Energy requirements during reproduction and reproductive effort in shrews (Soricidae)

The energy requirements of reproducing and non-reproducing females of three species of Crocidura (C. russula, C. viaria, C. olivieri), and two species of Sorex (S. coronatus, S. minutus) were measured. Members of these two genera show different rates of metabolism and reproductive strategies (extreme altriciality and larger litter size in Sorex). During pregnancy, the daily energy intake (on either an absolute or a mass-specific basis) remained close to the non-reproductive value in all species. The absolute energy intake increased strongly after parturition and was influenced by the litter size. Peak energy intake of lactating females was extremely high, typically between 100% and 200% above the non-reproductive requirements in the Crocidura and about 300% above the non-reproductive intake in the Sorex. The mass-specific daily energy intake was reduced during lactation in the three smaller species but not in C. viaria and C. olivieri. This decrease probably involves the different thermoregulatory abilities and/or basal rate of metabolism of the pups. Average reproductive effort was about 50%, in the Crocidura species and above 150% in the Sorex species. The higher effort in the latter is partly due to a larger litter size. But in addition, extreme altriciality in the Sorex leads to an earlier increase in the energy requirements and thus is an energetically more expensive reproductive mode. The present results support the hypothesis that a higher basal rate of metabolism is associated with a higher reproductive effort in shrews.

Sex- and melanism-specific variations in the oxidative status of adult tawny owls in response to manipulated reproductive effort.

Oxidative stress, determined by the balance between the production of damaging reactive oxygen species (ROS) and antioxidant defences, is hypothesized to play an important role in shaping the cost of reproduction and life history trade-offs. To test this hypothesis, we manipulated reproductive effort in 94 breeding pairs of tawny owls (Strix aluco) to investigate the sex- and melanism-specific effects on markers of oxidative stress in red blood cells (RBCs). This colour polymorphic bird species shows sex-specific division of labour and melanism-specific history strategies. Brood sizes at hatching were experimentally enlarged or reduced to increase or decrease reproductive effort, respectively. We obtained an integrative measure of the oxidative balance by measuring ROS production by RBCs, intracellular antioxidant glutathione levels and membrane resistance to ROS. We found that light melanic males (the sex undertaking offspring food provisioning) produced more ROS than darker conspecifics, but only when rearing an enlarged brood. In both sexes, light melanic individuals had also a larger pool of intracellular antioxidant glutathione than darker owls under relaxed reproductive conditions (i.e. reduced brood), but not when investing substantial effort in current reproduction (enlarged brood). Finally, resistance to oxidative stress was differently affected by the brood size manipulation experiment in males and females independently of their plumage coloration. Altogether, our results support the hypothesis that reproductive effort can alter the oxidative balance in a sex- and colour-specific way. This further emphasizes the close link between melanin-based coloration and life history strategies.

Male-biased reproductive effort in a long-lived seabird.

Background: In dimorphic seabirds, the larger sex tends to provision more than the smaller sex. In contrast, monogamy and biparental care are often associated with equal effort between the sexes. However, the few studies that have tested sex-specific effort in monomorphic seabirds have primarily examined the details of foraging at sea. Hypotheses: Parental effort is also sex-biased in a monomorphic seabird mating system for one of two reasons: (1) If females enter the period of parental care less able to invest in care due to the cost of egg production, male-biased effort may be necessary to avoid reproductive failure. (2) Alternatively, female-biased effort may occur due to the initial disparity in gamete size, particularly in species with internal fertilization. Organism: Leach’s storm-petrel (Oceanodroma leucorhoa), a monomorphic seabird with true monogamy and obligate biparental care. Site: A breeding colony of Oceanodroma leucorhoa at the Bowdoin Scientific Station on Kent Island, Bay of Fundy, New Brunswick, Canada. Methods: Across multiple breeding seasons, we assessed incubation behaviour and chickrearing behaviour through one manipulative and multiple observational studies. We assessed energetic investment by inducing feather replacement and measuring the resulting rate of feather growth during both the incubation and chick-rearing phases of parental care. Conclusions: We observed male-biased effort. Males incubated the egg for a greater proportion of time than did females and, when faced with an egg that would not hatch, males continued to incubate past the point when females abandoned it. Males made a higher percentage of total food deliveries to chicks than did females, resulting in greater mean daily food provisioning by males than by females. During chick rearing, males grew replacement feathers more slowly than did females, indicating that males were more likely to reduce their own nutritional condition while raising chicks than were females. These results support the hypothesis that females enter the period of parental care at a nutritional deficit and males must compensate to avoid reproductive failure.

Physiological Ecology and Reproductive Effort in a Migratory Seabird

Fluctuations of food availability, habitat quality, and environmental conditions throughout the year have been implicated in the breeding success and survival of migratory birds. Levels of circulating corticosterone, the hormone involved in energy balance and the stress response in birds, are also affected by fluctuations in these variables, and also play a role in self-maintenance and survival. In addition to changes in behaviors and resource allocation, the metabolic effects of corticosterone increase the amount of free radicals in the body, which can cause oxidative stress and damage lipids and DNA. In this thesis, I assessed if diet and physiology during the breeding and non-breeding seasons contributed to the reproductive success, survival, and oxidative stress of a long-lived migratory seabird, Leach’s storm-petrel (Oceanodroma leucorhoa). I tested the hypotheses that 1.) diet and physiology throughout the breeding and non-breeding seasons predict reproductive effort; and 2.) corticosterone affects telomere length, a measure of oxidative damage. Through analyses of stable isotopes, corticosterone, and antioxidant capacity, I found that although there was variation in these measures of diet and physiology within the population, none of these factors during the breeding or non-breeding seasons correlated with reproductive effort or success. I also found that feather and plasma corticosterone did not predict telomere length. The life history strategies of Leach’s storm-petrels appear to be complex, and many factors likely contribute to self-maintenance and the decision to breed. Long-term monitoring of these variables may help identify relationships between trends in oceanographic variables during both the breeding and non-breeding seasons with reproductive effort and success, and survival.

Sex- and melanism-specific variations in the oxidative status of adult tawny owls in response to manipulated reproductive effort

Funding: This work was supported by the Swiss National Science Foundation [grants PPOA-102913 and 3100AO_120517 to AR and 31003A_124988 to PB). © 2015. Published by The Company of Biologists Ltd.

Reproductive biology of Leptodactylus fuscus (Anura, Leptodactylidae) in the subtropical climate, Rio Grande do Sul, Brazil

The aim of this study was to characterize, for the central region of the State of Rio Grande do Sul, Brazil, the reproductive biology of Leptodactylus fuscus (Schneider, 1799), based on the analysis of gonadal development of males and females, reproductive effort, size-fecundity relationships, and occurrence of sexual dimorphism in body size. Mature individuals were found from October 1996 to February 1997 and from October 1997 to December 1997. The highest input of juveniles in the population was recorded in March 1997. There was a positive and significant correlation between the number of mature individuals and the mean monthly temperature. The population did not present sexual dimorphism in size. Males presented significant correlation only between snout-vent length and testes length. All females had oocytes at four different maturation stages and there were no significant correlations regarding size-fecundity variables. The correlation between ovarian size factor and females snout-vent length was not significant either. The main difference between this population and those that inhabit tropical climate was that temperature was responsible for stimulating the reproduction activity, instead of rainfall.

Twofold cost of reproduction: an increase in parental effort leads to higher malarial parasitaemia and to a decrease in resistance to oxidative stress.

Parental effort is usually associated with high metabolism that could lead to an increase in the production of reactive oxidative species giving rise to oxidative stress. Since many antioxidants involved in the resistance to oxidative stress can also enhance immune function, an increase in parental effort may diminish the level of antioxidants otherwise involved in parasite resistance. In the present study, we performed brood size manipulation in a population of great tits (Parus major) to create different levels of parental effort. We measured resistance to oxidative stress and used a newly developed quantitative PCR assay to quantify malarial parasitaemia. We found that males with an enlarged brood had significantly higher level of malarial parasites and lower red blood cell resistance to free radicals than males rearing control and reduced broods. Brood size manipulation did not affect female parasitaemia, although females with an enlarged brood had lower red blood cell resistance than females with control and reduced broods. However, for both sexes, there was no relationship between the level of parasitaemia and resistance to oxidative stress, suggesting a twofold cost of reproduction. Our results thus suggest the presence of two proximate and independent mechanisms for the well-documented trade-off between current reproductive effort and parental survival.

Reproductive biology of an endemic Physalaemus of the Brazilian Atlantic forest, and the trade-off between clutch and egg size in terrestrial breeders of the P. signifer group

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Reproductive biology of an endemic Physalaemus of the Brazilian Atlantic forest, and the trade-of between clutch and egg size in terrestrial breeders of the P. signifer group

Physalaemus crombiei is a small foam-nesting frog endemic to the Atlantic forest. It is a member of the P. signifer group known only from its type locality in Santa Teresa, State of Espírito Santo, and from another locality in the State of Bahia, Brazil. Most Physalaemus species are aquatic breeders, and species in the P. signifer group are the only ones exhibiting a tendency toward terrestrial reproduction in the genus. Here we describe the reproductive period, breeding site and reproductive modes of P. crombiei from a third population in the Atlantic forest, southeastern Brazil. We also investigated reproductive effort and size-fecundity relationships in females. Reproductive traits were compared to other species in the genus Physalaemus, especially those included in the P. signifer group. Physalaemus crombiei is a prolonged breeder, reproducing throughout the year with a peak of activity during the most rainy months (October-March). Males called from the humid forest foor and eggs embedded in foam nests were deposited in the water as well as on the humid foor amidst the leaf litter, or inside fallen leaves or tree holes containing rainwater on the forest foor. As expected, P. crombiei exhibited three alternative reproductive modes, as described for other species of the P. signifer group. The number of eggs produced per female varied from 91 to 250. Female body size is positively correlated both with ovary mass and clutch size (number of eggs per clutch). Variation in the number and size of eggs observed in Physalaemus species may be explained not only by female size, but also by the terrestrial reproductive mode exhibited by the species in the P. signifer group.

Feeding, body condition and reproductive investment of Astyanax intermedius (Characiformes, Characidae) in relation to rainfall and temperature in a Brazilian Atlantic Forest stream

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)

Maternal effort mediates the prevalence of trypanosomes in the offspring of a passerine bird.

The relationships between parental effort, offspring growth, and offspring blood parasitemias are poorly known. We examined the effect of parental effort on offspring size and prevalence of trypanosomes in peripheral blood of nestling Pied Flycatchers Ficedula hypoleuca aged 13 days. Trypanosome infections were likely to be shared by siblings, indicating the role of a common environment and/or shared genes in the susceptibility to infection. Broods infected by trypanosomes had reduced growth, but this was due to decreased parental, especially maternal, energy expenditure in broods with nestlings infected by trypanosomes. There was no association between parental infection with trypanosomes and both their energy expenditure and the infection of their broods. Under stressful conditions caused by low maternal energy expenditure, the immune response of nestlings during growth was probably impaired, in a way analogous to the relapses of blood parasitemias with reproductive effort in breeding animals.

The pre-reproductive period in a tropical bird: parental care, dispersal, survival, and avian life histories

The period between offspring birth and recruitment into the breeding population is considered one of the least understood components of animal life histories. Yet, examining this period is essential for studies of parental care, dispersal, demography, and life histories. Studies of the pre-reproductive period are particularly few in tropical regions, where the organization of life histories are predicted to differ compared to northern hemisphere species. For my dissertation I used radio-telemetry, mark-resighting, and field observations to study the pre-reproductive period in a Neotropical bird, the western slaty-antshrike (Thamnophilus atrinucha), in Panama. First, I found that parental care after offspring left the nest (the post-fledging period) was greater than care during the nestling period. Prolonged care resulted in a clear trade-off for parents as they did not nest again until fledglings from the first brood were independent. Parents fed offspring for a prolonged duration during the post-fledging period and higher post-fledging survival was observed compared to many northern hemisphere species. Second, I observed that offspring that remained with parents for longer periods on the natal territory had higher survival both while on the natal territory and after dispersal compared to those dispersing earlier. Parental aggression towards offspring increased with offspring age and offspring dispersed earlier when parents renested. Contrary to other family living species, only a small proportion of antshrike offspring remained on the natal territory until the following year and all dispersed to float. Floating is when juveniles wander within other breeding pairs’ territories. These results suggest that the benefits of delayed dispersal declined with offspring age and with renesting by parents. Third, I observed that survival during the dependent period and first year was greater in slaty antshrikes compared to that of northern hemisphere species. Pre-reproductive survival relative to adult survival was equal or greater than that observed in northern hemisphere species. The date offspring left the nest, mass, and age at dispersal influenced offspring survival, whereas offspring sex and year did not. Relatively high survival during the pre-reproductive period coupled with comparatively low annual productivity clarifies how many tropical species achieve replacement. High juvenile survival appears to obtain from extended post-fledging parental care, delayed dispersal, low costs of dispersal, and a less seasonal environment. Lastly, I experimentally manipulated begging at the nest to examine changes in parental behavior. Under elevated begging, parents increased provisioning rates and reduced the time between arrival to the nest and feeding of nestlings, potentially to reduce begging sounds. Furthermore, parents switched to preferentially feed the closest offspring during the begging treatment. This suggests parents either allowed sibling competition to influence feeding decisions, or feeding the closer nestling increased the efficiency of provisioning. In summary, I found that slaty antshrikes have delayed age at reproduction, higher post-fledging and first year survival, extended post-fledging parental care, equal or greater pre-reproductive survival relative to adult survival, and delayed dispersal compared to many northern hemisphere passerines. These results suggest that this tropical species has a strategy of high investment into few offspring. Furthermore, reproductive effort is equal or greater at least in slaty antshrikes compared to northern hemisphere species, suggesting that the latitudinal gradient in clutch size is not explained by a gradient in reproductive effort.