Energetic Costs Of Reproduction Research Articles

Can attraction to and competition for high-quality habitats shape breeding propensity?

In many animal species, sexually mature individuals may skip breeding opportunities despite a likely negative impact on fitness. In spatio‐temporally heterogeneous environments, habitat selection theory predicts that individuals select habitats where fitness prospects are maximized. Individuals are attracted to high‐quality habitat patches where they compete for high‐quality breeding sites. Since failures in contests to secure a site may prevent individuals from breeding, we hypothesized that attraction to and competition for high‐quality habitats could shape breeding propensity.Under this hypothesis, we predicted the two following associations between breeding propensity and two key population features. (1) When mean habitat quality in the population increases in multiple patches such that availability of high‐quality sites increases across the population, the resulting decrease in competition should positively affect breeding propensity. (2) When the number of individuals increases in the population, the resulting increase in competitors should negatively affect breeding propensity (negative density dependence).Using long‐term data from kittiwakes Rissa tridactyla, we checked the prerequisite of prediction (1), that availability of high‐quality sites is positively associated with current mean habitat quality in the population (represented by breeding success). We then applied integrated population modelling to quantify annual fluctuations in population mean breeding success, breeding propensity and number of individuals by breeding status (pre‐breeders, breeders, skippers and immigrants), and tested our predictions.Our results showed that breeding propensity acts as an important driver of population growth. As expected, breeding propensity was positively associated with preceding mean habitat quality in the population, and negatively with the number of competitors. These relationships varied depending on breeding status, which likely reflects status dependence in competitive ability.These findings highlight the importance of competition for high‐quality breeding sites in shaping breeding propensity. Thereby, we draw attention towards alternative and complementary explanations to more standard considerations regarding the energetic cost of reproduction, and point to possible side effects of habitat selection behaviours on individual life histories and population dynamics.

Breeding behaviour of ectotherms at high latitudes: the case of the natterjack toad Epidalea calamita at its northern range limit

Abstract We explored the breeding behaviour of a threatened amphibian, the natterjack toad, at its northern range limit in Estonia, to determine the extent to which reproduction is affected by harsh and unstable climatic conditions. Using photo identification of specimens, we found that in optimal weather conditions males formed three breeding cohorts, while in adverse conditions only a single cohort occurred and under extreme conditions reproduction was skipped entirely. During the extended breeding season, larger males participated in reproduction throughout the breeding period, while smaller males appeared in later cohorts. Breeding success was related to the calling effort of a male, where larger males had greater mating success than smaller ones. We found that the natterjack toad males exhibit significant plasticity in reproductive behaviour at the northern range limit, which, given the energetic cost of reproduction and the increased risk of predation, allows them to increase their fitness at high latitudes.

Mitochondrial physiology varies with parity and body mass in the laboratory mouse (Mus musculus).

The life-history patterns that animals display are a product of their ability to maximize reproductive performance while concurrently balancing numerous metabolic demands. For example, the energetic costs of reproduction may reduce an animal's ability to support self-maintenance and longevity. In this work, we evaluated the impact of parity on mitochondrial physiology in laboratory mice. The theory of mitohormesis suggests that modest exposure to reactive oxygen species can improve performance, while high levels of exposure are damaging. Following this theory, we hypothesized that females that experienced one bout of reproduction (primiparous) would display improved mitochondrial capacity and reduced oxidative damage relative to non-reproductive (nulliparous) mice, while females that had four reproductive events (multiparous) would have lower mitochondrial performance and greater oxidative damage than both nulliparous and primiparous females. We observed that multiple reproductive events enhanced the mitochondrial respiratory capacity of liver mitochondria in females with high body mass. Four-bout females showed a positive relationship between body mass and mitochondrial capacity. In contrast, non-reproductive females showed a negative relationship between body mass and mitochondrial capacity and primiparous females had a slope that did not differ from zero. Other measured variables, too, were highly dependent on body mass, suggesting that a female's body condition has strong impacts on mitochondrial physiology. We also evaluated the relationship between how much females allocated to reproduction (cumulative mass of all young weaned) and mitochondrial function and oxidative stress in the multiparous females. We found that females that allocated more to reproduction had lower basal respiration (state 4), lower mitochondrial density, and higher protein oxidation in liver mitochondria than females that allocated less. These results suggest that, at least through their first four reproductive events, female laboratory mice may experience bioenergetic benefits from reproduction but only those females that allocated the most to reproduction appear to experience a potential cost of reproduction.

Marmots

Walter Arnold introduces the biology of marmots.

The Energetic Cost of Reproduction and Its Effect on Optimal Life-History Strategies.

Trade-offs in energy allocation between growth, reproduction, and survival are at the core of life-history theory. While age-specific mortality is considered to be the main determinant of the optimal allocation, some life-history strategies, such as delayed or skipped reproduction, may be better understood when also accounting for reproduction costs. Here, we present a two-pool indeterminate grower model that includes survival and energetic costs of reproduction. The energetic cost sets a minimum reserve required for reproduction, while the survival cost reflects increased mortality from low postreproductive body condition. Three life-history parameters determining age-dependent energy allocation to soma, reserve, and reproduction are optimized, and we show that the optimal strategies can reproduce realistic emergent growth trajectories, maturation ages, and reproductive outputs for fish. The model predicts maturation phase shifts along the gradient of condition-related mortality and shows that increased harvesting will select for earlier maturation and higher energy allocation to reproduction. However, since the energetic reproduction cost sets limits on how early an individual can mature, an increase in fitness at high harvesting can only be achieved by diverting most reserves into reproduction. The model presented here can improve predictions of life-history responses to environmental change and human impacts because key life-history traits such as maturation age and size, maximum body size, and size-specific fecundity emerge dynamically.

Reproductive Energetics of Female Mantled Howlers (Alouatta palliata)

The energetic costs of reproduction have an important influence on the life histories of female primates. At present, however, the interplay of female reproductive state, food availability, and strategies aimed at maintaining energy balance has been described for only a few species, limiting our ability to understand intra- and interspecific variation in female life histories. We assessed how female mantled howlers (Alouatta palliata) are affected by reproductive seasonality, and whether they alter their behavior to cope with the energetic demands of reproduction. From August 2013 to July 2015 we measured the reproductive state, behavior (1100 h of focal animal observations), and energetic condition (312 urine samples collected for C-peptide analysis) of 7 adult females, and assessed food availability (weekly phenological sampling of 397 food trees). Female behavior did not vary with reproductive state or reproductive seasonality. There were, however, differences in how females responded to variation in food availability according to reproductive state. Cycling and gestating females spent more time feeding than lactating females, and cycling females less time resting than females in other reproductive states, when food was more available. C-peptide concentrations were unaffected by either individual or overall variation in reproductive state, except for cycling females, whose concentrations increased during periods of high food availability. The energetic condition of female mantled howlers is broadly maintained over different stages of reproduction, but is sensitive to variation in food availability.

Factors influencing survival and productivity of pronghorn in a semiarid grass-woodland in east-central New Mexico

Pronghorns (Antilocapra americana) are an important source of revenue and recreation for property managers throughout New Mexico, but have been declining in number. We documented body condition, survival, production of fawns, and trends in population size of pronghorns on the Corona Range and Livestock Research Center (CRLRC), a working research ranch and wildlife enterprise located in east-central New Mexico, from 2006 through 2011. Accrual of all indices of condition and size of both adult female and adult male pronghorns was positively associated with precipitation during June to July, August to September, and annually. Annual survival rates of females (0.33 to 0.78) and males (0.63 to 0.89) were highly variable on CRLRC. Survival of individuals was not related to any measure of condition or size taken the prior autumn. Survival of adult females was related to reproductive status the previous year; females that had successfully weaned >1 fawn the previous year were 0.11 times less likely to survive. Malnutrition was the most common cause of mortality (nine of 22 females; seven of 15 males), followed by suspected plant toxicities and enterotoxaemia (nine of 22 females) and harvest (six of 15 males). Most adult female mortality (73%) occurred after parturition and prior to weaning when energy demands are greatest on adult females; females that successfully weaned >1 fawn accrued significantly less condition by autumn. Survival of fawns was related to maternal condition, and fawn:adult female ratios were positively correlated with cumulative precipitation during late gestation and parturition. Low survival of adult females and fawns has resulted in the CRLRC pronghorn population declining from a minimum of 136 individuals to 66 from 2005 to 2011. Timing and causes of mortality highlight a strong nutritional limitation faced by lactating females related to the most energetic costs of reproduction being borne prior to the onset of summer monsoonal precipitation. The poor timing of reproduction to precipitation (and, thus, to forage phenology) in the southwestern United States will likely always limit productivity and survival of pronghorn relative to northern populations.

Mind the wind: microclimate effects on incubation effort of an arctic seabird.

The energetic costs of reproduction in birds strongly depend on the climate experienced during incubation. Climate change and increasing frequency of extreme weather events may severely affect these costs, especially for species incubating in extreme environments. In this 3‐year study, we used an experimental approach to investigate the effects of microclimate and nest shelter on the incubation effort of female common eiders (Somateria mollissima) in a wild Arctic population. We added artificial shelters to a random selection of nesting females, and compared incubation effort, measured as body mass loss during incubation, between females with and without shelter. Nonsheltered females had a higher incubation effort than females with artificial shelters. In nonsheltered females, higher wind speeds increased the incubation effort, while artificially sheltered females experienced no effect of wind. Although increasing ambient temperatures tended to decrease incubation effort, this effect was negligible in the absence of wind. Humidity had no marked effect on incubation effort. This study clearly displays the direct effect of a climatic variable on an important aspect of avian life‐history. By showing that increasing wind speed counteracts the energetic benefits of a rising ambient temperature, we were able to demonstrate that a climatic variable other than temperature may also affect wild populations and need to be taken into account when predicting the effects of climate change.

Sexual Dimorphisms in Metabolism, Organ Mass, and Reproductive Energetics in Pre-breeding American Toads (Anaxyrus americanus)

Sexual size dimorphisms are common in many species of anurans, and have often been ascribed to different selective forces that influence reproductive success in males and females. However, less is known about dimorphisms in whole-organism physiology or in internal morphology in anurans. In this study, we investigated potential differences in metabolism, visceral organ mass, and stored energy content between male and female American Toads (Anaxyrus americanus) collected en route to breeding areas during the spring. Female toads were both longer and more massive than males. Males demonstrated larger increases in metabolic rate, heart mass, liver mass, and nonpolar lipid content with increasing body size than did females, but kidney mass did not differ between the sexes. The ovaries of the females represented, on average, 38% of the total dry mass and 54% of the total caloric energy contained in their bodies. However, the body-size adjusted caloric content of the carcass did not differ between males and females. Our findings suggest that larger males are physiologically able to support greater levels of activity during the breeding season and thus will more likely engage in more strenuous activities such as calling, active seeking of females, and amplexus interference, compared to smaller males. Large females, on the other hand, appear to preferentially allocate resources to oogenesis. In addition, our findings suggest that although the overall energetic cost of reproduction may be greater for females, there may be other energetic constraints within or outside of the reproductive period that limit the ability of males to allocate resources to growth and storage.

Geographic and seasonal variation analysis of digestive morphology in the catfish Iheringichthys labrosus along lower Río Uruguay

The study of geographic variation of individual traits is an important component of evolutionary research, in that individual morphological features can be subjected to multiple selective pressures. The present work is aimed to analyze the geographic and seasonal varia- tion in several digestive traits in Iheringichthys labrosus along three localities in the lower Rio Uruguay. Statistically significant differences among locations and between seasons were found for all the variables assessed, the most noticeable of differences being observed were intestinal length, intestine weight, and liver weight. In part, these differences could be an adaptive response to changes in food availability and/or in the energetic costs of reproduction. Results obtained herein also suggest that individuals of this species spend enough time in each locality as to show

Life-history strategies of North American elk: trade-offs associated with reproduction and survival

The principle of energy allocation states that individuals should attempt to maximize fitness by allocating resources optimally among growth, maintenance, and reproduction. Such allocation may result in trade-offs between survival and reproduction, or between current and future reproduction. We used a marked population of North American elk (Cervus elaphus) to determine how energetic costs of reproduction in the current year affect survival and reproduction in the subsequent year. Using a multistate mark–recapture model we examined the influence of individual and environmental variation on trade-offs between these 2 life-history traits. We observed no difference in survival probabilities between pregnant and nonpregnant individuals or as a function of recruiting an offspring. Nonetheless, there was a negative effect of recruiting an offspring in the current year on becoming pregnant the following year. Increased body condition, and higher precipitation, contributed to greater probabilities of becoming pregnant in a particular year regardless of reproductive state and previous recruitment. Costs associated with reproduction led to a reduced probability of future reproduction rather than a reduction in survival. These findings are consistent with risk-sensitive reproductive allocation, where adult survival is maintained through variation in reproductive effort resulting in high and stable adult survival and more-variable reproduction.

Structural and Performance Costs of Reproduction in a Pure Capital Breeder, the Children’s PythonAntaresia childreni

Females often manage the high energy demands associated with reproduction by accumulating and storing energy in the form of fat before initiating their reproductive effort. However, fat stores cannot satisfy all reproductive resource demands, which include considerable investment of amino acids (e.g., for the production of yolk proteins or gluconeogenesis). Because capital breeders generally do not eat during reproduction, these amino acids must come from internal resources, typically muscle proteins. Although the energetic costs of reproduction have been fairly well studied, there are limited data on structural and performance costs associated with the muscle degradation required to meet amino acid demands. Thus, we examined structural changes (epaxial muscle width) and performance costs (constriction and strength) over the course of reproduction in a pure capital breeder, the children's python (Antaresia childreni). We found that both egg production (i.e., direct resource allocation) and maternal care (egg brooding) induce muscle catabolism and affect performance of the female. Although epaxial muscle loss was minimal in nonreproductive females, it reached up to 22% (in females after oviposition) and 34% (in females after brooding) of initial muscle width. Interestingly, we found that individuals with higher initial muscular condition allocated more of their muscle into reproduction. The amount of muscle loss was significantly linked to clutch mass, underscoring the role of structural protein in egg production. Egg brooding significantly increased proteolysis and epaxial loss despite no direct allocation to the offspring. Muscle loss was linked to a significant reduction in performance in postreproductive females. Overall, these results demonstrate that capital-breeding females experience dramatic costs that consume structural resources and jeopardize performance.

The energetics of oviparous reproduction in the African Brown House Snake

The energetic cost of reproduction in the oviparous snake, Lamprophis fuliginosus (African Brown House Snake) was compared to other elevated metabolic states, specifically exhaustive activity and digestion. To determine gravidity, female snakes were imaged with a portable ultrasound (CTS‐3300, SIUI America, Inc.). Oxygen consumption was determined using flow through respirometry with carbon dioxide and oxygen sensors (Sable Systems International & AEI Technologies, Inc.). Results indicate that female L. fuliginosus exhibit a significant 29.6% (P=.0310) increase in standard metabolic rate while gravid. An additive effect of gravidity in female snakes during digestion and/or activity could not be measured. Compared to the metabolic cost of exhaustive activity (scope = 4.3; P<.00100) or digestion (scope = 6.70; P=.00100), gravidity (scope = 1.30; P=.0310) is significantly less energetically expensive. Furthermore, our data demonstrate that gravidity does not have a significant influence on time to exhaustion during exhaustive activity (mean = 28.6 minutes P=.400), or the time to peak digestive peak oxygen consumption (mean = 41.7 hours; P=.260). Digestion and activity are inevitable stresses a gravid female must endure. The potentially vulnerable time periods between ingestion and peak oxygen consumption during a meal, and the time it takes for a female to become exhausted during activity are not altered during gravidity. Besides a modest gravid metabolic scope of 1.30, our research has not identified any additional energetic physiological constraints. These results may have significant fitness implications for this species, which we plan to examine further in subsequent studies. Funding for this research was provided by NSF grant IOS 0922756 to JWH.

Behavioral and physiological flexibility are used by birds to manage energy and support investment in the early stages of reproduction

Abstract Interest in phenotypic flexibility has increased dramatically over the last decade, but flexibility during reproduction has received relatively little attention from avian scientists, despite its possible impact on fitness. Because most avian species maintain atrophied reproductive organs when not active, reproduction in birds requires major tissue remodeling in preparation for breeding. Females undergo rapid (days) recrudescence and regression of their reproductive organs at each breeding attempt, while males grow their organs ahead of time at a much slower rate (weeks) and may maintain them at maximal size throughout the breeding season. Reproduction is associated with significant metabolic costs. Egg production leads to a 22%-27% increase in resting metabolic rate (RMR) over non-reproductive values. This is partly due to the activity of the oviduct, an organ that may allow females to adjust reproductive investment by modulating egg size and quality. In males, gonadal recrudescence may lead to a 30% increase in RMR, but the data are inconsistent and general conclusions regarding energetic costs of reproduction in males will require more research. Recent studies on captive female zebra finches describe the impacts of these costs on daily energy budgets and highlight the strategies used by birds to maintain their investment in reproduction when energy is limited. Whenever possible, birds use behavioral flexibility as a first means of saving energy. Decreasing locomotor activity saves energy during challenges such as egg production or exposure to cold temperatures and is an efficient way to buffer variation in individual daily energy budgets. However, when behavioral flexibility is not possible, birds must rely on flexibility at the physiological level to meet energy demands. In zebra finches breeding in the cold, this results in a reduced pace of laying, likely due to down-regulation of both reproductive and non-reproductive function, allowing females to defend minimal egg size and maintain reproductive success. More research involving a range of species in captive and free-living conditions is needed to determine how phenotypic flexibility during tissue remodeling and early reproductive investment translates to natural conditions and affects fitness.

Reproductive energetics in free-living female chimpanzees (Pan troglodytes schweinfurthii)

Mammalian females generally carry the bulk of reproductive costs. They gestate for relatively long periods of time and provide the majority of parental care for dependent offspring. For this reason, many studies have examined how females deal with the energetic costs of reproduction. Here, we examine the influence of reproductive state on activity budgets, diet quality, and sociality in free-living female chimpanzees (Pan troglodytes) at Gombe National Park, Tanzania. After controlling for dominance rank, we found that pregnant and lactating females consumed higher quality foods than nonpregnant, nonlactating females. However, pregnant females also traveled less. This result did not reflect differences in sociality, as the pregnant female group sizes included in our analyses were comparable to those in other reproductive categories.

Energetic costs of reproduction in female northern muriquis, Brachyteles hypoxanthus (Primates: Platyrrinhi: Atelidae)

Infant care is known to impose high energetic costs on female primates because in addition to lactation, most primate mothers also provide transport for their offspring. Many studies have documented the high energetic costs of lactation, but less is known about energetic costs of infant carrying and their effects on the recovery of maternal physical condition. We compared the activities of female northern muriquis (Brachyteles hypoxanthus Kuhl, 1820) over a 12-month period at the RPPN Feliciano Miguel Abdala, Minas Gerais, Brazil to investigate whether mothers during their weaning year behaved differently than mothers in their post-weaning year, when they resumed reproductive cycling and copulating, and conceived again. We found no significant differences in the behavioral activity budgets of mothers in their weaning year (n = 4) versus post-weaning year (n = 5), despite the significantly higher proportion of time that mothers in their weaning year spent in close proximity with their infants and carrying their infants compared to mothers in their post-weaning year. We suggest that the energy budgets of weaning are similar to those of post-weaning in female northern muriquis.

Seasonality and Sex Differences in Travel Distance and Resource Transport in Venezuelan Foragers

The anthropological literature generally describes forager women as less mobile than men because of their child-care responsibilities and the energetic costs of reproduction. Examination of resource transport among the savanna Pumé of southwestern Venezuela reveals, in contrast, that for certain food resources travel distances and resource weights relative to body weights are greater for women than for men. Male foraging is often associated with greater travel distances, but men frequently walk unencumbered because hunting trips may exhibit low or zero food returns and hunters usually carry only a minimum tool kit. Women, who target highly predictable foods that can be collected in large quantities, frequently carry firewood, tools, and large baskets of food for extended distances during gathering. It appears that the consistent and large returns of female foraging underwrite the large energetic effort of men's hunting.

A test of the reproductive cost hypothesis for sexual size dimorphism in Yarrow's spiny lizard Sceloporus jarrovii

1. Trade-offs between reproduction and growth are central assumptions of life-history theory, but their implications for sexual size dimorphism (SSD) are poorly understood. 2. Adult male Yarrow's spiny lizards Sceloporus jarrovii average 10% larger than adult females. In a low-altitude (1700 m) population, this SSD develops because males grow more quickly than females during the first year of life, particularly during the first female reproductive season. This study tests the hypothesis that SSD develops because female growth is constrained by energetic costs of reproduction. 3. To test for a growth cost of reproduction, I compared growth rates of free-living females that differed, either naturally or experimentally, in reproductive status. Females that naturally delayed reproduction until their second year grew more quickly than females that reproduced as yearlings, and ovariectomized yearlings grew more quickly and to larger sizes than reproductive controls. 4. To determine whether SSD develops in the absence of this inferred reproductive cost, I also studied a high-altitude (2500 m) population in which all females delay reproduction until their second year. Sex differences in growth trajectories were similar to those observed at low altitude, such that males averaged 10% larger than females even prior to female reproduction. 5. Although female growth may be constrained by reproduction, multiple lines of evidence indicate that this cost is insufficient to explain the full magnitude of SSD in S. jarrovii. First, differences in growth of reproductive and nonreproductive females are not observed until the final month of gestation, by which time SSD is already well developed. Second, the growth benefit accruing from experimental inhibition of reproduction accounts for only 32% of the natural sex difference in body size. Finally, SSD develops well in advance of female reproduction in a high-altitude population with delayed maturation.

The energy costs of sexual dimorphism in mole-rats are morphological not behavioural

Different reproductive strategies of males and females may lead to the evolution of differences in their energetic costs of reproduction, overall energetic requirements and physiological performances. Sexual dimorphism is often associated with costly behaviours (e.g. large males might have a competitive advantage in fighting, which is energetically expensive). However, few studies of mammals have directly compared the energy costs of reproductive activities between sexes. We compared the daily energy expenditure (DEE) and resting metabolic rate (RMR) of males and females of two species of mole-rat, Bathyergus janetta and Georychus capensis (the former is sexually dimorphic in body size and the latter is not) during a period of intense digging when males seek females. We hypothesized that large body size might be indicative of greater digging or fighting capabilities, and hence greater mass-independent DEE values in males of the sexually dimorphic species. In contrast to this prediction, although absolute values of DEE were greater in B. janetta males, mass-independent values were not. No differences were apparent between sexes in G. capensis. By comparison, although RMR values were greater in B. janetta than G. capensis, no differences were apparent between the sexes for either species. The energy cost of dimorphism is most likely to be the cost of maintenance of a large body size, and not the cost of behaviours performed when an individual is large.

Sexual abstinence and the cost of reproduction in adult male water snakes, Nerodia sipedon

Low frequency of reproduction among iteroparous organisms is most often observed among female ectothermic vertebrates and is thought to be a strategy used to defer reproductive costs. We assessed reproductive costs of male water snakes (Nerodia sipedon) to determine why half of adult males abstain from reproduction each year. There was no evidence of a short‐term energetic cost of reproduction. Change in mass did not differ between reproductive and non‐reproductive males during the one‐month mating season or during the entire four‐month activity season. Changes in mass of reproductive males were similar at two sites in which the spatial distribution of females differed. However, there were size‐specific differences in growth and survival between reproductive and non‐reproductive males. Among reproductive males growth rate decreased with body size at a lower rate than among non‐reproductive males. Survival increased with body size for reproductive males, but decreased with body size among non‐reproductive males. Most of the differential survival between reproductive and non‐reproductive males did not occur during the mating season but rather during hibernation. Size‐related differences between reproductive and non‐reproductive males may reflect selection having eliminated low quality males from the larger size classes. Overall our results appear most consistent with there being high variance in male quality, such that the best males can bear the cost of reproducing and still grow and survive as well or better than low quality males that abstain from reproduction.