Age, Sex, and Telomere Dynamics in a Long-Lived Seabird with Male-Biased Parental Care

The examination of telomere dynamics is a recent technique in ecology for assessing physiological state and age-related traits from individuals of unknown age. Telomeres shorten with age in most species and are expected to reflect physiological state, reproductive investment, and chronological age. Loss of telomere length is used as an indicator of biological aging, as this detrimental deterioration is associated with lowered survival. Lifespan dimorphism and more rapid senescence in the larger, shorter-lived sex are predicted in species with sexual size dimorphism, however, little is known about the effects of behavioral dimorphism on senescence and life history traits in species with sexual monomorphism. Here we compare telomere dynamics of thick-billed murres (Uria lomvia), a species with male-biased parental care, in two ways: 1) cross-sectionally in birds of known-age (0-28 years) from one colony and 2) longitudinally in birds from four colonies. Telomere dynamics are compared using three measures: the telomere restriction fragment (TRF), a lower window of TRF (TOE), and qPCR. All showed age-related shortening of telomeres, but the TRF measure also indicated that adult female murres have shorter telomere length than adult males, consistent with sex-specific patterns of ageing. Adult males had longer telomeres than adult females on all colonies examined, but chick telomere length did not differ by sex. Additionally, inter-annual telomere changes may be related to environmental conditions; birds from a potentially low quality colony lost telomeres, while those at more hospitable colonies maintained telomere length. We conclude that sex-specific patterns of telomere loss exist in the sexually monomorphic thick-billed murre but are likely to occur between fledging and recruitment. Longer telomeres in males may be related to their homogamous sex chromosomes (ZZ) or to selection for longer life in the care-giving sex. Environmental conditions appeared to be the primary drivers of annual changes in adult birds.

Asymmetric sexual conflict over parental care in a biparental cichlid

Theoretical models predict that parents should adjust the amount of care both to their own and their partner's body condition. In most biparental species, parental duties are switched repeatedly allowing for repeated mutual adjustment of the amount of care. In the mouthbrooding cichlid Eretmodus cyanostictus, terms are switched only once with females taking the first share. The timing of the shift of the clutch between mates strongly determines both partners' brooding period and thereby their parental investment. Females signal their readiness to transfer the young several days before the male finally takes them, suggesting sexual conflict over the timing of the shift. In a lab experiment, we reduced the body condition of either the female or the male of a pair to test whether energy reserves affect the timing of the shift and whether female signalling behaviour depends on energetic state. Males with a lowered condition took the young later and incubated for a shorter period, which prolonged the incubation time of their female partners. When female condition was lowered, female and male incubation durations remained unchanged, although females signalled their readiness to shift more intensely. Our results suggest that males adjust their parental investment to own energy reserves but are unresponsive to their mate's condition. Females appear to carry the entire costs for the male's adjustment of care. We propose that intrinsic asymmetries in the scope for mutual adjustment of parental investment and the costs of negotiation crucially influence solutions of the conflict between sexes over care.

Sex-specific foraging during parental care in a size-monomorphic seabird

Sex differences in foraging behaviour are typically studied in size-dimorphic taxa. Data on sex-specific behavior in monomorphic taxa are needed to test theories of reproductive investment. It has been suggested that in seabirds foraging niche separation may be related to decreased intersexual competition for food between cooperating pair-bonded individuals. Alternatively, sex differences in foraging niches may be driven by different nutritional requirements of females associated with the reproductive costs of egg production and oviposition. To assess these possibilities, we studied a size-monomorphic colonial seabird, the Australasian Gannet (Morus serrator) at the Cape Kidnappers gannetry, New Zealand. We recorded maximum dive depths, and distinct diet composition of incubating females as indicated by stable isotopic signatures. Results suggested greater female foraging effort during early times of incubation, indicated by significantly deeper maximum dives. Sex-specific foraging patterns across other breeding stages were more variable. Nitrogen stable isotopic values showed that incubating females occupied a different trophic position compared to males at the same breeding stage, and also from those of gannets of both sexes at later stages of parental care. Overall, the data are consistent with cost-of-oviposition compensation in females necessitating male-bias in parental care in biparental breeders. Further research is needed to unravel the implications for the evolution of sex differences in behavior in this and other monomorphic taxa.

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.

Feeding ecology and life-history strategy of nesting males in a fish with long parental care, Lusitanian toadfish (Halobatrachus didactylus, Batrachoididae)

The Lusitanian toadfish, Halobatrachus didactylus, like other batrachoidids, is a benthic fish species with nesting behaviour during the breeding season. During this prolonged period it engages in mating activities and remains in the nest providing parental care. It is not known whether males feed while providing parental care but it is likely that their limited mobility may restrict their diet and influence their fitness. As a consequence, egg cannibalism could occur as a life-history strategy. The aim of the present study is to ascertain the feeding behaviour of nesting males, in comparison to mature non-nesting males, and to identify potential life-history traits related to egg cannibalism. Nest-holders were sampled from artificial nests placed in an intertidal area of the Tagus estuary, only exposed during spring low tides. The diet of nest-holders was compared with that of non-nesting mature males from the same area, captured by otter trawl. The present study demonstrates that despite their constrained mobility nest-holders feed during the breeding season, although in a more opportunistic fashion than non-nesting males. Nest-holders showed a generalist feeding behaviour, with a more heterogeneous diet. Egg cannibalism was not related to male condition, paternity or brood size but showed a higher incidence early in the season when water temperatures were lower. The results suggest a possible seasonal trade-off strategy between care and energy recovery, triggered by environmental factors, where under unfavourable conditions to sustain viable eggs the male may recover energy by eating eggs, thus benefiting future reproductive success, later in the season.

Convergent maternal care strategies in ungulates and macropods

Mammals show extensive interspecific variation in the form of maternal care. Among ungulates, there is a dichotomy between species in which offspring follow the mother (following strategy) versus species in which offspring remain concealed (hiding strategy). Here we reveal that the same dichotomy exists among macropods (kangaroos, wallabies and allies). We test three traditional adaptive explanations and one new life history hypothesis. and find very similar patterns among both ungulates and macropods. The three traditional explanations that we tested were that a ''following'' strategy is associated with (1) open habitat, (2) large mothers, and (3) gregariousness. Our new life-history hypothesis is that a following strategy'' is associated with delayed weaning, and thus with the slow end of the slow-fast mammalian life-history continuum, because offspring devote resources to locomotion rather than rapid growth. Our comparative test strongly supports the habitat structure hypothesis and provides some support for this new delayed weaning hypothesis for both ungulates and macropods. We propose that sedentary young in closed habitats benefit energetically by having milk brought to them. In open habitats, predation pressure will select against hiding. Followers will suffer slower growth to independence. Taken together, therefore, our results provide the first quantitative evidence that macropods and ungulates are convergent with respect to interspecific variation in maternal care strategy. In both clades, differences between species in the form of parental care are due to a similar interaction between habitat, social behavior, and life history.

Maternal care in Gargaphia decoris (Heteroptera, Tingidae), with comments on this behavior within the genus and family

Maternal care in Gargaphia decoris is described for the first time. A video is presented as supplementary material. The knowledge on such trait within Tingidae is summarized. The behavior within the family is discussed, and the potential as a source of phylogenetic characters for further analyses is stressed.

Alloparental care in a solitary bee

Research into the evolutionary origins of sociality in insect colonies is changing emphasis from understanding how eusociality is maintained to how insects transition from solitary to social lifestyles. The pygmy carpenter bees (Ceratina spp.) offer an excellent model for investigating such factors as they have been historically thought of as solitary but have recently been shown to be socially polymorphic, which may indicate that they are currently in a transitive phase. By utilizing behavioural observation and experimental removal protocols, I show that extended parental care, as well as sibling care in Ceratina calcarata plays an important role in offspring development. I found, upon removal of the mother, that specifically produced ‘dwarf’ female offspring take over parental care roles in the nest. The existence of alloparental care and generational overlap suggests that although they are classified as solitary bees, C. calcarata possess the prerequisite behavioural repertoire for sociality.

Mating system and exclusive postzygotic paternal care in a Neotropical harvestman (Arachnida: Opiliones)

This study tests predictions of the hypothesis of evolution of paternal care via sexual selection by using the Neotropical harvestman Pseudopucrolia sp. as the model organism. Females use natural cavities in roadside banks as nesting sites, which are defended by males against other males. Females leave the nests after oviposition, and all postzygotic parental care is accomplished by males, which protect the eggs and nymphs from predators. We provided artificial mud nests to individuals in the laboratory and conducted observations on the reproduction of the species. Male reproductive success was directly related to nest ownership time: the longer a male held a nest, the higher his chances of obtaining copulations. All males that succeeded in mating and obtaining one clutch eventually mated with additional females that added eggs to the clutch. Thus, desirable males were not limited to monogamy by paternal care. Experimental manipulations demonstrated that guarding males were more attractive to females than were nonguarding males and also that males guarded unrelated eggs. Finally, we found that females and nonguarding males spent more time foraging than guarding males. We use our data to contrast hypotheses on the origin and maintenance of paternal care and to provide a critical assessment of the hypothesis of the evolution of paternal care via sexual selection. (C) 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.