Fecal hormones (Spanish)

HORMONAS EN HECES: ESTUDIOS USANDO TECNICAS NO INVASIVAS EN POBLACIONES DE PRIMATES SILVESTRES EN EL SUR DE MEXICO

LABORATORIO DE PRIMATOLOGIA

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


Investigaciones de los ciclos hormonales, conducta sexual y fenología de la reproducción en monos aulladores y monos araña

Sarie Van Belle sarievanbelle@primatesmx.com


Tanto el mono aullador de manto (Alouatta palliata) como el mono aullador negro (Alouatta pigra) que se encuentran en el sur de México y la región Mesoamericana están considerados como especies en peligro en la lista de CITES, con las presiones para su conservación provenientes principalmente de la destrucción de sus hábitats y el tráfico de mascotas. Decrementos adicionales como resultado de estas presiones sobre las poblaciones tendrán implicaciones importantes para su recuperación y para la conservación de las selvas que constituyen sus hábitats. La biología de la reproduccón y conductas asociadas forman la base de la historia de vida de las especies y su estudio es crítico para la conservación y manejo de las poblaciones de primates silvestres.

El caso de Alouatta: debido a que no existen signos visuales de la ciclidad ovárica de miembros del género, poco es lo que se conoce acerca de la ciclidad de las hormonas reproductivas. Hasta ahora, solo existen dos investigaciones enfocadas a este problema. Una sobre la fisiología reproductiva de Alouatta caraya. La otra aporta observaciones preliminares sobre el ciclo estral y gestación en Alouatta seniculus.

La disponibilidad de técnicas no invasivas para la extracción de hormonas a partir de las heces de los primates ha resultado ser un procedimiento confiable para la obtención de perfiles de esteroides gonádicos en varias especies de primates (por ejemplo, chimpancés, macacos, monos ardilla, monos araña y las dos especies de monos aulladores mencionadas arriba). En virtud de la vida arbórea de los primates silvestres que existen en el sur de México, este procedimiento es uno de los más adecuados para investigar aspectos de la fisiología de la reproducción en poblaciones de las dos especies de monos aulladores que existen en el sureste de México: A. palliata and A. pigra.


Las hormonas relacionadas al comportamiento reproductivo en las hembras son progesterona, estradiol y pregnandiol. Con la obtención de perfiles hormonales para hembras de diferentes edades y poblaciones, uno puede calcular la edad a la madurez sexual, edad al primer parto, duración de la gestación, intervalos entre nacimientos y/o concepciones y la duración del ciclo estral, todo esto en combinación con la variación intra y inter grupal causada por diferencias entre tropas unimachos y multimachos.

Con esta información, uno puede examinar la conducta reproductiva en relación al tiempo de ovulación y la resultante paternidad en grupos multimachos. También se puede verificar si la función ovárica es sensible a variaciones en la calidad de la dieta, que a su vez puede resultar en patrones estaciones en la biología reproductiva o si esta es sensible al estrés causado, por ejemplo, por la fragmentación y aislamiento del hábitat.

La testosterona es la principal hormona relacionada a la biología de la reproducción en los machos. Esta hormona es indicativa de la edad y madurez sexual y junto con el cortisol juega un papel importante en las relaciones de dominio en la tropa.

Los perfiles obtenidos para cortisol a partir de muestras fec ales también pueden ser indicadores del nivel general de estrés en la población causado por la fragmentación del hábitat.

Nuestro trabajo de campo consiste en la recolecta de muestras fecales de poblaciones silvestres de monos aulladores y araña en varios puntos del sureste de México (ver mapa en hoja sobre investigaciones con primates) y son parte de un programa comprensivo de estudios de hormonas, genética y carga parasitaria usando técnicas no invasivas. Estas muestras son almacenadas en alcohol al 95% para su posterior análisis en el laboratorio, en donde se hacen las extracciones de testosterona, estradiol, progesterona, pregnadiol y cortisol por medio de radioinmunoensayos, construyendo así los perfiles individuales. Dicha colecta se acopla a observaciones regulares de la conducta social y sexual de los individuos en tropas selectas y a aquellas relacionadas a evaluar la calidad del hábitat y su grado de perturbación por la actividad humana.


Algunos comentarios sobre la reproducción en monos aulladores (versión en Español en breve)

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.


Algunos comentarios sobre la reproducción en monos araña (versión en Español en breve)

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 monkyes 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)

 

Referencias citadas 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.

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

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.

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.

Referencias citadas 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.

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Otras referencias relevantes:

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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