Low Residual Reproductive Value Research Articles

Flirting with danger: predation risk interacts with male condition to influence sexual display

AbstractSexual signaling coevolves with the sensory systems of intended receivers; however, predators may be unintended receivers of sexual signals. Conspicuous aerial displays in some species may place males at high risk of predation from eavesdropping predators. There are three different hypotheses to explain how signaling males can deal with increased predation risk: (1) males invest in survival by decreasing signal conspicuousness; (2) males invest in reproduction by increasing signal conspicuousness; and (3) male response is condition-dependent according to his residual reproductive value. Here, we used blue-black grassquits (Volatinia jacarina) to test these hypotheses, asking whether males modify leap displays under different levels of predation risk. Grassquit males develop an iridescent nuptial plumage and spend considerable time emitting a multimodal signal: while leaping from a perch, males clap their wings above their heads and emit a high-pitched short song. We exposed males to predator and nonpredator playbacks while video recording their displays. We found interactions between predation risk and 2 male condition variables (ectoparasite infestation and proportion of nuptial plumage coverage) that influenced display behavior. Less parasitized males and those with higher proportion of nuptial plumage showed no change in display behavior, while more parasitized males and those with lower proportion of nuptial plumage increased the vigor of displays under predation risk. In other words, males with low residual reproductive value increased reproductive effort when there was a high risk of extrinsic death. Our study provides some empirical support for the terminal investment hypothesis.

State-dependent changes in risk-taking behaviour as a result of age and residual reproductive value

Animals are able to modify their behaviour in response to changes in their internal and environmental state. The asset protection principle predicts that an animal's risk-taking behaviour should vary as a result of its residual reproductive value (RRV); animals with greater RRV would incur a greater cost if injured or killed and should therefore take fewer risks than those with low RRV. Despite the intuitive appeal of this hypothesis, few studies have effectively separated the effects of RRV on behaviour from those of age. We addressed this weakness in the widely invoked hypothesis by measuring the risk-taking behaviour of female Australian field crickets, Teleogryllus oceanicus, at various points in the animal's lifetime. We found significant effects of age on risk-taking behaviour: older females emerged from a shelter sooner after a simulated predation threat and exhibited greater mobility in an open arena. Importantly, there was also a significant marginal effect of RRV on risk-taking behaviour. Females with lower RRV displayed greater levels of risk taking than females with high RRV. Our results thereby offer support for the asset protection principle as an explanation for state-dependent variation in risk-taking behaviour.

Aging male loons make a terminal investment in territory defense

Animals that senesce experience a decline in residual reproductive value (RRV), such that old individuals can expect reduced breeding success compared to young ones. According to life history theory, animals with low RRV, which thus have less to lose, should shift resources away from self-maintenance and towards reproduction, an expectation called terminal investment. In a population of common loons whose survival and territorial behavior were measured throughout life, males 14 years and older exhibited clear senescence, as they showed lower survival, reduced body mass, and far greater susceptibility to territorial eviction than younger males. While older males invested no more effort than young males in feeding or protecting their chicks, they increased territorial yodeling by 35%, showed more aggression towards territorial intruders, and, following eviction from original territories, resettled with great frequency on vacant, unproductive territories nearby. Our findings thus provide support for terminal investment in territorial behavior. Hyper-aggressive behavior by old, declining males might explain the unusual occurrence of lethal combat for territories in this species. Life history theory holds that animals that decline with age should invest less energy in staying alive and more in reproduction when they become old, because they have less to lose in doing so. Evidence for such terminal investment, however, is scanty. We measured rates of survival and territorial behavior in a known-age population of common loons and found that males, but not females, suffered a decrease in survival rate and ability to hold a territory after age 14. At the same time, territorial males older than 14 behaved more aggressively and were more apt to give a territorial yodel call towards territorial intruders. Hence, our study appears a rare example of terminal investment in aggressive behavior, whereby old, declining males cling desperately to their territories in hopes of producing a few more offspring before they die.

Seasonal fecundity and costs to λ are more strongly affected by direct than indirect predation effects across species

Increased perceived predation risk can cause behavioral and physiological responses to reduce direct predation mortality, but these responses can also cause demographic costs through reduced reproductive output. Such indirect costs of predation risk have received increased attention in recent years, but the relative importance of direct vs. indirect predation costs to population growth (λ) across species remains unclear. We measured direct nest predation rates as well as indirect benefits (i.e., reduced predation rates) and costs (i.e., decreased reproductive output) arising from parental responses to perceived offspring predation risk for 10 songbird species breeding along natural gradients in nest predation risk. We show that reductions in seasonal fecundity from behavioral responses to perceived predation risk represent significant demographic costs for six of the 10 species. However, demographic costs from these indirect predation effects on seasonal fecundity comprised only 12% of cumulative predation costs averaged across species. In contrast, costs from direct predation mortality comprised 88% of cumulative predation costs averaged across species. Demographic costs from direct offspring predation were relatively more important for species with higher within-season residual-reproductive value (i.e., multiple-brooded species) than for species with lower residual-reproductive value (i.e., single-brooded species). Costs from indirect predation effects were significant across single- but not multiple-brooded species. Ultimately, demographic costs from behavioral responses to offspring predation risk differed among species as a function of their life-history strategies. Yet direct predation mortality generally wielded a stronger influence than indirect effects on seasonal fecundity and projected λ across species.

Control of parental investment changes plastically over time with residual reproductive value.

Evolutionary conflict between parents and offspring over parental resource investment is a significant selective force on the traits of both parents and offspring. Empirical studies have shown that for some species, the amount of parental investment is controlled by the parents, whereas in other species, it is controlled by the offspring. The main difference between these two strategies is the residual reproductive value of the parents or opportunities for future reproduction. Therefore, this could explain the patterns of control of parental investment at the species level. However, the residual reproductive value of the parents will change during their lifetime; therefore, parental influence on the amount of investment can be expected to change plastically. Here, we investigated control of parental investment when parents were young and had a high residual reproductive value, compared to when they were old and had a low residual reproductive value using a cross-fostering experiment in the burying beetle Nicrophorus quadripunctatus. We found that parents exert greater control over parental investment when they are young, but parental control is weakened as the parents age. Our results demonstrate that control of parental investment is not fixed, but changes plastically during the parent's lifetime.

Mating rock shrimp hedge their bets: old males take greater risk, but only after careful assessment of the investment scenario

Mature organisms often have to trade reproductive opportunities against the need to survive, especially in species with exaggerated, sexually selected traits. Life history theory predicts that old males with low residual reproductive value (RRV) would accept greater risk for current reproduction than their younger counterparts. Accordingly, we tested the prediction that, under predation risk, old males of the rock shrimp Rhynchocinetes typus pair with females faster and for a longer time than young males do. We exposed young and old dominant males (in the final ontogenetic stage, called “robustus”) to a female in the absence and presence of a predator. As predicted, older robustus males modified their mating behavior when exposed to a predator. However, in contrast to the prediction, they delayed female seizure under predation risk, possibly to carefully assess the actual threat before initiating female guarding. Once they had established the mate-guarding position, old robustus males did not interrupt it until the end of female spawning and, in the presence of predators, even guarded the female significantly longer than in predator-free treatments. In contrast, younger robustus males did not delay female seizure but abandoned the female repeatedly when a predator was present, suggesting that they perceived and responded to the predation risk. Our results suggest that older robustus males have the experience to assess threats before engaging in risky behaviors that bolster their reproductive success. Although consistent with the theory that low RRV individuals should accept greater reproductive risk, we suggest that old individuals do not recklessly engage in risky behaviors but rather cautiously evaluate the threats before investing in a potentially terminal reproductive event.

Animal personality and pace-of-life syndromes: do fast-exploring fairy-wrens die young?

The pace-of-life syndrome (POLS) hypothesis for animal personality proposes that variation among individuals in life-history strategies is associated with consistent differences in behavior. We tested predictions of this hypothesis in the superb fairy-wren, Malurus cyaneus, by investigating long-term individual differences in risk-related behaviors (latency to enter a novel artificial environment, exploration, activity and response to mirror image stimulation) and survival. We found consistent differences between individuals in these behaviors (adjusted repeatability of exploration of artificial novel environment = 0.37). Individual differences were consistent over several years and bi-variate analyses showed a significant among-individual correlation (‘behavioral syndrome’) between exploration behavior at two life stages (young adult and old adult). Docility at the nestling stage predicted exploration behavior of juveniles. Behavioral traits measured in a risky context were correlated with one another, forming a behavioral syndrome of coping strategies ranging from ‘proactive’ to ‘reactive’. Nestlings that were more active and exploratory in isolation were less docile during handling, while adults that entered the artificial environment fast were more exploratory, active, and aggressive in the artificial environment. Exploration behavior increased within individuals as they aged and when they were in poorer condition, consistent with expectations of more risk-prone behavior with lower residual reproductive value (reduced ‘asset protection’). Risk-related behavior predicted the probability of apparent survival: more exploratory individuals were less likely to be present in the population twelve months later. Our findings suggest that, consistent with the predictions of the POLS hypothesis, individual variation in survival is associated with consistent individual differences in risk-related behavior that are maintained long-term and span developmental boundaries.

Age affects escape behavior by the zebra-tailed lizard (Callisaurus draconoides) more strongly than in other lizards

Prey of different ages may exhibit differences in escape behavior, including flight initiation distance (FID – predator-prey distance when escape begins) and distance fled before stopping (DF). Escape theory predicts FID and, in some circumstance, DF, based on trade-offs between conflicting cost of not fleeing (predation risk) and cost of fleeing (primarily opportunities to enhance fitness lost by fleeing). The prey’s expected lifetime fitness when an encounter begins also affects escape decisions. Because hatchling and adult lizards may differ in ways that affect all three of these factors, a priori prediction of age differences is not possible without measurements of all three. In a field study I found that hatchling zebra-tailed lizards (Callisaurs draconoides) had much shorter FID and DF than adults. These relationships were not affected by distance to refuge, which did not differ between ages, and refuge use was infrequent. The findings agree with those of all but one previous study of age differences, suggesting that hatchling lizards typically have shorter FID and DF than adults because they 1) assess risk as being lower due to lower attractiveness to or detectability by predators, lack of experience or greater maneuverability, 2) have greater opportunity cost due to the need for rapid growth and good body condition before winter, and possibly 3) have lower residual reproductive value due to higher mortality rate than adults. Effects of age and size are confounded, and smaller size may be the major reason for the shorter FID and distance fled of hatchlings.

Changing reproductive effort within a semelparous reproductive episode.

• Life-history theory predicts a trade-off between current and future reproduction for iteroparous organisms-as individuals age, the expected value of future reproduction declines, and thus reproductive effort is expected to be higher in later clutches than in earlier. In contrast, models explaining the evolution of semelparity treat semelparous reproduction as instantaneous, with no scope for intraindividual variation. However, semelparous reproduction is also extended, but over shorter time scales; whether there are similar age- or stage-specific changes in reproductive effort within a semelparous episode is unclear. In this study, we assessed whether semelparous individuals increase reproductive effort as residual reproductive value declines by comparing the reproductive phenotype of flowers at five different floral positions along a main inflorescence.• Using the herbaceous monocarp Lobelia inflata, we conducted a longitudinal study of 409 individuals including both laboratory and field populations over three seasons. We recorded six reproductive traits-including the length of three phenological intervals as well as fruit size, seed size, and seed number-for all plants across floral positions produced throughout the reproductive episode.• We found that while the rate of flower initiation did not change, flowers at distal (late) floral positions developed more quickly and contained larger seed than flowers at basal (early) floral positions did.• Our results were consistent with the hypothesis that, like iteroparous organisms, L. inflata increases reproductive effort in response to low residual reproductive value.

Pheromone Blend Does not Explain Old Male Mating Advantage in a Butterfly

In several insect species, male mating success is higher in older than in younger males, although condition diminishes dramatically with age. Two hypotheses are under debate to explain the counterintuitive pattern of old male mating advantage: first, an increased eagerness of older males to mate, driven by their low residual reproductive value, and second female preference for older males based on chemical cues such as sex pheromones (female choice hypothesis). In a series of experiments, we manipulated female olfaction, male pheromone blend and female age to test whether old male mating advantage prevails when the influence of male sex pheromones is controlled for, using the tropical butterfly Bicyclus anynana as model. We found that older males had a higher mating success than younger ones irrespective of female scent-sensitivity and irrespective of male pheromone blend. Interestingly, older males were found to court more often and for longer time bouts than younger males. These results were independent of female age, although younger males courted younger females more often and for longer bouts than older females. Taken together, our results indicate that male courtship activity (1) is higher in older compared to younger males and (2) increases the mating success of older males. Olfaction and sensing pheromones, in contrast, were not a necessary prerequisite for old male mating advantage to occur and may use other cues than pheromones to assess male quality.

Old‐male paternity advantage is a function of accumulating sperm and last‐male precedence in a butterfly

Old-male mating advantage has been convincingly demonstrated in Bicyclus anynana butterflies. This intriguing pattern may be explained by two alternative hypotheses: (i) an increased aggressiveness and persistence of older males during courtship, being caused by the older males' low residual reproductive value; and (ii) an active preference of females towards older males what reflects a good genes hypothesis. Against this background, we here investigate postcopulatory sexual selection by double-mating Bicyclus anynana females to older and younger males, thus allowing for sperm competition and cryptic mate choice, and by genotyping the resulting offspring. Virgin females were mated with a younger virgin (2-3days old) and afterwards an older virgin male (12-13days old) or vice versa. Older males had a higher paternity success than younger ones, but only when being the second (=last) mating partner, while paternity success was equal among older and younger males when older males were the first mating partner. Older males produced larger spermatophores with much higher numbers of fertile sperm than younger males. Thus, we found no evidence for cryptic female mate choice. Rather, the findings reported here seem to result from a combination of last-male precedence and the number of sperm transferred upon mating, both increasing paternity success.

Seasonal variation in the behaviour of a short-lived rodent

BackgroundShort lived, iteroparous animals in seasonal environments experience variable social and environmental conditions over their lifetime. Animals can be divided into those with a “young-of-the-year” life history (YY, reproducing and dying in the summer of birth) and an “overwinter” life history (OW, overwintering in a subadult state before reproducing next spring).We investigated how behavioural patterns across the population were affected by season and sex, and whether variation in behaviour reflects the variation in life history patterns of each season. Applications of pace-of-life (POL) theory would suggest that long-lived OW animals are shyer in order to increase survival, and YY are bolder in order to increase reproduction. Therefore, we expected that in winter and spring samples, when only OW can be sampled, the animals should be shyer than in summer and autumn, when both OW and YY animals can be sampled.We studied common vole (Microtus arvalis) populations, which express typical, intra-annual density fluctuation. We captured a total of 492 voles at different months over 3 years and examined boldness and activity level with two standardised behavioural experiments.ResultsBehavioural variables of the two tests were correlated with each other. Boldness, measured as short latencies in both tests, was extremely high in spring compared to other seasons. Activity level was highest in spring and summer, and higher in males than in females.ConclusionBeing bold in laboratory tests may translate into higher risk-taking in nature by being more mobile while seeking out partners or valuable territories. Possible explanations include asset-protection, with OW animals being rather old with low residual reproductive value in spring. Therefore, OW may take higher risks during this season. Offspring born in spring encounter a lower population density and may have higher reproductive value than offspring of later cohorts. A constant connection between life history and animal personality, as suggested by the POL theory, however, was not found. Nevertheless, correlations of traits suggest the existence of animal personalities. In conclusion, complex patterns of population dynamics, seasonal variation in life histories, and variability of behaviour due to asset-protection may cause complex seasonal behavioural dynamics in a population.

Age-dependent changes in calling effort in the bell cricket Meloimorpha japonica

We investigated how male age and body weight influence male mating effort in the bell cricket Meloimorpha japonica. We adopted a longitudinal approach to study resource allocation to male mating effort (calling duration during 24 h) in the bell cricket. Calling durations and body weight of each male were measured at 7–8 days (young age), 14–15 days (middle age), and 22–25 days (old age) after the final molt. Calling duration increased between young and middle age. During the period between middle and old age, the amount of change in the calling duration was positively correlated with the body weight. The results suggested that older (i.e., low residual reproductive value) and better quality males invested more resources in mating effort.

Parent age differentially influences offspring size over the course of development in Laysan albatross

AbstractOffspring growth and survival are predicted to be higher for older parents, due to a variety of mechanisms, such as increased breeding experience or greater investment favored by low residual reproductive value. Yet the extent to which parent age affects offspring viability is likely to vary between different aspects of growth and survival, perhaps being most pronounced at the most stressful stages of reproduction. We studied the link between parent age and nestling growth and survival in the Laysan albatross, a long‐lived seabird with a mean first breeding age of 8 years. Offspring of older parents were more likely to survive to fledging. Among those that did fledge, nestlings of older parents grew more rapidly. However, parent age did not influence the eventual asymptotic size that nestlings reached before fledging: fast‐growing nestlings of older parents reached 90% of asymptotic size roughly 1 week sooner, but slow‐growing nestlings of younger parents eventually caught up in size before fledging. Older parents bred c. 2 days earlier than younger parents, but hatch date did not explain observed variation in offspring success. The extent to which parent age accounted for variation in size of individual nestlings was not constant but peaked near the midpoint of development. This could reflect a time period when demands on parents reveal age‐based differences in parental quality. Overall, growth and survival of offspring increased with parent age in this species, even though the late age of first breeding potentially provides a 7‐year period for birds to hone their foraging skills or for selection to eliminate low‐quality individuals.

Flight distance and blood parasites in birds

Flight distance reflects the risk that an individual animal is willing to take when approached by a potential predator. Because residual reproductive value is the average number of offspring that an individual of a given age class is expected to produce after the current reproductive event, individuals with low residual reproductive value should take greater risks than the average individual to make them more likely to gain at least some reproductive success. Therefore, I predicted that individuals belonging to bird species with intense infections with virulent parasites to take greater risks than individuals of species with few or no virulent parasites. In a comparative study of mean flight distance of 133 different bird species, as estimated from the distance at which individuals fled when approached by a human, relative flight distance decreased with the number of blood parasite species and the prevalence of blood parasites, as expected if parasitism reduces residual reproductive value. Birds that take great risks in terms of reduced flight distance run elevated risks of mortality by predators that are allowed to approach potential prey. However, relative flight distance decreased independently for species richness and prevalence of blood parasites and for risk of predation due to the European sparrow hawk Accipiter nisus. These findings suggest that standardized measures of flight distance provide reliable information about risk taking by individuals, with important consequences for life history, parasitism, and risk of predation.

Does mass change of primiparous bighorn ewes reflect reproductive effort?

Reproductive effort during a female's first breeding attempt could affect subsequent fitness, particularly in species that reproduce before completing body growth. We analyzed 26 years of data on marked bighorn (Ovis canadensis) ewes to assess how variation in first reproductive effort affected other life-history traits. We measured reproductive effort as the residual of the regression of mass of primiparous ewes in late lactation on their mass 1 year earlier. Survival of the first-born lamb to weaning reduced maternal mass gain, suggesting a trade-off between reproduction and growth. Mass gain during the year of primiparity therefore appears to reflect reproductive effort. Lower mass gain was associated with lower adult mass and longevity, two important determinants of lifetime reproductive success. Reproductive effort at first parity therefore appears to lower residual reproductive value. Over their lifetime, females with low mass gain as primiparae produced proportionately more daughters than did females with high mass gain. Reproductive effort at first reproduction was not heritable, and may affect the evolutionary potential of adult mass and longevity, two fitness-related traits that are highly heritable in the study population.

Recruitment in White-Footed Mice (Peromyscus leucopus) as a Function of Litter Size, Parity, and Season

We explored the relationship between reproductive success and parity in white-footed mice. Because these small mammals are short-lived and have low residual reproductive value in the field, we predicted, contrary to laboratory results, that litter size, weaning rates, and recruitment would not increase as a function of female age or parity. We used data from 3 years of mark-and-recapture trapping data and from nest boxes to estimate weaning and recruitment rates in a 2-ha woodlot in northwest Ohio. Of 401 mice from 82 litters born in nest boxes, 87 were recruited into the population as adults. We observed no increase in litter size, weaning rates, or recruitment with maternal age or parity. Season interacted with parity such that recruitment from spring-born litters produced by females having their first or second litters was four times higher than from all other litters. Litter size did not influence weaning rates and only affected recruitment when season and parity also were considered.