Obligate Biparental Care Research Articles

Female and male Leach's Storm Petrels (Hydrobates leucorhous) pursue different foraging strategies during the incubation period.

Reproduction in procellariiform birds is characterized by a single egg clutch, slow development, a long breeding season and obligate biparental care. Female Leach's Storm Petrels Hydrobates leucorhous, nearly monomorphic members of this order, produce eggs that are between 20 and 25% of adult body weight. We tested whether female foraging behaviour differs from male foraging behaviour during the ~ 44-day incubation period across seven breeding colonies in the Northwest Atlantic. Over six breeding seasons, we used a combination of Global Positioning System and Global Location Sensor devices to measure characteristics of individual foraging trips during the incubation period. Females travelled significantly greater distances and went farther from the breeding colony than did males on individual foraging trips. For both sexes, the longer the foraging trip, the greater the distance. Independent of trip duration, females travelled farther, and spent a greater proportion of their foraging trips prospecting widely as defined by behavioural categories derived from a Hidden Markov Model. For both sexes, trip duration decreased with date. Sex differences in these foraging metrics were apparently not a consequence of morphological differences or spatial segregation. Our data are consistent with the idea that female foraging strategies differed from male foraging strategies during incubation in ways that would be expected if females were still compensating for egg formation.

Variation in male-built nest volume with nesting-support quality, colony, and egg production in whiskered terns.

Nest building can represent an energetically costly activity for a variety of animal taxa. Besides, the determinants of within‐species variation in the design of nests, notably with respect to natural and sexual selection, are still insufficiently documented. Based on an observational study, we examined the influence of nesting conditions (nesting‐support quality, colony, laying date, and year) on male‐built nest volume and also its potential role as a postmating sexually selected display in the whiskered tern Chlidonias hybrida. This tern species is a monogamous colonial bird with obligate biparental care breeding on aquatic vegetation. Hence, large nesting platforms are expected to be a selective advantage because they would better withstand adverse environmental conditions and provide a secure structure for eggs. Nest size may also serve as a postmating sexual trait, and variation in egg production would be positively associated with nest size. We found that nest volume was adjusted to different environmental cues. A positive relationship was found between nest volume and nesting‐support quality, indicating that the leaf density of white waterlily is essential for nest stability. Variation in nest volume was not correlated to colony size but varied among colonies and years. Male‐built nest volume was also positively associated with mean egg volume per clutch but not with clutch size. The fitness consequences of building a large nest are yet to be studied, and additional investigations are recommended to better understand whether the activity of males early during breeding season (e.g., nest building and courtship feeding performance) really serves as postmating sexually selected signals.

Cooperative nest building in wild jackdaw pairs

Animals create diverse structures, both individually and cooperatively, using materials from their environment. One striking example is the nests birds build for reproduction, which protect the offspring from external stressors such as predators and temperature, promoting reproductive success. To construct a nest successfully, birds need to make various decisions, for example regarding the nest material and their time budgets. Research has focused mainly on species where one sex is primarily responsible for building the nest. In contrast, the cooperative strategies of monogamous species in which both sexes contribute to nest building are poorly understood. Here we investigated the role of both sexes in nest building and fitness correlates of behaviour in wild, monogamous jackdaw pairs, Corvus monedula . We show that both partners contributed to nest building and behaved similarly, with females and males present in the nestbox for a comparable duration and transporting material to the nest equally often. However, while females spent more time constructing the nest, males tended to invest more time in vigilance, potentially as a means of coping with competition for nest cavities. These findings suggest a moderate degree of division of labour, which may facilitate cooperation. Moreover, some aspects of behaviour were related to proxies of reproductive success (lay date and egg volume). Females that contributed relatively more to bringing material laid earlier clutches and pairs that spent less time together in the nestbox had larger eggs. Thus, selection pressures may act on how nest-building pairs spend their time and cooperatively divide the labour. We conclude that cooperative nest building in birds could be associated with monogamy and obligate biparental care and provides a vital but relatively untapped context through which to study the evolution of cooperation. • In monogamous jackdaws, mates behaved similarly and cooperated to build their nest. • Females built more and called more frequently; males tended to be more vigilant. • Females that contributed relatively more to bringing material had earlier clutches. • Pairs that spent more time together in the nestbox laid smaller eggs. • Cooperation may be crucial in light of genetic monogamy and nest site competition.

Observations of infant conflict and avoidance in San Martin titi monkeys (Plecturocebus oenanthe).

Conflict between caregivers and infants typically centers on disagreements over the amount and frequency of care provided. Prior research has identified many variables that impact patterns of mother-infant conflict. These include wide-ranging factors such as individual temperament, reproductive status, and availability of resources. By contrast, no studies have investigated the variables that influence father-infant conflict. To better understand the nature of caregiver-infant conflict in a species with obligate biparental care, I observed two groups of San Martin titi monkeys inhabiting disturbed secondary forest fragments in the San Martín region of Peru. Using instantaneous focal sampling of infants, I recorded physical conflict between infants and caregivers and instances of infant avoidance (leaving the infant) by adult males. I summarized data as the percentage of records in which these activities occurred for each focal day and report the estimates for caregivers. I further calculated mean percentages by month of infant age to assess the relative timing of infant conflict, for each group and age/sex class, and infant avoidance by males. Percentages of conflict and avoidance were markedly higher in the larger group living in a smaller habitat than in the other group. This pattern occurred across all age/sex classes. In both groups, the greatest amount of infant conflict occurred with siblings. I discuss the substantial variation in conflict and avoidance in relation to the various socioecological conditions that may have played a role. This study provides an in-depth description and exploration of parent-offspring and sibling conflict, which has not been examined previously in this species.

Sex-Specific Contributions to Reproduction in Whiskered Tern Chlidonias hybrida Colonies of Varying Breeding Density

Addressing the question of the parental effort allocation when breeding remains central to life-history theory. This is particularly the case for monogamous species with obligate bi-parental care, where each parent should evaluate its contribution throughout the breeding season taking into account both the effort of its mate and environmental constraints. In colonial species, social environments may influence the activities of breeders. Here we compared patterns of mate effort in the Whiskered Tern Chlidonias hybrida, throughout breeding in two regions that differed greatly in colony nest density. This species builds large floating nesting platforms on aquatic plant beds. Accordingly, we explored whether nest building was sex-specific and influenced the activities of breeders throughout the season. In both regions, parental effort was indeed differentiated by sex; males invested strongly in nest-material delivery and mate provisioning during the nest-building stage, and females displayed increased investment during chick rearing. Contrary to expectations, courtship feeding and social interactions were less frequent in the region with high nest density. Our findings demonstrate that each parent clearly adjusted its reproductive effort throughout the season, whereas the contrast in social conditions between the two study regions weakly affected the activities of breeders.—Chambon, R., Latraube, F., Bretagnolle, V. & Paillisson, J.-M. (2019). Sex-specific contributions to reproduction in Whiskered Tern Chlidonias hybrida colonies of varying breeding density. Ardeola, 67: 113-125.

Sex-biased survival contributes to population decline in a long-lived seabird, the Magellanic Penguin.

We developed a Hidden Markov mark–recapture model (R package marked) to examine sex‐specific demography in Magellanic Penguins (Spheniscus magellanicus). Our model was based on 33 yr of resightings at Punta Tombo, Argentina, where we banded ~44,000 chicks from 1983 to 2010. Because we sexed only 57% of individuals over their lifetime, we treated sex as an uncertain state in our model. Our goals were to provide insight into the population dynamics of this declining colony, to inform conservation of this species, and to highlight the importance of considering sex‐specific vital rates in demographic seabird studies. Like many other seabirds, Magellanic Penguins are long‐lived, serially monogamous, and exhibit obligate biparental care. We found that the non‐breeding‐season survival of females was lower than that of males and that the magnitude of this bias was highest for juveniles. Biases in survival accumulated as cohorts aged, leading to increasingly skewed sex ratios. The survival bias was greatest in years when overall survival was low, that is, females fared disproportionality worse when conditions were unfavorable. Our model‐estimated survival patterns are consistent with independent data on carcasses from the species’ non‐breeding grounds, showing that mortality is higher for juveniles than for adults and higher for females than for males. Juveniles may be less efficient foragers than adults are and, because of their smaller size, females may show less resilience to food scarcity than males. We used perturbation analysis of a population matrix model to determine the impact of sex‐biased survival on adult sex ratio and population growth rate at Punta Tombo. We found that adult sex ratio and population growth rate have the greatest proportional response, that is, elasticity, to female pre‐breeder and adult survival. Sex bias in juvenile survival (i.e., lower survival of females) made the greatest contribution to population declines from 1990 to 2009. Because starvation is a leading cause of morality in juveniles and adults, precautionary fisheries and spatial management in the region could help to slow population decline. Our data add to growing evidence that knowledge of sex‐specific demography and sex ratios are necessary for accurate assessment of seabird population trends.

Genetic mating system of Australasian Gannets (Morus serrator)

ABSTRACT We studied genetic similarity between adults and nestlings in putative social families (i.e., 2 adults and a chick) of a seabird that provides obligate biparental care, the Australasian Gannet (Morus serrator), in New Zealand. We detected DNA fingerprint mismatches in 12% of 26 nests between the chick and 1 of the 2 attending adults sampled. No parent–offspring genetic mismatch was detected in nests with 4-week-old or younger and sedentary nestlings, whereas adult–nestling mismatches were detected only in nests with 5-week or older and more mobile young sampled. We conclude that the genetic mating system of this sulid species is predominantly monogamous.

Adaptive value of same-sex pairing in Laysan albatross

Same-sex pairing is widespread among animals but is difficult to explain in an evolutionary context because it does not result in reproduction, and thus same-sex behaviour often is viewed as maladaptive. Here, we compare survival, fecundity and transition probabilities of female Laysan albatross in different pair types, and we show how female-female pairing could be an adaptive alternative mating strategy, albeit one that resulted in lower fitness than male-female pairing. Females in same-sex pairs produced 80% fewer chicks, had lower survival and skipped breeding more often than those in male-female pairs. Females in same-sex pairs that raised a chick sometimes acquired a male mate in the following year, but females in failed same-sex pairs never did, suggesting that males exert sexual selection by assessing female quality and relegating low-quality females into same-sex pairs. Sexual selection by males in a monomorphic, non-ornamented species is rare and suggests that reconsideration is needed of the circumstances in which alternative reproductive behaviour evolves. Given the lack of males and obligate biparental care in this species, this research demonstrates how same-sex pairing was better than not breeding and highlights how it could be an adaptive strategy under certain demographic conditions.

Pair-living in the Absence of Obligate Biparental Care in a Lizard: Trading-off Sex and Food?

A pair-living social organisation can typically be explained by obligate biparental care. We investigated pair-living in the absence of biparental care in the Australian sleepy lizard, Tiliqua rugosa, which forms exceptionally strong pair bonds. We fitted 10 lizards, five male–female pairs, with Global Positioning System (GPS) recorders and continuously monitored social associations and separations between active pair partners, based on location records taken every 10 min over 3 mo. Males temporarily separated and reunited the pair more frequently than females, but females also contributed to the maintenance of the pair bond. These behavioural data were consistent with the hypothesis that females successfully coerce males into associations with one female. Lower frequencies of social association between pair partners once mating had finished support this interpretation. Males that are coerced into pair associations appear to experience higher costs of pair-living than females, because males initiated temporary separations of the pair more frequently than females. Males showed higher movement activity and remained active later each day. This sex bias in activity may be an important mechanism to mitigate the higher costs of pair-living for males. Costs for males might include within-pair competition for food as females appear more competitive. Our study provides detailed empirical data on a lizard pair bond and provides important insights into pair-living in the absence of biparental care.

Seaweed provisioning behaviour confers thermal benefit for nesting Australasian gannets (Morus serrator)

Despite prolonged and obligate biparental care for a single offspring in the Australasian gannet Morus serrator , several reproductive behaviours are presumed to be sex specific and might indicate sexual dimorphism in mating and parental effort in this broadly monomorphic seabird. For instance, the delivery of seaweed as a nesting material has been typically considered a male specific trait. We assessed this assumption and determined whether the potential role of this behaviour is to serve as a nuptial trait preceeding copulation or to impart a thermal benefit for incubation. First, as predicted, all arriving individuals at the colony that mated following seaweed delivery assumed the top copulatory position, which is consistent with male behaviour in this species. In comparison, the likelihood of birds without seaweed copulating in top position upon arrival at the nest site was approx. 50%, indicating an even mix of the sexes. However, the sex of those individuals in our sample that did not copulate during our observations remains unresolved. Second, seaweed delivery was not related to copulation following arrival, as individuals arriving with seaweed in our sample had a lower probability of mating than did individuals arriving without seaweed. Third, to determine if seaweed provides thermoregulatory benefits to alleviate the physiological costs of incubation, the foot temperatures of incubating and non-incubating individuals and temperatures of nests with or without seaweed were recorded. Temperatures of the foot-webbings during incubation were significantly higher above ambient temperatures than those of non-incubating gannets at the colony. Nests that contained seaweed were significantly warmer at sunrise than those without seaweed. There was no consistent difference between the temperatures of nesting material in the evenings alone, with a large variance of evening nest temperatures. These correlative data are consistent with male specificity and thermoregulatory benefits associated with seaweed delivery in M. serrator , implying that further experimental work on known-sexed birds should focus on physiological benefits and reproductive consequences of seaweed delivery in this species.

Incidental and intentional catch threatens Galápagos waved albatross

As large, long-lived seabirds with delayed and slow reproduction, albatrosses have low intrinsic mortality rates and are especially vulnerable to extinction from extrinsic sources of mortality such as fishery bycatch. Leg-band recovery information for waved albatrosses revealed mortality from both incidental catch and intentional catch for human consumption. Annual adult survival in 1999–2005, estimated from capture-mark-recapture data, was lower than historical estimates. This recent increase in adult mortality probably contributed to recent and dramatic shrinkage of the breeding population; periodic matrix models confirm that population growth rate is most sensitive to changes in adult survival. Banding data and recovery information also suggest that capture by fisheries is male-biased, which should reduce fecundity in this species with obligate bi-parental care. This new documentation of bycatch, harvesting, and associated demographic consequences provides reason for serious concern about the persistence of the single breeding population of the waved albatross.

Reduced parental care, compensatory behaviour and reproductive costs of thick-billed murres equipped with data loggers

Theoretical models predict that in species with obligate biparental care, individuals will partially compensate for decreased parental effort by their partners as a stable evolutionary strategy. Full compensation may occur when breeding success is an accelerating function of parental effort, especially in long-lived bird species. We experimentally examined the effect of time-depth recorders (TDRs) on body mass and parental behaviour of thick-billed murres, Uria lomvia, and evaluated the effect of TDRs as handicaps to test whether individuals compensate for decreased partner effort and whether compensation is sex biased. Compared with control birds, TDR-equipped birds had reduced body mass, offspring attendance, number of foraging trips and feeding rates, and males had increased foraging trip duration. In general, males lost mass at a higher rate and made longer foraging trips than females. Partners of TDR-equipped birds compensated for their mates' reduced parental effort by increasing offspring attendance and by increasing chick provisioning above average rates of control birds. Although partners of TDR-equipped birds fully compensated for their mates' reduced offspring attendance (i.e. chicks were never observed to be left unattended), total provisioning rates of pairs with a TDR-equipped bird ( X ¯ ± SE = 4.38 ± 0.26 meals / day ) were significantly lower than those of control pairs (5.74 ± 0.31 meals/day). However, fledgling success of control and TDR-equipped birds did not differ between reproductive seasons. TDR-equipped birds also had a significantly lower rate of return to breed than their non-TDR-equipped partners or control birds, and those that did return the following season were more likely to change mates (32%) compared with controls (0%). Taken together, our results underline the need to quantify the effects of monitoring equipment used to measure seabirds' activities, and indicate the ability of female and male thick-billed murres to compensate for reduced partner effort due to handicapping. Compensatory behaviour seems to be a necessary response of this single-brooded species to ensure current breeding success; however, it may affect the stability of pair bonds in some individuals.

Parental investment, adult sex ratios, and sexual selection in a socially monogamous seabird

Although most birds are monogamous, theory predicts that greater female parental investment and female-biased adult sex ratios will lower the polygyny threshold. This should result in polygynous mating, unless obligate biparental care or the spatial and temporal distribution of fertilizable females constrains a male’s ability to take advantage of a lowered polygyny threshold. Here we present data on the extent of male sexually dimorphic plumage, adult sex ratios and breeding season synchrony in three populations of a socially monogamous seabird, the brown booby Sula leucogaster. For one of these populations, San Pedro Martir Island, we also present data on differences in male and female parental investment, mortality and probability of pairing. The extent of plumage dimorphism varied among populations. Sex ratios were female biased in all populations. On San Pedro Martir Island, parental investment was female biased, females failed more often than males to find a mate, but there was no polygyny. We suggest that on San Pedro Martir: (1) a period of obligate biparental care coupled with a relatively synchronous breeding season constrained the ability of males to take advantage of a high environmental polygamy potential and (2) the resulting socially monogamous mating system, in combination with the female-biased adult sex ratio, caused females to be limited by the availability of males despite their greater parental investment.