Investigating infant feeding development in wild chimpanzees using stable isotopes of naturally shed hair.

Measuring the relative contributions of milk and non-milk foods in the diets of primate infants is difficult from observations. Stable carbon (δ13 C) and nitrogen (δ15 N) isotopes in hair can be used to physiologically track infant feeding through development, but few wild studies have done so, likely due to the difficulty in collecting hair non-invasively. We assessed infant feeding at different ages in wild chimpanzees (Pan troglodytes) at Ngogo, Uganda using δ13 C and δ15 N of keratin in 164 naturally shed hairs from 29 infants (61 hairs), 6 juveniles (7 hairs), 28 mothers (67 hairs) and 14 adult males (29 hairs). Hairs were collected when they stuck to feces during defecation or from the ground after chimpanzees groomed or rested. We could not distinguish between the hairs of infants and mothers using strand length and diameter. Infants 1-2 years old were most enriched in 13 C and 15 N and showed means of 1.1‰ in δ13 C and 2.1‰ in δ15 N above their mothers. Infants at 2 years had hair δ13 C values like those of their mothers, which suggests infants began relying more heavily on plants around this age. While mother-infant δ13 C and δ15 N differences generally decreased with offspring age, as is expected when infants rely increasingly more on independent foraging through development, milk seemed to remain an important dietary component for infants older than 2.5 years, as evidenced by continuing elevated δ15 N. We showed that stable carbon and nitrogen isotopes in naturally shed hairs can feasibly detect trophic level differences between chimpanzee infants and mothers. Since it can mitigate some of the limitations associated with behavioral and fecal stable isotope data, the use of hair stable isotopes is a useful, non-invasive tool for assessing infant feeding development in wild primates.

Premasticated food transfer by wild chimpanzee mothers with their infants: Effects of maternal parity, infant age and sex, and food properties.

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.

Valorisation possibilities of exhausted biosorbents loaded with metal ions - A review.

Biosorption is considered one of the most promising methods for removal of metal ions from aqueous effluents, due to its low-cost and eco-friendly characteristics. However, the exhausted biosorbents loaded with metal ions, obtained at the end of biosorption processes, are still a problem which should be solved to increase the applicability of biosorption on an industrial scale. In this study are examined three possibilities for the valorisation of exhausted biosorbents loaded with metal ions, namely: (i) regeneration and reuse of biosorbents in multiple biosorption cycles, (ii) the use of exhausted biosorbents as fertilizers for soils poor in essential microelements, and (iii) the pyrolysis of exhausted biosorbents, under well defined conditions. The main advantages and disadvantages of each valorisation possibility are reviewed in order to find the best way to use these cheap materials in accordance with the principles of the circular economy and thereby contributing to the development of sustainable biosorption technology.

A novel fecal stable isotope approach to determine the timing of age-related feeding transitions in wild infant chimpanzees.

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 (δ13 C, δ15 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. RESULTS: Infants ≤1 year old showed average δ15 N, δ13 C and %N ratios that were 2.0‰, 0.8‰ and 1.3% greater than their mothers, respectively, interpreted as trophic level effects. Although data collected on newborns were few, results suggest that solid foods were consumed within 2-5 months after birth. Trophic level differences decreased steadily after 1 year, which indicates a decreasing relative contribution of milk to the diet. Isotopic results indicated infants were weaned by 4.5 years old-more than a year earlier than observations of nipple contacts ceased, which revealed the occurrence of "comfort nursing." Juvenile isotopic signatures indicate no nursing overlap between siblings. DISCUSSION: Our results resemble the stable isotope differences of human babies. This study contributes to a model of chimpanzee nutritional development required to understand early life history patterns in hominins.

The influence of male takeovers on female dispersal in Colobus vellerosus.

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. 79:e22436, 2017. © 2015 Wiley Periodicals, Inc.

Female parity, maternal kinship, infant age and sex influence natal attraction and infant handling in a wild colobine (Colobus vellerosus).

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.

Same-sex sexual behaviour among mammals is widely observed, yet seldomly reported: Evidence from an online expert survey.

Same-sex sexual behaviour (SSSB) occurs in most animal clades, but published reports are largely concentrated in a few taxa. Thus, there remains a paucity of published reports for most mammalian species. We conducted a cross-sectional expert survey to better understand the underlying reasons for the lack of publications on this topic. Most respondents researched Primates (83.6%, N = 61), while the rest studied Carnivora (6.9%, N = 5), Rodentia (4.1%, N = 3), Artiodactyla (2.7%, N = 2), and Proboscidea (2.7%, N = 2). Most respondents (76.7%, N = 56) had observed SSSB in their study species, but only 48.2% (N = 27) collected data on SSSB, and few (18.5%, N = 5) had published papers on SSSB. Of the unique species identified as engaging in SSSB in the survey, 38.6% (N = 17) have no existing reports of SSSB to the knowledge of the authors. In both the survey questions and freeform responses, most respondents indicated that their lack of data collection or publication on SSSB was because the behaviours were rare, or because it was not a research priority of their lab. No respondents reported discomfort or sociopolitical concerns at their university or field site as a reason for why they did not collect data or publish on SSSB. Multiple logistic regressions were performed to assess whether taxa studied, education level, or identification within the LGBTQ+ community predicted observing, collecting data on, or publishing on SSSB, but none of these variables were significant predictors. These results provide preliminary evidence that SSSB occurs more frequently than what is available in the published record and suggest that this may be due to a publishing bias against anecdotal evidence.

Effects of infant age and sex, and maternal parity on the interaction of lactation with infant feeding development in chimpanzees.

The interaction between infant feeding and maternal lactational physiology influences female inter-birth intervals and mediates maternal reproductive trade-offs. We investigated variation in feeding development in 72 immature wild chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda, and made inferences about maternal lactation over the course of infancy. We compared the percentage (%) of time that mothers nursed infants as a function of infant age and assessed how hourly rates and bout durations of nursing and foraging varied in association with differences in offspring age, sex, and maternal parity. Nursing % times, rates and durations were highest for infants ≤ 6 months old but did not change significantly from 6 months to 5 years old. Nursing continued at a decreasing rate for some 5- to 7-year-olds. Infants ≤ 6 months old foraged little. Foraging rates did not change after 1 year old, but foraging durations and the % time devoted to foraging increased with age. Independent foraging probably became a dietary requirement for infants at 1 year old, when their energy needs may have surpassed the available milk energy. Infants spent as much time foraging by the time they were 4 to 5 years old as adults did. No sex effect on infant nursing or foraging was apparent, but infants of primiparous females had higher foraging rates and spent more time foraging than the infants of multiparous females did. Although no data on milk composition were collected, these findings are consistent with a working hypothesis that like other hominoids, chimpanzee mothers maintained a fixed level of lactation effort over several years as infants increasingly supplemented their growing energy, micronutrient and hydration needs via independent foraging. Plateauing lactation may be a more widespread adaptation that allows hominoid infants time to attain the physiology and skills necessary for independent feeding, while also providing them with a steady dietary base on which they could rely consistently through infancy, and enabling mothers to maintain a fixed, predictable level of lactation effort.

High levels of infant handling by adult males in Rwenzori Angolan colobus (Colobus angolensis ruwenzorii) compared to two closely related species, C. guereza and C. vellerosus.

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.

Alloparenting is associated with reduced maternal lactation effort and faster weaning in wild chimpanzees.

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 (δ15N). 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 δ15N 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.