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  1. Article ; Online: Detection of nonhuman primate gonadotropins in polyacrylamide gels: An alternative to the western blot.

    Matteri, Robert L / Ziegler, Toni E

    American journal of primatology

    2020  Volume 26, Issue 3, Page(s) 155–166

    Language English
    Publishing date 2020-01-05
    Publishing country United States
    Document type Journal Article
    ZDB-ID 1495834-X
    ISSN 1098-2345 ; 0275-2565
    ISSN (online) 1098-2345
    ISSN 0275-2565
    DOI 10.1002/ajp.1350260302
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  2. Article ; Online: Measuring peripheral oxytocin and vasopressin in nonhuman primates.

    Ziegler, Toni E

    American journal of primatology

    2018  Volume 80, Issue 10, Page(s) e22871

    Abstract: Studying the neural and hormonal changes that modulate behavior is critical to understanding social relationships. Of particular interest is measuring oxytocin (OT) and arginine vasopressin (AVP) peripherally, and preferably, non-invasively, in nonhuman ... ...

    Abstract Studying the neural and hormonal changes that modulate behavior is critical to understanding social relationships. Of particular interest is measuring oxytocin (OT) and arginine vasopressin (AVP) peripherally, and preferably, non-invasively, in nonhuman primates. Due to these peptides' neural origin and their stimulation of brain areas that influence social behavior, there has been debate whether peripheral measures in blood, urine, and saliva reflect central levels in the brain. This review elucidates the challenges of OT measurement and the solutions that provide valuable data on OT's role in social behavior. This review discusses the recent studies in rhesus macaques which indicate that exogenous OT delivered by nasal spray results in increased OT in cerebrospinal fluid, and it notes the new methodologies that can measure both endogenous and exogenous OT simultaneously, which thereby determine the source of measured OT in biological fluids. Next, this review highlights the utility of measuring urinary OT by summarizing the results of clearance rate studies in humans and marmosets, which characterize the timing that circulating OT enters urine and illustrate that endogenous releasers of OT also increase urinary OT. With the ability to reliably measure OT and AVP in urine and in blood, we can now study free-ranging captive, and non-captive primates to answer questions about the biology of social bonding that were not possible before. One procedural concern that this review also highlights is whether extraction of the peptides prior to assay is needed, as the values are higher in samples that have not been extracted. Studies indicate that extractions eliminate the interfering compounds that cause higher values. Across studies, to ensure the reliability of measuring OT for nonhuman primates, this review makes suggestions based on empirical evidence for how to correctly preserve samples and emphasizes the need to validate each assay for individual species.
    MeSH term(s) Administration, Intranasal ; Animals ; Arginine Vasopressin/analysis ; Arginine Vasopressin/blood ; Arginine Vasopressin/urine ; Humans ; Immunoassay/methods ; Oxytocin/analysis ; Oxytocin/blood ; Oxytocin/cerebrospinal fluid ; Oxytocin/urine ; Primates ; Saliva/chemistry
    Chemical Substances Arginine Vasopressin (113-79-1) ; Oxytocin (50-56-6)
    Language English
    Publishing date 2018-05-14
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Review
    ZDB-ID 1495834-X
    ISSN 1098-2345 ; 0275-2565
    ISSN (online) 1098-2345
    ISSN 0275-2565
    DOI 10.1002/ajp.22871
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  3. Article ; Online: Insights into ovarian function in wild muriqui monkeys (Brachyteles arachnoides).

    Strier, Karen B / Ziegler, Toni E

    American journal of primatology

    2020  Volume 32, Issue 1, Page(s) 31–40

    Abstract: Fecal samples were collected systematically during a 6-week period, from 13 September-24 October, 1990, from four nonlactating female muriquis (Brachyteles arachnoides) inhabiting an 800 ha forest at Fazenda Montes Claros in Minas Gerais, Brazil. All ... ...

    Abstract Fecal samples were collected systematically during a 6-week period, from 13 September-24 October, 1990, from four nonlactating female muriquis (Brachyteles arachnoides) inhabiting an 800 ha forest at Fazenda Montes Claros in Minas Gerais, Brazil. All four females were experienced mothers; one had most recently given birth in June 1988; the other three had most recently given birth in August 1988. Fecal assays measuring progesterone, estradiol, and estrone indicated consistently low levels in the one female who had given birth in June 1988 and in two of the three females who had given birth in August 1988. Elevated steroid levels did, however, appear in fecal samples from the fourth female on day 15 of the collection period. Steroid levels subsequently dropped and then began to rise again during what appeared to be a second cycle. The cycling female was the only one of the four females examined observed to copulate during the collection period. These preliminary data indicate that nonlactating female muriquis do not cycle year-round, resumption of cycling is not tightly synchronized among females even when their prior parturitions were tightly synchronized, and resumed sexual activity appears to be associated with resumed cycling. © 1994 Wiley-Liss, Inc.
    Language English
    Publishing date 2020-01-10
    Publishing country United States
    Document type Journal Article
    ZDB-ID 1495834-X
    ISSN 1098-2345 ; 0275-2565
    ISSN (online) 1098-2345
    ISSN 0275-2565
    DOI 10.1002/ajp.1350320104
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  4. Article ; Online: Contextual complexity of chemical signals in callitrichids.

    Snowdon, Charles T / Ziegler, Toni E

    American journal of primatology

    2020  Volume 83, Issue 6, Page(s) e23172

    Abstract: In nearly four decades our research and that of others on chemical signaling in callitrichid primates suggest a high degree of contextual complexity in both the use of signals and the response to these signals. We describe our research including ... ...

    Abstract In nearly four decades our research and that of others on chemical signaling in callitrichid primates suggest a high degree of contextual complexity in both the use of signals and the response to these signals. We describe our research including observational field studies, behavioral bioassays ("playbacks"), functional imaging, and conditioning studies. Scent marking in both captivity and the wild is used for more than just territorial marking. Social contextual effects are seen in responses by subordinate females responding with ovulatory inhibition only to chemical signals from familiar dominant reproductive females. Males detect ovulation through changes in scent marks. Males responded behaviorally and hormonally to chemical signals of novel ovulating females as a function of their reproductive status (fathers, males paired with a female but not fathers, and single males). Multiple brain areas are activated in males by female chemical signals of ovulation including areas relating to memory, evaluation, and motivation. Furthermore, males can be conditioned to respond sexually to a nonsexual odor demonstrating that learning plays an important role in response to chemical signals. Male androgen and estrone levels changed significantly in response to infant chemical signals as a function of whether the males were fathers or not, whether the odors were from their own versus other infants, as well as the infant's stage of development. Chemical signals in callitrichids are providing a rich source of understanding the context and function of the chemical sensory system and its stimulation of neural, behavioral, and hormonal actions in the recipients.
    MeSH term(s) Animals ; Female ; Male ; Odorants ; Ovulation ; Territoriality
    Language English
    Publishing date 2020-07-09
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Review
    ZDB-ID 1495834-X
    ISSN 1098-2345 ; 0275-2565
    ISSN (online) 1098-2345
    ISSN 0275-2565
    DOI 10.1002/ajp.23172
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  5. Article ; Online: Cognitive development from infancy to young adulthood in common marmosets (Callithrix jacchus): Effect of age, sex, and hormones on learning and affective state.

    Ash, Hayley / Goy, Robinson W / Spaulding, Abigail / Colman, Ricki J / Corbett, Cody J / Ziegler, Toni E

    Developmental psychobiology

    2023  Volume 65, Issue 7, Page(s) e22430

    Abstract: Studies looking at individual variability in cognition have increased in recent years. We followed 43 marmosets (21 males, 22 females) from infancy to young adulthood. At 3-months old, marmosets were trained to touch a rewarded stimulus. At 9-, 15-, and ... ...

    Abstract Studies looking at individual variability in cognition have increased in recent years. We followed 43 marmosets (21 males, 22 females) from infancy to young adulthood. At 3-months old, marmosets were trained to touch a rewarded stimulus. At 9-, 15-, and 21-months old, they were given visual discrimination and cognitive bias tests, and urine samples were collected to examine hormone levels. Marmosets were significantly more successful learners at 15 months than 9 months. Individuals who were more successful learners at 9 months were also more successful at 15 months, with more male learners than expected at 15 months. At 9 months, learning success was associated with higher cortisol levels. At 15 months, males with higher estradiol levels were more successful learners, whereas at 21 months, females with higher estradiol and cortisol levels tended to be less successful learners and more pessimistic. Nine months, therefore, appears to be an important developmental timepoint for acquiring cognitive control, which has developed by 15 months. Steroids may have differential effects on each sex, with complex interactions between gonadal and adrenal hormones having an influence on cognitive function over the lifespan. This longitudinal study offers new insight into cognition, including its development and biological underpinnings.
    MeSH term(s) Animals ; Female ; Male ; Infant ; Humans ; Young Adult ; Adult ; Callithrix/psychology ; Hydrocortisone ; Longitudinal Studies ; Cognition ; Estradiol
    Chemical Substances Hydrocortisone (WI4X0X7BPJ) ; Estradiol (4TI98Z838E)
    Language English
    Publishing date 2023-10-19
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural
    ZDB-ID 4107-5
    ISSN 1098-2302 ; 0012-1630
    ISSN (online) 1098-2302
    ISSN 0012-1630
    DOI 10.1002/dev.22430
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  6. Article ; Online: Reproductive endocrinology of wild female woolly monkeys (Lagothrix lagotricha poeppigii) during puberty, ovarian cyclicity, and pregnancy.

    Abondano, Laura A / Ziegler, Toni E / Di Fiore, Anthony

    American journal of primatology

    2021  Volume 84, Issue 6, Page(s) e23303

    Abstract: Behavioral observations can provide clues about female reproductive status. However, the study of the endocrine dynamics that underlie processes such as puberty, ovulation, conception, and gestation, may help increase our understanding of female ... ...

    Abstract Behavioral observations can provide clues about female reproductive status. However, the study of the endocrine dynamics that underlie processes such as puberty, ovulation, conception, and gestation, may help increase our understanding of female reproductive biology. We used noninvasive methods to study female reproductive endocrinology in wild woolly monkeys (genus Lagothrix). We extracted ovarian steroid hormones from fecal samples collected non-invasively to examine changes in the concentrations of progesterone and estrogen metabolites (pregnanediol-3-glucuronide and estrone-3-glucuronide, respectively) during periods of female puberty, ovarian cyclicity, and pregnancy. The two subadult females in our study showed significant increases in ovarian hormone concentrations before disappearing and presumably dispersing, suggesting that they might reach the onset of puberty before emigrating from their natal groups. Ovarian cycle length in adult females was, on average, ~22 days (N = 21). Of the 10 cycling females, five conceived and four gave birth to offspring, with an average gestation period of ~214 days, but the infant born to the female with the shortest estimated gestation period (182 days) disappeared within a month after parturition. The fact that less than half of all cycling females conceived, and that only three out of five of those females gave birth to offspring that survived past the first month, suggests that reproduction is energetically costly for female woolly monkeys. Ovarian cycle length and gestation period among woolly monkeys are similar to those in their closest relatives, spider monkeys and muriquis suggesting that reproductive physiology may be highly conserved among females within the Tribe Atelini.
    MeSH term(s) Animals ; Atelinae ; Estrogens ; Feces ; Female ; Humans ; Menstrual Cycle ; Periodicity ; Pregnancy ; Puberty
    Chemical Substances Estrogens
    Language English
    Publishing date 2021-07-13
    Publishing country United States
    Document type Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
    ZDB-ID 1495834-X
    ISSN 1098-2345 ; 0275-2565
    ISSN (online) 1098-2345
    ISSN 0275-2565
    DOI 10.1002/ajp.23303
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  7. Article: Nonhuman Primate Paternal Care: Species and Individual Differences in Behavior and Mechanisms.

    Ziegler, Toni E / Tecot, Stacey R / Fernandez-Duque, Eduardo / Savage, Anne / Snowdon, Charles T

    Advances in neurobiology

    2022  Volume 27, Page(s) 213–238

    Abstract: Direct care of offspring by the father (sire) is relatively rare in primates. Besides humans, there are a number of species where the male is essential for the survival of offspring: marmosets, tamarins, titis and owl monkeys, some lemurs, and siamangs. ... ...

    Abstract Direct care of offspring by the father (sire) is relatively rare in primates. Besides humans, there are a number of species where the male is essential for the survival of offspring: marmosets, tamarins, titis and owl monkeys, some lemurs, and siamangs. All these species show reduced sexual dimorphism, territoriality, and biparental care. However, timing and levels of direct care may vary among these species. Here, relying on both lab and field data, we address the variability found in father's involvement with his infants, the behavioral, neuroendocrine and sensory systems that are a cause and consequence of paternal care, and social bonds between the breeding pair. We integrate studies of laboratory animals (where detailed observations and experimentation are possible) with field studies (which illuminate the ecological and evolutionary functions of paternal care) and discuss the future directions for examining the proximate and ultimate mechanisms of paternal care in nonhuman primates.
    MeSH term(s) Animals ; Fathers ; Humans ; Individuality ; Male ; Primates ; Social Behavior
    Language English
    Publishing date 2022-09-27
    Publishing country United States
    Document type Journal Article
    ISSN 2190-5215
    ISSN 2190-5215
    DOI 10.1007/978-3-030-97762-7_7
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  8. Article ; Online: Reproductive performance and excretion of urinary estrogens and gonadotropins in the female pygmy marmoset (Cebuella pygmaea).

    Ziegler, Toni E / Snowdon, Charles T / Bridson, William E

    American journal of primatology

    2020  Volume 22, Issue 3, Page(s) 191–203

    Abstract: By retrospective review of colony records and determinations of urinary hormones we have described the reproductive profile of the female pygmy marmoset (Cebuella pygmaea). The pygmy marmoset is a nonseasonal breeder and gives birth to twins 76% of the ... ...

    Abstract By retrospective review of colony records and determinations of urinary hormones we have described the reproductive profile of the female pygmy marmoset (Cebuella pygmaea). The pygmy marmoset is a nonseasonal breeder and gives birth to twins 76% of the time with single births occurring 16% and triplet births 8% of the time. Interbirth intervals ranged from 149-746 days. First births occurred to females between 24-42 months of age and 5-27 months post pairing. We measured urinary estrone, estradiol and estrone conjugates along with immunoreactive luteinizing hormone/chorionic gonadotropin (LH/CG). The postpartum LH peak occurred a mean of 15.6 days following parturition. The conception rate was 69% following the postpartum ovulation. Levels of CG rose a mean of 19 days following the LH peak in conceptive cycles and remained elevated for a mean of 76 days. Gestational length was a mean of 141.9 days from the LH peak to parturition. Only one female of the five studied displayed ovarian cycles which were a mean of 27 days in length. Estradiol was the predominant urinary estrogen, however both estrone and estradiol were excreted in extremely high concentrations. LH peaks were discrete with urinary estrogens increasing at the time of the LH peak and remaining elevated throughout the luteal phase of the cycle.
    Language English
    Publishing date 2020-01-15
    Publishing country United States
    Document type Journal Article
    ZDB-ID 1495834-X
    ISSN 1098-2345 ; 0275-2565
    ISSN (online) 1098-2345
    ISSN 0275-2565
    DOI 10.1002/ajp.1350220305
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  9. Article ; Online: From the field to the lab: Muriqui endocrinology from a collaborative perspective.

    Strier, Karen B / Ziegler, Toni E

    American journal of primatology

    2018  Volume 81, Issue 5, Page(s) e22928

    Abstract: The northern muriqui (Brachyteles hypoxanthus) is a critically endangered species endemic to the Atlantic Forest of southeastern Brazil. Long-term observational studies of wild muriquis have provided many insights into the behavioral ecology and life ... ...

    Abstract The northern muriqui (Brachyteles hypoxanthus) is a critically endangered species endemic to the Atlantic Forest of southeastern Brazil. Long-term observational studies of wild muriquis have provided many insights into the behavioral ecology and life history of this species. However, nearly everything that is currently known about the northern muriqui's behavioral endocrinology has come from combining our respective expertise in noninvasive field and laboratory research. Here, we reflect on the history of our collaboration, focusing on major challenges, key scientific findings, and factors that contributed to its success. Challenges included insuring the reliable collection of frequent fecal samples from a large enough number of known individuals over extended periods of time, preserving the steroids in the field and transporting them, developing and validating the fecal steroid assays, and interpreting the hormonal profiles within the behavioral and ecological contexts of the study subjects. Major findings included our thorough description of the fecal progesterone and estradiol profiles associated with muriqui ovarian cycling and gestation, the seasonal resumption of cycling, its onset during puberty of dispersing females, and the differences between fertile and infertile cycles. We also documented the relationship between fecal cortisol and testosterone in sexually active males across breeding and nonbreeding seasons, and sex differences in cortisol levels across the mating and conception seasons. We attribute the success of our collaboration to a number of factors including our mutual appreciation for one another's high standards for ethics, data quality, and data interpretation.
    MeSH term(s) Animals ; Atelinae/growth & development ; Atelinae/physiology ; Brazil ; Endangered Species ; Endocrine System/physiology ; Feces/chemistry ; Female ; Hormones/analysis ; Male ; Menstrual Cycle ; Research Design ; Seasons ; Sexual Behavior, Animal/physiology
    Chemical Substances Hormones
    Language English
    Publishing date 2018-10-30
    Publishing country United States
    Document type Journal Article
    ZDB-ID 1495834-X
    ISSN 1098-2345 ; 0275-2565
    ISSN (online) 1098-2345
    ISSN 0275-2565
    DOI 10.1002/ajp.22928
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  10. Article ; Online: Detection of urinary gonadotropins in callitrichid monkeys with a sensitive immunoassay based upan a unique monoclonal antibody.

    Ziegler, Toni E / Matteri, Robert L / Wegner, Frederick H

    American journal of primatology

    2020  Volume 31, Issue 3, Page(s) 181–188

    Abstract: A radioimmunological method for measuring urinary luteinizing hormone (LH) and chorionic gonadotropin (CG) excretion in the family Callitrichidae is described. The method uses a monoclonal antibody that will be available in virtually unlimited quantity. ... ...

    Abstract A radioimmunological method for measuring urinary luteinizing hormone (LH) and chorionic gonadotropin (CG) excretion in the family Callitrichidae is described. The method uses a monoclonal antibody that will be available in virtually unlimited quantity. Several polyclonal antisera that have been useful for the detection of callitrichid gonadotropins are near depletion. The monoclonal antibody-based RIA provided similar results when compared with the mouse Leydig cell bioassay for LH and a previously validated polyclonal antibody-based RIA. When the monoclonal antibody is used for immunodetection of Saguinus oedipus LH by non-reducing SDS-PAGE, a single entity is recognized that corresponds with the molecular weight range of bioactive LH and appears to be in the normal range for LH in nonhuman primates. LH and CG were detected by the monoclonal antibody-based RIA in urine from representatives of species from all genera of callitrichids. Hormonal profiles of daily urine samples revealed the detection of the preovulatory LH surge by both RIA methods in the cotton-top tamarin (Saguinus Oedipus) and pygmy marmoset (Cebuella pygmea) and the increase CG due to pregnancy in both species. Serial dilutions of midcycle and pregnancy urine from Saguinus, Callithrix, Leontopithecus, and Cebuella exhibited parallelism when compared with our in-house reference standard of rhesus monkey CG. Cultured Saguinus oedipus pituitary cells showed an increased release of LH when challenged by gonadotropin releasing hormone (GnRH) providing further support that the monoclonal antibody-based RIA measures LH in this species. © 1993 Wiley-Liss, Inc.
    Language English
    Publishing date 2020-01-10
    Publishing country United States
    Document type Journal Article
    ZDB-ID 1495834-X
    ISSN 1098-2345 ; 0275-2565
    ISSN (online) 1098-2345
    ISSN 0275-2565
    DOI 10.1002/ajp.1350310303
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