Iulia Bădescu | Université de Montréal (original) (raw)

Papers by Iulia Bădescu

Behavioral Ecology and Sociobiology, 2022

Maternal lactational investment can affect female reproductive rates and offspring survival in ma... more Maternal lactational investment can affect female reproductive rates and offspring survival in mammals and can be biased towards infants of one sex. We compared estimates of lactation effort among mothers, assessed as their potential milk contribution to age-specific infant diets (mother-infant differences in fecal stable nitrogen isotopes, δ15N), to the timing of weaning (infant age at last nursing bout) and to maternal inter-birth interval lengths for male and female infant chimpanzees (Pan troglodytes) at Ngogo, Uganda. Infant males had greater proportions of milk in their age-specific diets, indicated by higher mother-infant differences in δ15N (Generalized Estimating Equation, GEE: p

Cave and Karst Systems of Romania, 2018

The Pârgavului Cave is located in the Vâlcan Mountains (South Carpathians) and develops in Lower ... more The Pârgavului Cave is located in the Vâlcan Mountains (South Carpathians) and develops in Lower and Middle Jurassic limestones. Due to various carbonate facies, the dissolution acted selectively; thus, cave passages show different morphologies. The Mesozoic tectonics events combined with the hydrogeological conditions existing during the Quaternary, created a unique imprint on various geomorphological aspect of the cave. Speleothems are present in the sub-horizontal part of the cave. The progressive incision of the underground river led to the formation of several generations of shelfstones.

Primates, 2021

Infant handling (holding or carrying) by adult males is rare in mammals; however, high levels hav... more Infant handling (holding or carrying) by adult males is rare in mammals; however, high levels have been reported in some primates. Though infant handling is a costly behaviour, there are many benefits that male handlers can accrue. Infant handling by males is most conspicuous in platyrrhines and tends to be uncommon in catarrhines. In the latter species, research on male-infant interactions has focused on low-cost behaviours, such as proximity and grooming. However, to better understand the evolution of infant handling by males, more data on its occurrence across the Primate order are essential, even in species where it is relatively uncommon. We compare the occurrence of infant handling by males in three closely related species of catarrhine: Colobus vellerosus, C. guereza, and C. angolensis ruwenzorii. We collected focal animal samples on infants to quantify infant handling rates and durations, and found that adult male C. a. ruwenzorii handled infants much more frequently and for much longer than males in the other two species. We discuss how C. a. ruwenzorii's unique social organization may explain high levels of infant handling by adult males in this species. More long-term and detailed comparisons of infant handling across species and populations will shed light on how sociality has shaped the evolution of this behaviour in the Primate order.

Journal of Human Evolution, 2020

Premasticated food transfer, when an individual partially breaks down food through chewing and fe... more Premasticated food transfer, when an individual partially breaks down food through chewing and feeds it to another individual, usually mouth-to-mouth, is described widely across human cultures. This behavior plays an important role in modern humans' strategy of complementary feeding, which involves supplementing maternal milk in infant diets with processed, easily digestible versions of adult foods. The extent to which other primates engage in premasticated food transfer with infants is unclear, as premasticated food transfers have been only occasionally reported in other ape species. We investigated premasticated food transfers in 62 mother-infant pairs of wild chimpanzees at Ngogo, Uganda, as well as unresisted food taking, when mothers passively allow infants to seize food. We evaluated the presence or absence and rates of premasticated food transfer and unresisted food taking relative to maternal parity and infant age and sex and assessed the food species and part used. We found that chimpanzee mothers regularly shared premasticated food with their infants aged between 6 months and 4 years, but they were more likely to share, and more frequently shared, with younger infants. The frequency with which females shared premasticated food may relate to maternal experience, as multiparous females shared premasticated food more often than did first-time mothers, which we did not find with unresisted food taking. Both easy-to-chew, commonly eaten foods and tougher, rarely eaten foods were shared. Premasticated food transfer and unresisted food taking may be infant-rearing strategies to facilitate the transition from a diet of exclusive maternal milk to solid food during early infancy. Premasticated food transfer in particular may provide energetic, immune, or growth benefits to infants through reduced chewing effort and maternal saliva. Given our findings in chimpanzees and earlier reports in other ape species, we suggest that the foundation of complementary feeding, a uniquely hominin strategy, might have been present in a common ancestor shared with the other great apes in the form of premasticated, mouth-to-mouth food transfer by mothers with their offspring.

American journal of physical anthropology, 2017

Determining nutritional development in wild primates is difficult through observations because co... more Determining nutritional development in wild primates is difficult through observations because confirming dietary intake is challenging. Physiological measures are needed to determine the relative contributions of maternal milk and other foods at different ages, and time of weaning. We used fecal stable carbon and nitrogen isotopes (δ(13) C, δ(15) N) and fecal nitrogen concentrations (%N) from wild chimpanzees at Ngogo, Uganda, to derive physiological dietary indicators during the transition from total reliance on maternal milk to adult foods after weaning. We analyzed 560 fecal samples collected non-invasively from 48 infants, their mothers, and 6 juvenile siblings. Most infant and juvenile samples (90%) were matched to samples collected from mothers on the same day. Isotopic assessments were compared with observations of nursing and feeding. Infants ≤1 year old showed average δ(15) N, δ(13) C and %N ratios that were 2.0‰, 0.8‰ and 1.3% greater than their mothers, respectively, int...

Royal Society open science, 2016

Alloparenting, when individuals other than the mother assist with infant care, can vary between a... more Alloparenting, when individuals other than the mother assist with infant care, can vary between and within populations and has potential fitness costs and benefits for individuals involved. We investigated the effects of alloparenting on the speed with which infants were weaned, a potential component of maternal fitness because of how it can affect inter-birth intervals, in wild chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Uganda. We also provide, to our knowledge, the first description of alloparenting in this population and present a novel measure of the contribution of milk to infant diets through faecal stable nitrogen isotopes (δ(15)N). Using 42 mother-infant pairs, we tested associations of two alloparenting dimensions, natal attraction (interest in infants) and infant handling (holding, carrying), to the proportion of time mothers spent feeding and to maternal lactation effort (mean nursing rates and mother-infant δ(15)N differences). Neither natal attraction nor in...

American journal of primatology, 2015

Primate females often inspect, touch and groom others' infants (natal attraction) and they ma... more Primate females often inspect, touch and groom others' infants (natal attraction) and they may hold and carry these infants in a manner resembling maternal care (infant handling). While natal attraction and infant handling occur in most wild colobines, little is known about the factors influencing the expression of these behaviors. We examined the effects of female parity, kinship, and dominance rank, as well as infant age and sex in wild Colobus vellerosus at Boabeng-Fiema Monkey Sanctuary, Ghana. We collected data via focal sampling of females in 2008 and 2009 (N = 61) and of infants in 2010 (N = 12). Accounting for the individuals who interacted with our focal subjects, this study includes 74 females and 66 infants in 8 groups. We recorded female agonistic interactions ad libitum to determine dominance ranks. We used partial pedigree information and genotypes at 17 short tandem repeat loci to determine kinship. We knew female parity, infant age and sex from demographic record...

Behaviour, 2013

Females that do not experience strong contest competition for food are presumed to form 'egalitar... more Females that do not experience strong contest competition for food are presumed to form 'egalitarian' relationships (i.e., lacking strong, linear dominance hierarchies). However, recent studies of Gorilla beringei beringei (mountain gorilla) have documented relatively strong, linear female dominance hierarchies despite them having a highly folivorous diet that generates relatively low levels of within-group contest competition (Robbins et al., 2005, 2007). To investigate if this pattern holds true for other highly folivorous species that may experience low levels of contest competition, we examined the linearity and strength of female dominance hierarchies in a population of Colobus vellerosus (ursine colobus or white-thighed colobus) at Boabeng-Fiema, Ghana. From 2004 to 2011, we collected data via ad libitum and focal sampling of 75 adult and subadult females in eight groups. Half of the study groups had few unknown submissive relationships, and females formed individualistic hierarchies with high linearity indices ranging from 0.9 to 1. There was between-group variation in all components of hierarchical strength (i.e., hierarchical expression, consistency, and stability). Groups showed varying rates of submission, and there was a short latency to detect a linear hierarchy in some groups and a long latency in other groups (i.e., varying levels of hierarchical expression). Females in most groups formed unidirectional and stable relationships. Maturing females challenged older females in some groups, and these groups had more non-linear relationships (i.e., dyads with more submissive interactions down rather than up the hierarchy) and higher rates of individual rank change than other groups. Based on low rates of submission, long latencies, and/or some inconsistencies, we conclude that most groups form relatively

American Journal of Primatology, 2015

Male takeovers affect male tenure, female mate choice and ultimately, individual reproductive suc... more Male takeovers affect male tenure, female mate choice and ultimately, individual reproductive success in group-living primates. In social systems with female philopatry and high male reproductive skew, male takeovers largely determine female mate choice, whereas in species with female dispersal, females have the option of deserting a new male. We focused on a species with facultative female dispersal to investigate which factors promote female desertion of males after takeover, using 15 cases (12 for which we have complete data on the takeover process and the female dispersal outcome). These cases took place in nine groups of Colobus vellerosus between 2001 and 2013 at the Boabeng-Fiema Monkey Sanctuary, Ghana. Quick takeovers were usually achieved by single adult males and were never followed by female dispersal. Slow takeovers involved several males, and these takeovers were regularly accompanied by female emigration. Infant attacks and infanticide by males occurred during both kinds of takeovers, but females with dependent offspring never dispersed, regardless of whether their infant was attacked or killed by the new male(s). Subadult females, who were not constrained by the presence of infants, dispersed more often after slow takeovers than after quick takeovers. Whether female dispersal post-takeover is an expression of female mate choice, or occurs to avoid the social upheaval surrounding slow takeovers, remains to be investigated. Am. J. Primatol.

Objectives: Determining nutritional development in wild primates is difficult through observation... more Objectives: Determining nutritional development in wild primates is difficult through observations because confirming dietary intake is challenging. Physiological measures are needed to determine the relative contributions of maternal milk and other foods at different ages, and time of weaning. We used fecal stable carbon and nitrogen isotopes (d 13 C, d 15 N) and fecal nitrogen concentrations (%N) from wild chimpanzees at Ngogo, Uganda, to derive physiological dietary indicators during the transition from total reliance on maternal milk to adult foods after weaning. Materials and Methods: We analyzed 560 fecal samples collected non-invasively from 48 infants, their mothers, and 6 juvenile siblings. Most infant and juvenile samples (90%) were matched to samples collected from mothers on the same day. Isotopic assessments were compared with observations of nursing and feeding.

Alloparenting, when individuals other than the mother assist with infant care, can vary between a... more Alloparenting, when individuals other than the mother assist with infant care, can vary between and within populations and has potential fitness costs and benefits for individuals involved. We investigated the effects of alloparenting on the speed with which infants were weaned, a potential component of maternal fitness because of how it can affect inter-birth intervals, in wild chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Uganda. We also provide, to our knowledge, the first description of alloparenting in this population and present a novel measure of the contribution of milk to infant diets through faecal stable nitrogen isotopes (δ 15 N). Using 42 mother–infant pairs, we tested associations of two alloparenting dimensions, natal attraction (interest in infants) and infant handling (holding, carrying), to the proportion of time mothers spent feeding and to maternal lactation effort (mean nursing rates and mother–infant δ 15 N differences). Neither natal attraction nor infant handling was significantly associated with feeding time. Infant handling was inversely associated with both measures of lactation effort, although natal attraction showed no association. Alloparenting may benefit mothers by enabling females to invest in their next offspring sooner through accelerated weaning. Our findings emphasize the significance of alloparenting as a flexible component of female reproductive strategies in some species.

Keywords: feeding competition infant development infanticide maternal investment strategy natal c... more Keywords: feeding competition infant development infanticide maternal investment strategy natal coat predation The rate at which infants develop can vary within species. This variation may be due to differences between infants in their nutritional intake and physiology, or the ability of females to adjust the amount and timing of maternal investment to maximize their lifetime reproductive success. This is the first primate study that uses a large sample size and multivariate analyses to investigate whether variation in early infant development (measured visually using durations of natal coat stages) is explained by differences in infanticide pressure, predation pressure or feeding competition among mothers. We recorded the number of days that infants took to transition through each of the two natal coat stages (white to grey: N ¼ 32; grey to black-and-white: N ¼ 22), as well as through their entire natal coats (white to black-and-white: N ¼ 38) in a population of wild ursine colobus, Colobus vellerosus. Infant males, which are at greater risk of infanticidal attacks, transitioned coat colours earlier than females, and infants in multimale groups, where infanticide occurs more frequently, transitioned earlier than infants in unimale groups. Variation in group size did not affect natal coat durations, which suggests that the intensity of predation risk and feeding competition do not influence development. Instead of terminating investment in offspring before birth, as in the 'Bruce effect', females may invest more heavily in infants after birth in order to speed up infant development and reduce the time period during which offspring are the most vulnerable to infanticide. Mothers may therefore have flexible means of exerting choice over maternal investment in relation to infanticide risk. However, the extent to which mothers and infants are responsible for adjusting the speed of development is unknown.

Primate females often inspect, touch and groom others' infants (natal attraction) and they may ho... more Primate females often inspect, touch and groom others' infants (natal attraction) and they may hold and carry these infants in a manner resembling maternal care (infant handling). While natal attraction and infant handling occur in most wild colobines, little is known about the factors influencing the expression of these behaviors. We examined the effects of female parity, kinship, and dominance rank, as well as infant age and sex in wild Colobus vellerosus at Boabeng-Fiema Monkey Sanctuary, Ghana. We collected data via focal sampling of females in 2008 and 2009 (N = 61) and of infants in 2010 (N = 12). Accounting for the individuals who interacted with our focal subjects, this study includes 74 females and 66 infants in 8 groups. We recorded female agonistic interactions ad libitum to determine dominance ranks. We used partial pedigree information and genotypes at 17 short tandem repeat loci to determine kinship. We knew female parity, infant age and sex from demographic records. Nulliparous females showed more natal attraction and infant handling than parous females, which may suggest that interactions with infants are more adaptive for nulliparous females because they learn mothering skills through these behaviors. Compared to non-kin, maternal kin were more likely to handle infants. Maternal kin may be permitted greater access to infants because mothers are most familiar with them. Handlers may incur inclusive fitness benefits from infant handling. Dominance rank did not affect female interactions with infants. The youngest infants received the most natal attraction and infant handling, and male infants were handled more than female infants. The potential benefits of learning to mother and inclusive fitness, in combination with the relatively low costs of natal attraction and infant handling, may explain the high rates of these behaviors in many colobines. Am. J. Primatol. 77:376–387, 2015. © 2014 Wiley Periodicals, Inc.Primate females often inspect, touch and groom others' infants (natal attraction) and they may hold and carry these infants in a manner resembling maternal care (infant handling). While natal attraction and infant handling occur in most wild colobines, little is known about the factors influencing the expression of these behaviors. We examined the effects of female parity, kinship, and dominance rank, as well as infant age and sex in wild Colobus vellerosus at Boabeng-Fiema Monkey Sanctuary, Ghana. We collected data via focal sampling of females in 2008 and 2009 (N = 61) and of infants in 2010 (N = 12). Accounting for the individuals who interacted with our focal subjects, this study includes 74 females and 66 infants in 8 groups. We recorded female agonistic interactions ad libitum to determine dominance ranks. We used partial pedigree information and genotypes at 17 short tandem repeat loci to determine kinship. We knew female parity, infant age and sex from demographic records. Nulliparous females showed more natal attraction and infant handling than parous females, which may suggest that interactions with infants are more adaptive for nulliparous females because they learn mothering skills through these behaviors. Compared to non-kin, maternal kin were more likely to handle infants. Maternal kin may be permitted greater access to infants because mothers are most familiar with them. Handlers may incur inclusive fitness benefits from infant handling. Dominance rank did not affect female interactions with infants. The youngest infants received the most natal attraction and infant handling, and male infants were handled more than female infants. The potential benefits of learning to mother and inclusive fitness, in combination with the relatively low costs of natal attraction and infant handling, may explain the high rates of these behaviors in many colobines. Am. J. Primatol. 77:376–387, 2015. © 2014 Wiley Periodicals, Inc.

Male takeovers affect male tenure, female mate choice and ultimately, individual reproductive suc... more Male takeovers affect male tenure, female mate choice and ultimately, individual reproductive success in group-living primates. In social systems with female philopatry and high male reproductive skew, male takeovers largely determine female mate choice, whereas in species with female dispersal, females have the option of deserting a new male. We focused on a species with facultative female dispersal to investigate which factors promote female desertion of males after takeover, using 15 cases (12 for which we have complete data on the takeover process and the female dispersal outcome). These cases took place in nine groups of Colobus vellerosus between 2001 and 2013 at the Boabeng-Fiema Monkey Sanctuary, Ghana. Quick takeovers were usually achieved by single adult males and were never followed by female dispersal. Slow takeovers involved several males, and these takeovers were regularly accompanied by female emigration. Infant attacks and infanticide by males occurred during both kinds of takeovers, but females with dependent offspring never dispersed, regardless of whether their infant was attacked or killed by the new male(s). Subadult females, who were not constrained by the presence of infants, dispersed more often after slow takeovers than after quick takeovers. Whether female dispersal post-takeover is an expression of female mate choice, or occurs to avoid the social upheaval surrounding slow takeovers, remains to be investigated. Am. J. Primatol.

Females that do not experience strong contest competition for food are presumed to form 'egalitar... more Females that do not experience strong contest competition for food are presumed to form 'egalitarian' relationships (i.e., lacking strong, linear dominance hierarchies). However, recent studies of Gorilla beringei beringei (mountain gorilla) have documented relatively strong, linear female dominance hierarchies despite them having a highly folivorous diet that generates relatively low levels of within-group contest competition (Robbins et al., 2005(Robbins et al., , 2007. To investigate if this pattern holds true for other highly folivorous species that may experience low levels of contest competition, we examined the linearity and strength of female dominance hierarchies in a population of Colobus vellerosus (ursine colobus or white-thighed colobus) at Boabeng-Fiema, Ghana. From 2004 to 2011, we collected data via ad libitum and focal sampling of 75 adult and subadult females in eight groups. Half of the study groups had few unknown submissive relationships, and females formed individualistic hierarchies with high linearity indices ranging from 0.9 to 1. There was between-group variation in all components of hierarchical strength (i.e., hierarchical expression, consistency, and stability). Groups showed varying rates of submission, and there was a short latency to detect a linear hierarchy in some groups and a long latency in other groups (i.e., varying levels of hierarchical expression). Females in most groups formed unidirectional and stable relationships. Maturing females challenged older females in some groups, and these groups had more non-linear relationships (i.e., dyads with more submissive interactions down rather than up the hierarchy) and higher rates of individual rank change than other groups. Based on low rates of submission, long latencies, and/or some inconsistencies, we conclude that most groups form relatively

The threat of infanticide by males is suggested to determine upper group size limits for some fol... more The threat of infanticide by males is suggested to determine upper group size limits for some folivores because large female aggregations attract immigrating males. When groups get large enough to become multimale, infanticide risk should decline because, all other things being equal, more males should deter outside takeovers and the counterstrategies of mothers and sires should lower the consequences of inside takeovers. To determine if this scenario can be generalized to all folivorous primates, we began by examining the influence of female and male group size on 4 increasing levels of infanticide risk in folivorous ursine colobus monkeys (Colobus vellerosus) at Boabeng-Fiema, Ghana. Data from 2004 to 2010 on 7 groups analyzed with generalized estimating equation models showed that infanticide risk is heightened in groups with more females and absolutely more males because male immigration is more frequent. However, when controlling for the effect of female group size on male group size, groups with relatively more males have significantly more male immigration and higher infanticide rates. Thus, multimale groups of C. vellerosus show higher infanticide risk compared with unimale groups. Resident males in unimale groups may be higher quality than those in multimale groups because they perform more energetically costly displays and win more encounters. However, males in multimale groups may also suffer from collective action problems making them unable to prevent male immigration and infanticide. This study highlights the importance of the quality of male defenders in infanticide risk and demonstrates intersexual and intrasexual conflict in group composition in C. vellerosus.

I examined the effect of female kinship and relatedness on natal attraction and infant handling i... more I examined the effect of female kinship and relatedness on natal attraction and infant handling in wild Colobus vellerosus, an egalitarian, female philopatric species.

Behavioral Ecology and Sociobiology, 2022

Maternal lactational investment can affect female reproductive rates and offspring survival in ma... more Maternal lactational investment can affect female reproductive rates and offspring survival in mammals and can be biased towards infants of one sex. We compared estimates of lactation effort among mothers, assessed as their potential milk contribution to age-specific infant diets (mother-infant differences in fecal stable nitrogen isotopes, δ15N), to the timing of weaning (infant age at last nursing bout) and to maternal inter-birth interval lengths for male and female infant chimpanzees (Pan troglodytes) at Ngogo, Uganda. Infant males had greater proportions of milk in their age-specific diets, indicated by higher mother-infant differences in δ15N (Generalized Estimating Equation, GEE: p

Cave and Karst Systems of Romania, 2018

The Pârgavului Cave is located in the Vâlcan Mountains (South Carpathians) and develops in Lower ... more The Pârgavului Cave is located in the Vâlcan Mountains (South Carpathians) and develops in Lower and Middle Jurassic limestones. Due to various carbonate facies, the dissolution acted selectively; thus, cave passages show different morphologies. The Mesozoic tectonics events combined with the hydrogeological conditions existing during the Quaternary, created a unique imprint on various geomorphological aspect of the cave. Speleothems are present in the sub-horizontal part of the cave. The progressive incision of the underground river led to the formation of several generations of shelfstones.

Primates, 2021

Infant handling (holding or carrying) by adult males is rare in mammals; however, high levels hav... more Infant handling (holding or carrying) by adult males is rare in mammals; however, high levels have been reported in some primates. Though infant handling is a costly behaviour, there are many benefits that male handlers can accrue. Infant handling by males is most conspicuous in platyrrhines and tends to be uncommon in catarrhines. In the latter species, research on male-infant interactions has focused on low-cost behaviours, such as proximity and grooming. However, to better understand the evolution of infant handling by males, more data on its occurrence across the Primate order are essential, even in species where it is relatively uncommon. We compare the occurrence of infant handling by males in three closely related species of catarrhine: Colobus vellerosus, C. guereza, and C. angolensis ruwenzorii. We collected focal animal samples on infants to quantify infant handling rates and durations, and found that adult male C. a. ruwenzorii handled infants much more frequently and for much longer than males in the other two species. We discuss how C. a. ruwenzorii's unique social organization may explain high levels of infant handling by adult males in this species. More long-term and detailed comparisons of infant handling across species and populations will shed light on how sociality has shaped the evolution of this behaviour in the Primate order.

Journal of Human Evolution, 2020

Premasticated food transfer, when an individual partially breaks down food through chewing and fe... more Premasticated food transfer, when an individual partially breaks down food through chewing and feeds it to another individual, usually mouth-to-mouth, is described widely across human cultures. This behavior plays an important role in modern humans' strategy of complementary feeding, which involves supplementing maternal milk in infant diets with processed, easily digestible versions of adult foods. The extent to which other primates engage in premasticated food transfer with infants is unclear, as premasticated food transfers have been only occasionally reported in other ape species. We investigated premasticated food transfers in 62 mother-infant pairs of wild chimpanzees at Ngogo, Uganda, as well as unresisted food taking, when mothers passively allow infants to seize food. We evaluated the presence or absence and rates of premasticated food transfer and unresisted food taking relative to maternal parity and infant age and sex and assessed the food species and part used. We found that chimpanzee mothers regularly shared premasticated food with their infants aged between 6 months and 4 years, but they were more likely to share, and more frequently shared, with younger infants. The frequency with which females shared premasticated food may relate to maternal experience, as multiparous females shared premasticated food more often than did first-time mothers, which we did not find with unresisted food taking. Both easy-to-chew, commonly eaten foods and tougher, rarely eaten foods were shared. Premasticated food transfer and unresisted food taking may be infant-rearing strategies to facilitate the transition from a diet of exclusive maternal milk to solid food during early infancy. Premasticated food transfer in particular may provide energetic, immune, or growth benefits to infants through reduced chewing effort and maternal saliva. Given our findings in chimpanzees and earlier reports in other ape species, we suggest that the foundation of complementary feeding, a uniquely hominin strategy, might have been present in a common ancestor shared with the other great apes in the form of premasticated, mouth-to-mouth food transfer by mothers with their offspring.

American journal of physical anthropology, 2017

Determining nutritional development in wild primates is difficult through observations because co... more Determining nutritional development in wild primates is difficult through observations because confirming dietary intake is challenging. Physiological measures are needed to determine the relative contributions of maternal milk and other foods at different ages, and time of weaning. We used fecal stable carbon and nitrogen isotopes (δ(13) C, δ(15) N) and fecal nitrogen concentrations (%N) from wild chimpanzees at Ngogo, Uganda, to derive physiological dietary indicators during the transition from total reliance on maternal milk to adult foods after weaning. We analyzed 560 fecal samples collected non-invasively from 48 infants, their mothers, and 6 juvenile siblings. Most infant and juvenile samples (90%) were matched to samples collected from mothers on the same day. Isotopic assessments were compared with observations of nursing and feeding. Infants ≤1 year old showed average δ(15) N, δ(13) C and %N ratios that were 2.0‰, 0.8‰ and 1.3% greater than their mothers, respectively, int...

Royal Society open science, 2016

Alloparenting, when individuals other than the mother assist with infant care, can vary between a... more Alloparenting, when individuals other than the mother assist with infant care, can vary between and within populations and has potential fitness costs and benefits for individuals involved. We investigated the effects of alloparenting on the speed with which infants were weaned, a potential component of maternal fitness because of how it can affect inter-birth intervals, in wild chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Uganda. We also provide, to our knowledge, the first description of alloparenting in this population and present a novel measure of the contribution of milk to infant diets through faecal stable nitrogen isotopes (δ(15)N). Using 42 mother-infant pairs, we tested associations of two alloparenting dimensions, natal attraction (interest in infants) and infant handling (holding, carrying), to the proportion of time mothers spent feeding and to maternal lactation effort (mean nursing rates and mother-infant δ(15)N differences). Neither natal attraction nor in...

American journal of primatology, 2015

Primate females often inspect, touch and groom others' infants (natal attraction) and they ma... more Primate females often inspect, touch and groom others' infants (natal attraction) and they may hold and carry these infants in a manner resembling maternal care (infant handling). While natal attraction and infant handling occur in most wild colobines, little is known about the factors influencing the expression of these behaviors. We examined the effects of female parity, kinship, and dominance rank, as well as infant age and sex in wild Colobus vellerosus at Boabeng-Fiema Monkey Sanctuary, Ghana. We collected data via focal sampling of females in 2008 and 2009 (N = 61) and of infants in 2010 (N = 12). Accounting for the individuals who interacted with our focal subjects, this study includes 74 females and 66 infants in 8 groups. We recorded female agonistic interactions ad libitum to determine dominance ranks. We used partial pedigree information and genotypes at 17 short tandem repeat loci to determine kinship. We knew female parity, infant age and sex from demographic record...

Behaviour, 2013

Females that do not experience strong contest competition for food are presumed to form 'egalitar... more Females that do not experience strong contest competition for food are presumed to form 'egalitarian' relationships (i.e., lacking strong, linear dominance hierarchies). However, recent studies of Gorilla beringei beringei (mountain gorilla) have documented relatively strong, linear female dominance hierarchies despite them having a highly folivorous diet that generates relatively low levels of within-group contest competition (Robbins et al., 2005, 2007). To investigate if this pattern holds true for other highly folivorous species that may experience low levels of contest competition, we examined the linearity and strength of female dominance hierarchies in a population of Colobus vellerosus (ursine colobus or white-thighed colobus) at Boabeng-Fiema, Ghana. From 2004 to 2011, we collected data via ad libitum and focal sampling of 75 adult and subadult females in eight groups. Half of the study groups had few unknown submissive relationships, and females formed individualistic hierarchies with high linearity indices ranging from 0.9 to 1. There was between-group variation in all components of hierarchical strength (i.e., hierarchical expression, consistency, and stability). Groups showed varying rates of submission, and there was a short latency to detect a linear hierarchy in some groups and a long latency in other groups (i.e., varying levels of hierarchical expression). Females in most groups formed unidirectional and stable relationships. Maturing females challenged older females in some groups, and these groups had more non-linear relationships (i.e., dyads with more submissive interactions down rather than up the hierarchy) and higher rates of individual rank change than other groups. Based on low rates of submission, long latencies, and/or some inconsistencies, we conclude that most groups form relatively

American Journal of Primatology, 2015

Male takeovers affect male tenure, female mate choice and ultimately, individual reproductive suc... more Male takeovers affect male tenure, female mate choice and ultimately, individual reproductive success in group-living primates. In social systems with female philopatry and high male reproductive skew, male takeovers largely determine female mate choice, whereas in species with female dispersal, females have the option of deserting a new male. We focused on a species with facultative female dispersal to investigate which factors promote female desertion of males after takeover, using 15 cases (12 for which we have complete data on the takeover process and the female dispersal outcome). These cases took place in nine groups of Colobus vellerosus between 2001 and 2013 at the Boabeng-Fiema Monkey Sanctuary, Ghana. Quick takeovers were usually achieved by single adult males and were never followed by female dispersal. Slow takeovers involved several males, and these takeovers were regularly accompanied by female emigration. Infant attacks and infanticide by males occurred during both kinds of takeovers, but females with dependent offspring never dispersed, regardless of whether their infant was attacked or killed by the new male(s). Subadult females, who were not constrained by the presence of infants, dispersed more often after slow takeovers than after quick takeovers. Whether female dispersal post-takeover is an expression of female mate choice, or occurs to avoid the social upheaval surrounding slow takeovers, remains to be investigated. Am. J. Primatol.

Objectives: Determining nutritional development in wild primates is difficult through observation... more Objectives: Determining nutritional development in wild primates is difficult through observations because confirming dietary intake is challenging. Physiological measures are needed to determine the relative contributions of maternal milk and other foods at different ages, and time of weaning. We used fecal stable carbon and nitrogen isotopes (d 13 C, d 15 N) and fecal nitrogen concentrations (%N) from wild chimpanzees at Ngogo, Uganda, to derive physiological dietary indicators during the transition from total reliance on maternal milk to adult foods after weaning. Materials and Methods: We analyzed 560 fecal samples collected non-invasively from 48 infants, their mothers, and 6 juvenile siblings. Most infant and juvenile samples (90%) were matched to samples collected from mothers on the same day. Isotopic assessments were compared with observations of nursing and feeding.

Alloparenting, when individuals other than the mother assist with infant care, can vary between a... more Alloparenting, when individuals other than the mother assist with infant care, can vary between and within populations and has potential fitness costs and benefits for individuals involved. We investigated the effects of alloparenting on the speed with which infants were weaned, a potential component of maternal fitness because of how it can affect inter-birth intervals, in wild chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Uganda. We also provide, to our knowledge, the first description of alloparenting in this population and present a novel measure of the contribution of milk to infant diets through faecal stable nitrogen isotopes (δ 15 N). Using 42 mother–infant pairs, we tested associations of two alloparenting dimensions, natal attraction (interest in infants) and infant handling (holding, carrying), to the proportion of time mothers spent feeding and to maternal lactation effort (mean nursing rates and mother–infant δ 15 N differences). Neither natal attraction nor infant handling was significantly associated with feeding time. Infant handling was inversely associated with both measures of lactation effort, although natal attraction showed no association. Alloparenting may benefit mothers by enabling females to invest in their next offspring sooner through accelerated weaning. Our findings emphasize the significance of alloparenting as a flexible component of female reproductive strategies in some species.

Keywords: feeding competition infant development infanticide maternal investment strategy natal c... more Keywords: feeding competition infant development infanticide maternal investment strategy natal coat predation The rate at which infants develop can vary within species. This variation may be due to differences between infants in their nutritional intake and physiology, or the ability of females to adjust the amount and timing of maternal investment to maximize their lifetime reproductive success. This is the first primate study that uses a large sample size and multivariate analyses to investigate whether variation in early infant development (measured visually using durations of natal coat stages) is explained by differences in infanticide pressure, predation pressure or feeding competition among mothers. We recorded the number of days that infants took to transition through each of the two natal coat stages (white to grey: N ¼ 32; grey to black-and-white: N ¼ 22), as well as through their entire natal coats (white to black-and-white: N ¼ 38) in a population of wild ursine colobus, Colobus vellerosus. Infant males, which are at greater risk of infanticidal attacks, transitioned coat colours earlier than females, and infants in multimale groups, where infanticide occurs more frequently, transitioned earlier than infants in unimale groups. Variation in group size did not affect natal coat durations, which suggests that the intensity of predation risk and feeding competition do not influence development. Instead of terminating investment in offspring before birth, as in the 'Bruce effect', females may invest more heavily in infants after birth in order to speed up infant development and reduce the time period during which offspring are the most vulnerable to infanticide. Mothers may therefore have flexible means of exerting choice over maternal investment in relation to infanticide risk. However, the extent to which mothers and infants are responsible for adjusting the speed of development is unknown.

Primate females often inspect, touch and groom others' infants (natal attraction) and they may ho... more Primate females often inspect, touch and groom others' infants (natal attraction) and they may hold and carry these infants in a manner resembling maternal care (infant handling). While natal attraction and infant handling occur in most wild colobines, little is known about the factors influencing the expression of these behaviors. We examined the effects of female parity, kinship, and dominance rank, as well as infant age and sex in wild Colobus vellerosus at Boabeng-Fiema Monkey Sanctuary, Ghana. We collected data via focal sampling of females in 2008 and 2009 (N = 61) and of infants in 2010 (N = 12). Accounting for the individuals who interacted with our focal subjects, this study includes 74 females and 66 infants in 8 groups. We recorded female agonistic interactions ad libitum to determine dominance ranks. We used partial pedigree information and genotypes at 17 short tandem repeat loci to determine kinship. We knew female parity, infant age and sex from demographic records. Nulliparous females showed more natal attraction and infant handling than parous females, which may suggest that interactions with infants are more adaptive for nulliparous females because they learn mothering skills through these behaviors. Compared to non-kin, maternal kin were more likely to handle infants. Maternal kin may be permitted greater access to infants because mothers are most familiar with them. Handlers may incur inclusive fitness benefits from infant handling. Dominance rank did not affect female interactions with infants. The youngest infants received the most natal attraction and infant handling, and male infants were handled more than female infants. The potential benefits of learning to mother and inclusive fitness, in combination with the relatively low costs of natal attraction and infant handling, may explain the high rates of these behaviors in many colobines. Am. J. Primatol. 77:376–387, 2015. © 2014 Wiley Periodicals, Inc.Primate females often inspect, touch and groom others' infants (natal attraction) and they may hold and carry these infants in a manner resembling maternal care (infant handling). While natal attraction and infant handling occur in most wild colobines, little is known about the factors influencing the expression of these behaviors. We examined the effects of female parity, kinship, and dominance rank, as well as infant age and sex in wild Colobus vellerosus at Boabeng-Fiema Monkey Sanctuary, Ghana. We collected data via focal sampling of females in 2008 and 2009 (N = 61) and of infants in 2010 (N = 12). Accounting for the individuals who interacted with our focal subjects, this study includes 74 females and 66 infants in 8 groups. We recorded female agonistic interactions ad libitum to determine dominance ranks. We used partial pedigree information and genotypes at 17 short tandem repeat loci to determine kinship. We knew female parity, infant age and sex from demographic records. Nulliparous females showed more natal attraction and infant handling than parous females, which may suggest that interactions with infants are more adaptive for nulliparous females because they learn mothering skills through these behaviors. Compared to non-kin, maternal kin were more likely to handle infants. Maternal kin may be permitted greater access to infants because mothers are most familiar with them. Handlers may incur inclusive fitness benefits from infant handling. Dominance rank did not affect female interactions with infants. The youngest infants received the most natal attraction and infant handling, and male infants were handled more than female infants. The potential benefits of learning to mother and inclusive fitness, in combination with the relatively low costs of natal attraction and infant handling, may explain the high rates of these behaviors in many colobines. Am. J. Primatol. 77:376–387, 2015. © 2014 Wiley Periodicals, Inc.

Male takeovers affect male tenure, female mate choice and ultimately, individual reproductive suc... more Male takeovers affect male tenure, female mate choice and ultimately, individual reproductive success in group-living primates. In social systems with female philopatry and high male reproductive skew, male takeovers largely determine female mate choice, whereas in species with female dispersal, females have the option of deserting a new male. We focused on a species with facultative female dispersal to investigate which factors promote female desertion of males after takeover, using 15 cases (12 for which we have complete data on the takeover process and the female dispersal outcome). These cases took place in nine groups of Colobus vellerosus between 2001 and 2013 at the Boabeng-Fiema Monkey Sanctuary, Ghana. Quick takeovers were usually achieved by single adult males and were never followed by female dispersal. Slow takeovers involved several males, and these takeovers were regularly accompanied by female emigration. Infant attacks and infanticide by males occurred during both kinds of takeovers, but females with dependent offspring never dispersed, regardless of whether their infant was attacked or killed by the new male(s). Subadult females, who were not constrained by the presence of infants, dispersed more often after slow takeovers than after quick takeovers. Whether female dispersal post-takeover is an expression of female mate choice, or occurs to avoid the social upheaval surrounding slow takeovers, remains to be investigated. Am. J. Primatol.

Females that do not experience strong contest competition for food are presumed to form 'egalitar... more Females that do not experience strong contest competition for food are presumed to form 'egalitarian' relationships (i.e., lacking strong, linear dominance hierarchies). However, recent studies of Gorilla beringei beringei (mountain gorilla) have documented relatively strong, linear female dominance hierarchies despite them having a highly folivorous diet that generates relatively low levels of within-group contest competition (Robbins et al., 2005(Robbins et al., , 2007. To investigate if this pattern holds true for other highly folivorous species that may experience low levels of contest competition, we examined the linearity and strength of female dominance hierarchies in a population of Colobus vellerosus (ursine colobus or white-thighed colobus) at Boabeng-Fiema, Ghana. From 2004 to 2011, we collected data via ad libitum and focal sampling of 75 adult and subadult females in eight groups. Half of the study groups had few unknown submissive relationships, and females formed individualistic hierarchies with high linearity indices ranging from 0.9 to 1. There was between-group variation in all components of hierarchical strength (i.e., hierarchical expression, consistency, and stability). Groups showed varying rates of submission, and there was a short latency to detect a linear hierarchy in some groups and a long latency in other groups (i.e., varying levels of hierarchical expression). Females in most groups formed unidirectional and stable relationships. Maturing females challenged older females in some groups, and these groups had more non-linear relationships (i.e., dyads with more submissive interactions down rather than up the hierarchy) and higher rates of individual rank change than other groups. Based on low rates of submission, long latencies, and/or some inconsistencies, we conclude that most groups form relatively

The threat of infanticide by males is suggested to determine upper group size limits for some fol... more The threat of infanticide by males is suggested to determine upper group size limits for some folivores because large female aggregations attract immigrating males. When groups get large enough to become multimale, infanticide risk should decline because, all other things being equal, more males should deter outside takeovers and the counterstrategies of mothers and sires should lower the consequences of inside takeovers. To determine if this scenario can be generalized to all folivorous primates, we began by examining the influence of female and male group size on 4 increasing levels of infanticide risk in folivorous ursine colobus monkeys (Colobus vellerosus) at Boabeng-Fiema, Ghana. Data from 2004 to 2010 on 7 groups analyzed with generalized estimating equation models showed that infanticide risk is heightened in groups with more females and absolutely more males because male immigration is more frequent. However, when controlling for the effect of female group size on male group size, groups with relatively more males have significantly more male immigration and higher infanticide rates. Thus, multimale groups of C. vellerosus show higher infanticide risk compared with unimale groups. Resident males in unimale groups may be higher quality than those in multimale groups because they perform more energetically costly displays and win more encounters. However, males in multimale groups may also suffer from collective action problems making them unable to prevent male immigration and infanticide. This study highlights the importance of the quality of male defenders in infanticide risk and demonstrates intersexual and intrasexual conflict in group composition in C. vellerosus.

I examined the effect of female kinship and relatedness on natal attraction and infant handling i... more I examined the effect of female kinship and relatedness on natal attraction and infant handling in wild Colobus vellerosus, an egalitarian, female philopatric species.