that all of these species collapse the gonads completely when not breeding (with the exception of zebra finches from the most unpredictable areas), requiring substantial ramping-up of reproductive physiology before onset of nesting can occur, it seems appropriate to think of these non-photic cues—which are often equated with ‘‘short term” cues in direct contrast to photoperiod—as operating at first as initial predictive cues. They may later continue to act as supplementary cues (cf. Wingfield, 1980, 1983) affecting onset of actual nesting, as well. In this context it is critical to keep in mind the important distinctions made by Wingfield (2008) regarding how environmental cues can regulate transitions among annual life history states. The dogma regarding the effects of rain (zebra finches and Darwin’s finches) and conifer seeds (crossbills) being ‘‘supplementary” (i.e., short term) cues (cf. Wingfield, 1980, 1983) presumes that these birds would already have been at or near the point of full reproductive competence at the time these cues have their proximate effects, precipitating at most only the final stages of reproductive development, and possibly only regulating onset of nesting in individuals already in full reproductive condition. We are suggesting that all of these opportunists in fact do use environmental cues to regulate the development phase of the reproductive life history stage (cf. Wingfield, 2008), and that these initial predictive cues may be photic, non-photic, or both.

temperature, declining body condition). In zebra finches it appears likely to reflect an integrated response to multiple external cues, such as low environmental temperature combined with short days and reduced tendency of grasses to produce seeds in response to rain (see Zann et al., 1995), rather than a longer term endogenous decline in responsiveness to environmental stimuli (Fig. 1C). Despite regular termination of breeding activity in September through most of November in at least some Darwin’s finch species (see Hahn et al., 1997 for review; Fig. 2), Darwin’s finches probably are not reproductively refractory at this time. Small ground finches kept in outdoor aviaries at the Charles Darwin Research Station on St. Cruz Island in September and October grew their gonads within about two weeks of unseasonal rainfall, the increase in gonad sizes actually being indistinguishable in birds either kept on a mediocre or on a nutritionally enriched diet (Hau, Schmidl, Gwinner, unpublished data). Further, ground finch gonads are already large, with birds beginning to nest, by November in some instances (Hau et al., 2004). This casts doubt on the hypothesis suggested by Hahn and colleagues (1997) that the general lack of breeding from September through early November in these birds has some basis in an internal relative refractory period (see also Grant et al., 2000). It is worth exploring experimentally the possibilities that the birds simply become exhausted following prolonged breeding (cf. Grant and Grant, 1989), leading to reduced responsiveness to favorable conditions, or that increases in population density inhibit reproductive responses to other cues (see Grant et al., 2000). Such direct inhibitory proximate inputs may be important even if endogenous changes in responsiveness to environmental stimuli also are present. The fact that Darwin’s finches live precisely on the equator seems to make it likely that there would be a strong endogenous component to any cycle of responsiveness that does exist, even if the amplitude of the change in responsiveness to cues was small.

5.3. Prediction 1.3

The idea that gonads will remain in a ready or near-ready state to facilitate rapid onset of breeding when conditions improve can be rejected for all but the zebra finches living in the most unpredictable interior regions of Australia. Crossbills completely collapse the gonads on an annual basis (Fig. 3), and zebra finches living in a climatically seasonal section of their range collapse their gonads outside the breeding season (Perfito et al., 2007). Zebra finches around Alice Springs, in the arid interior, only partially shrink the gonads when not breeding, and males retain significant spermatogenesis even in these partially regressed gonads. It appears likely that under conditions of extreme prolonged drought the gonads of these birds would collapse further (see Keast and Marshall, 1954; see Fig. 1C). However given that conditions permitting nesting by these granivores would take 2–3 months to develop once drought-breaking rainfall occurred (see Zann et al., 1995), this does not seem like it would be problematic for these birds. It should be noted that the situation could be different for insectivores, like woodswallows, or for aquatic birds such as ducks, and this issue warrants further study (Nix,1976). Given the spectacular opportunistic abilities of Darwin’s finches exposed to periods of extended rain during ENSO events, it is striking that they also completely collapse the gonads outside breeding periods (Hau et al., 2004). It seems worth noting here that one profound difference between zebra finches and Darwin’s finches is movement patterns. The Darwin’s finches are tightly constrained to simply tolerate whatever conditions exist during the dry season, whereas the zebra finches can move widely and therefore may not be exposed to such strictly poor conditions. Overall, for these three species, it appears that only the populations of zebra finches living in the most unpredictable areas come close to conforming to the hypothesis that the gonads should be maintained continuously ready.

Continuous breeding will be possible. The evidence clearly indicates that crossbills and zebra finches lack absolute reproductive refractoriness to environmental cues. Neither crossbills nor zebra finches held on constant long days regress their gonads spontaneously (Sossinka, 1974; Hahn, 1995, unpublished). This distinguishes these two taxa from almost every other songbird studied to date (Hahn and MacDougall-Shackleton, 2008). This trait means that the birds would always await direct proximate input of deterioration in external or internal conditions (declining photoperiod, dropping temperatures, declining food supply, decline in body reserves) before collapsing the gonads, and very probably represents an adaptive specialization to facilitate a flexible reproductive schedule (Hahn and MacDougall-Shackleton, 2008). On the other hand, there are parts of the year when crossbills (mid autumn) and zebra finches (very late autumn and early winter in relatively seasonal environments; see Fig. 2) are much less likely to breed (see Hahn et al., 1997 for review). Crossbills (Fig. 3; Hahn, 1998; Cornelius et al., unpublished) and at least some populations of zebra finches (Perfito et al., 2007) collapse the gonads during this period. This suggests that something is inhibiting the activity of the reproductive axis at this time, even if some environmental cues (e.g., conifer seeds and rainfall) are favorable. But is this inhibitory effect mechanistically similar in these two groups? In crossbills, it appears likely that some form of relative reproductive refractoriness to environmental cues is involved, as has been observed in some other birds (e.g., Robinson and Follett, 1982; Sharp, 1993; see also Small et al., 2007; see Fig. 1B), although this does not mean that they may not also be integrating several other potentially inhibitory factors (i.e., reduced time to forage as days shorten, declining

5.4. Prediction 2.1

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5.5. Prediction 2.2 The tonic activity of the neuroendocrine systems of both zebra finches and crossbills is unique among songbirds studied to date. Gonadal regression induced by water restriction in zebra finches, or gonadal collapse under declining daylength in autumn in crossbills did not lead to a decline in hypothalamic GnRH (Perfito et al., 2006; MacDougall-Shackleton et al., 2001). In this respect, zebra finches and crossbills do appear to be adaptively specialized for flexible breeding schedules, since a tonically active GnRH system, combined with a lack of absolute reproductive refractoriness (see above), should facilitate flexible reproductive timing (Farner, 1967; Farner and Serventy, 1960; Hahn et al., 1997; MacDougallShackleton et al., 2005; Dawson and Sharp, 2007; Hahn and MacDougall-Shackleton, 2008).

ductive competence, underlain by internal changes in responsiveness to cues rather than simply by a direct proximate response to declining conditions. Under this scenario, the birds can afford to devote themselves more strictly to self-maintenance processes such as molt and perhaps improvement of body condition even though doing so comes at the cost of a missed current reproductive opportunity. Individuals that take a brief breeding hiatus in autumn would maximize chances for long-term survival and then more than compensate in terms of lifetime reproductive success by exploiting what may be reliable, rather than sporadic, opportunities to resume breeding in winter and spring. The existence of a period of relative refractoriness in crossbills (Fig. 1B) makes sense in this light.

6. Conclusions 5.6. Prediction 3.1 All three of the focal groups we discuss here seem to conform to the predictions for opportunists regarding development of young birds. Although none of these species has been experimentally tested specifically for a juvenile refractory period, all evidence suggests that this is absent, and the young birds can achieve reproductive maturity and breed at very young ages. Zebra finches can be breeding by the time they are about 60 days of age (Zann, 1996), crossbills regularly acquire full reproductive competence in the same calendar year as they were born (e.g., McCabe and McCabe, 1933; Hahn and Cornelius, unpublished data), and Darwin’s finches born near the beginning of an ENSO event can themselves be nesting before the end at about 3 months of age (Gibbs and Grant, 1987; Gibbs et al., 1984). 5.7. Synthesis These opportunists appear both to resemble and differ from regular seasonal breeders in significant ways. It appears that zebra finches and perhaps Darwin’s finches conform more broadly to expectations for opportunists than do crossbills, though both warrant further study. This could stem in part from the fact that crossbills occupy such climatically seasonal temperate-zone habitats. In such habitats, timely production of a fresh, high-quality plumage will be particularly important for survival through the thermally challenging days of late autumn and winter (Benkman, 1990). It appears that although crossbills and zebra finches both overlap molt far more extensively than is typical of most temperate-zone species, crossbills compress molt into a seasonal time window much more than do zebra finches (Cornelius, unpublished; Perfito, unpublished; Zann 1985). Consequently, retention of ancestral traits, such as some form of a refractory period facilitating a seasonal molt that does not completely overlap with breeding competence, will likely be favored more strongly in the most climatically seasonal environments. It is also worth considering the possibility that most crossbill populations may not actually be strongly selected for complete temporal flexibility at all. Nomadic forms of crossbills appear to be extremely good at locating newly developing bumper crops of cones in early summer, and finding such a cone crop may virtually assure a high-quality food source that is adequate not only for survival but for both summer and winter/spring breeding over the subsequent 9 months without any further search. If this is true, then the view presented above (cf. Tordoff and Dawson, 1965) of flocks wandering through largely unproductive habitat until they happen upon an occasional and transient bonanza may be misleading. If the norm for crossbills is instead that large proportions of populations find and occupy high-quality habitat the vast majority of the time, then selection may favor an autumn hiatus in repro-

We suggest in closing that the focal opportunists discussed here may not all be alike. We confess to being unsure whether zebra finches experience an environment that is any more unpredictable than either Darwin’s finches or crossbills. Zebra finch mobility could at least minimize their exposure to the worst conditions, or even keep them primarily in locations with favorable conditions. Better data on their movements are needed. Nevertheless, the data summarized above suggest that they may in fact be qualitatively more flexible than are crossbills (cf. Fig. 1B and C), and this seems an appropriate adaptive response to selection imposed by unpredictably timed reproductive opportunities that may be few and far between. Although they may not need to be able to nest instantly, they certainly appear able to initiate appropriate preparations for subsequent breeding in a timely fashion whenever cues predicting favorable conditions occur. They probably lack any form of refractoriness, and the periods when reproductive responses to rainfall appear reduced (e.g., Davies, 1977; Frith and Tilt, 1959) most likely are the consequence of an integrated response to a suite of mostly inhibitory external cues that directly attenuate a response to stimulatory rainfall. In contrast, selection on crossbills probably has not favored complete abandonment of photoperiodism and the concomitant refractory period, because there may be no advantage—and there could even be significant disadvantages—to unlimited temporal flexibility in their case (Fig. 1B). Rather, selection appears to have favored a fundamentally seasonal annual cycle in crossbills with two main modifications: (1) replacement of the absolute refractory period with relative refractoriness, which favors flexible prolongation of summer breeding when cones are abundant, and (2) relaxation of a long-day requirement for breeding after the autumn breeding hiatus is over. Together, these modifications of the basic seasonal breeder pattern lead to such a flexible reproductive schedule that many researchers have understandably concluded that it represented essentially infinite flexibility, or pure opportunism (see Hahn et al., 1995). The biology of Darwin’s finches differs fundamentally from both crossbills and zebra finches in one critical way: lack of mobility. Owing to their confinement to small, arid, extremely isolated islands, they have no opportunity to reduce their exposure to poor conditions by moving from one rich patch to another (the ‘‘Rich Patch Fugitive” approach, see Ford et al., 1993) the way both crossbills and zebra finches may. They must submit to periods of adverse conditions, and must consequently be capable of exploiting favorable local conditions maximally whenever they arise. Indeed, lifetime reproductive success of individual Darwin’s finches can be dictated largely by how successfully they exploit the prolonged favorable conditions of an ENSO event (Gibbs and Grant, 1987). It is, therefore, all the more surprising that they still display complete gonadal regression when not breeding, contrary to expectation for an opportunist. It seems likely that the harsh, arid environment

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and mortality selection during the dry season (exaggerated during prolonged droughts) has selected for complete gonadal regression as an energy-saving mechanism (Hau et al., 2004). Based on current data it is not possible to tell whether Darwin’s finches possess any kind of relative refractory period (e.g., Fig. 1B) or not (Fig. 1C), but our suspicion is that they do not, and therefore more closely resemble zebra finches than they do crossbills. The fact that all three of these extremely flexible groups of birds nevertheless at least sometimes display characteristics that seem far more suited to strict seasonal breeders (e.g., collapse of the gonads outside breeding, and fundamentally seasonal reproductive schedules in many areas) emphasizes just how strong and all-pervasive the selective advantage must be for animals to make use of any long-term predictive information that may be available for helping time major life cycle events such as breeding. The advantages of unrestricted temporal flexibility are intuitively clear for animals coping with unpredictable habitats, but the patterns that have emerged for zebra finches, crossbills and Darwin’s finches suggest that in all but the most extremely capricious situations the advantages of flexibility may be at least partly outweighed by contrasting advantages of following a reliable temporal schedule. Acknowledgments We are deeply indebted to John Wingfield for his seminal work in the field of ecological endocrinology, and also for his superb mentorship during various parts of our careers. M.H. is indebted to Ebo and Helga Gwinner, Martin Wikelski, and many field assistants for their help with the Darwin’s finch project. Logistical support was provided by the Charles-Darwin-Station; funding was provided by the Max-Planck Society. N.P. wishes to thank Richard Zann for his gracious collaboration, many field assistants for their hard work, and the Center for Arid Zone Research for logistical support on the zebra finch project. T.P.H. thanks John Wingfield for his support and guidance during the early stages of his work on crossbills, and the National Science Foundation for financial support during some parts of data collection and preparation of this manuscript. J.M. Cornelius, K.B. Sewall, and T.R. Kelsey acknowledge support from the Animal Behavior Graduate Group, UC Davis, while formulating the ideas presented here. References Adkins-Regan, E., 2008. Do hormonal control mechanisms produce evolutionary inertia? Philos. Trans. Roy. Soc. B 363, 1599–1609. Adkisson, C.G., 1996. Red crossbill (Loxia curvirostra). In: Poole, A., Gill, F. (Eds.), The Birds of North America, vol. 256. Academy of Natural Sciences, Philadelphia. and American Ornithologists’ Union, Washington, DC. Bailey, A.M., Niedrach, R.J., Bailey, A.L., 1953. The Red Crossbills of Colorado. Denver Museum of Natural History, Museum Pictorial No. 9. Ball, G.F., Hahn, T.P., 1997. GnRH neuronal systems in birds and their relation to the control of seasonal reproduction. In: Parhar, I.S., Sakuma, Y. (Eds.), GnRH Neurons: Gene to Behavior. Brain Shuppan Publications, Tokyo, pp. 325–342. Benkman, C.W., 1990. Foraging rates and the timing of crossbill reproduction. Auk 107, 376–386. Benkman, C.W., 1992. White-winged crossbill (Loxia leucoptera). In: Poole, A., Stettenheim, P., Gill, F. (Eds.), The Birds of North America, vol. 27. Academy of Natural Sciences, Philadelphia. and American Ornithologists’ Union, Washington, DC.. Benkman, C.W., 1993. Adaptation to single resources and the evolution of crossbill (Loxia) diversity. Ecol. Monogr. 65, 305–325. Bentley, G.E., Spar, B.D., MacDougall-Shackleton, S.A., Hahn, T.P., Ball, G.F., 2000. Photoperiodic regulation of the reproductive axis in male zebra finches, Taeniopygia guttata. Gen. Comp. Endocrinol. 117, 449–455. Berthold, P., Gwinner, E., 1978. Jahresperiodik der Gonadengroesse beim Fichtenkreuzschnabel (Loxia curvirostra). J. Ornithol. 119, 338–339. Birkhead, T.R., Moller, A.P., 1992. Sperm Competition in Birds: Evolutionary Causes and Consequences. Academic Press, London, San Diego. Boag, P.T., Grant, P.R., 1984. Darwin’s finches (Geospiza) on Isla Daphne Major, Galapagos: breeding and feeding ecology in a climatically variable environment. Ecol. Monogr. 54, 463–489.

225

Brehm, A.E., 1924. Brehms Tierleben, vol. 4. C.W. Neumann, Leipzig. Burleigh, T.D., 1972. Birds of Idaho. Claxton Printers, Caldwell, Idaho. Butler, M.P., Trumbull, J.J., Turner, K.W., Zucker, I., 2007. Timing of puberty and synchronization of seasonal rhythms by simulated natural photoperiods in female Siberian hamsters. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R413–R420. Clouet, M., 2000. The breeding biology of the common crossbill Loxia curvirostra in the central Pyrenees. Bird Study 47, 186–194. Cramp, S., Perrins, C.M., 1994. Handbook of the Birds of Europe and the Middle East and North Africa: The Birds of the Western Palearctic. Volume VIII. Crows to Finches. Oxford University Press, Oxford, New York. Davies, S.J.J.F., 1977. The timing of breeding by the zebra finch Taeniopygia castanotis at Mileura, western Australia. Ibis 119, 369–372. Dawson, A., Sharp, P.J., 2007. Photorefractoriness in birds—photoperiodic and nonphotoperiodic control. Gen. Comp. Endocrinol. 153, 378–384. Dawson, A., King, V.M., Bentley, G.E., Ball, G.F., 2001. Photoperiodic control of seasonality in birds. J. Biol. Rhythms 16, 366–381. Deviche, P., 2000. Timing, pattern and extent of first prebasic molt of white-winged crossbills in Alaska. J. Field Ornithol. 71, 217–226. Deviche, P., Sharp, P.J., 2001. Reproductive endocrinology of a free-living, opportunistically breeding passerine (white-winged crossbill, Loxia leucoptera). Gen. Comp. Endocrinol. 123, 268–279. Farner, D.S., 1967. The control of avian reproductive cycles. In: Proceedings of the 14th Int. Ornithol. Congr. Blackwell, Oxford. Farner, D.S., Lewis, R.A., 1971. Photoperiodism and reproductive cycles in birds. Photophysiology 6, 325–370. Farner, D.S., Serventy, D.L., 1960. The timing of reproduction in birds in the arid regions of Australia. Anat. Rec. 137, 354. Farner, D.S., Wilson, A.C., 1957. A quantitative examination of testicular growth in the white-crowned sparrow. Biol. Bull. 113, 254–267. Farner, D.S., Wingfield, J.C., 1980. Reproductive endocrinology of birds. Ann. Rev. Physiol. 42, 457–472. Farner, D.S., Donham, R.S., Matt, K.S., Mattocks, Jr., P.W., Moore, M.C., Wingfield, J.C., 1983. The nature of photorefractoriness. In: Mikami, S.I., Homma, K., Wada, M. (Eds.), Avian Endocrinology: Environmental and Ecological Perspectives. Japan Scientific Society Press/Springer-Verlag, Tokyo/Berlin, pp. 149–166. Follett, B.K., Pearce-Kelly, A., 1990. Photoperiodic control of the termination of reproduction in Japanese quail (Coturnix coturnix japonica). Proc. Roy. Soc. Lond. B 242, 225–230. Ford, H., Davis, W.E., Debus, S., Ley, A., Recher, H., Williams, B., 1993. Foraging and aggressive behaviour of the regent honeyeater Xanthomyza phrygia in northern New South Wales. Emu 93, 277–281. Formasov, A.N., 1960. La production de graines dans les forets de conifers de la taiga de l’U.R.S.S. et l’envahisement de l’Europe occidentale par certaines especes d’oiseaux. In: Proc. 12th Int. Ornithol. Congr. 1958, pp. 216–229. Foster, R.G., Panzica, G.C., Parry, D.M., Viglietti-Panzica, C., 1988. Immunocytochemical studies on the LHRH system of the Japanese quail: influence by photoperiod and aspects of sexual differentiation. Cell Tissue Res. 253, 327–335. Fowells, H.A., 1965. Silvics of Forest Trees in the United States. USDA, Forest Service, Washington, DC. Frith, H.J., Tilt, R.A., 1959. Breeding of the zebra finch in the Murrumbridgee irrigation area, New South Wales. Emu 59, 289–295. Gibbs, H.L., Grant, P.R., 1987. Ecological consequences of an exceptionally strong El Nino event on Darwin’s finches. Ecology 68, 1735–1746. Gibbs, H.L., Grant, P.R., Weiland, J., 1984. Breeding of Darwin’s finches at an unusually early age in an El Nino year. Auk 101, 872–874. Gorman, M.R., Zucker, I., 1997. Environmental induction of photononresponsiveness in the Siberian hamster, Phodopus sungorus. American Journal of Physiology– Regulatory, Integrative and Comparative Physiology 272, R887–R895. Grant, B.R., 1996. Pollen digestion by Darwin’s finches and its importance for early breeding. Ecology 77, 489–499. Grant, B.R., Grant, P.R., 1989. Evolutionary Dynamics of a Natural Population. University of Chicago Press, Chicago. Grant, P.R., Boag, P.T., 1980. Rainfall on the Galapagos and the demography of Darwin’s finches. Auk 97, 227–244. Grant, P.R., Grant, B.R., Keller, L.F., Petren, K., 2000. Effects of El Nino events on Darwin’s finch productivity. Ecology 81, 2442–2457. Griscom, L., 1937. A monographic study of the red crossbill. Proc. Boston Soc. Nat. Hist. 41, 77–210. Gwinner, E., 1986. Circannual Rhythms: Endogenous Clocks in the Organization of Seasonal Processes. Springer-Verlag, Berlin. Hahn, T.P., 1995. Integration of photoperiodic and food cues to time changes in reproductive physiology by an opportunistic breeder, the red crossbill, Loxia curvirostra (Aves: Carduelinae). J. Exp. Zool. 272, 213–226. Hahn, T.P., 1998. Reproductive seasonality in an opportunistic breeder, the Red Crossbill, Loxia curvirostra. Ecology 79, 2365–2375. Hahn, T.P., MacDougall-Shackleton, S.A., 2008. Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response systems of birds. Philos. Trans. Roy. Soc. B 363, 267–286. Hahn, T.P., Boswell, T., Wingfield, J.C., Ball, G.F., 1997. Temporal flexibility in avian reproduction. In: Nolan, V., Ketterson, E.D., Thompson, C.F. (Eds.), Current Ornithology. Plenum Press, New York, London, pp. 39–80. Hahn, T.P., Pereyra, M.E., Katti, M., Ward, G.M., MacDougall-Shackleton, S.A., 2005. Effects of food availability on the reproductive system. In: Dawson, A., Sharp, P.J. (Eds.), Functional Avian Endocrinology. Narosa Publishing House, New Delhi, India, pp. 167–180.

226

T.P. Hahn et al. / General and Comparative Endocrinology 157 (2008) 217–226

Hahn, T.P., Pereyra, M.E., Sharbaugh, S.M., Bentley, G.E., 2004. Physiological responses to photoperiod in three cardueline finch species. Gen. Comp. Endocrinol. 137, 99–108. Hahn, T.P., Wingfield, J.C., Mullen, R., Deviche, P.J., 1995. Endocrine bases of spatial and temporal opportunism in arctic-breeding birds. Am. Zool. 35, 259–273. Hamner, W.M., 1968. The photorefractory period of the house finch. Ecology 49, 211–227. Hau, M., Perfito, N., Moore, I.T., 2008. Timing of breeding in tropical birds: mechanisms and evolutionary implications. Ornithol. Neotrop. 19 (Suppl.), 39– 59. Hau, M., Wikelski, M., Gwinner, H., Gwinner, E., 2004. Timing of reproduction in a Darwin’s finch: temporal opportunism under spatial constraints. Oikos 106, 489–500. Immelmann, K., 1963. Drought adaptations in Australian desert birds. In: Proc. 13th Int. Ornithol. Congr. 1962, pp. 649–657. Immelmann, K., 1971. Ecological aspects of periodic reproduction. In: Farner, D.S., King, J.R. (Eds.), Avian Biology I. Academic Press Inc., N.Y, pp. 341–389. Jewett, S.G., Taylor, W.P., Shaw, W.T., Aldrich, J.W., 1953. Birds of Washington State. University of Washington Press, Seattle. Keast, J.A., 1959. Australian birds: their zoogeography and adaptations to an arid continent. In: Keast, A., Crocker, R.L., Christian, C.S. (Eds.), Biogeography and Ecology in Australia. Junk Publications, The Hague, pp. 89–114. Keast, J.A., Marshall, A.J., 1954. The influence of drought and rainfall on reproduction in Australian desert birds. Proc. Zool. Soc. Lond. 124, 493–499. Kikkawa, J., 1980. Seasonality of nesting by zebra finches at Armidale, NSW. Emu 80, 13–20. Koenig, W.D., Knops, J.M.H., 2000. Patterns of annual seed production by northern hemisphere trees: A global perspective. Am. Nat. 155, 59–69. Lofts, B., Murton, R.K., 1968. Photoperiodic and physiological adaptations regulating avian breeding cycles and their ecological significance. J. Zool. (Lond.) 155, 327– 394. Marshall, A.J., 1961. Breeding seasons and migration. In: Marshall, A.J. (Ed.), Biology and Comparative Physiology of Birds. Academic Press, New York, pp. 307–339. MacDougall-Shackleton, S.A., Deviche, P.J., Crain, R.D., Ball, G.F., Hahn, T.P., 2001. Seasonal changes in brain GnRH immunoreactivity and song-control nuclei volumes in an opportunistically breeding songbird. Brain Behav. Evol. 58, 38– 48. MacDougall-Shackleton, S.A., Katti, M., Hahn, T.P., 2006. Tests of absolute refractoriness in four species of cardueline finch that differ in reproductive schedule. J. Exp. Biol. 209, 3786–3794. MacDougall-Shackleton, S.A., Pereyra, M.E., Hahn, T.P., 2005. GnRH, photorefractoriness, and breeding schedules of cardueline finches. In: Dawson, A., Sharp, P.J. (Eds.), Functional Avian Endocrinology. Narosa Publishing House, New Delhi, India, pp. 97–110. McCabe, T.T., McCabe, E.B., 1933. Notes on the anatomy and breeding habits of crossbills. Condor 35, 136–147. Millington, S.J., Grant, P.R., 1984. The breeding ecology of the cactus finch (Geospiza scandens) on the Isla Daphne Major, Galapagos. Ardea 72, 177–188. Newton, I., 1972. Finches. Collins, Glasgow. Nicholls, T.J., Goldsmith, A.R., Dawson, A., 1988. Photorefractoriness in birds and comparison with mammals. Physiol. Rev. 68, 133–176. Nix, H.A. 1976. Environmental Control of Breeding, Post-Breeding Dispersal and Migration of Birds in the Australian Region. In: Proc. XVI Int. Ornithol. Cong., Australian Academy of Sciences, Canberra, pp. 272–305. Park, J.H., Kauffman, A.S., Paul, M.J., Butler, M.P., Beery, A.K., Constantini, R.M., Zucker, I., 2006. J. Biol. Rhythms 21, 373–383. Pereyra, M.E., Sharbaugh, S.M., Hahn, T.P., 2005. Interspecific variation in photoinduced GnRH plasticity among nomadic cardueline finches. Brain Behav. Evol. 66, 35–49. Perfito, N., Bentley, G.E., Hau, M., 2006. Tonic activation of brain GnRH immunoreactivity despite reduction of peripheral reproductive parameters in opportunistically breeding zebra finches. Brain Behav. Evol. 67, 123–134.

Perfito, N., Kwong, J.M.Y., Bentley, G.E., Hau, M., 2008. Cue hierarchies and testicular development: is food a more potent stimulus than day length in an opportunistic breeder (Taeniopygia g. guttata)? Horm. Behav. 53, 567–572. Perfito, N., Zann, R., Bentley, G.E., Hau, M., 2007. Opportunism at work: habitat predictability affects reproductive strategy in free-living zebra finches. Funct. Ecol. 21, 291–301. Priedkalns, J., Oksche, A., Vleck, C., Bennett, B.K., 1984. The response of the hypothalamo-gonadal system to environmental factors in the Zebra Finch, Poephila guttata castanotis. Cell Tissue Res. 238, 23–25. Robinson, J.E., Follett, B.K., 1982. Photoperiodism in Japanese quail: the termination of seasonal breeding by photorefractoriness. Proc. Roy. Soc. Lond. B 215, 95–116. Rowan, W., 1925. Relation of light to bird migration and developmental changes. Nature 115, 494–495. Rowan, W., 1926. On photoperiodism, reproductive periodicity, and the annual migrations of birds and certain fishes. Proc. Boston Soc. Nat. Hist. 38, 147–189. Serventy, D.L., 1971. Biology of desert birds. In: Farner, D.S., King, J.L. (Eds.), Avian Biology 1. Academic Press, New York, pp. 287–339. Serventy, D.L., Marshall, A.J., 1957. Breeding periodicity in western Australian birds: with and account of unseasonal nestings in 1953 and 1955. Emu 57, 99–126. Sharp, P.J., 1993. Photoperiodic control of reproduction in the domestic hen. Poultry Sci. 72, 897–905. Small, T.W., Sharp, P.J., Deviche, P., 2007. Environmental regulation of the reproductive system in a flexibly breeding Sonoran Desert bird, the rufouswinged sparrow, Aimophila carpalis. Horm. Behav. 51, 483–495. Sossinka, R., 1974. Der Einfluss von Durstperioden auf die Schilddruessen- und Gonadenaktivitat und ihre Bedeutung fur die Brutperiodik des Zebrafinken (Taeniopygia castanotis Gould). J. Ornithol. 115, 128–141. Tordoff, H.B., Dawson, W.R., 1965. The influence of daylength on reproductive timing in the red crossbill. Condor 67, 416–422. Vleck, C.M., Priedkalns, J., 1985. Reproduction in zebra finches–hormone levels and effect of dehydration. Condor 87, 37–46. Wingfield, J.C., 1980. Fine temporal adjustments of reproductive functions. In: Epple, A., Stetson, M.H. (Eds.), Avian Endocrinology. Academic Press Inc., NY, pp. 367–389. Wingfield, J.C., 1983. Environmental and endocrine control of avian reproduction: an ecological approach. In: Mikami, S., Homma, K., Wada, M. (Eds.), Avian Endocrinology. Japan Sci. Soc./Springer-Verlag, Tokyo/Berlin, pp. 265–288. Wingfield, J.C., 1985. Influences of weather on reproductive function in male Song sparrows, Melospiza melodia. J. Zool. (Lond.) 205, 525–544. Wingfield, J.C., 2008. Organization of vertebrate annual cycles: implications for control mechanisms. Phil. Trans. Roy. Soc. B 363, 425–441. Wingfield, J.C., Farner, D.S., 1978. The endocrinology of a naturally-breeding population of the White-crowned sparrow, Zonotrichia leucophrys pugetensis. Physiol. Zool. 51, 188–205. Wingfield, J.C., Farner, D.S., 1993. Endocrinology of reproduction in wild species. Avian Biol. 9, 163–327. Wingfield, J.C., Kenagy, G.J., 1991. Natural control of reproduction. In: Pang, P.K.T., Schreibman, M.P. (Eds.), Handbook of Comparative Endocrinology, vol. 4. Academic Press, New York, pp. 181–241. Wingfield, J.C., Hahn, T.P., Levin, R., Honey, P., 1992. Environmental predictability and control of gonadal cycles in birds. J. Exp. Zool. 261, 214–231. Wingfield, J.C., Hahn, T.P., Doak, D., 1993. Integration of environmental factors regulating transitions of physiological state, morphology and behaviour. In: Sharp, P. (Ed.), Avian Endocrinology. Journal of Endocrinology Ltd.,, Bristol, UK, pp. 111–122. Zann, R.A., 1985. Slow continuous wing-moult of zebra finches Poephila guttata from southeast Australia. Ibis 127, 184–196. Zann, R.A., 1996. The Zebra Finch: A Synthesis of Field and Laboratory Studies. Oxford University Press, Oxford. Zann, R.A., Straw, B., 1984. Feeding ecology and breeding of zebra finches in farmland in northern Victoria. Austral. Wildlife Res. 11, 533–552. Zann, R.A., Morton, S.R., Jones, K.R., Burley, N.T., 1995. The timing of breeding by zebra finches in relation to rainfall in central Australia. Emu 95, 208–222.