---
_id: '61026'
abstract:
- lang: eng
text: In mammals, pregnancy and lactation are marked by calcium stress and bone
resorption, leading to reduced bone mineral density. In humans, these periods
may partly explain the higher prevalence of osteoporosis in older women compared
with men, but lactation patterns in modern humans may reflect cultural influences
rather than natural conditions. The extent to which these findings apply to wild-living
mammals remains unknown. We measured urinary C-terminal crosslinking telopeptide
of Type I collagen (CTX-I) levels, a bone resorption marker, during pregnancy
in wild and zoo-housed bonobos (Pan paniscus) and during lactation in wild bonobos.
Studying wild-living primates such as bonobos can provide insights into ancestral
reproductive adaptations. We found an increase in CTX-I levels towards the end
of pregnancy in zoo-housed and primiparous wild females. Contrary to expectations,
CTX-I levels during early lactation are lower than in other reproductive phases.
This pattern diverges from the assumption that lactation increases bone resorption.
Our findings suggest that wild bonobos may use physiological or behavioral strategies
to modulate bone metabolism during lactation. These adaptations, shaped in natural
environments, provide insight into evolutionary pressures on skeletal health and
may inform strategies to mitigate bone loss in humans.
author:
- first_name: Verena
full_name: Behringer, Verena
last_name: Behringer
- first_name: Ruth
full_name: Sonnweber, Ruth
last_name: Sonnweber
- first_name: Barbara
full_name: Fruth, Barbara
last_name: Fruth
- first_name: Genevieve
full_name: Housman, Genevieve
last_name: Housman
- first_name: Pamela Heidi
full_name: Douglas, Pamela Heidi
id: '72311'
last_name: Douglas
- first_name: Jeroen M. G.
full_name: Stevens, Jeroen M. G.
last_name: Stevens
- first_name: Gottfried
full_name: Hohmann, Gottfried
last_name: Hohmann
- first_name: Tracy L.
full_name: Kivell, Tracy L.
last_name: Kivell
citation:
ama: Behringer V, Sonnweber R, Fruth B, et al. Wild bonobos experience unusually
low bone resorption during early lactation relative to humans and other mammals.
Evolutionary Human Sciences. 2025;7(e27):1-23. doi:10.1017/ehs.2025.10013
apa: Behringer, V., Sonnweber, R., Fruth, B., Housman, G., Douglas, P. H., Stevens,
J. M. G., Hohmann, G., & Kivell, T. L. (2025). Wild bonobos experience unusually
low bone resorption during early lactation relative to humans and other mammals.
Evolutionary Human Sciences, 7(e27), 1–23. https://doi.org/10.1017/ehs.2025.10013
bibtex: '@article{Behringer_Sonnweber_Fruth_Housman_Douglas_Stevens_Hohmann_Kivell_2025,
title={Wild bonobos experience unusually low bone resorption during early lactation
relative to humans and other mammals}, volume={7}, DOI={10.1017/ehs.2025.10013},
number={e27}, journal={Evolutionary Human Sciences}, publisher={Cambridge University
Press (CUP)}, author={Behringer, Verena and Sonnweber, Ruth and Fruth, Barbara
and Housman, Genevieve and Douglas, Pamela Heidi and Stevens, Jeroen M. G. and
Hohmann, Gottfried and Kivell, Tracy L.}, year={2025}, pages={1–23} }'
chicago: 'Behringer, Verena, Ruth Sonnweber, Barbara Fruth, Genevieve Housman, Pamela
Heidi Douglas, Jeroen M. G. Stevens, Gottfried Hohmann, and Tracy L. Kivell. “Wild
Bonobos Experience Unusually Low Bone Resorption during Early Lactation Relative
to Humans and Other Mammals.” Evolutionary Human Sciences 7, no. e27 (2025):
1–23. https://doi.org/10.1017/ehs.2025.10013.'
ieee: 'V. Behringer et al., “Wild bonobos experience unusually low bone resorption
during early lactation relative to humans and other mammals,” Evolutionary
Human Sciences, vol. 7, no. e27, pp. 1–23, 2025, doi: 10.1017/ehs.2025.10013.'
mla: Behringer, Verena, et al. “Wild Bonobos Experience Unusually Low Bone Resorption
during Early Lactation Relative to Humans and Other Mammals.” Evolutionary
Human Sciences, vol. 7, no. e27, Cambridge University Press (CUP), 2025, pp.
1–23, doi:10.1017/ehs.2025.10013.
short: V. Behringer, R. Sonnweber, B. Fruth, G. Housman, P.H. Douglas, J.M.G. Stevens,
G. Hohmann, T.L. Kivell, Evolutionary Human Sciences 7 (2025) 1–23.
date_created: 2025-08-26T19:28:20Z
date_updated: 2025-09-04T11:44:28Z
ddc:
- '590'
department:
- _id: '40'
doi: 10.1017/ehs.2025.10013
file:
- access_level: open_access
content_type: application/pdf
creator: hdouglas
date_created: 2025-09-04T11:39:04Z
date_updated: 2025-09-04T11:39:04Z
file_id: '61133'
file_name: Behringer et al - 2025 - Wild-bonobos-experience-unusually-low-bone-resorption-during-early-lactation-relative-to-humans-and-other-mammals.pdf
file_size: 1473060
relation: main_file
file_date_updated: 2025-09-04T11:39:04Z
has_accepted_license: '1'
intvolume: ' 7'
issue: e27
keyword:
- Reproductive phase
- Hominoid
- CTX-I
- Bone turnover markers
- Pan paniscus
- Bone density
language:
- iso: eng
main_file_link:
- open_access: '1'
url: https://www.cambridge.org/core/services/aop-cambridge-core/content/view/E819AFD9F17034D21F2F39FC9817C35E/S2513843X25100133a.pdf/wild-bonobos-experience-unusually-low-bone-resorption-during-early-lactation-relative-to-humans-and-other-mammals.pdf
oa: '1'
page: 1-23
publication: Evolutionary Human Sciences
publication_identifier:
issn:
- 2513-843X
publication_status: published
publisher: Cambridge University Press (CUP)
status: public
title: Wild bonobos experience unusually low bone resorption during early lactation
relative to humans and other mammals
type: journal_article
user_id: '72311'
volume: 7
year: '2025'
...
---
_id: '61023'
abstract:
- lang: eng
text: "Objectives: \r\nFemale bonobos (Pan paniscus) are characterized as highly
affiliative and cooperative,but few studies have quantified the strength and stability
of female intra-sexual relationships or explored how variation in social relationships
influences cooperation. We measure female social preferences, identify causes
of variation in preferences, and test whether variation in social preferences
predicts food sharing or coalitionary support.\r\nMethods: Data were collected
over 3 years from females in the Bompusa community at LuiKotale,DRC. We measured
genetic relatedness and constructed social preference indices for party association,
proximity, grooming, GG-rubbing and aggression. We identified preferred social
partners based on permutation tests and measured stability using Mantel tests.
We used factor analysis to identify inter-relationships between preference indices
and used LMMs to test whether variation in social preferences was explained by
relatedness, rank differences, having dependent young or co-residency time. We
used GLMMs to test whether variation in social preferences predicted food sharing
or coalitionary support.\r\nResults: All females had preferred non-kin partners
for proximity, grooming or GG-rubbing, but only grooming preferences were stable
across years. Association indices were higher among lactating females, and aggression
was lower among females with longer co-residency times. The factor analysis identified
one factor, representing proximity and GG-rubbing preferences, labeled behavioral
coordination. Dyads with higher levels of behavioral coordination were more likely
to share food.\r\nConclusions: Female bonobos exhibit stable, differentiated grooming
relationships outside of kinship and philopatry. Females also exhibit flexible
proximity and GG-rubbing preferences that may facilitate cooperation with a wider
range of social partners."
article_type: original
author:
- first_name: Liza R.
full_name: Moscovice, Liza R.
last_name: Moscovice
- first_name: Pamela Heidi
full_name: Douglas, Pamela Heidi
id: '72311'
last_name: Douglas
- first_name: Laura
full_name: Martinez‐Iñigo, Laura
last_name: Martinez‐Iñigo
- first_name: Martin
full_name: Surbeck, Martin
last_name: Surbeck
- first_name: Linda
full_name: Vigilant, Linda
last_name: Vigilant
- first_name: Gottfried
full_name: Hohmann, Gottfried
last_name: Hohmann
citation:
ama: Moscovice LR, Douglas PH, Martinez‐Iñigo L, Surbeck M, Vigilant L, Hohmann
G. Stable and fluctuating social preferences and implications for cooperation
among female bonobos at LuiKotale, Salonga National Park, DRC. American Journal
of Physical Anthropology. 2017;163(1):158-172. doi:10.1002/ajpa.23197
apa: Moscovice, L. R., Douglas, P. H., Martinez‐Iñigo, L., Surbeck, M., Vigilant,
L., & Hohmann, G. (2017). Stable and fluctuating social preferences and implications
for cooperation among female bonobos at LuiKotale, Salonga National Park, DRC.
American Journal of Physical Anthropology, 163(1), 158–172. https://doi.org/10.1002/ajpa.23197
bibtex: '@article{Moscovice_Douglas_Martinez‐Iñigo_Surbeck_Vigilant_Hohmann_2017,
title={Stable and fluctuating social preferences and implications for cooperation
among female bonobos at LuiKotale, Salonga National Park, DRC}, volume={163},
DOI={10.1002/ajpa.23197}, number={1},
journal={American Journal of Physical Anthropology}, publisher={Wiley}, author={Moscovice,
Liza R. and Douglas, Pamela Heidi and Martinez‐Iñigo, Laura and Surbeck, Martin
and Vigilant, Linda and Hohmann, Gottfried}, year={2017}, pages={158–172} }'
chicago: 'Moscovice, Liza R., Pamela Heidi Douglas, Laura Martinez‐Iñigo, Martin
Surbeck, Linda Vigilant, and Gottfried Hohmann. “Stable and Fluctuating Social
Preferences and Implications for Cooperation among Female Bonobos at LuiKotale,
Salonga National Park, DRC.” American Journal of Physical Anthropology
163, no. 1 (2017): 158–72. https://doi.org/10.1002/ajpa.23197.'
ieee: 'L. R. Moscovice, P. H. Douglas, L. Martinez‐Iñigo, M. Surbeck, L. Vigilant,
and G. Hohmann, “Stable and fluctuating social preferences and implications for
cooperation among female bonobos at LuiKotale, Salonga National Park, DRC,” American
Journal of Physical Anthropology, vol. 163, no. 1, pp. 158–172, 2017, doi:
10.1002/ajpa.23197.'
mla: Moscovice, Liza R., et al. “Stable and Fluctuating Social Preferences and Implications
for Cooperation among Female Bonobos at LuiKotale, Salonga National Park, DRC.”
American Journal of Physical Anthropology, vol. 163, no. 1, Wiley, 2017,
pp. 158–72, doi:10.1002/ajpa.23197.
short: L.R. Moscovice, P.H. Douglas, L. Martinez‐Iñigo, M. Surbeck, L. Vigilant,
G. Hohmann, American Journal of Physical Anthropology 163 (2017) 158–172.
date_created: 2025-08-26T18:57:51Z
date_updated: 2025-08-26T19:07:49Z
doi: 10.1002/ajpa.23197
extern: '1'
intvolume: ' 163'
issue: '1'
keyword:
- Pan paniscus
- mtDNA
- proximity
- genito-genital rubbing
- food sharing
language:
- iso: eng
page: 158-172
publication: American Journal of Physical Anthropology
publication_identifier:
issn:
- 0002-9483
- 1096-8644
publication_status: published
publisher: Wiley
status: public
title: Stable and fluctuating social preferences and implications for cooperation
among female bonobos at LuiKotale, Salonga National Park, DRC
type: journal_article
user_id: '72311'
volume: 163
year: '2017'
...
---
_id: '61024'
abstract:
- lang: eng
text: "Background: The evolution of primate sexual swellings and their influence
on mating strategies have captivated the\r\ninterest of biologists for over a
century. Across the primate order, variability in the timing of ovulation with
respect to\r\nfemales’ sexual swelling patterns differs greatly. Since sexual
swellings typically function as signals of female fecundity,\r\nthe temporal relation
between ovulation and sexual swellings can impact the ability of males to pinpoint
ovulation\r\nand thereby affect male mating strategies. Here, we used endocrine
parameters to detect ovulation and examined the\r\ntemporal relation between the
maximum swelling phase (MSP) and ovulation in wild female bonobos (Pan paniscus).\r\nData
were collected at the Luikotale field site, Democratic Republic of Congo, spanning
36 months. Observational data\r\nfrom 13 females were used to characterise female
swelling cycles (N = 70). Furthermore, we measured urinary oestrone\r\nand pregnanediol
using liquid chromatography–tandem mass spectrometry, and used pregnanediol to
determine the\r\ntiming of ovulation in 34 cycles (N = 9 females).\r\nResults:
We found that the duration of females’ MSP was highly variable, ranging from 1
to 31 days. Timing of ovulation\r\nvaried considerably in relation to the onset
of the MSP, resulting in a very low day-specific probability of ovulation and\r\nfecundity
across female cycles. Ovulation occurred during the MSP in only 52.9 % of the
analysed swelling cycles, and\r\nfemales showed regular sexual swelling patterns
in N = 8 swelling cycles where ovulation did not occur. These findings\r\nreveal
that sexual swellings of bonobos are less reliable indicators of ovulation compared
to other species of primates.\r\nConclusions: Female bonobos show unusual variability
in the duration of the MSP and in the timing of ovulation\r\nrelative to the sexual
swelling signal. These data are important for understanding the evolution of sexual
signals, how\r\nthey influence male and female mating strategies, and how decoupling
visual signals of fecundity from the periovulatory\r\nperiod may affect intersexual
conflict. By prolonging the period during which males would need to mate guard
females\r\nto ascertain paternity, the temporal variability of this signal may
constrain mate-guarding efforts by male bonobos."
article_number: '140'
article_type: original
author:
- first_name: Pamela Heidi
full_name: Douglas, Pamela Heidi
id: '72311'
last_name: Douglas
- first_name: Gottfried
full_name: Hohmann, Gottfried
last_name: Hohmann
- first_name: Róisín
full_name: Murtagh, Róisín
last_name: Murtagh
- first_name: Robyn
full_name: Thiessen-Bock, Robyn
last_name: Thiessen-Bock
- first_name: Tobias
full_name: Deschner, Tobias
last_name: Deschner
citation:
ama: 'Douglas PH, Hohmann G, Murtagh R, Thiessen-Bock R, Deschner T. Mixed messages:
wild female bonobos show high variability in the timing of ovulation in relation
to sexual swelling patterns. BMC Evolutionary Biology. 2016;16(1). doi:10.1186/s12862-016-0691-3'
apa: 'Douglas, P. H., Hohmann, G., Murtagh, R., Thiessen-Bock, R., & Deschner,
T. (2016). Mixed messages: wild female bonobos show high variability in the timing
of ovulation in relation to sexual swelling patterns. BMC Evolutionary Biology,
16(1), Article 140. https://doi.org/10.1186/s12862-016-0691-3'
bibtex: '@article{Douglas_Hohmann_Murtagh_Thiessen-Bock_Deschner_2016, title={Mixed
messages: wild female bonobos show high variability in the timing of ovulation
in relation to sexual swelling patterns}, volume={16}, DOI={10.1186/s12862-016-0691-3},
number={1140}, journal={BMC Evolutionary Biology}, publisher={Springer Science
and Business Media LLC}, author={Douglas, Pamela Heidi and Hohmann, Gottfried
and Murtagh, Róisín and Thiessen-Bock, Robyn and Deschner, Tobias}, year={2016}
}'
chicago: 'Douglas, Pamela Heidi, Gottfried Hohmann, Róisín Murtagh, Robyn Thiessen-Bock,
and Tobias Deschner. “Mixed Messages: Wild Female Bonobos Show High Variability
in the Timing of Ovulation in Relation to Sexual Swelling Patterns.” BMC Evolutionary
Biology 16, no. 1 (2016). https://doi.org/10.1186/s12862-016-0691-3.'
ieee: 'P. H. Douglas, G. Hohmann, R. Murtagh, R. Thiessen-Bock, and T. Deschner,
“Mixed messages: wild female bonobos show high variability in the timing of ovulation
in relation to sexual swelling patterns,” BMC Evolutionary Biology, vol.
16, no. 1, Art. no. 140, 2016, doi: 10.1186/s12862-016-0691-3.'
mla: 'Douglas, Pamela Heidi, et al. “Mixed Messages: Wild Female Bonobos Show High
Variability in the Timing of Ovulation in Relation to Sexual Swelling Patterns.”
BMC Evolutionary Biology, vol. 16, no. 1, 140, Springer Science and Business
Media LLC, 2016, doi:10.1186/s12862-016-0691-3.'
short: P.H. Douglas, G. Hohmann, R. Murtagh, R. Thiessen-Bock, T. Deschner, BMC
Evolutionary Biology 16 (2016).
date_created: 2025-08-26T19:10:36Z
date_updated: 2025-08-26T19:52:41Z
department:
- _id: '40'
doi: 10.1186/s12862-016-0691-3
extern: '1'
intvolume: ' 16'
issue: '1'
keyword:
- Primate
- Sexual signalling
- Fecundity
- Endocrine analysis
- LC–MS/MS
- Estrogen
- Pan paniscus
- Pregnanediol
- Mate guarding
language:
- iso: eng
main_file_link:
- open_access: '1'
url: https://bmcecolevol.biomedcentral.com/articles/10.1186/s12862-016-0691-3
oa: '1'
publication: BMC Evolutionary Biology
publication_identifier:
issn:
- 1471-2148
publication_status: published
publisher: Springer Science and Business Media LLC
status: public
title: 'Mixed messages: wild female bonobos show high variability in the timing of
ovulation in relation to sexual swelling patterns'
type: journal_article
user_id: '72311'
volume: 16
year: '2016'
...
---
_id: '61027'
abstract:
- lang: eng
text: Parturition is one of the most important yet least observed events in studies
of primate life history and reproduction. Here, I report the first documented
observation of a bonobo (Pan paniscus) birth event in the wild, at the Luikotale
Bonobo Project field site, Democratic Republic of the Congo. The nulliparous mother’s
behaviour before, during and after parturition is described, along with reactions
of other community members to the birth and the neonate. Data were collected through
focal-animal observations, and the events postpartum were photo-documented. The
behaviour and spatial distribution of party members were recorded using scan samples.
Parturition occurred during the late morning in a social context, with parous
females in close proximity to the parturient mother. Placentophagia occurred immediately
after delivery, and the parturient shared the placenta with two of the attending
females. I compare this observation with reports of parturition in captive bonobos,
and highlight the observed female sociality and social support during the birth
event. Plausible adaptive advantages of parturition occurring in a social context
are discussed, and accrued observations of birth events in wild and free-ranging
primates suggest that females may give birth within proximity of others more frequently
than previously thought. This account contributes rare empirical data for examining
the interface between female sociality and parturition, and the evolution of parturitional
behaviours in primates.
article_type: original
author:
- first_name: Pamela Heidi
full_name: Douglas, Pamela Heidi
id: '72311'
last_name: Douglas
citation:
ama: Douglas PH. Female sociality during the daytime birth of a wild bonobo at Luikotale,
Democratic Republic of the Congo. Primates. 2014;55(4):533-542. doi:10.1007/s10329-014-0436-0
apa: Douglas, P. H. (2014). Female sociality during the daytime birth of a wild
bonobo at Luikotale, Democratic Republic of the Congo. Primates, 55(4),
533–542. https://doi.org/10.1007/s10329-014-0436-0
bibtex: '@article{Douglas_2014, title={Female sociality during the daytime birth
of a wild bonobo at Luikotale, Democratic Republic of the Congo}, volume={55},
DOI={10.1007/s10329-014-0436-0},
number={4}, journal={Primates}, publisher={Springer Science and Business Media
LLC}, author={Douglas, Pamela Heidi}, year={2014}, pages={533–542} }'
chicago: 'Douglas, Pamela Heidi. “Female Sociality during the Daytime Birth of a
Wild Bonobo at Luikotale, Democratic Republic of the Congo.” Primates 55,
no. 4 (2014): 533–42. https://doi.org/10.1007/s10329-014-0436-0.'
ieee: 'P. H. Douglas, “Female sociality during the daytime birth of a wild bonobo
at Luikotale, Democratic Republic of the Congo,” Primates, vol. 55, no.
4, pp. 533–542, 2014, doi: 10.1007/s10329-014-0436-0.'
mla: Douglas, Pamela Heidi. “Female Sociality during the Daytime Birth of a Wild
Bonobo at Luikotale, Democratic Republic of the Congo.” Primates, vol.
55, no. 4, Springer Science and Business Media LLC, 2014, pp. 533–42, doi:10.1007/s10329-014-0436-0.
short: P.H. Douglas, Primates 55 (2014) 533–542.
date_created: 2025-08-26T19:35:29Z
date_updated: 2025-08-26T19:53:09Z
department:
- _id: '40'
doi: 10.1007/s10329-014-0436-0
extern: '1'
intvolume: ' 55'
issue: '4'
keyword:
- Birth
- Pan paniscus
- Parturition
- Perinatal behaviour
- Placentophagia
- Female sociality
language:
- iso: eng
main_file_link:
- url: https://rdcu.be/eCzPP
page: 533-542
publication: Primates
publication_identifier:
issn:
- 0032-8332
- 1610-7365
publication_status: published
publisher: Springer Science and Business Media LLC
status: public
title: Female sociality during the daytime birth of a wild bonobo at Luikotale, Democratic
Republic of the Congo
type: journal_article
user_id: '72311'
volume: 55
year: '2014'
...