Phytochemicals and reproductive function in wild female Phayre's leaf monkeys (Trachypithecus phayrei crepusculus)

Hormones and Behavior

Volumn 59, Issue 1, 2011, Pages 28-36

  Lu, Amy ^a,b   Beehner, Jacinta C ^b   Czekala, Nancy M ^c   Koenig, Andreas ^a   Larney, Eileen ^a   Borries, Carola ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c Papoose Conservation Wildlife Foundation   (United States)

Author keywords

Cycle length; Energetic balance; Fecal hormone; Ovulation; Physical condition; Phytosteroid; Probability of conception; Seasonality; Vitex

Indexed keywords

ESTROGEN; GESTAGEN;

ANIMAL EXPERIMENT; ANIMAL FOOD; ARTICLE; CONCEPTION; FECES ANALYSIS; FEMALE; FOLLICULAR PHASE; FOOD AVAILABILITY; HAPLORHINI; HORMONE DETERMINATION; NONHUMAN; OVULATION; PHENOLOGY; PHYTOCHEMISTRY; PRIORITY JOURNAL; REPRODUCTION; SEXUAL BEHAVIOR; VITEX; WILD ANIMAL;

ANIMALS; COLOBINAE; ENERGY METABOLISM; ESTROGENS; FECES; FEMALE; MALE; PROGESTINS; REPRODUCTION; SEASONS; SEXUAL BEHAVIOR, ANIMAL; VITEX;

EID: 78651451105     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2010.09.012     Document Type: Article

References (82)

1. Adams N.R. Detection of the effects of phytoestrogens on sheep and cattle. J. Anim. Sci. 1995, 73:1509-1515.
2. Altmann J. Observational study of behavior-sampling methods. Behaviour 1974, 49:227-267.
3. Beach F.A. Sexual attractivity, proceptivity, and receptivity in female mammals. Horm. Behav. 1976, 7:105-138.
4. Beck V., Unterrieder E., Krenn L., Kubelka W., Jungbauer A. Comparison of hormonal activity (estrogen, androgen, and progestin) of standardized plant extracts for large scale use in hormone replacement therapy. J. Steroid Biochem. Mol. Biol. 2003, 84:259-268.
5. Benie T., Thieulant M.L. Interactions of some traditional plant extracts with uterine oestrogen or progestin receptors. Phytother. Res. 2003, 17:756-760.
6. Bennetau-Pelissero C., Breton B., Bennetau B., Le Menn F., Kaushik S.J. Effect of genistein enriched diet on the sex steroid endocrinology and the reproductive efficiency of the rainbow trout Oncorhynchus mykiss. Rev. Med. Vet. 2002, 153:513-516.
7. Berman C.M. Maternal condition and offspring sex ratio in a group of free-ranging rhesus monkeys: an 11-year study. Am. Nat. 1988, 131:307-328.
8. Berman C.M., Li J.H. Impact of translocation, provisioning and range restriction on a group of Macaca thibetana. Int. J. Primatol. 2002, 23:383-397.
9. Berman C.M., Schwartz S. A nonintrusive method for determining relative body fat in free-ranging monkeys. Am. J. Primatol. 1988, 14:53-64.
10. Bettinger T., Cougar D., Lee D.R., Lasley B.L., Wallis J. Ovarian hormone concentrations and genital swelling patterns in female chimpanzees with norplant implants. Zool. Biol. 1997, 16:209-223.
11. Bhargava S.K. Antiandrogenic effects of a flavonoid-rich fraction of Vitex negundo seeds: a histological and biochemical study in dogs. J. Ethnopharmacol. 1989, 27:327-339.
12. Borries C., Koenig A., Winkler P. Variation of life history traits and mating patterns in female langur monkeys (Semnopithecus entellus). Behav. Ecol. Sociobiol. 2001, 50:391-402.
13. Borries C., Larney E., Lu A., Ossi K., Koenig A. Costs of group size: lower developmental and reproductive rates in larger groups of leaf monkeys. Behav. Ecol. 2008, 19:1186-1191.
14. Borries, C., Lu, A., Ossi-Lupo, K., Larney, E., Koenig, A. 2010. Primate life histories and dietary adaptations: a comparison of Asian colobines and macaques. Am. J. Phys. Anthropol. doi:10.1002/ajpa.21403.
15. Brockman D.K., van Schaik C.P. Seasonality and reproductive function. Seasonality in Primates: Studies of Living and Extinct Human and Non-human Primates 2005, 269-305. Cambridge University Press, New York. D.K. Brockman, C.P. van Schaik (Eds.).
16. Bronson F.H. Mammalian reproduction: an ecological perspective. Biol. Reprod. 1985, 32:1-26.
17. Clotfelter E.D., Bell A.M., Levering K.R. The role of animal behaviour in the study of endocrine-disrupting chemicals. Anim. Behav. 2004, 68:665-676.
18. Czekala N.M., Roser J.F., Mortensen R.B., Reichard T., Lasley B. Urinary hormone analysis as a diagnostic tool to evaluate the ovarian function of female gorillas (Gorilla gorilla). J. Reprod. Fertil. 1988, 82:255-161.
19. Dailey R.A., Neill J.D. Seasonal variation in reproductive hormones of rhesus monkeys: anovulatory and short luteal phase menstrual cycles. Biol. Reprod. 1981, 25:560-567.
20. Das M., Parveen S., Kundra C.P., Pereira B.M.J. Reproduction in male rats is vulnerable to treatment with the flavonoid-rich seed extracts of Vitex negundo. Phytother. Res. 2004, 18:8-13.
21. Ellison P.T. Ecology and ovarian function among Lese women of the Ituri Forest, Zaire. Am. J. Phys. Anthropol. 1989, 78:519-526.
22. Ellison P.T. Energetics and reproductive effort. Am. J. Hum. Biol. 2003, 15:342-351.
23. Ellison P.T., Valeggia C.R., Sherry D.S. Human birth seasonality. Seasonality in Primates: Studies of Living and Extinct Human and Non-human Primates 2005, 379-399. Cambridge University Press, Cambridge. D.K. Brockman, C.P. van Schaik (Eds.).
24. Emery Thompson M., Wrangham R.W. Diet and reproductive function in wild female chimpanzees (Pan troglodytes schweinfurthii) at Kibale National Park, Uganda. Am. J. Phys. Anthropol. 2008, 135:171-181.
25. Emery Thompson M., Wilson M.L., Gobbo G., Muller M.N., Pusey A.E. Hyperprogesteronemia in response to Vitex fischeri consumption in wild chimpanzees (Pan troglodytes schweinfurthii). Am. J. Primatol. 2008, 70:1064-1071.
26. Frisch R.E., McArthur J.W. Menstrual cycles-fatness as a determinant of minimum weight for height necessary for their maintenance or onset. Science 1974, 185:949-951.
27. Fritsche S., Steinhart H. Occurrence of hormonally active compounds in food: a review. Eur. Food Res. Technol. 1999, 209:153-179.
28. Garey J. Acacia flowers from wild vervet diets are reproductive stimulators. Am. J. Primatol. 1991, 24:102-103.
29. Garey J., Markiewicz L., Gurpide E. Estrogenic flowers, a stimulus for mating activity in female vervet monkeys. Proceedings of the XIV Congress of the International Primatological Society 1992, 210-211. IPS, Strasbourg.
30. Gerhard I., Patek A., Monga B., Blank A., Gorkow C. Mastodynon (R) for female infertility. Randomized, placebo-controlled clinical double-blind study. Forsch. Komplementärmed. 1998, 5:272-278.
31. Girman A., Lee R., Kligler B. An integrative medicine approach to premenstrual syndrome. Am. J. Obstet. Gynecol. 2002, 188:S56-S65.
32. Glander K.E. Non-human primate self-medication with wild plant foods. Eating of the Wild Side: The Pharmacologic, Ecologic, and Social Implications of Using Non-Cultigens 1994, 239-256. University of Arizona Press, Tuscon. N.L. Etkin (Ed.).
33. Heistermann M., Ademmer C., Kaumanns W. Ovarian cycle and effect of social changes on adrenal and ovarian function in Pygathrix nemaeus. Int. J. Primatol. 2004, 25:689-708.
34. Higham J.P., Ross C., Warren Y., Heistermann M., MacLarnon A.M. Reduced reproductive function in wild baboons (Papio hamadryas anubis) related to natural consumption of the African black plum (Vitex doniana). Horm. Behav. 2007, 52:384-390.
35. Hu Y., Hou T., Zhang Q., Xin H., Zheng H., Rahman K., Qin L. Evaluation of the estrogenic activity of the constituents in the fruits of Vitex rotundifolia L. for the potential treatment of premenstrual syndrome. J. Pharm. Pharmacol. 2007, 59:1307-1312.
36. Iino M., Nomura T., Tamaki Y., Yamada Y., Yoneyama K., Takeuchi Y., Mori M., Asami T., Nakano T., Yokota T. Progesterone: its occurrence in plants and involvement in plant growth. Phytochemistry 2007, 68:1664-1673.
37. Janeczko A., Skoczowski A. Mammalian sex hormones in plants. Folia Histochem. Cytobiol. 2005, 43:71-79.
38. Janson C.H., Chapman C.A. Resources and primate community structure. Primate Communities 1999, 237-267. Cambridge University Press, Cambridge. J.G. Fleagle, C.H. Janson, K. Reed (Eds.).
39. Johnson M.H. Essential Reproduction 2007, Blackwell, Massachusetts.
40. Knott C. Female reproductive ecology of the apes: implications for human evolution. Reproductive Ecology and Human Evolution 2001, 429-458. Aldine de Gruyter, New York. P.T. Ellison (Ed.).
41. Koenig A. Competitive regimes in forest-dwelling Hanuman langur females (Semnopithecus entellus). Behav. Ecol. Sociobiol. 2000, 48:93-109.
42. Koenig A., Borries C. Socioecology of Hanuman langurs: the story of their success. Evol. Anthropol. 2001, 10:122-137.
43. Koenig A., Borries C., Chalise M.K., Winkler P. Ecology, nutrition, and timing of reproductive events in an Asian primate, the Hanuman langur (Presbytis entellus). J. Zool. Lond. 1997, 243:215-235.
44. Landgren B.M. Mechanism of action of gestagens. Int. J. Gynecol. Obstet. 1990, 32:95-110.
45. Larney E., Koenig A. Speed of infant development in Phayre's leaf monkeys: a mother's influence. Am. J. Phys. Anthropol. 2007, 132:150-151.
46. Leopold A.S., Erwin M., Oh J., Browning B. Phytoestrogens-adverse effects on reproduction in California quail. Science 1976, 191:98-100.
47. Liu J., Burdette J.E., Xu H., Gu C., van Breemen R.B., Bhat K.P.L., Booth N., Constantinou A.I., Pezzuto J.M., Fong H.H.S., Farnsworth N.R., Bolton J.L. Evaluation of estrogenic activity of plant extracts for the potential treatment of menopausal symptoms. J. Agric. Food Chem. 2001, 49:2472-2479.
48. Liu J., Burdette J.E., Sun Y., Deng S., Schlecht S.M., Zheng W., Nikolic D., Mahady G., van Breemen R.B., Fong H.H.S., Pezzuto J.M., Bolton J.L., Farnsworth N.R. Isolation of linoleic acid as an estrogenic compound from the fruits of Vitex agnus-castus L. (chaste-berry). Phytomedicine 2004, 11:18-23.
49. Lu A., Borries C., Czekala N.M., Beehner J.C. Reproductive characteristics of wild female Phayre's leaf monkeys. Am. J. Primatol. 2010, 10.1002/ajp. 20866.
50. Maninger N., Sackett G.P., Ruppenthal G.C. Weaning, body weight, and postpartum amenorrhea duration in pigtailed macaques (Macaca nemestrina). Am. J. Primatol. 2000, 52:81-91.
51. Michael R.P., Zumpe D. Medroxyprogesterone acetate decreases the sexual activity of male cynomolgus monkeys (Macaca fascicularis): an action on the brain?. Physiol. Behav. 1993, 53:783-788.
52. Milewicz A., Gejdel E., Sworen H., Sienkiewicz K., Jedrzejak J., Teucher T., Schmitz H. Vitex agnus castus extract in the treatment of luteal phase defects due to latent hyperprolactinemia: results of a randomized placebo-controlled double-blind study. Arzneimittel-Forschung/Drug Res. 1993, 43:752-756.
53. Pazol K., Wilson M.E., Wallen K. Medroxyprogesterone acetate antagonizes the effects of estrogen treatment on social and sexual behavior in female macaques. J. Clin. Endocrinol. Metab. 2004, 89:2998-3006.
54. Portugal M.M., Asa C.S. Effects of chronic melengestrol acetate contraceptive treatment on perineal tumescence, body weight, and sociosexual behavior of hamadryas baboons (Papio hamadryas). Zool. Biol. 1995, 14:251-259.
55. Rochester J.R., Klasing K.C., Stevenson L., Denison M.S., Berry W., Millam J.R. Dietary red clover (Trifolium pratense) induces oviduct growth and decreases ovary and testes growth in Japanese quail chicks. Reprod. Toxicol. 2009, 27:63-71.
56. Roemheld-Hamm B. Chasteberry. Am. Fam. Physician 2005, 72:821-824.
57. Sadenkrehula M., Kustrak D., Blazevic N. Delta-4-3-ketosteroids in flowers and leaves of Vitex-agnus-castus. Acta Pharm. Jugoslav. 1991, 41:237-241.
58. Shelmidine N., Borries C., McCann C. Patterns of reproduction in Malayan silvered leaf monkeys at the Bronx Zoo. Am. J. Primatol. 2009, 71:852-859.
59. Shimizu K., Takenoshita Y., Mitsunaga F., Nozaki M. Suppression of ovarian function and successful contraception in macaque monkeys following a single injection of medroxyprogesterone acetate. J. Reprod. Dev. 1996, 42:147-155.
60. Simons R.G., Grinwich D.L. Immunoreactive detection of four mammalian steroids in plants. Can. J. Bot. 1989, 67:288-296.
61. Sliutz G., Speiser P., Schultz A.M., Spona J., Zeillinger R. Agnus-castus extracts inhibit prolactin secretion of rat pituitary cells. Horm. Metab. Res. 1993, 25:253-255.
62. Sokal R.R., Rohlf F.J. Biometry 1995, W.H. Freeman and Company, New York. 3rd edition.
63. Sommer V., Srivastava A., Borries C. Cycles, sexuality, and conception in free-ranging langurs (Presbytis entellus). Am. J. Primatol. 1992, 28:1-27.
64. Steklis H.D., Linn G.S., Howard S.M., Kling A.S., Tiger L. Effects of medroxyprogesterone acetate on socio-sexual behavior of stumptail macaques. Physiol. Behav. 1982, 28:535-544.
65. Suarez, S., in preparation. Diet of the Phayre's leaf monkey in the Phu Khieo Wildlife Sanctuary, Thailand. Int. J. Primatol.
66. Trisomboon H., Malaivijitnond S., Watanabe G., Taya K. Estrogenic effects of Pueraria mirifica on the menstrual cycle and hormone-related ovarian functions in cyclic female cynomolgus monkeys. J. Pharmacol. Sci. 2004, 94:51-59.
67. Trisomboon H., Malaivijitnond S., Watanabe G., Taya K. Ovulation block by Pueraria mirifica-a study of its endocrinological effect in female monkeys. Endocrine 2005, 26:33-39.
68. Trisomboon H., Malaivijitnond S., Cherdshewasart W., Watanabe G., Taya K. Effect of Pueraria mirifica on the sexual skin coloration of aged menopausal cynomolgus monkeys. J. Reprod. Dev. 2006, 52:537-542.
69. Trisomboon H., Malaivijitnond S., Watanabe G., Cherdshewasart W., Taya K. The estrogenic effect of Pueraria mirifica on gonadotrophin levels in aged monkeys. Endocrine 2006, 29:129-134.
70. van Schaik C.P., van Noordwijk M.A. Interannual variability in fruit abundance and the reproductive seasonality in Sumatran long-tailed macaques (Macaca fascicularis). J. Zool. Lond. 1985, 206:533-549.
71. Walker M.L., Gordon T.P., Wilson M.E. Menstrual cycle characteristics of seasonally breeding rhesus monkeys. Biol. Reprod. 1983, 29:841-848.
72. Wallis J. A survey of reproductive parameters in the free-ranging chimpanzees of Gombe National Park. J. Reprod. Fertil. 1997, 109:297-307.
73. Wasser S.K., Monfort S.L., Southers J., Wildt D.E. Excretion rates and metabolites of oestradiol and progesterone in baboon (Papio cynocephalus cynocephalus) faeces. J. Reprod. Fertil. 1994, 101:213-220.
74. Westphal L.M., Polan M.L., Trant A.S., Mooney S.B. A nutritional supplement for improving fertility in women-a pilot study. J. Reprod. Med. 2004, 49:289-293.
75. Whitten P.L. Flowers, fertility, and females. Am. J. Phys. Anthropol. 1983, 60:269-270.
76. Whitten P.L., Naftolin F. Reproductive actions of phytoestrogens. Baillières Clin. Endocrinol. Metab. 1998, 12:667-690.
77. Whitten P.L., Patisaul H.B. Cross-species and interassay comparisons of phytoestrogen action. Environ. Health Perspect. 2001, 109:5-20.
78. Wuttke W., Jarry H., Christoffel V., Spengler B., Seidlova-Wuttke D. Chaste tree (Vitex agnus-castus) pharmacology and clinical indications. Phytomedicine 2003, 10:348-357.
79. Ziegler T., Hodges J.K., Winkler P., Heistermann M. Hormonal correlates of reproductive seasonality in wild female Hanuman langurs (Presbytis entellus). Am. J. Primatol. 2000, 51:119-134.
80. Zumpe D., Clancy A.N., Michael R.P. Effects of progesterone on the sexual behavior of castrated, testosterone-treated male cynomolgus monkeys (Macaca fascicularis). Physiol. Behav. 1997, 62:61-67.
81. Zumpe D., Clancy A.N., Michael R.P. Progesterone decreases mating and estradiol uptake in preoptic areas of male monkeys. Physiol. Behav. 2001, 74:603-612.
82. Global Biodiversity and Information Facility, last accessed (June 20, 2010). http://data.gbif.org/species/13194840.