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Cited by 133Neuroendocrine regulation and behaviorPrimate Behavior and EcologyAnimal Behavior and Reproduction

Variation in oxytocin is related to variation in affiliative behavior in monogamous, pairbonded tamarins

Open access
Snowdon, Charles T., Pieper, Bridget A., Boe, Carla Y., Cronin, Katherine A., Kurian, Aimee V., Ziegler, Toni E.·2010·Hormones and Behavior
DOI 10.1016/j.yhbeh.2010.06.014PMC PMC2933949
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Abstract

Oxytocin plays an important role in monogamous pairbonded female voles, but not in polygamous voles. Here we examined a socially-monogamous cooperatively breeding primate where both sexes share in parental care and territory defense for within species variation in behavior and female and male oxytocin levels in 14 pairs of cotton-top tamarins (Saguinus oedipus), In order to obtain a stable chronic assessment of hormones and behavior, we observed behavior and collected urinary hormonal samples across the tamarins’ three week ovulatory cycle. We found similar levels of urinary oxytocin in both sexes. However, basal urinary oxytocin levels varied ten-fold across pairs and pair-mates displayed similar oxytocin levels. Affiliative behavior (contact, grooming, sex) also varied greatly across the sample and explained more than half the variance in pair oxytocin levels. The variables accounting for variation in oxytocin levels differed by sex. Mutual contact and grooming explained most of the variance in female oxytocin levels whereas sexual behavior explained most of the variance in male oxytocin levels. The initiation of contact by males and solicitation of sex by females were related to increased levels of oxytocin in both. This study demonstrates within-species variation in oxytocin that is directly related to levels of affiliative and sexual behavior. However, different behavioral mechanisms influence oxytocin levels in males and females and a strong pair relationship (as indexed by high levels of oxytocin) may require the activation of appropriate mechanisms for both sexes.

AI snapshot

Written from the paper’s full text.

TL;DR

In 14 pairs of cotton-top tamarins, urinary oxytocin varied ten-fold across individuals but did not differ by sex, and pair mates had correlated oxytocin levels. Affiliative and sexual behavior explained substantial variance in oxytocin, with different behavioral predictors for females and males.

Key findings

  • No sex difference in mean urinary oxytocin: females 23.69 ± 5.25 vs males 16.26 ± 3.56 pg/mg Cr, t(26)=1.17, P=0.25; within pairs, male and female oxytocin levels were significantly correlated (RS=0.714, N=14, P=0.02).
  • Oxytocin varied ten-fold across individuals: females ranged 4.5 to 46.4 pg/mg Cr and males ranged 3.89 to 39.92 ng/mg Cr, as reported. Pair oxytocin correlated with affiliative behavior (RS=0.783, N=14, P<0.01), and remained significant when sexual behavior was excluded (RS=0.72, N=14, P<0.02).
  • Stepwise regressions: mean pair oxytocin was predicted by total sexual behavior plus affiliative frequency (F(2,11)=9.54, P=0.004, adjusted r²=0.57); female oxytocin by affiliation duration and frequency (F(3,10)=3.937, P=0.04, adjusted r²=0.40); male oxytocin by sexual behavior only (F(1,12)=7.46, P=0.02, adjusted r²=0.33).
  • Individual behaviors explained more pair oxytocin variance: male sexual behavior, male huddle initiation, and female solicitation (F(3,10)=21.54, P=.001, adjusted r²=0.83).

Methods

  • Subjects were 14 male-female cotton-top tamarin pairs housed together for more than one year; one animal per pair was sterilized for colony management but all had intact gonads, and no offspring were present.
  • Behavior was observed in 30-min sessions three times weekly, and first-morning urine samples were collected three times weekly across the female’s three-week ovarian cycle; hormonal and behavioral measures were averaged to assess chronic/basal levels.
  • Urinary oxytocin was measured by enzyme immunoassay, creatinine-corrected, with biological validation via estradiol implants and pairing; analyses used Spearman rank correlations, t-tests, and stepwise multiple regressions.

Limitations

  • The paper states that the data represent chronic/baseline hormone and behavior levels, and that it is unknown whether or how quickly oxytocin levels change in response to sexual behavior or female fertility.
  • Evident from the text: the study is correlational with a small sample of 14 captive pairs, so causal direction between oxytocin and behavior cannot be established; urinary oxytocin is used as a peripheral proxy for biobehavioral oxytocin function.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1016/j.yhbeh.2010.06.014

Cites

41 of 41 references verified0 citation errors · 0 not checkable

Statistics

8 tests recomputed · 0 with the reported and recomputed p on opposite sides of .05

Claims the paper makes

0 of 5 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    In 14 pairs of cotton-top tamarins, basal urinary oxytocin levels did not differ between males and females.

    “We found similar levels of urinary oxytocin in both sexes.”
    • Also stated in: § Results · plain
      “Male and female oxytocin levels did not differ across the sample (Mean ± SEM: Female 23.69 ± 5.25, Male 16.26 ± 3.56 pg/mg Cr, t (26) = 1.17, P = 0.25).”
    • Also stated in: § Discussion · plain
      “we found no sex differences in oxytocin levels.”
    Quote in the paperSubstantial claim
  • Findingown data

    In a stepwise multiple regression, total sexual behavior and frequency of affiliative behavior together explained 57% (adjusted R2=0.57) of variance in mean pair oxytocin levels.

    “The model that explained the greatest variance in mean pair oxytocin levels included both total sexual behavior and frequency of affiliative behavior (F (2, 11) = 9.54, P = 0.004, adjusted r square = 0.57”
    • Also stated in: § Discussion · plain
      “Our multiple regression analyses identified two pair behavioral components (sexual behavior and frequency of affiliative contact) that explained 60% of the variance in the mean oxytocin levels within pairs.”
    Quote in the paperSubstantial claim
  • Findingown data

    Pair oxytocin levels correlated significantly with affiliative behavior (RS=0.783, N=14, P<0.01).

    “Pair oxytocin levels correlated significantly with affiliative behavior (RS = 0.783, N = 14, P < 0.01; Figure 3).”
    Quote in the paperSubstantial claim
  • Findingown data

    In females, male huddle initiation and female solicitation together explained 54% (adjusted R2=0.54) of variance in female oxytocin levels.

    “The model that explained the greatest variance included male huddle initiation and female solicitation (F (2, 11) = 8.53, P =0.006, adjusted r square = 0.54”
    • Also stated in: § Discussion · plain
      “Male initiation of huddles with females and female solicitation of sex were both important variables in explaining variation in both pair and female oxytocin levels.”
    Quote in the paperSubstantial claim
  • Findingown data

    Affiliative and sexual behavior varied greatly across the 14 tamarin pairs.

    “Affiliative behavior (contact, grooming, sex) also varied greatly across the sample”
    • Also stated in: § Results · boosted
      “The striking within-species variation also appeared for the behavioral measures with sexual behavior ranging from 1.5 to 6.9 acts per 30 min, huddling and grooming duration ranging from 14.6 to 556.8 sec per 30 min and huddling and grooming frequency ranging from 1.9 to 18.2 acts per 30 min.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim. 9
  • May combine two claims. 10

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Findingown data

    No significant relationships were found between cortisol and oxytocin or between cortisol and behavior.

    “We measured cortisol levels according to the methods of Ziegler et al. (1995), but found no significant relationships between cortisol and oxytocin or cortisol and behavior and do not discuss this further.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data

    The oxytocin assay had mean intra-assay coefficient of variation 5.85% and inter-assay coefficient of variation 16.11%.

    “Mean intra-assay coefficients of variation were 5.85% and inter-assay coefficients of variation were 16.11%.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Rates of nonconceptive sex and female solicitation increase after minor threats to the relationship, such as brief separations and olfactory stimuli from novel reproductive females.

    “We have reported (Snowdon and Ziegler, 2007) that rates of nonconceptive sex and female solicitation increase after minor threats to the relationship (brief separations, and olfactory stimuli from novel reproductive females) suggesting that nonconceptive sex may be important in restoring or maintaining a relationship.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Snowdon and Ziegler, 2007

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationreasoning

    The amount and quality of close contact and non-conceptive sex may play an important role in predicting the quality and duration of human heterosexual relationships.

    “We suggest that the amount and quality of close contact and non-conceptive sex may also play an important role in predicting the quality and duration of human heterosexual relationships.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Behavioral observers were trained to a criterion of >85% reliability prior to observations.

    “All observers were trained to a criterion of >85% reliability prior to observations.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Study design and conductcitation

    The oxytocin enzyme immunoassay used had greater specificity than the earlier RIA, responding only to the fraction eluted at the location of oxytocin, with less than 0.3% reactivity with arginine vasopressin.

    “A direct enzyme immunoassay (EIA) (Assay Designs, Ann Arbor, MI) has been shown to have greater specificity than the earlier RIA, responding only to the fraction eluded at the location of oxytocin (Carter et al., 2007). EIA reactivity with arginine vasopressin was less than 0.3%.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Carter et al., 2007 source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Previous research on rodents found that sexually-naïve females had increased oxytocin levels compared to sexually-naïve males.

    “In contrast to previous research on rodents (polygynous rats and monogamous prairie voles) where sexually-naïve females had increased levels of oxytocin compared to sexually-naïve males (Kramer et al., 2004) we found no sex differences in oxytocin levels.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Kramer et al., 2004 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Males and females have complementary behavioral strategies, with female oxytocin levels influenced by amount of proximity and contact received and male levels affected by amount of sexual activity.

    “These results based on pair behaviors suggest males and females have complementary behavioral strategies with female oxytocin levels being influenced by amount of proximity and contact they receive whereas male levels are affected by amount of sexual activity.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The natural establishment of pairbonds in prairie voles is usually accompanied by extensive sexual behavior over one to two days, which also induces ovulation in females.

    “The natural establishment of pairbonds in prairie voles is usually accompanied by extensive sexual behavior over one to two days (Carter 1998) which also induces ovulation in females.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Carter 1998 source

      Not checked in the free run.

  • May combine two claims.

    Study design and conductown data

    Serial diluted pooled tamarin urine was parallel to oxytocin standards (t=1.21, P>0.05) and accuracy was 101.9 ± 4.7%.

    “Serial diluted pooled tamarin urine was parallel to oxytocin standards (t = 1.21, P >0.05) and accuracy was 101.9 + 4.7% (mean +SEM).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data

    These behaviors may have a tonic effect on oxytocin levels, and peripheral oxytocin levels reflect the quality of a pair relationship.

    “These results suggest that these behaviors may have a tonic effect on oxytocin levels, and that peripheral oxytocin levels reflect the quality of a pair relationship.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Interpretationreasoning

    A good relationship between pair mates may be one where each sex can respond to the behavioral needs of its mate.

    “A good relationship between pair mates may be one where each sex can respond to the behavioral needs of its mate.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable). May combine two claims.

    Interpretationreasoning

    The demonstration that both sexes of tamarins have equal oxytocin levels within a pair, but that these levels are influenced by different behaviors for each sex and that each sex engages in behavior that complements the needs of the mate, suggests ways in which human relationships might be improved.

    “The demonstration that both sexes of tamarins have equal levels of oxytocin within a pair, but that these levels are influenced by different behaviors for each sex and that each sex engages in behavior that complements the needs of the mate suggest ways in which human relationships might be improved.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    Variation in affiliative and sexual behavior may have a significant effect on oxytocin levels, or vice versa.

    “Our results suggest that variation in affiliative and sexual behavior may have a significant effect on hormones or vice versa.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    Urinary oxytocin concentrations were divided by creatinine levels to control for variation in urine concentration.

    “All concentrations were divided by creatinine levels to control for variation in urine concentration.”
    Quote in the paperSubstantial claim
15 of 15

  • The paper relies on this without support.

    In both marmosets and tamarins, sexual roles are not highly differentiated, with both sexes taking part in infant care, vigilance, and territory defense.

    “In both marmosets and tamarins sexual roles are not highly differentiated, with both taking part in infant care, vigilance and territory defense, which may be related to the lack of sex differences in peripheral oxytocin levels.”
1 of 1

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • In pair-bonded tamarins, pairs with a closer bond (higher rates of affiliative and sexual behaviors over several weeks) had higher urinary oxytocin concentrations during the same period.

    “In primates, a study in pair-bonded tamarins examining behavioral correlates over time with repeated samples of urinary oxytocin, showed that pairs that had a closer bond, defined as engaging in higher rather than lower rates of affiliative and sexual behaviors over several weeks also had higher urinary oxytocin concentrations during the same time period (Snowdon et al., 2010).”

    From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Snowdon et al., 2010

  • Congruent patterns are observed when linking social behaviors to endogenous measures of oxytocin in plasma, urine or saliva in non-human primates and humans.

    “Congruent patterns are observed when linking social behaviors to endogenous measures of oxytocin in plasma, urine or saliva in non-human primates (Seltzer and Ziegler, 2007; Maestripieri et al., 2009; Snowdon et al., 2010; Crockford et al., 2013) and humans (Christensson et al., 1989; Holt-Lunstad et al., 2008; Morhenn et al., 2008; Gordon et al., 2010).”

    From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Snowdon et al., 2010

  • In tamarins, estradiol pellet implantation increased estradiol significantly in all three males, and two of three males showed a large increase in oxytocin following estradiol elevation, indicating that functional changes in oxytocin can be measured in urine.

    “In tamarins, for example, Snowdon et al. (2010) implanted three males with an estradiol pellet (1.5 mg continuous release over 30 days) and collected urine samples before and during the period of the implant. Estradiol increased significantly in all three males (t = 3.64, P = 0.04) ensuring the effectiveness of the pellets in raising estradiol. Male oxytocin response varied substantially, but two”

    From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Snowdon et al., 2010

  • Validations to test for this have been performed for several primate species (cotton-top tamarins, marmoset, humans, chimpanzees).

    “Validations to test for this have been performed for several primate species (cotton-top tamarins: Snowdon et al., 2010; marmoset: Seltzer and Ziegler, 2007; humans: Seltzer et al., 2010; chimpanzees: Ziegler et al., unpublished data).”

    From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Snowdon et al., 2010

  • Urinary levels of OT co-vary with social behavior in male and female cotton-top tamarins, with female OT levels associated with grooming and mutual physical contact with a partner, and male OT levels associated with sexual behavior.

    “Urinary levels of OT co-vary with social behavior in male and female cotton-top tamarins (Saguinus oedipus), with variance in female OT levels associated with grooming behavior and mutual physical contact with a partner, and variance in male OT levels associated with sexual behavior (Snowdon et al., 2010).”

    From Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers (2014) · cites this paper as Snowdon et al., 2010

Statistics that don’t add up

Each reported p-value recomputed from its test statistic and degrees of freedom.

  • Inconsistent p-value: F (1, 12) = 10.69, p = .006

    Minor

    The paper reports p = .006 here; recomputing from the test statistic and its degrees of freedom gives p = .007. The check cannot tell whether the statistic or the p-value is the misprint.

    Reported p = .006 · recomputed p = .007

1 of 1

Statistics recomputed

Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.

  • Doesn’t add upF(1, 12) = 10.69reported p = .006 · recomputed p = .007

    “F (1, 12) = 10.69, p = .006”

  • Consistentt(26) = 1.17reported p = .25 · recomputed p = .253

    “t (26) = 1.17, p = .25”

  • Consistentt(13) = 1.35reported p = .199 · recomputed p = .200

    “t (13) = 1.35, p = .199”

  • ConsistentF(2, 11) = 9.54reported p = .004 · recomputed p = .004

    “F (2, 11) = 9.54, p = .004”

  • ConsistentF(3, 10) = 3.937reported p = .04 · recomputed p = .043

    “F (3, 10) = 3.937, p = .04”

  • ConsistentF(1, 12) = 7.46reported p = .02 · recomputed p = .018

    “F (1, 12) = 7.46, p = .02”

  • ConsistentF(3, 10) = 21.54reported p = .001 · recomputed p < .001

    “F (3, 10) = 21.54, p = .001”

    The paper prints p at a floor (such as p < .001)

  • ConsistentF(2, 11) = 8.53reported p = .006 · recomputed p = .006

    “F (2, 11) = 8.53, p = .006”

8 of 8

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Female regression lists two predictors but reports three predictor degrees of freedom

    Minor

    The description identifies affiliation duration and frequency as the model's predictors and says sex was excluded. Its F(3, 10) statistic instead indicates three predictors, leaving a predictor unaccounted for.

  • Erection-model F statistic does not equal the squared t statistic

    Minor

    For a regression with one predictor, the predictor's t statistic squared must equal the model F statistic. The reported t of 3.31 gives 10.9561, rather than the reported F of 10.69; the gap exceeds rounding to the printed precision.

    Reported 10.69 · recomputed 10.9561

  • Male oxytocin range uses inconsistent units

    Minor

    The male range is given in ng/mg Cr, whereas the assay values and the reported male mean are in pg/mg Cr. The stated units differ by a factor of 1,000.

  • Male sexual behavior does not explain the stated 45% of variance

    Minor

    The discussion says sexual behavior explained 45% of male oxytocin variance. The corresponding results report an adjusted R-squared of 0.33; their F statistic gives an unadjusted R-squared of about 0.38, not 0.45.

4 of 4

Cites

Flagged first, then by citations

Research works printed but not linked: 1

  1. Snowdon, 2007, Growing up cooperatively: family processes and infant development in marmosets and tamarins, J. Devel. Proc., 2, 40

Cited by

Sorted by citations

Related

Authors
Snowdon, C. T., Pieper, B. A., Boe, C. Y., Cronin, K. A., Kurian, A. V., & Ziegler, T. E.
Affiliations
  • University of Wisconsin–Madison (US)
  • University of Wisconsin System (US)
Corresponding author
Snowdon, Charles T.
ORCID
Venue
Hormones and Behavior
Publisher
Elsevier BV
Published
2010-09
Volume
58
Issue
4
Pages
614-618
ISSN
0018-506X (ISSN-L)
DOI
10.1016/j.yhbeh.2010.06.014
PMC
PMC2933949
OpenAlex
W2105122295
Semantic Scholar
9ee3a5c7e1485fed3d1ce8b026bf4f80dc824966
Cited by
133
References
41
Citations by year
2026: 2 · 2025: 1 · 2024: 6 · 2023: 2 · 2022: 9 · 2021: 7 · 2020: 6 · 2019: 8 · 2018: 15 · 2017: 7 · 2016: 8 · 2015: 10 · 2014: 15 · 2013: 16 · 2012: 12
FWCI
16.18
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Hormones and Behavior (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
  • Max Planck Institute for Plasma Physics (submittedVersion)
  • Max Planck Digital Library (submittedVersion, other-oa)
Funders
  • National Institutes of Health (RR000167, P51OD011106)
  • U.S. Public Health Service
  • National Institute of Mental Health (MH 035215, R01MH035215)
  • National Center for Research Resources (RR 000167, P51RR000167)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords
oxytocin, affiliative behavior, pair bonding, monogamy, cotton-top tamarin, Saguinus oedipus, grooming, sexual behavior, contact behavior, sex differences, social bonds, ovulatory cycle
MeSH terms
Animals, Behavior, Animal, Estradiol, Female, Hydrocortisone, Individuality, Male, Oxytocin, Pair Bond, Saguinus, Social Behavior

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