Survival costs of reproduction are mediated by parasite infection in wild Soay sheep

A trade‐off between current and future fitness potentially explains variation in life‐history strategies. A proposed mechanism behind this is parasite‐mediated reproductive costs: individuals that allocate more resources to reproduction have fewer to allocate to defence against parasites, reducing future fitness. We examined how reproduction influenced faecal egg counts (FEC) of strongyle nematodes using data collected between 1989 and 2008 from a wild population of Soay sheep in the St. Kilda archipelago, Scotland (741 individuals). Increased reproduction was associated with increased FEC during the lambing season: females that gave birth, and particularly those that weaned a lamb, had higher FEC than females that failed to reproduce. Structural equation modelling revealed future reproductive costs: a positive effect of reproduction on spring FEC and a negative effect on summer body weight were negatively associated with overwinter survival. Overall, we provide evidence that parasite resistance and body weight are important mediators of survival costs of reproduction.     

Relationships among fecal lungworm loads, fecal glucocorticoid metabolites, and lamb recruitment in free-ranging Rocky Mountain bighorn sheep

Most wild Rocky Mountain big-horn sheep (Ovis canadensis canadensis) in northern latitudes are infected with lungworms. Indirect effects of lungworms on bighorn sheep are unknown, but high pulmonary burdens might increase stress (i.e., elevated glucocorticoid levels), and chronic stress could in turn decrease fitness. We hypothesized that high lungworm burdens in Rocky Mountain bighorn ewes increase stress, thereby increasing lamb mortality. To test our hypothesis, one subherd of bighorn sheep in Custer State Park, South Dakota was provided a free-choice loose mineral mix containing the anthelmintic fenbendazole every six weeks from March 1999 to August 2000 to eliminate lungworms; another subherd served as the control. Daily, individually marked ewes were located telemetrically from the ground and uniquely marked animals were observed until they defecated. After the herd moved from the area, fecal samples were collected and stored at -23 C. A consistent number of samples per season per herd (x-=16.56+/-3.99 samples) were collected. Fecal larval lungworm levels (LPG) in the treatment subherd were lower than levels in the control subherd; however, there was no difference in fecal glucocorticoid metabolite (FGM) levels between the two subherds. Fecal glucocorticoid metabolite levels varied by season in both subherds, with levels in winter lower than during the other three seasons. Lamb:ewe ratios were not different between the control and treatment subherds at the end of summer 1999. In contrast, the treatment group had a lower lamb:ewe ratio at the end of summer 2000 despite having lower LPG. However, this result was attributed to lower ewe production, not lower lamb survival. The LPG levels were not correlated with FGM concentrations; instead, FGM levels might reflect normal seasonal patterns. Other factors, including contagious ecthyma, were more important for determining lamb mortality than LPG and FGM levels during our study. We suggest further experimental work over a longer duration to address these relationships.     

Parasitism and alternative reproductive tactics in Northern chamois

Alternative reproductive tactics (ARTs), discrete phenotypic variations evolved to maximize fitness, may entail different cost‐benefit trade‐offs. In large mammals, differences in costs associated with ARTs—including energy expenditure and parasite infection—are typically greatest during the breeding season. Nonetheless, physiological and behavioral differences between ARTs can manifest throughout the year, possibly involving costs that may contribute to maintain ARTs within populations. Using the number of nematode larvae per gram of feces (LPG) as a proxy, we explored the temporal changes in lung parasite infection in territorial and nonterritorial male chamois Rupicapra in the Gran Paradiso National Park (Italy), between 2011 and 2012. We aimed to identify which tactic‐specific physiological and behavioral features (including age, hormonal levels, inter‐ and intrasexual interactions, and space use) or climatic factors (temperature and precipitation) best explained yearly variation in parasite infection within and between ARTs. Generalized additive mixed models showed that the fecal larval counts of lung nematodes underwent strong temporal changes in both male types. Differences between ARTs (with higher LPG values in territorial than nonterritorial males) were greatest during the rut and—to a lesser extent—in spring, respectively, at the peak and at the onset of territoriality. The difference in LPG between tactics was largely explained by the greater levels of hormone metabolites in territorial males during the rut. The other variables did not contribute significantly to explain the different shedding of larvae within and between ARTs. Our analysis suggests that different values of LPG between territorial and nonterritorial males are largely a result of tactic‐specific differences in the secretion of hormone metabolites, but only during the rut. To clarify whether rut‐related parasitism contributes to the maintenance of ARTs, tactic‐specific life history trade‐offs, for example, between reproduction and parasite‐related mortality, must be investigated.     

Ecology of gastropod and bighorn sheep hosts of lungworm on isolated, semiarid mountain ranges in Utah, USA

Isolated, nonmigratory populations of bighorn sheep (Ovis canadensis) may experience high exposure to lungworms (Protostrongylus spp.) through a build-up of fecal material. However, semiarid climates may hinder lungworm transmission by limiting terrestrial gastropods, the intermediate hosts. We assessed potential for lungworm transmission, documented occurrence of transmission, and identified habitat types where transmission was likely to occur on ranges of two recently introduced populations of bighorn sheep in northern Utah. Gastropods were collected weekly on Antelope Island and the Newfoundland Mountains, May-August 2001-02, from each of the four major habitat types (riparian, rock, desert shrub, and grass). Distribution of 113 bighorn sheep groups was observed, and 421 fecal pellet groups were collected to estimate lungworm levels. A total of 1,595 gastropods representing five genera were collected from both ranges. Vallonia made up 85% of all gastropods collected. Of 980 gastropods collected on Antelope Island in 2002, only Vallonia were found infected with protostrongylid-type larvae (10 of 980=1%). Lungworm prevalence in bighorn fecal samples was 97% on Antelope Island and 90% on the Newfoundland Mountains. Lungworm prevalence in lambs indicated lungworm transmission was occurring on Antelope Island. Lungworm transmission was likely occurring in riparian habitat due to abundant gastropods, presence of infected gastropods, and reliance by bighorn sheep on few water sources. Differences in spatial distribution between ram and nursery groups may partly explain higher fecal larvae counts in nursery than in ram groups. We suggest lungworm levels in bighorn sheep on semiarid ranges may increase in dry years as bighorn sheep concentrate use on fewer perennial water sources.     

Determinants and consequences of age of primiparity in bighorn ewes

Because variation in age of first reproduction can have major effects on individual fitness and population dynamics, it is important to understand what maintains that variability. Although early primiparity is assumed to be costly, it is sometimes associated with high lifetime reproductive success. We used a long‐term study on bighorn sheep Ovis canadensis to determine what variables affect age at first reproduction, investigate the impact of primiparity on body resources and quantify the reproductive performance of primiparous ewes. We then examined the consequences of delayed primiparity on adult body mass, longevity and lifetime reproductive success. Environmental conditions during early development, body mass as a yearling, genotype and maternal effects affected age of primiparity. Primiparous ewes lost more mass in winter and gained less mass in summer than multiparous ewes. Small yearling ewes that postponed reproduction attained similar adult mass than heavy yearling ewes who reproduced at a younger age. Early primiparity did not reduce longevity and was positively associated with lifetime reproductive success. Starting to reproduce as soon as possible appears to maximize fitness of females. When early life conditions are unfavorable, however, delayed primiparity allows greater body growth and likely maximizes survival. The combination of a conservative reproductive strategy and maternal effects on age of primiparity may partly delay population recovery following density‐dependent declines.     

Individual variation in reproductive costs of reproduction: high-quality females always do better

1. Although life-history theory predicts substantial costs of reproduction, individuals often show positive correlations among life-history traits, rather than trade-offs. The apparent absence of reproductive costs may result from heterogeneity in individual quality. 2. Using detailed longitudinal data from three contrasted ungulate populations (mountain goats, Oreamnos americanus; bighorn sheep, Ovis canadensis; and roe deer, Capreolus capreolus), we assessed how individual quality affects the probability of detecting a cost of current reproduction on future reproduction for females. We used a composite measure of individual quality based on variations in longevity (all species), success in the last breeding opportunity before death (goats and sheep), adult mass (all species), and social rank (goats only). 3. In all species, high-quality females consistently had a higher probability of reproduction, irrespective of previous reproductive status. In mountain goats, we detected a cost of reproduction only after accounting for differences in individual quality. Only low-quality female goats were less likely to reproduce following years of breeding than of nonbreeding. Offspring survival was lower in bighorn ewes following years of successful breeding than after years when no lamb was produced, but only for low-quality females, suggesting that a cost of reproduction only occurred for low-quality females. 4. Because costs of reproduction differ among females, studies of life-history evolution must account for heterogeneity in individual quality.     

Muellerius capillaris (Mueller, 1889) (Nematoda: Protostrongylidae): an unusual finding in Rocky Mountain bighorn sheep (Ovis canadensis canadensis Shaw) in South Dakota

Lungs and fecal samples from nine hunter-killed Rocky Mountain bighorn sheep were examined for lungworms. All samples contained adults and/or larvae of Muellerius capillaris (Mueller, 1889). Protostrongylus spp., the lungworms commonly reported from bighorn sheep, were not present in any samples. Larvae of M. capillaris bear a spine on the dorsal side of the posterior end and are shorter than dorsal-spined larvae of other lungworms recorded from North American ungulates. Larvae similar in shape but longer than those of Muellerius were found in free-ranging bighorn sheep in Alberta and British Columbia. In addition, dorsal-spined larvae have been found in bighorn sheep in Montana, North Dakota, and Washington. The identity of the dorsal-spined larvae is known only from sheep in South Dakota. Thus, caution must be taken when diagnosing lungworm infections in Rocky Mountain bighorn sheep.     

Mass- and density-dependent reproductive success and reproductive costs in a capital breeder

For capital breeders, mass may affect reproductive potential. Reproductive expenditure may reduce future reproductive potential, particularly when resources are scarce. To test the hypothesis that reproductive success and the costs of reproduction vary according to mass and population density, we analyzed 25 yr of data on bighorn ewes (Ovis canadensis). The number of adult females was first limited by yearly removals, then allowed to triple. We found no survival costs of reproduction for ewes aged 4-7 yr. For ewes aged 8-14 yr, survival was density dependent for barren ewes but not for ewes that weaned lambs. Failure to lamb was rare and negatively correlated with fertility the following year. At low population density, lactation had a negative effect on mass gain but had a limited reproductive cost. At high density, heavy ewes had higher reproductive success than light ewes, and the reproductive cost and somatic costs of reproduction increased. The cost of reproduction was greater for light than for heavy ewes. Survival of weaned lambs to 1 yr was affected by population density but not by maternal mass or previous reproductive success. In large mammals, manipulations of reproductive effort are problematic, but long-term monitoring of individual mass and reproductive success under varying conditions of resource availability can provide insights into the evolution of life histories.     

Mass‐dependent reproductive strategies in wild bighorn ewes: a quantitative genetic approach

In the Ram Mountain bighorn sheep (Ovis canadensis) population, ewes differing by more than 30% in body mass weaned lambs with an average mass difference of only 3%. Variability in adult body mass was partly due to additive genetic effects, but inheritance of weaning mass was weak. Maternal effects could obscure genetic effects in the phenotypic expression of weaning mass, particularly if they reflected strategies of maternal expenditure that varied according to ewe mass. We performed a quantitative genetic analysis to assess genetic and environmental influences on ewe mass and on maternal expenditure. We used the mean daughters/mother regression method and Derivative Free Restricted Maximum Likelihood models to estimate heritability (h²) of ewe mass and indices of maternal expenditure. We found additive genetic effects on phenotypic variation in maternal mass, in lamb mass at weaning (absolute maternal expenditure) and in weaning mass relative to maternal mass at weaning (relative maternal expenditure). Heritability suggests that maternal expenditure has the potential to evolve. The genetic correlation of ewe mass and absolute maternal expenditure was weak, while ewe mass and relative maternal expenditure were strongly negatively correlated. These results suggest additive genetic effects on mass‐dependent reproductive strategies in bighorn ewes. Mass‐dependent reproductive strategies could affect lamb survival and phenotypic variation in adult mass. As population density increased and reproduction became costlier, small females reduced maternal expenditure more than large females. Constraints on reproductive strategy imposed by variations in resource availability are therefore likely to differ according to ewe mass. A general trend for a decrease in maternal expenditure relative to maternal size in mammals suggests that size‐dependent negative maternal effects may be common.     

Decreased reproductive investment of female threespine stickleback Gasterosteus aculeatus infected with the cestode Schistocephalus solidus: parasite adaptation,host adaptation,or side effect?

Parasitic infections may cause alterations in host life history, including changes in reproductive investment (absolute amount of energy allocated to reproduction) and reproductive effort (proportion of available energy allocated to reproduction). Such changes in host life history may reflect: 1) a parasite tactic: the parasite adaptively manipulates energy flow within the host so that the host is induced to make a reduction in reproductive effort and reproductive investment, making more energy available to the parasite; 2) no tactic: there is no change in host reproductive effort and reproductive investment simply decreases as a side effect of the parasite depleting host energy stores; 3) a host tactic: the host adaptively increases reproductive effort in the face of infection and loss of body condition, reproductive investment possibly being reduced despite the increased reproductive effort. Females in Alaskan lake populations of threespine sticklebacks ( Gasterosteus aculeatus ) are capable of clutch production when parasitized by the cestode Schistocephalus solidus despite large relative parasite masses. We analyzed the somatic energy reserves, maturation stage and ovarian mass of female sticklebacks collected from an Alaska lake during a single reproductive season. We found that parasitized females were less likely to carry fully-matured gametes, had smaller ovarian masses, and had lower somatic energy stores than unparasitized females. The relationship between reproductive investment and energy storage did not differ between parasitized and unparasitized females. Thus, reproductive effort did not change in response to parasitic infection. We conclude there was no indication of either a parasite tactic or a host tactic. Simple nutrient theft is involved in the parasite's influence on host reproduction, consistent with an earlier hypothesis that reproductive curtailment in threespine sticklebacks is a side effect.     

Condition-dependent reproductive success in bighorn ewes

Individual bighorn ewes ( Ovis canadensis ) at 4–14 years of age were 1.5% heavier preceding years when they weaned a lamb than preceding years when their lamb died before weaning. Intra-individual differences in mass between years of successful and unsuccessful reproduction appeared independent of a ewe's multiyear average mass. Relative mass loss both in the winter before and in the winter after a given repro-ductive episode increased with reproductive success. Long-term monitoring of individual mass and reproductive success is a promising technique to study life histories in capital breeders, because it allows to partially account for differences in reproductive potential.     

Reproductive costs of sons and daughters in Rocky Mountain bighorn sheep

Differential maternal investment theory predicts that in sexuallydimorphic and polygynous species mothers should invest morein sons than in daughters. We tested the hypothesis that bighornewes that raise sons incur greater reproductive costs than ewesthat raise daughters. Although ewe mass gain during lactationand subsequent winter body mass loss were independent of lambsex, lambs born the year following the weaning of a son hadlower survival than lambs born after a daughter. The effectsof lamb sex on subsequent reproductive success of ewes becamemore evident at high population density. Lamb sex did not affectmaternal survival. Population density, weather, and ewe agedid not alter the relationship between lamb sex and subsequentreproductive success of the ewe. The year after weaning a son,ewes were more likely to have a daughter than a son, while ewesthat had previously weaned a daughter had similar numbers ofsons and daughters. Our results show that for bighorn sheepewes, sons have a greater life-history cost than daughters,suggesting a differential maternal investment in the sexes.     

Social status in female bighorn sheep (Ovis canadensis): expression, development and reproductive correlates

Female bighorn sheep were studied over a 27-month period to quantify linearity and stability of social rank; expression of behaviour as a function of rank; development of rank relationships; and reproductive correlates of rank. Females exhibited a stable, non-linear hierarchy that correlated strongly with age. Dominant females used proportionally more threats, whereas subordinates used more subordinance patterns. Females integrated into the hierarchy at1–2 years of age and then fought their way to high social status. Dominant and subordinate females did not differ in pre-natal maternal investment, but dominant females nursed lambs at higher rates, and were more likely than subordinates to nurse alien lambs after their own lamb died.     

Maternal condition and offspring sex ratio in polygynous ungulates: a case study of bighorn sheep

The Trivers and Willard model (TWM) predicts that for sexuallydimorphic polygynous mammals, mothers able to provide a highlevel of care should bias offspring sex ratio in favor of sons.Contradictory results of empirical studies, however, suggestthat selective pressures for adaptive offspring sex ratio varywith species and environmental conditions. We report the resultsof a 29-year study of marked bighorn sheep (Ovis canadensis)in a population that underwent wide changes in density and wheremost females were weighed each year. Lamb sex ratio was independentof absolute ewe mass and yearly deviations from individual orpopulation average mass, but there was a nonsignificant trendtowards fewer males being born at high population density. Bighornsheep satisfy all the assumptions of the TWM but not its prediction:lamb sex ratio is independent of maternal ability to providecare. Recent hypotheses to explain the lack of relationshipbetween maternal condition and offspring sex in ungulates areunlikely to apply to bighorn sheep. We suggest that the TWMmay only apply when social rank strongly affects the abilityto provide maternal care. Those circumstances are likely tooccur for only a few species and within a narrow range of environmentalconditions.     

Early development, adult mass, and reproductive success in bighorn sheep

Despite considerable empirical and theoretical work on the individualand population consequences of early development, little isknown about the correlations between early mass and adult sizeor lifetime reproductive success of free-ranging mammals. Usinga 26-year study of bighorn sheep (Ovis canadensis), we examinedhow mass as a lamb and mass gain as a yearling affected adultmass for both sexes, horn length of males and lifetime reproductivesuccess of females at different population densities. Mass asa 3-week-old lamb was either weakly or not correlated withadult mass, horn length of adult males, or the number of lambsweaned over a ewe's lifetime. Weaning mass was correlated withmost of these variables when the number of ewes in the populationwas taken into account. When weaning mass was controlled throughpartial correlation, mass as a yearling was correlated with adult mass of ewes but not with ewe reproductive success orwith adult mass or horn length of rams. Lamb mass and numberof ewes explained more of the variance in adult characteristicsfor males than for females. Our results suggest that mass gainduring lactation, possibly but not necessarily related to theamount of maternal care received, affects adult mass and reproductive success. Females appear better able than males to compensatefor poor early development, likely by postponing their firstreproduction. Mass gain over several years and the number ofewes in the population strongly affect adult mass of both sexesand therefore can have profound effects on reproductive successof this long-lived species with a multi-year growth period.     

No adaptation of Haemonchus contortus to genetically resistant sheep.

A composite population of Haemonchus contortus was established with larvae from seven diverse sources, then maintained in Merino sheep bred to have either increased or decreased resistance to Haemonchus. After five, seven and 14 parasite generations, the two resulting lines of parasites were used to infect sheep from the increased resistance line, an unselected control line and the decreased resistance line. Line of sheep had a highly significant effect on average faecal egg counts 4 and 5 weeks after infection (geometric means 329, 735 and 1490 epg, respectively after the 14th generation), but the two lines of parasites yielded similar egg counts. There was no significant interaction between line of sheep and line of parasite, indicating that the parasite populations had not diverged significantly in their reproductive fitness, as measured by faecal egg count.     

Rut-Induced Hypophagia in Male Bighorn Sheep and Mountain Goats: Foraging Under Time Budget Constraints

In polygynous ungulates, the rut imposes constraints on male time budgets that generate a trade‐off between maintenance and reproduction, leading to a reduction in time spent foraging. As mating activities can incur substantial somatic costs, males are expected to spend their ‘non‐rutting’ time recovering during the breeding season. If the diminution in time allocated to foraging by males is only a consequence of time budget constraints, males should keep a similar ratio of time spent foraging to lying to that observed in the pre‐rut, leading to an overall reduction of these two activities (the ‘foraging constraint’ hypothesis). Alternatively, if males adopt an energy‐saving strategy, they should limit energy expenditures by reducing foraging but not lying time, as the energy gains of forage intake may not meet the basal energetic requirements, especially in northern and temperate regions (the ‘energy‐saving’ hypothesis). Here, we contrast these two hypotheses by comparing individual daily time budgets of marked adult bighorn sheep rams (Ovis canadensis) and male mountain goats (Oreamnos americanus) during the pre‐rut and the rut. Concordant results for both species support the ‘foraging constraint’ hypothesis, as sexually‐active males reduced time spent foraging and lying from the pre‐rut to the rut because of an increase in time spent in mating‐related activities. Bighorn sheep rams also increased time spent foraging when not engaged in mating tactics, providing further support for a ‘maximisation’ of energy intake in the absence of reproductive opportunities. Because there are also known physiological changes that occur during the rut which may cause appetite suppression, for example to produce metabolic compounds linked with olfactory communication (the ‘scent‐urination’ hypothesis) or to cope with increased burden of parasites (the ‘parasite‐induced anorexia’ hypothesis), further research should aim at simultaneously testing these current hypotheses to better understand rut‐induced hypophagia and its effects on the life histories of male ungulates.     

Survival costs of reproduction in the blue tit (Parus caeruleus): a role for blood parasites?

One of the central tenets in life-history theory is that there is a trade-off between current and future reproduction (i.e. a cost of reproduction). The mechanism for this cost of reproduction is, however, largely unknown. One hypothesis is that the high workload during reproduction compromises resistance to parasites and that the resulting increase in parasitaemia has negative effects on the prospects of future survival. Although empirical evidence for a negative relationship between reproductive effort and parasite resistance exists, the causal relationships between reproductive effort, parasite resistance and future reproduction are still unclear. We use a path analytical approach to investigate whether a change in parasite resistance (as measured by intensities of infections by the blood parasite Haemoproteus) after manipulation of reproductive effort, translates into altered survival in female blue tits. Our results show a negative relationship between reproductive effort and parasite resistance, although evident only in first-year breeders. Moreover, we found survival costs of reproduction in first-year breeders. These costs were, however, not mediated by the blood parasite studied.     

The timing of male reproductive effort relative to female ovulation in a capital breeder

1. In large herbivores, the timing of breeding is important for females to hit peak plant protein levels. For males, the timing of reproductive effort is important to maximize the number of females they can mate during autumn rut in competition with other males. The latter depends on when most females are ovulating, but also on how other males with a different competitive ability are timing use of their capital (fat); it may pay younger males to invest more heavily later when prime aged males are exhausted. 2. Based on estimates of body mass loss, we quantify how much timing (start, peak and end dates) of male reproductive effort during rutting varies depending on male age, density and climate as well as timing of female ovulation. 3. Ovulation in adult females was delayed by 5 days from low to high density, and ovulation was also more synchronous at high density. The starting date of decline in male body mass was only later in yearlings than among other age groups. However, at low density, peak and end dates of rut became increasingly earlier and close to peak female ovulation with increasing age up to 7 years of age. Prime-aged males matched peak effort closely with peak rate of prime-aged female ovulation, while younger males were delayed. This is consistent with the view that younger males have a better chance when the prime-aged males are becoming exhausted. 4. Apart from yearlings, male age groups were synchronized in both the starting, peak and end dates of mass decline at high density. Thus, this partly follows change in female ovulation patterns, but also suggests that competition among males decreased with increasing density due probably to lower intensity of sexual selection. The lowered sexual selection may be due not only to more synchronous female ovulation, but also increasingly female-biased sex ratios and a younger male age structure with increasing density. 5. The onset of rutting is somewhat independent of male age (apart from the youngest males), but the peak and end of rutting effort is dependent strongly upon age, density and peak female ovulation. Male rutting phenology is thus best interpreted as a compromise between hitting peak female ovulation and intensity of sexual selection.     

A field laparotomy technique for observing the reproductive tract of free-ranging desert bighorn sheep (Ovis canadensis cremnobates)

A surgical procedure was developed to observe the reproductive tract of free-ranging desert bighorn sheep (Ovis canadensis cremnobates) ewes. Ventral laparotomies were performed on 37 bighorn ewes (ages: lamb — 9 years of age), 24 of which were unilaterally ovariectomized. A second laparotomy was done on 31 ewes. Diazepam (1.5 mg/kg) was injected intramuscularly as a preanesthetic followed by 5 mg etorphine hydrochloride (M99) for restraint and anesthesia. Atropine sulfate (0.03 mg/kg) was used to control hypersalivation and bronchial mucus secretion. Diazepam was evaluated as a preanesthetic on a control group of 42 ewes not submitted to surgery. Pretreatment with diazepam significantly (P < 0.001) reduced the induction time of the anesthetic. All bighorn sheep subjected to surgery recovered without postoperative complications. Ambulation time was similar whether or not diazepam was used as a preanesthetic. Subsequent reproductive performance and mortality rates were similar to those bighorn sheep in the remaining population.