Alexander Scheuerlein

Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs?

The activation of an immune response is beneficial for organisms but may also have costs that affect fitness. Documented immune costs include those associated with acquisition of special nutrients, as well as immunopathology or autoimmunity. Here, we test whether an experimental induction of the immune system with a non–pathological stimulant can elevate energy turnover in passerine birds. We injected phytohaemagglutinin (PHA), a commonly used mitogen that activates the cell–mediated immune response, into the wing web of house sparrows, Passer domesticus. We then examined energetic costs resulting from this immune activity and related those costs to other physiological activities. We found that PHA injection significantly elevated resting metabolic rate (RMR) of challenged sparrows relative to saline controls. We calculated the total cost of this immune activity to be ca. 4.20 kJ per day (29% RMR), which is equivalent to the cost of production of half of an egg (8.23 kJ egg−1) in this species. We suggest that immune activity in wild passerines increases energy expenditure, which in turn may influence important life–history characteristics such as clutch size, timing of breeding or the scheduling of moult.

Diversity of ageing across the tree of life

Evolution drives, and is driven by, demography. A genotype moulds its phenotype’s age patterns of mortality and fertility in an environment; these two patterns in turn determine the genotype’s fitness in that environment. Hence, to understand the evolution of ageing, age patterns of mortality and reproduction need to be compared for species across the tree of life. However, few studies have done so and only for a limited range of taxa. Here we contrast standardized patterns over age for 11 mammals, 12 other vertebrates, 10 invertebrates, 12 vascular plants and a green alga. Although it has been predicted that evolution should inevitably lead to increasing mortality and declining fertility with age after maturity, there is great variation among these species, including increasing, constant, decreasing, humped and bowed trajectories for both long- and short-lived species. This diversity challenges theoreticians to develop broader perspectives on the evolution of ageing and empiricists to study the demography of more species.

Predators as stressors? Physiological and reproductive consequences of predation risk in tropical stonechats (Saxicola torquata axillaris)

Tropical birds usually lay smaller clutches and are less likely to initiate a second brood than their temperate–zone relatives. This reduction in annual fecundity is generally explained as an adaptation either to higher rates of nest predation or to a more limited food supply concurrent with higher adult survival in the tropics. However, the physiological parameters associated with lower annual fecundity in tropical birds have not been well investigated. We compared the annual fecundity, behaviour and a number of physiological parameters of stonechat parents feeding fledged juveniles in territories with and without fiscal shrikes, a predator on adult and fledged birds. Stonechat pairs in territories with shrikes were less likely to initiate a second brood and delayed successive broods compared to pairs in territories without shrikes. After fledging of their young, males showed a greater propensity than females to initiate distraction calls after a human intrusion into their territory and, therefore, invested more in the defence of their young. In territories with shrikes stonechat males had higher initial plasma corticosterone levels and lower body conditions than males in territories without shrikes, suggesting that they were chronically stressed. In contrast, the females from both types of territory had low initial plasma corticosterone levels. We conclude that shrike presence might account for the delay in initiation of a second brood and the reduction in the tendency to initiate a second brood. Whether these effects are mediated by the elevated levels of corticosterone remains to be demonstrated.

Deterioration, death and the evolution of reproductive restraint in late life

Explaining why organisms schedule reproduction over their lifetimes in the various ways that they do is an enduring challenge in biology. An influential theoretical prediction states that organisms should increasingly invest in reproduction as they approach the end of their life. An apparent mismatch of empirical data with this prediction has been attributed to age-related constraints on the ability to reproduce. Here we present a general framework for the evolution of age-related reproductive trajectories. Instead of characterizing an organism by its age, we characterize it by its physiological condition. We develop a common currency that if maximized at each time guarantees the whole life history is optimal. This currency integrates reproduction, mortality and changes in condition. We predict that under broad conditions it will be optimal for organisms to invest less in reproduction as they age, thus challenging traditional interpretations of age-related traits and renewing debate about the extent to which observed life histories are shaped by constraint versus adaptation. Our analysis gives a striking illustration of the differences between an age-based and a condition-based approach to life-history theory. It also provides a unified account of not only standard life-history models but of related models involving the allocation of limited resources.

The COMPADRE Plant Matrix Database: an open online repository for plant demography.

Summary 1. Schedules of survival, growth and reproduction are key life-history traits. Data on how these traits vary among species and populations are fundamental to our understanding of the ecological conditions that have shaped plant evolution. Because these demographic schedules determine population

Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control

Endogenous circannual clocks are found in many long-lived organisms, but are best studied in mammal and bird species. Circannual clocks are synchronized with the environment by changes in photoperiod, light intensity and possibly temperature and seasonal rainfall patterns. Annual timing mechanisms are presumed to have important ultimate functions in seasonally regulating reproduction, moult, hibernation, migration, body weight and fat deposition/stores. Birds that live in habitats where environmental cues such as photoperiod are poor predictors of seasons (e.g. equatorial residents, migrants to equatorial/tropical latitudes) rely more on their endogenous clocks than birds living in environments that show a tight correlation between photoperiod and seasonal events. Such population-specific/interspecific variation in reliance on endogenous clocks may indicate that annual timing mechanisms are adaptive. However, despite the apparent adaptive importance of circannual clocks, (i) what specific adaptive value they have in the wild and (ii) how they function are still largely untested. Whereas circadian clocks are hypothesized to be generated by molecular feedback loops, it has been suggested that circannual clocks are either based upon (i) a de-multiplication (‘counting’) of circadian days, (ii) a sequence of interdependent physiological states, or (iii) one or more endogenous oscillators, similar to circadian rhythms. We tested the de-multiplication of days (i) versus endogenous regulation hypotheses (ii) and (iii) in captive male and female house sparrows (Passer domesticus). We assessed the period of reproductive (testicular and follicular) cycles in four groups of birds kept either under photoperiods of LD 12 L : 12 D (period length: 24 h), 13.5 L : 13.5 D (27 h), 10.5 L : 10.5 D (23 h) or 12 D : 8 L : 3 D : 1 L (24-h skeleton photoperiod), respectively, for 15 months. Contrary to predictions from the de-multiplication hypothesis, individuals experiencing 27-h days did not differ (i.e. did not have longer) annual reproductive rhythms than individuals from the 21- or 24-h day groups. However, in line with predictions from endogenous regulation, birds in the skeleton group had significantly longer circannual period lengths than all other groups. Birds exposed to skeleton photoperiods experienced fewer light hours per year than all other groups (3285 versus 4380) and had a lower daily energy expenditure, as tested during one point of the annual cycle using respirometry. Although our results are tantalizing, they are still preliminary as birds were only studied over a period of 15 months. Nevertheless, the present data fail to support a ‘counting of circadian days’ and instead support hypotheses proposing whole-organism processes as the mechanistic basis for circannual rhythms. We propose a novel energy turnover hypothesis which predicts a dependence of the speed of the circannual clock on the overall energy expenditure of an organism.

Is Food Availability a Circannual Zeitgeber in Tropical Birds? A Field Experiment on Stonechats in Tropical Africa

Equatorial stonechats (Saxicola torquata axillaris) in Africa are seasonal breeders like their temperate-zone conspecifics (S.t. rubicola). Their annual cycle in gonadal size and function is controlled by an endogenous circannual rhythmicity that has been shown to run for up to 10 years in a constant equatorial photoperiod under laboratory conditions, with a period deviating from 12 months. In nature, however, this rhythm is synchronized with the actual year. Because photoperiod is essentially constant at the equator, it is likely that other environmental factors act as zeitgebers. The authors test whether food availability affects reproductive cycles of free-living East African stonechats. The authors offered supplemental food to the birds 2 months before the regular onset of the breeding season. Supplementally fed males started to sing and display earlier than males of control pairs that did not receive extra food. Although the supplemented food advanced the onset of the breeding season in the pairs that were fed, the onset of the postnuptial molt following the breeding season was not correspondingly shifted. Furthermore, in the year following the experiment, all pairs initiated breeding at the same time. The authors conclude that food availability does not act as a zeitgeber, but rather as a factor that modifies the timing of reproduction without affecting the underlying rhythmicity. The authors propose that this is adaptive under environmental conditions that are relatively constant within a given year but may vary considerably between years. The zeitgeber synchronizing the endogenous rhythmicity remains to be identified.

Photoperiodic responsiveness of equatorial and temperate-zone stonechats

The gonads of equatorial stonechats in East Africa (African Stonechats, Saxicola torquata axillaris) develop in anticipation of the short rainy season, the major reproductive period. After the breeding season, gonads regress and birds undergo a complete molt. This annual cycle of reproduction and molt is based on an endogenous circannual rhythmicity that is highly sensitive to photoperiodic changes. By exposing birds to sinusoidal day-length variations with an amplitude of 7 hr, simulating in shape and amplitude those occurring at 47.5°N, gonadal and molt cycles could be synchronized to periods of either 12 or 6 months. In this respect, equatorial birds behaved essentially like temperate-zone stonechats (S. t. rubicola). In both subspecies, photoperiodic synchronization results from seasonal changes in responsiveness to photoperiodic stimuli, reflected in the alternation between a state of photosensitivity and a state of photore-fractoriness. When exposed to a 6-month photoperiodic cycle with an amplitude of only I hr and 10 min, birds of both subspecies no longer synchronized their rhythms with it. Under these conditions, the two subspecies differed in the way testis size changed after the initial phase of testicular growth: whereas the testes of most of the temperate-zone birds stayed enlarged for 6 to 11 months, those of most equatorial birds started to regress within only 2 to 3 months. This difference probably reflects evolutionary adjustments of the two subspecies to the different photoperiodic conditions prevailing in their respective breeding grounds: the equatorial birds appear to initiate refractoriness under shorter photoperiods than do the temperate-zone stonechats. It is not clear as yet whether the very small photoperiodic changes that occur at the equator are sufficient to synchronize circannual rhythms of birds in this region. Possibly the photoperiodic responsiveness of equatorial stonechats is only the unavoidable consequence of gene flow from adjacent, more northerly or more southerly populations.

Seasonal changes in day-light intensity as a potential zeitgeber of circannual rhythms in equatorial Stonechats@@@Saisonale Änderungen der Tageslicht-Intensität als potentieller Zeitgeber circannualer Rhythmen bei tropischen Schwarzkehlchen

The annual rhythms of reproduction and molt of equatorial Stonechats in East Africa (Saxicola torquata axillaris) are controlled by an endogenous circannual rhythmicity. This has been demonstrated in previous experiments in which birds from Africa were kept in a seasonally constant environment: the annual cycles of gonadal size and molt were found to persist for up to 10 years. Since in such constant environmental conditions the period of the rhythms tended to deviate from 12 months, we postulate that seasonally changing factors in the normal environment of these birds normally synchronize the rhythms with the natural year. In the present study we examined the possibility that annual variations in daytime light intensity that occur as a result of changing cloud cover associated with the dry and rainy seasons may provide a circannual zeitgeber. An experimental group consisting of 6 male Stonechats was kept for 25 months in a light-dark cycle in which the light period had a constant duration of 12.5 hours and an intensity alternating between high and low in a 300-day rhythm. Changes in testicular size and molt of these birds were compared with those of a control group of 6 birds that were exposed to the same photoperiod but with bright daylight throughout the experiment. In the control group, only one bird went through 2 testicular cycles and two birds went through one cycle. All these birds showed a molt rhythm, but periods were highly variable among individuals. In contrast, all experimental birds went through two testicular cycles and exhibited rather synchronous molt rhythms (Fig. 1). These findings support the hypothesis that changing light intensity during daytime may provide synchronizing stimuli for circannual rhythms. Nevertheless, premature conclusions should be avoided; possible shortcomings of the experiment are discussed. Die Jahresrhythmik der Fortpflanzung und der Mauser äquatorialer Schwarzkehlchen aus Ost-Afrika (Saxicola torquata axillaris) werden von einer endogenen circannualen Rhythmik kontrolliert. Dies zeigten frühere Versuche, in denen nachgewiesen wurde, daß der Rhythmik der Gonadengröße und der Mauser auch bei solchen Vögeln fortbestand, die über mindestens 10 Jahre in einer konstanten Umwelt lebten. Die Periode dieser Rhythmik wich unter solchen konstanten Versuchsbedingungen allerdings von 12 Monaten ab, was impliziert, daß es in der natürlichen Umwelt der Schwarzkehlchen jahresperiodisch schwankende Umweltfaktoren gibt, die die endogenen Rhythmen mit dem astronomischen Jahr synchronisieren. In der vorliegenden Arbeit untersuchten wir die Möglichkeit, daß jahresperiodische Änderungen der Tageslicht-Intensität, wie sie als Folge von Bewölkungsänderungen mit dem Wechsel zwischen Regen — und Trockenzeiten auftreten, einen solchen Zeitgeber darstellen. Eine Versuchsgruppe von 6 männlichen Schwarzkehlchen wurde 25 Monate lang in einer konstanten äquatorialen Photoperiode von 12,25 Stunden gehalten, in der die Tageslicht Intensität in einem 300-tägigen Rhythmus zwischen einer Phase mit hoher Lichtintensität und einer Phase mit niedriger Lichtintensität abwechselte. Die Zyklen der Hodengröße und der Mauser dieser Vögel wurden mit denen von 6 Kontrollvögeln verglichen, die 25 Monate lang unter derselben Photoperiode aber bei gleichbleibend hellem Tageslicht gehalten wurden. In der Kontrollgruppe durchlief nur ein Vogel zwei Gonadenzyklen und zwei durchliefen je einen Zyklus. Alle 6 Vögel gingen durch einen Mauserzyklus mit großen interindividuellen Unterschieden in der Periodenlänge. Im Gegensatz dazu zeigten alle 6 Versuchsvögel zwei Gonaden- und Mauserzyklen (Abb 1). Die Ergebnisse stützen somit die Hypothese, daß Änderungen in der Beleuchtungsstärke am Tage die circannualen Rhythmen dieser Vögel synchronisieren können. Vorsicht vor zu weitgehenden Schlußfolgerungen scheint allerdings angebracht und mögliche Mängel im Experiment werden diskutiert.

Constant mortality and fertility over age in Hydra

Significance How an organism changes with age and why the pattern of change differs across species are questions that have intrigued biologists since Aristotle. Patterns of change can be described by trajectories of birth and death rates over age. For humans and many other mammals, mortality increases and fertility declines with age among adults. For other species, however, a remarkable variety of patterns has been observed. Although roughly constant mortality and fertility trajectories have been reported for some species, the data are problematic because sample sizes are small, especially at older ages. Here, we present compelling evidence for constant mortality and reproduction of Hydra using data from careful, large-scale studies over 8 y with 2,256 individuals. Senescence, the increase in mortality and decline in fertility with age after maturity, was thought to be inevitable for all multicellular species capable of repeated breeding. Recent theoretical advances and compilations of data suggest that mortality and fertility trajectories can go up or down, or remain constant with age, but the data are scanty and problematic. Here, we present compelling evidence for constant age-specific death and reproduction rates in Hydra, a basal metazoan, in a set of experiments comprising more than 3.9 million days of observations of individual Hydra. Our data show that 2,256 Hydra from two closely related species in two laboratories in 12 cohorts, with cohort age ranging from 0 to more than 41 y, have extremely low, constant rates of mortality. Fertility rates for Hydra did not systematically decline with advancing age. This falsifies the universality of the theories of the evolution of aging that posit that all species deteriorate with age after maturity. The nonsenescent life history of Hydra implies levels of maintenance and repair that are sufficient to prevent the accumulation of damage for at least decades after maturity, far longer than the short life expectancy of Hydra in the wild. A high proportion of stem cells, constant and rapid cell turnover, few cell types, a simple body plan, and the fact that the germ line is not segregated from the soma are characteristics of Hydra that may make nonsenescence feasible. Nonsenescence may be optimal because lifetime reproduction may be enhanced more by extending adult life spans than by increasing daily fertility.