Estación de Biología "Los Tuxtlas", Instituto de Biología-UNAM 

Studies of hormonal cycles, sexual behavior and the phenology of reproduction in howler and spider monkeys

by Sarie Van Belle sarievanbelle@primatesmx.com

The particular interests of this research program is to determine the hormonal profiles for males and females in social groups of howler monkeys (Alouatta palliata and A. pigra) and of spider monkeys (Ateles geoffroyi) existing in large and protected tracts of forest as well as in landscapes with different degrees of fragmentation. We expect to collect data as well on the phenology of hormonal cycles, reproductive behaviors and resulting births/conceptions.

This approach will yield basic information on species reproductive physiology and associated behaviors and it will allow us as well to assess how labile the physiological systems and behaviors associated to reproduction may be to contrasting ecological conditions and stress levels.

The field work consists of collection of fecal material in combination with observations of social and sexual behavior in populations of howler and spider monkeys in several sites in southern Mexico. Fecal material is stored in 95 % alcohol and kept under refrigeration until analysis. Laboratory work consists of extracting the hormones using radioimmunoassay procedures.

Both the mantled howler monkey (Alouatta palliata) and the black howler monkey (Alouatta pigra) of the Mesoamerican region are considered to be endangered species in the list of CITES with the pressure mostly coming from tropical rainforest destruction and fragmentation and the pet traffick. Further declines will have a severe implication on the ability of populations to recover and on tropical ecosystem conservation since howler monkeys play important ecological roles in their habitats (e.g. as seed dispersal agents thus promoting the regeneration of the tropical rainforest). The reproductive biology and behaviour forms the basis in the life history information of a species and its understanding is critical to management and conservation of wild populations.

Since there are no visual signs of ovarian cycling, little is known about the reproductive hormones in the genus of Alouatta. Untill now only two investigations have been conducted. One focusing on the male reproductive physiology of Alouatta caraya while the other study provides preliminary observations of the estrus cycle and gestation of Alouatta seniculus. The non-invasive method of extracting hormones from fecal material have proven to be a reliable way of obtaining gonad steroid profiles in several wild primates, e.g. chimpanzees, macaques, squirrel monkey, spider monkeys and the two howler monkey species mentioned above. With their arboreal life style this methods will be the most adequate to investigate the reproduction of howler monkey species present in southern Mexico such as A. palliata and A. pigra.

The hormones related to the female reproductive behaviour are progesterone, estradiol and pregnandiol. With the profiles from females of different ages and populations one can calculate the age of sexual maturity, the age of the first birth, gestation length, birth interval and the estrus cycle length in combination with the intra and inter troop variation and the variation caused by the difference between single male and multi-male troops. One can examine mating behavior in relation to timing of ovulation and paternity outcome in multi-male troops. One can test if ovarian function is sensitive to dietary quality which leads to seasonality in the reproductive biology or if it is sensitive to stress caused by, for example, habitat fragmentation and isolation.

Testosterone is the main hormone concerning the male reproductive biology. This hormone indicates the age of sexual maturity and together with cortisol, it plays a role in the behavior of dominance rank in their troop.

Cortisol profiles obtained from fecal samples can also indicate the level of general stress caused by habitat fragmentation.

The use of non invasive techniques has proven to be a useful method to investigate aspects of the physiology of widllife, including hormonal profiles and hormonal cycles related to reproduction, as well as aspects of population genetics and others such as parasite load, foods consumed and ingestion of pollutants. Such techniques do not disturb the widlife of interest and a vast amount of information can thus be gathered under wild conditions, without the need to capture the individuals.

Concomitantly with the increased interest to examine social behavior and life history through hormonal investigation in a natural setting a great advance has been made in techniques to monitor hormone-behavior interaction. I will give a brief synopsis of exciting methods but for a complete and intelligible review, see Whitten et al. (1998).

In field conditions, urine and feces are the major sources used to investigate hormonal activity and status of feral animals.  In both sources, hormone concentrations reflect the cumulative secretion and elimination of hormones over a number of hours (Whitten et al. 1998) meaning that the obtained concentrations reflect events occurring hours to days before: on average 4-8 h for urine steroids and 0.3-3 days for fecal steroids depending on the duration of the species specific gastrointestinal transit (Whitten et al. 1998 and citations therein).It also implies that the concentrations in urine and feces are those of the metabolites rather than the steroid itself.    Studies with primates reveal that estradiol is excreted primarily as estradiol and estrone or its conjugates whereas progesterone is often metabolized into a number of progestin metabolites, eg. pregnanelones and pregnanediols (Ziegler et al. 1989, Shideler et al. 1993, Wasser et al. 1994 cited in Whitten et al. 1998).

Several methods have been applied to preserve the fecal and urine steroids since oxidation and bacterial metabolism can alter steroid concentration in unpreserved samples.  Wasser et al. (1988) showed that changes in fecal estradiol and progesterone concentrations occurred very rapidly (within 6 h) in unpreserved samples kept at room temperature. To overcome this alternation a variety of preservation techniques have been used in the fields with freezing in 95% ethanol as the most successful, but see Khan et al. (2002) for further details on fecal sample storage for steroid analysis. Until now only three studies have been investigating hormonal profiles in the genus Alouatta. Studies with A. palliata in Costa Rica yielded fecal estradiol values of three pregnant, 8 lactating and 21 cycling females with means of 53.6 ng/g, 164.6 ng/g and 417.8 ng/g, respectively.Zucker et al. (1995) concluded that in general, cycling females have higher estradiol values than do females in other reproductive status, although even among cycling females, estradiol values are highly variable. They also find that copulation coincide with elevation in fecal estradiol but poorly associated with sexual swelling ( Clarke et al. 1991 cited in Whitten et al. 1998) on which oestrous cycles are based to infer its duration (16.3 days on average (Glander 1980).

Moreland et al. (2001) monitored fecal testosterone metabolites levels in A. caraya males in captivity.  Four male exhibited constant levels of 3.66 ± 0.45 ng/g throughout the year while testosterone levels in 2 males of a bachelor troop elevated to 43 ng/g during the months may and June.

A more detailed study was conducted on A. seniculus to monitor observations of oestrous cycle and gestation through urine progesterone profiles (Herrick et al. 2000).  Based on two profiles, the length of the eostrous cycle in the red howler monkeys were estimated to be 29.5 ± 1.5 days. Previous estimation of the cycle duration assuming that copulation exclusively occurred in the periovulatory period of the cycle resulted in a length of 17 days (range = 16-27 days) (Crockett and Sekulic 1982).  One female was observed copulating throughout two cycles suggesting that previous estimations of the length of the eostrous cycle in red howler monkeys might be unreliable (Herrick et al. 2000).

Some comments on howler monkey reproduction

In general, the reproductive biology and behavior of the genus Alouatta is scarcely documented. Most information comes from investigations on A. palliata and A. seniculus in a few localities in Central and South America. The following is a synopsis of aspects of reproduction of a free-ranging population of A. palliata in Hacienda La Pacifica, Costa Rica (Glander 1980).

Female howler monkeys reach the age of sexual maturity after 36 months with the onset of the estrus cycling. Glander (1980) observed a color change and swelling of the vulvar with maximum swelling considered as the periovulatory phase. The length of the estrus cycle varied between 11- 24 days with a mean of 16.3 days. Since there doesn’t occur any visual change of the vulvar in A. pigra, such data is still lacking for this specie. Mantled howler monkey males are estimated to reach sexual maturity at an age of 36 months when the testicles descend and the scrotum become pendulous. Due to social ranking effects, males are observed to mate for the first time at an older age, 52 months. In contrast, all A. pigra males observed from at least 3 to 4 months of age exhibited white-pink descended testis (Horwich 1983) and therefore the age of sexual maturity can not be estimated by visual signs.

No individual of either sex has been observed to copulate until attained dominance rank. The “alpha” male copulates significantly more frequently than the lowest ranking group male and is more likely to copulate with peak estrus females (Jones 1980). In contrast, lower ranking females are reproductively more successful since all “alpha” positioned females were primiparous and lost the first infant. By the time they gave birth to their second infant, another next female was the dominant one. Females are receptive to copulation for 2 to 4 days during each cycle and participate in multiple mating before becoming pregnant. The adult males routinely sniffed the urine and licked the genitalia of females during inferred estrus to presumably obtain olfactory and gustatory information about the female’s sexual condition.Both sexes solicited for sexual interaction by tongue flicking, a rapid in and out the mouth movement of the tongue.  Although Horwich (1983) described this behavior in A. pigra more as the alleged “lipsmacks” observed in Old World Monkeys: “the tongue was not extruded and instead the mouth was slowly opened and closed with the tongue barely extended”.  This behavior with both partners facing each other, but sometimes the female forces herself upon the male by pulling his face over to her by the side hairs on his beard.  A consort between the two concerned individuals is formed for several days in which both animals solicit and copulate various times. Copulatory mounts usually included the male’s grasping the female with his hands and sometimes his feet.The main constancy was his holding her shoulder hairs with his hands. Each copulation lasted between a half and one minute (Horwich 1983).

Glander (1980) divided the time between a A. palliata female’s successive births in a period of gestation, one of postpartum acyclicity and a sexual receptive phase. Gestation length has been calculated for A. palliata based on four female’s pregnancies as 186 days on average, ranging between 180 and 196 days (Glander 1980). Similar, though slightly higher figures were estimated for A. seniculus (Crockett & Sekulic 1982). After the birth of the infant, the female did not accept or solicit sexual advances for three or four months. If the infant died within this period, this phase of acyclicity ended abruptly and the interbirth interval was shortened to 9-10 months. The interbirth interval of infants surviving at least their first year is estimated to be 22.4 months for A. palliata. The length of the interval spent cycling before primiparous and multiparous females become pregnant varied from 8 to 15 months.

The howler monkeys seem to be the least seasonal of all the New World primates. All howler populations with large enough sample sizes show predictable seasonal variation of birth throughout the year (Crockett and Rudran 1987; Rumiz 1990; Di Bitetti and Janson 2000 and references therein; Strier et al. 2001). The time of the year with fewer births tends to be around the peak period for new leaves and fruits. Crockett and Rudran (1987 cited in Di Bitetti and Janson 2000) give two main reasons that may account for their lack of strict seasonality: 1) their ability to rely on leaves and on unripe fruits and 2) their large body size that makes them less sensitive to food shortage.

Some comments on Spider monkey reproduction


Spider monkeys are considered to be very vulnerable to the fragmentation and disappearance of their habitats. Due to difficulties of observing and investigating wild spider monkeys little is known about their reproductive biology and behavior, basic data needed in the design of conservation management plans.

The multimale, multifemale social organisation implies that Ateles are polygamous. Both males and females reach maturity at the age of 5 years. Aggression between males is infrequent, estrous females choose their mating partners, and both promiscuous matings and consortships have been observed (Robinson and Janson, 1987). Females initiate sexual activity, and the face-to-face copulation may last for up to 25 minutes( Eisenberg 1976, van Roosmalen 1980 cited in Robinson and Janson, 1987). The duration of gestation lay in the range between 226 and 232 days. Females do not resume cycling during the 3 year period of infant dependency (Robinson and Janson, 1987). Campbell et al (2001) report that females cycle for approximately 3-6 months prior to conception. This results in an interbirth interval of 17-46 months (whether the infant survives the first 3 years) and there is no pattern of birth seasonality.

The reproductive endocrinology of female spider monkeys remains largely unreported, but Campbell et al. (2001) showed the high reliabilty of using fecal material for obtaining profiles for ovarian steroids for Ateles in captivity and in the wild. Length of mentrual cycle was calculated at an average of 22.7 days (range = 13-43 days) in free-ranging females. These figures lies within the range observed in captive females: 20-22 days and 22-24 days (Hodges et al. 1981 and Hernández-López et al. 1998 respectively)

Cited references Alouatta:

Crockett, C.M. & Rudran R. (1987).  Red howler monkey birth data I: seasonal variation.  AM. J. PRIMATOL. 13: 347-368

Crockett, C.M. & Sekulic, R. (1982).  Gestation length in red howler monkeys.  AM. J. PRIMATOL. 3: 291-294.

Di Bitetti M.S. & Janson J.H. (2000).  When will the stork arrive?  Patterns of birth seasonality in Neotropical primates.  AM. J. PRIMATOL. 50: 109-130.

Glander, K.E. (1980).  Reproduction and population growth in free-ranging mantled howler monkeys.  AM. J. PHYS. ANTHROPOL. 53: 25-36.

Herrick J.R.; G. Agoramoorthy; R. Rudran; and J.D. Harder (2000).  Urinary progesterone in free-ranging red howler monkeys (Alouatta seniculus): preliminary observations of estrous cycle and gestation. AM. J. PRIMATOL. 51: 257-263.

Horwich, R.H. (1983).  Breeding behaviors in black howler monkey (Alouatta pigra) of Belize.  PRIMATES 24: 222-230.

Khan, M.Z.; J. Altman; S.S. Isani and J. Yu (2002).  A matter of time: evaluating the storage of feacl samples for steroid analysis.  GENERAL AND COMPARATIVE ENDOCRINOLOGY :8 PP.

Jones, C.B. (1980).  The functions of status in the mantled howler monkeys, Alouatta palliata Gray: intraspecific competition for group membership in a folivorous Neotropical primate.  PRIMATES 21:389-405.

Jones, C.B. (1985).  Reproductive patterns in mantled howler monkeys: estrus, mate choice and copulation.  PRIMATES 26: 130-142.

 Moreland R.B.; M.E. Richardson; N. Lamberski and J.A. Long  (2001).  Characterizing the reproductive physiology of the male southern black howler monkey, Alouatta caraya.  J. ANDROLOGY

Rumiz, D.I. (1990).  Alouatta caraya: population density and demography in northern Argentina.  AM. J. PRIMATOL. 21: 279-294.

Strier K.B., Mendes S.L. & Santos R.R. (2001).  Timing of births in sympatric howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachoides hypoxanthus).  AM. J. PRIMATOL. 55: 87-100.

Zunino G.E. (1996).  Análisis de nacimientos en Alouatta caraya (Primates, Cebidae), en el noreste de la Argentina.  REV. MUS. ARG. CIENCIAS NAT., NUEVA SERIA 133: 1-10.

Zucker E.L.; M.R. Clarke and R.M. Harrison (1995).  Fecal estradiol values for group-living cycling, pregnant, and lactating female howling monkeys (Alouatta palliata).  AM. J. PRIMATOL. 36: 167 [Abstract].


Zucker E.L.; M.R. Clarke; P.M. Putman and R.M. Harrison (1994).  Validity of measures assessing reproductive status of female howling monkeys (Alouatta palliata).  AM. J. PRIMATOL. 33: 225 [Abstract].

Whitten P.L.; D.K. Brockman and R.C. Stavisky  (1998).  Recent advances in noninvasive techniques to monitor hormone-behavior interections.  YB OF PHYS. ANTHROPOL. 41: 1-23.

Cited References Ateles

Campbell CJ, Shideler SE, Todd HE & Lasley BL (2001). Fecal analysis of ovarian cycles in female black-handed spider monkeys (Ateles geoffroyi).Am. J. Primatol. 54: 79-89

Hernández-López L, Mayagoita L, Esquivel-Lacroix C, Rojas-Maya S & Mondragon-Ceballos R (1998).The menstrual cycle of the spider monkey (Ateles geoffroyi).Am. J. Primatol. 44:183-195.

Hodges JK, Gulick BA, Czekala NM & Lasley BL (1981). Comparison of urinary oestrogen excretion in South American primates.J. Reprod. Fertil. 61: 83-90.

Robinson JG & Janson CH (1986). Capuchins, squirrel monkeys, and Atelines: socioecological convergence with Old World primates In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW & Struhsaker TT (eds). Primate societes. The University of Chicago Press: 69-82.


Other relevant references:

Hernandez-Lopez L; Cerezo Parra G; Cerda-Molina AL; Perez-Bolanos SC; Diaz Sanchez V; Mondragon-Ceballos R. Sperm quality differences between the rainy and dry seasons in captive black-handed spider monkeys (Ateles geoffroyi). AMERICAN JOURNAL OF PRIMATOLOGY. 2002. 57(1), Pgs: 35-41

Campbell CJ. The reproductive biology of black-handed spider monkeys (Ateles geoffroyi): Integrating behavior and endocrinology. DISSERTATION ABSTRACTS INTERNATIONAL. 2001. A62(1), Pgs: 229

Eisenberg JF (1973) Reproduction of spider monkeys (Ateles fusciceps and A. geoffroyi). J Mammal 54: 955-957.

McDaniel PS, Janzow FT, Porton I, Asa Cs (1993). The reproductive and social dynamics of captive Atels geoffroyi. Am Zool 33:173- 179.

Pastor-Nieto R.Female reproductive advertisement and social factors affecting the sexual behavior of captive spider monkeys. LABORATORY PRIMATE NEWSLETTER. 2000. 39(3), Pgs: 5-9

Cortes-Ortiz L; Rodriguez-Luna E. [Natural history of species: Ateles geoffroyi.]. HISTORIA NATURAL DE LOS TUXTLAS. Gonzalez Soriano E, Dirzo R, Vogt RC, Editors. Mexico: Univ Nac Auton Mexico, Instituto de Biología. 1997, Pgs: 616-622

Long JA; Lamberski N; Shoemaker AH. Ejaculate characteristics of the black-handed spider, southern black howler and Diana monkey. JOURNAL OF ANDROLOGY. 1997. (Suppl), Pgs: P41

Vick L; Taub D. Poco a poco: Steps toward spider monkey conservation in Mexico's Yucatan peninsula. [Abstract] . CHIMPANZOO CONFERENCE PROCEEDINGS. 1996. (1995), Pgs: 91

Wallace RB. The behavioural ecology of black spider monkeys in north-eastern Bolivia. NEOTROPICAL PRIMATES. 1999. 7(3), Pgs: 93-94

Nunes A; Chapman CA. A re-evaluation of factors influencing the sex ratio of spider monkey populations with new data from Maraca Island, Brazil. FOLIA PRIMATOLOGICA. 1997. 68(1), Pgs: 31-33

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