Flexibility in annual cycles of birds: implications for endocrine control mechanisms

Life cycles of birds and other vertebrates are composed of series of life history stages each with unique combinations of morphological, physiological and behavioral characteristics. For example, in the white-crowned sparrow, Zonotrichia leucophrys, the nonbreeding stage (winter), vernal migration, breeding, moult and autumn migration stages occur in a fixed and repeated sequence where each cycle is 1 year. The sequence of stages cannot be reversed. Transition from one life history stage to the next and the duration of each stage are dependent upon a combination of genetic factors and environmental cues. The latter include the annual change in photoperiod and the former may involve endogenous circannual rhythms. All vertebrates also express the emergency life history stage in response to perturbations of the environment that allow individuals to cope with the unpredictable. Each stage has a unique repertoire of sub-stages (physiological and behavioral, and to a lesser extent morphological), which can be expressed in any sequence or combination to give the state of the individual at any point in its life cycle. This state is presumably maximally adapted to the environmental conditions at that time. Although the sequence of life history stages appears to be innate, the rate of transition from stage to stage, and the expression of sub-stages can be modified by the local environmental factors and, particularly, by social cues. These environmental cues acting on the phenotype result in neuroendocrine and endocrine secretions that regulate development of the life history stage, its onset once mature capability has been attained, and then terminate it at the appropriate times. The environmental cues (from the physical and social environment) impart a strong experiential component. Because, there is a set number of life history stages and their sub-stages, there is a finite number of states that can be expressed in response to the environmental variation experienced by the individual. The more life history stages a phenotype expresses, the less flexibility is there in the overall timing of these stages owing to the time taken to develop one stage and terminate the last (about 1 month). However, many phenotypes have increased flexibility in their life cycles by overlapping some life history stages (i.e., with overlapping mature capability of two or perhaps even more stages). Another potential strategy is to dissociate some components of a life history stage so they are expressed at other times of year thus spreading out potential costs associated with that life history stage. Examples of both overlap and dissociation of life history stages are given including implications for hormonal control mechanisms.     

The impacts of climate change on the annual cycles of birds

Organisms living today are descended from ancestors that experienced considerable climate change in the past. However, they are currently presented with many new, man-made challenges, including rapid climate change. Migration and reproduction of many avian species are controlled by endogenous mechanisms that have been under intense selection over time to ensure that arrival to and departure from breeding grounds is synchronized with moderate temperatures, peak food availability and availability of nesting sites. The timing of egg laying is determined, usually by both endogenous clocks and local factors, so that food availability is near optimal for raising young. Climate change is causing mismatches in food supplies, snow cover and other factors that could severely impact successful migration and reproduction of avian populations unless they are able to adjust to new conditions. Resident (non-migratory) birds also face challenges if precipitation and/or temperature patterns vary in ways that result in mismatches of food and breeding. Predictions that many existing climates will disappear and novel climates will appear in the future suggest that communities will be dramatically restructured by extinctions and changes in range distributions. Species that persist into future climates may be able to do so in part owing to the genetic heritage passed down from ancestors who survived climate changes in the past.     

Adaptations to migration in birds: behavioural strategies, morphology and scaling effects

The annual life cycle of many birds includes breeding, moult and migration. All these processes are time and energy consuming and the extent of investment in any one may compromise the others. The output from breeding is of course the ultimate goal for all birds, while the investment in moult and migration should be selected so that lifetime fitness is maximized. In particular, long-distance migrants breeding at high latitudes face severe time pressures, which is a probable reason why natural selection has evolved efficient behaviours, physiological and morphological adaptations allowing the maximum possible migration speed. Optimal migration theory commonly assumes time minimization as an overall strategy, but the minimization of energy cost and predation risk may also be involved. Based on these assumptions, it is possible to derive adaptive behaviours such as when and at which fuel load a stopover site should be abandoned. I review some core components of optimal migration theory together with some key predictions. A review of accumulated empirical tests of the departure rule indicates that time minimization is an important component of the overall migration strategy, and hence gives support to the assumption about time-selected migration. I also briefly discuss how the optimal policy may be implemented by the bird by applying a set of simple rules. The time constraints on migrants increase with increasing body size. Some consequences of this are discussed.     

Travelling on a budget: predictions and ecological evidence for bottlenecks in the annual cycle of long-distance migrants

Long-distance migration, and the study of the migrants who undertake these journeys, has fascinated generations of biologists. However, many aspects of the annual cycles of these migrants remain a mystery as do many of the driving forces behind the evolution and maintenance of the migrations themselves. In this article we discuss nutritional, energetic, temporal and disease-risk bottlenecks in the annual cycle of long-distance migrants, taking a sandpiper, the red knot Calidris canutus, as a focal species. Red knots have six recognized subspecies each with different migratory routes, well-known patterns of connectivity and contrasting annual cycles. The diversity of red knot annual cycles allows us to discuss the existence and the effects of bottlenecks in a comparative framework. We examine the evidence for bottlenecks focusing on the quality of breeding plumage and the timing of moult as indicators in the six subspecies. In terms of breeding plumage coloration, quality and timing of prealternate body moult (from non-breeding into breeding plumage), the longest migrating knot subspecies, Calidris canutus rogersi and Calidris canutus rufa, show the greatest impact of bottlenecking. The same is true in terms of prebasic body moult (from breeding into non-breeding plumage) which in case of both C. c. rogersi and C. c. rufa overlaps with southward migration and may even commence in the breeding grounds. To close our discussion of bottlenecks in long-distance migrants, we make predictions about how migrants might be impacted via physiological 'trade-offs' throughout the annual cycle, using investment in immune function as an example. We also predict how bottlenecks may affect the distribution of mortality throughout the annual cycle. We hope that this framework will be applicable to other species and types of migrants, thus expanding the comparative database for the future evaluation of seasonal selection pressures and the evolution of annual cycles in long-distance migrants. Furthermore, we hope that this synthesis of recent advancements in the knowledge of red knot annual cycles will prove useful in the ongoing attempts to model annual cycles in migratory birds.     

The reproductive tactics of dace in central Siberia: evidence for temperature regulation of the spatio-temporal variability of its life history

Major life history characteristics of dace Leuciscus leuciscus from the R. Yenisei at Mirnoye (66° N, Central Siberia, Russia) were determined in June 1993 and were compared with those available throughout the distribution range of the species. Differences between populations located 25° further south and 8000 km away are smaller than those described for other freshwater fishes, whose distributions fall within that of dace. For all the populations, the growth rates ( K ) are inversely correlated with latitude but these rates for the actual growing season are faster in northern dace. The latitudinal (spatial) variations in the growth rates resemble the temporal variation described for the R. Frome (U.K.). Also, the variations in fecundity between populations are comparable to the temporal variations reported for this British river. Fecundity of the Yenisei dace was correlated with female length [log F=– 3–6284+4–0424 x log L ] but these females spawned lower numbers of eggs than other populations; and the size of their eggs, like those of the Siberian Ust'Ilim dace, did not vary with female length. We hypothesize that a similar spatio-temporal response to low water temperature, coupled with limitations of energy for reproduction, may result in a constant egg size in Siberian dace. The effects of other selective forces cannot, however, be excluded.     

Evolution of life-history timing in a leafmining moth: Phenotypic selection in patches with manipulated development time

Phyllonorycter mespilella (Hübner) is a leafmining moth with two stages of larval development: the initial sap-feeding (SF) stage followed by the tissue-feeding (TF) stage. Phenotypic selection by parasitoids on the duration of the SF stage (SF duration) was measured in artificial patches of larvae placed in the field during the diapausing generation. Pretreatment of larvae with different photoperiods allowed creation of patches that varied in the time-course of appearance of TF larvae. The shorter the photoperiod pretreatment, the sooner TF larvae tended to appear. Some patches were left exposed and others were caged to exclude parasitoids. Positive directional selection on SF duration was detected in exposed patches, and no selection was detected in caged patches. Directional selection in exposed patches was caused by both parasitoid oviposition and other unidentified sources of mortality. The other sources of mortality may have included host feeding by parasitoids on TF larvae. A larger proportion of parasitoid eggs were oviposited on TF larvae in patches where TF larvae appeared the earliest, but this variation in parasitoid oviposition did not result in significant differences in directional selection intensity among patches with early, intermediate and late appearance of TF larvae. Although the general form of the fitness function was very similar when compared among patch types, no significant directional selection could be detected in patches where TF larvae appeared late, and the causes of directional selection appeared to vary between patches where TF larvae appeared at early and intermediate dates.     

Phenological variation in annual timing of hibernation and breeding in nearby populations of Arctic ground squirrels

Ecologists need an empirical understanding of physiological and behavioural adjustments that animals can make in response to seasonal and long-term variations in environmental conditions. Because many species experience trade-offs between timing and duration of one seasonal event versus another and because interacting species may also shift phenologies at different rates, it is possible that, in aggregate, phenological shifts could result in mismatches that disrupt ecological communities. We investigated the timing of seasonal events over 14 years in two Arctic ground squirrel populations living 20 km apart in Northern Alaska. At Atigun River, snow melt occurred 27 days earlier and snow cover began 17 days later than at Toolik Lake. This spatial differential was reflected in significant variation in the timing of most seasonal events in ground squirrels living at the two sites. Although reproductive males ended seasonal torpor on the same date at both sites, Atigun males emerged from hibernation 9 days earlier and entered hibernation 5 days later than Toolik males. Atigun females emerged and bred 13 days earlier and entered hibernation 9 days earlier than those at Toolik. We propose that this variation in phenology over a small spatial scale is likely generated by plasticity of physiological mechanisms that may also provide individuals the ability to respond to variation in environmental conditions over time.     

The cost of floral longevity in Clarkia tembloriensis: An experimental investigation

The hypothesis that flower maintenance requires resources that would be used to support other plant functions (i.e. a cost of floral maintenance) was tested by experimentally manipulating floral longevity. Plants of Clarkia tembloriensis, a species with pollination-induced flower senescence, received either early or late pollinations (long and short longevities, respectively). We examined the effect of this manipulation on (1) per-flower allocation to nectar production and (2) flower, fruit and seed production per plant under two levels of resource availability. The direct costs of floral longevity measured in terms of nectar sugar were high: flowers that were maintained 35% longer invested proportionately more in nectar sugar (30%). At the whole-plant level, a cost of floral longevity was manifested as reduced seed production, but the magnitude of this cost varied with resource level. While plants with longer-lived flowers showed a 12% reduction in seed production, those that experienced reduced resource levels via partial defoliation, showed a decrement in seed production that was almost three times larger (34%). These differences were not brought about by changes in the number of flowers and fruits, but by significant alterations in their sizes. A model that expresses the cost of flower maintenance as a trade-off between floral longevity and seed production shows that an optimal flower longevity is determined by both the rate of fitness accrual and the cost of floral maintenance.     

Reversed plumage ontogeny in a female hummingbird: implications for the evolution of iridescent colours and sexual dichromatism

In polygynous birds, bright plumage is typically more extensive in the sexually competitive males and develops at or after sexual maturity. These patterns, coupled with the importance of male plumage in sexual displays, fostered the traditional hypothesis that bright plumages and sexual dichromatism develop through the actions of sexual selection on males. This view remains problematic for hummingbirds, all of which are polygynous, because their bright iridescent plumages are also important non-sexual signals associated with dominance at floral nectar sources. Here I show that female amethyst-throated sunangels [ Heliangelus amethysticollis (d'Orbigny & Lafresnaye)], moult from an immature plumage with an iridescent gorget to an adult plumage with a non-iridescent gorget. This 'reversed' ontogeny contradicts the notion that iridescent plumage has a sexual function because sexual selection in polygynous birds should be lowest among non-reproductive immature females. Moreover, loss of iridescent plumage in adult females indicates that adult sexual dichromatism in H. amethysticollis is due in large part to changes in female ontogeny. I suggest that both the ontogeny and sexual dichromatism evolved in response to competition for nectar.