Ageing effects in an iteroparous plant species with a variable life span

Background and Aims

Ageing effects may be due to dysfunction leading to decreasing reproduction and survival with age. In plants, however, other (physiological) causes, associated with size for example, may also play a role. Iteroparous plants with genetically variable life spans can be helpful in unravelling these two aspects of changes associated with growing older.

Methods

In a long-term experiment, Beta vulgaris ssp. maritima (sea beet) plants from the same set of populations but with different ages were compared for flowering date over several years. Flowering date, root growth and seed production were measured in a synthetic population and in progenies derived from reciprocal crosses over three consecutive years and analysed with respect to the number of years yet to live. Heritabilities of these three characters and of life span were estimated.

Key Results

Flowering occurred on average 1·3 d later each year over a plant''s whole lifetime. In the year before dying, plants flowered on average 3·3 d later and both root investment and seed production decreased significantly compared with plants that remained alive for at least 1 further year. The negative relationship (trade-off) between reproduction and root investment in early life became positive near the end of life, and the positive relationship between flowering date and root growth became negative.

Conclusions

Effects of ageing – in the sense of a decline in reproduction and root storage – combined with later flowering were particularly pronounced in the year before death. The gradual change in flowering phenology, observed over the whole lifetime, could have a physiological basis unrelated to dysfunction.Key words: Ageing, Beta vulgaris ssp. maritima (sea beet), flowering phenology, longevity, perennial, root investment, seed production, trade-offs, whole-plant senescence     

Senescence and costs of reproduction in the life history of a small precocial species

Species following a fast life history are expected to express fitness costs mainly as increased mortality, while slow‐lived species should suffer fertility costs. Because observational studies have limited power to disentangle intrinsic and extrinsic factors influencing senescence, we manipulated reproductive effort experimentally in the cavy (Cavia aperea) which produces extremely precocial young. We created two experimental groups: One was allowed continuous reproduction (CR) and the other intermittent reproduction (IR) by removing males at regular intervals. We predicted that the CR females should senesce (and die) earlier and produce either fewer and/or smaller, slower growing offspring per litter than those of the IR group. CR females had 16% more litters during three years than IR females. CR females increased mass and body condition more steeply and both remained higher until the experiment ended. Female survival showed no group difference. Reproductive senescence in litter size, litter mass, and reproductive effort (litter mass/maternal mass) began after about 600 days and was slightly stronger in CR than IR females. Litter size, litter mass, and offspring survival declined with maternal age and were influenced by seasonality. IR females decreased reproductive effort less during cold seasons and only at higher age than CR females. Nevertheless, offspring winter mortality was higher in IR females. Our results show small costs of reproduction despite high reproductive effort, suggesting that under ad libitum food conditions costs depend largely on internal regulation of allocation decisions.     

Evolutionary demography of iteroparous plants: incorporating non-lethal costs of reproduction into integral projection models

Understanding the selective forces that shape reproductive strategies is a central goal of evolutionary ecology. Selection on the timing of reproduction is well studied in semelparous organisms because the cost of reproduction (death) can be easily incorporated into demographic models. Iteroparous organisms also exhibit delayed reproduction and experience reproductive costs, although these are not necessarily lethal. How non-lethal costs shape iteroparous life histories remains unresolved. We analysed long-term demographic data for the iteroparous orchid Orchis purpurea from two habitat types (light and shade). In both the habitats, flowering plants had lower growth rates and this cost was greater for smaller plants. We detected an additional growth cost of fruit production in the light habitat. We incorporated these non-lethal costs into integral projection models to identify the flowering size that maximizes fitness. In both habitats, observed flowering sizes were well predicted by the models. We also estimated optimal parameters for size-dependent flowering effort, but found a strong mismatch with the observed flower production. Our study highlights the role of context-dependent non-lethal reproductive costs as selective forces in the evolution of iteroparous life histories, and provides a novel and broadly applicable approach to studying the evolutionary demography of iteroparous organisms.     

Optimal life histories and the age-specific costs of reproduction

Increases in reproduction at a given age may carry costs measured as reductions in subsequent survival and/or future fertility. Such costs generate constraints within which natural selection may mould life histories to maximize fitness. In this paper, I derive expressions predicting the age-specific costs of reproduction conditional on the maximization of fitness. Survival costs should, on this hypothesis, vary as the inverse of the reproductive value curve; fertility costs should vary as the ratio of successive terms in the stable age distribution. For many organisms, this means that survival costs should increase markedly with age, while fertility costs should be nearly age-invariant. Data on such age-specific costs is scarce, but that which is available (mainly for humans) agrees with these predictions.     

Risk spreading as an adaptive strategy in iteroparous life histories

It has long been conjectured, though without satisfactory proof, that life tables with a long reproductive span are advantageous in an environment where fecundity or immature survival rates fluctuate randomly. In the present analysis we recast the nonlinear Leslie matrix problem as an autoregressive time series model for the birth rate, with random addition and removal of newborn. This transformation renders the model linear with respect to the environmental variation, allowing ready solution for the ultimate population size and for the conditions resulting in stationarity of the population distribution. We show that for life tables where the fecundities of all adult age classes are the same (no restrictions are put on the survivorship schedule, or on the age at first reproduction), and where density dependence operates via total adult density, the realized growth rate is less than the growth rate calculated from the mean Leslie matrix associated with the population's growth history. The degree of the discrepancy increases with the environmental variability, and decreases with iteroparity, thus completing a proof which confirms the correctness of the initial conjecture for a class of biologically reasonable lifetable models.     

Reduced habitat quality increases intrinsic but not ecological costs of reproduction

Although the costs of reproduction are predicted to vary with the quality of the breeding habitat thereby affecting population dynamics and life‐history trade‐offs, empirical evidence for this pattern remains sparse and equivocal. Costs of reproduction can operate through immediate ecological mechanisms or through delayed intrinsic mechanisms. Ignoring these separate pathways might hinder the identification of costs and the understanding of their consequences. We experimentally investigated the survival costs of reproduction for adult little owls (Athene noctua) within a gradient of habitat quality. We supplemented food to nestlings, thereby relieving the parents’ effort for brood provisioning. We used radio‐tracking and Bayesian multistate modeling based on marked recapture and dead recovery to estimate survival rates of adult little owls across the year as a function of food supplementation and habitat characteristics. Food supplementation to nestlings during the breeding season increased parental survival not only during the breeding season but also during the rest of the year. Thus, the low survival of parents of unfed broods likely represents both, strong ecological and strong intrinsic costs of reproduction. However, while immediate ecological costs occurred also in high‐quality habitats, intrinsic costs carrying over to the post‐breeding period occurred only in low‐quality habitats. Our results suggest that immediate costs resulting from ecological mechanisms such as predation, are high also in territories of high habitat quality. Long‐term costs resulting from intrinsic trade‐offs, however, are only paid in low‐quality habitats. Consequently, differential effects of habitat quality on immediate ecological and delayed intrinsic mechanisms can mask the increase of costs of reproduction in low‐quality breeding habitats. Intrinsic costs may represent an underrated mechanism of habitat quality affecting adult survival rate thereby considerably accelerating population decline in degrading habitats. This study therefore highlights the need for a long‐term perspective to fully assess the costs of reproduction and the role of habitat quality in modifying these costs.     

Evolution of life history strategies for an asexual annual plant model

At any given moment in time a plant is partitioning total growth mass into its various component parts such as leaves, roots, reproductive material, etc. The view is taken that the plant has evolved a life history strategy to control this partitioning process. This paper illustrates the utility of optimal control theory for use in determining life history strategies which maximize fitness for a given asexual plant model. The optimal control methods are first used on a model previously analyzed by Professor Dan Cohen, who used a different method. His results of a change from 100% vegetable growth to 100% reproductive growth at a fixed switching time is again obtained. This 100% switching result is shown to be more generally applicable by using a qualitatively described model. However the switching time in general is shown to be a function of both leaf mass and time remaining to the end of the growing season. The allocation to toxin production is also considered. It is shown that under this model an inequality between system parameters must be satisfied before the plant should allocate growth to toxin production. Although the particular model explored here may rarely be realistic in nature, these same methods of optimal control theory can be applied in a similar fashion to many other proposed models of plant resource allocation.     

Mammalian reproduction: an ecological perspective

The objectives of this paper are to organize our concepts about the environmental regulation of reproduction in mammals and to delineate important gaps in our knowledge of this subject. The environmental factors of major importance for mammalian reproduction are food availability, ambient temperature, rainfall, the day/night cycle and a variety of social cues. The synthesis offered here uses as its core the bioenergetic control of reproduction. Thus, for example, annual patterns of breeding are viewed as reflecting primarily the caloric costs of the female's reproductive effort as they relate to the energetic costs and gains associated with her foraging effort. Body size of the female is an important consideration since it is correlated with both potential fat reserves and life span. Variation in nutrient availability may or may not be an important consideration. The evolutionary forces that have shaped the breeding success of males usually are fundamentally different from those acting on females and, by implication, the environmental controls governing reproduction probably also often differ either qualitatively or quantitatively in the two sexes. Mammals often live in habitats where energetic and nutrient challenges vary seasonally, even in the tropics. When seasonal breeding is required, a mammal may use a predictor such as photoperiod or a secondary plant compound to prepare metabolically for reproduction. A reasonable argument can be made, however, that opportunistic breeding, unenforced by a predictor, may be the most prevalent strategy extant among today's mammals. Social cues can have potent modulating actions. They can act either via discrete neural and endocrine pathways to alter specific processes such as ovulation, or they can induce nonspecific emotional states that secondarily affect reproduction. Many major gaps remain in our knowledge about the environmental regulation of mammalian reproduction. For one, we have a paucity of information about the annual patterns of breeding and about the mechanisms controlling these patterns in the most common mammals on the planet-the small to average-sized mammals living in the tropics. We probably have only a shallow conceptualization of the way available energy and nutrients control reproduction and, likewise, we may have only a narrow view of the potential kinds and uses of seasonal predictors. Finally, we have little appreciation of the way environmental cues interact with each other to control reproduction.     

Controlling resource acquisition to reveal a life history trade-off: egg mass and clutch size in an iteroparous seed predator, Prostephanus truncatus

1. A trade-off constraining egg production was investigated and the consequences of egg mass for the offspring life history in Prostephanus truncatus investigated. Fresh egg mass was found to vary between 0.065 and 0.109 mg (about 20% of fresh body mass at emergence) and was correlated both with dry egg mass ( r = 0.8) and with the mass of first-instar larvae ( r = 0.8).
2. There was a negative correlation between egg mass and clutch size: doubling clutch size from eight to sixteen eggs resulted in a reduction in egg mass from 0.09 to 0.07 mg. Resource allocation per clutch was not constant but increased with clutch size. After allowing for the relationship between egg mass and clutch size, heavier females were found to oviposit both heavier eggs and more eggs in a clutch.
3. By placing eggs in prepared seeds that minimized variation in resource acquisition, it was discovered that development period of females, but not of males, was negatively correlated with egg mass. Egg size was not correlated with body size at emergence in either sex.
4. The results are interpreted as revealing a resource-allocation trade-off in egg production.     

Measuring the costs of reproduction

The measurement of costs of reproduction is of interest because such costs are generally assumed by life history theory. There is some controversy concerning how to measure costs: common methods include experimental manipulations of life history, such as preventing some individuals from reproducing, or estimates of genetic correlations. These two methods often yield similar results, suggesting that one can serve as a substitute for the other. There are now experiments which demonstrate that there are different mechanisms underlying the response to an experimental manipulation versus a genetic correlation, so the two methods are not equivalent in estimating costs.     

A review of the life history,reproduction and phenology of Gracilaria

The basic life history of the red alga Gracilaria is of the three-phase Polysiphonia type but a number of species show deviations. Plants can bear both gametangia and tetrasporangia, either on separate parts of the thallus or on the same. Explanations include the in situ germination of tetraspores (allowing gametophytic thalli to be epiphytic on tetrasporophytes), the coalescence of spores or developing discs (resulting in chimaeras), mitotic recombination during cell division in the mature diploid thallus (resulting in patches of diploid male and female cells on the tetrasporophyte), a mutation eliminating the repression of female expression allowing haploid male plants to be bisexual and initial failure of cell walls to form during the development of tetraspores. Polyploids can be produced from plants with diploid gametangia. The sexes and phases are usually morphologically identical but gametophytes or their parts may be smaller. The growth rates of the sexes may differ and diploid juveniles may survive better than haploid. Neither polyploidy nor hybridization results in superior growth. The sex ratio is probably 1:1 but females may appear to be more abundant. Diploid and haploid phases are usually either about equal or diploids predominate, often depending on the type of substratum. At high latitudes reproduction peaks in late summer whereas in the tropics it may be high all year. In temperate regions growth rate is fastest and biomass highest in late summer; in the tropics peak biomass is mainly in the winter. Spermatia are effective for only a few h. Spores vary in size around 25 \m, diploid ones usually being larger. Cystocarps or tetrasporangia in the field may not currently be releasing spores. In the laboratory spore release shows a diurnal rhythm, peaking during the night or day according to the species. All the above attributes are potentially important in planning and executing Gracilaria cultivation.     

Differential costs of reproduction in females and hermaphrodites in a gynodioecious plant

Background and Aims

Plants exhibit a variety of reproductive systems where unisexual (females or males) morphs coexist with hermaphrodites. The maintenance of dimorphic and polymorphic reproductive systems may be problematic. For example, to coexist with hermaphrodites the females of gynodioecious species have to compensate for the lack of male function. In our study species, Geranium sylvaticum, a perennial gynodioecious herb, the relative seed fitness advantage of females varies significantly between years within populations as well as among populations. Differences in reproductive investment between females and hermaphrodites may lead to differences in future survival, growth and reproductive success, i.e. to differential costs of reproduction. Since females of this species produce more seeds, higher costs of reproduction in females than in hermaphrodites were expected. Due to the higher costs of reproduction, the yearly variation in reproductive output of females might be more pronounced than that of hermaphrodites.

Methods

Using supplemental hand-pollination of females and hermaphrodites of G. sylvaticum we examined if increased reproductive output leads to differential costs of reproduction in terms of survival, probability of flowering, and seed production in the following year.

Key Results

Experimentally increased reproductive output had differential effects on the reproduction of females and hermaphrodites. In hermaphrodites, the probability of flowering decreased significantly in the following year, whereas in females the costs were expressed in terms of decreased future seed production.

Conclusions

When combining the probability of flowering and seed production per plant to estimate the multiplicative change in fitness, female plants showed a 56 % and hermaphrodites showed a 39 % decrease in fitness due to experimentally increased reproduction. Therefore, in total, female plants seem to be more sensitive to the cost of reproduction in terms of seed fitness than hermaphrodites.     

Cost of reproduction and covariation of life history traits in birds

Evolution of life history traits can be studied at two different levels: (1) current selection processes, including trade-offs in life history traits in natural populations as revealed by observations or, preferably, exieriments; and (2) patterns of variation in life history traits with each other and with ecology among extant species. Selection is not evolution, but selection pressures must have caused evolutionary change and led to current patterns of life history traits. These problems are exemplified by recent research on clutch size in birds.     

Generation specific life history traits of winged shape Sitobion avenae

When reared under constant conditions from egg hatch the proportion of offspring of Sitobion avenae (F.) (Aphididae: Macrosiphini) that developed into winged individuals declined from the second to fourth generation. The winged individuals produced in these three generations showed a progressive decrease in their wet and dry weights and an increase in the length of their largest embryo with generation. The trend in winged individual production and also the trends in their size and reproductive strategy appear to be programmed and are similar to the generation specific strategies that have been described in other species of aphid.     

Plant life history stage and nurse age change the development of ecological networks in an arid ecosystem

Understanding how ecological networks are organised over the course of an organism's lifetime is crucial for predicting the dynamics of interacting populations and communities across temporal scales. However, most studies so far considered only one life history stage at a time, such as adult, when studying networks of interacting species. Therefore, knowledge about how multiple life history stages affect the development and stability of plant–plant association networks is lacking. We measured the understory adult plant community and the soil seed bank across a plant age gradient of the nurse shrub Retama sphaerocarpa in an arid ecosystem in Spain. Using a multilayer network approach, we built adult understory–nurse and seed bank–nurse networks and analysed how network nestedness, species’ role, and species specificity varied between them and with nurse plant age. We found that seed bank and adult understory networks changed depending on nurse plant age in two different ways. With increasing nurse plant age, adult understory networks became significantly more nested than seed bank networks. The nested architecture of seed bank networks was therefore a poor predictor of adult understory network nestedness. The contribution and specificity of species to network nestedness increased with increasing nurse plant age more in the adult understory than in seed bank networks, despite high species turnover. Our data show that life history and ontogeny affect the development of plant–plant association networks. Niche construction and environmental filtering along nurse ontogeny seem pivotal mechanisms structuring adult understory networks while the assembly of seed bank networks seems rather stochastic. We highlight the importance of mature plant communities for maintaining rare species populations and supporting the stability of ecological communities through time.     

The direct and ecological costs of an ant-plant symbiosis

How strong is selection for cheating in mutualisms? The answer depends on the type and magnitude of the costs of the mutualism. Here we investigated the direct and ecological costs of plant defense by ants in the association between Cordia nodosa, a myrmecophytic plant, and Allomerus octoarticulatus, a phytoecious ant. Cordia nodosa trees produce food and housing to reward ants that protect them against herbivores. For nearly 1 year, we manipulated the presence of A. octoarticulatus ants and most insect herbivores on C. nodosa in a full-factorial experiment. Ants increased plant growth when herbivores were present but decreased plant growth when herbivores were absent, indicating that hosting ants can be costly to plants. However, we did not detect a cost to ant colonies of defending host plants against herbivores. Although this asymmetry in costs suggests that the plants may be under stronger selection than the ants to cheat by withholding investment in their partner, the costs to C. nodosa are probably at least partly ecological, arising because ants tend scale insects on their host plants. We argue that ecological costs should favor resistance or traits other than cheating and thus that neither partner may face much temptation to cheat.     

The ecological significance of long-distance water transport: short-term regulation, long-term acclimation and the hydraulic costs of stature across plant life forms

Plant hydraulic conductance, namely the rate of water flow inside plants per unit time and unit pressure difference, varies largely from plant to plant and under different environmental conditions. Herein the main factors affecting: (a) the scaling between whole‐plant hydraulic conductance and leaf area; (b) the relationship between gas exchange at the leaf level and leaf‐specific xylem hydraulic conductance; (c) the short‐term physiological regulation of plant hydraulic conductance under conditions of ample soil water, and (d) the long‐term structural acclimation of xylem hydraulic conductance to changes in environmental conditions are reviewed. It is shown that plant hydraulic conductance is a highly plastic character that varies as a result of multiple processes acting at several time scales. Across species ranging from coniferous and broad‐leaved trees to shrubs, crop and herbaceous species, and desert subshrubs, hydraulic conductance scaled linearly with leaf area, as expected from first principles. Despite considerable convergence in the scaling of hydraulic properties, significant differences were apparent across life forms that underlie their different abilities to conduct gas exchange at the leaf level. A simple model of carbon allocation between leaves and support tissues explained the observed patterns and correctly predicted the inverse relationships with plant height. Therefore, stature appears as a fundamental factor affecting gas exchange across plant life forms. Both short‐term physiological regulation and long‐term structural acclimation can change the levels of hydraulic conductance significantly. Based on a meta‐analysis of the existing literature, any change in environmental parameters that increases the availability of resources (either above‐ or below‐ground) results in the long‐term acclimation of a less efficient (per unit leaf area) hydraulic system.     

Environmentally induced clonal reproduction and life history traits of the liana Machaerium cuspidatum in an Amazonian rain forest,Ecuador

The population structure of the canopy liana Machaerium cuspidatum Kuhlm. & Hoehne (Fabaceae) was studied in ten transects covering a total of 2.5 ha of tropical rain forest in Yasuní National Park, eastern Ecuador. The aim was to investigate how trellis availability, topographic position and light availability affected the population density and structure of the most abundant liana species in the area. The environmental variation affected plants in different size classes differently. Large plants (diameter 1 cm) were almost exclusively found in areas with low canopy and dense undergrowth. These areas had the highest density of suitable host plants. Seedling-sized plants (height < 30 cm) and saplings (height 30 cm but diameter < 1 cm) occurred more frequently and withhigher density in steep upland areas than in the floodplains, presumably due to elevated seedling mortality in the periodically flooded areas. Seedling-sized plants and saplings did not grow in areas with elevated light levels, and although plants of all sizes were highly clumped, this clumping rarely coincided with patches with abundant canopy gaps. Machaerium cuspidatum reproduces clonally when branches re-root and break off from the parentplant. The density of clonally produced plants was high in areas where the density of sexually produced plants was low, whereas the total density varied little among habitat types. A higher proportion of the seedling-sized plants were of sexual origin in the upland areas. An environmentally induced increase in the production of independent ramets enables M. cuspidatum to persist in the floodplains. This shows that plants may expand theirrealised niches to habitats with a low potential for seedling survival if high seedling mortality can be compensated for by increased clonal reproduction.