(Bolivian red Howler monkey)
Alouatta seniculus sara
1) General Zoological Data
Alouatta is the most widely distributed genus "of neotropical primates, with a geographic range extending from Mexico to northern Argentina" (Lima & Seuanez, 1991). It is also one of the largest cebids and is relentlessly pursued for food in South America. Thus, many species and subspecies are in peril of extinction. Just how many species there are, and which should be nominated as subspecies, are questions that are under frequent and continuing debate. An example is had in the discussion by Smith (1970) who described sympatry of two different, yet nominally different subspecies of black howler monkeys in Mexico. Howlers differ is size and, especially, in pelage. But coloration is not necessarily a good means of assigning species name, as was alluded to by Lima & Seuanez (1991). Moreover, there is extensive karyotypic evolution in this genus. Thus, precise point of origin is perhaps the best indicator for species designation. This is best brought out in the detailed discussion of the various species in Groves' new book (2001). He referred to "the xxx group" (e.g. "the seniculus group") and then assigns specific localities to the nominated species. Nowak (1999) listed nine species of howler monkeys, others consider there to be ten. Molecular studies by Harana et al. (1995) found evidence that links Ateles and Alouatta into one subfamily, the Atelinae. Hugot (1998) came to similar conclusions from studying the specific pinworms (Oxyuris) in the platyrrhine monkeys and considered these to have been co-evolved with platyrrhine speciation. Using mitochondrial and nuclear genes, Cortes-Ortiz et al. (2003) suggested that "the contemporary howler monkey species originated in the late Miocene and Pliocene, not the Pleistocene". mtDNA was more declarative than nuclear genes and they differentiated "cis- and trans-Andean clades". According to Gotch (1979), Alouatta is a combination of French and Latin to denote "a lot of shaggy hair".
The weight of male howler monkeys is usually larger than that of females but there is considerable variation. Generally speaking, weights between 4.4 and 11.5 kg have been listed for adults. The howler monkey is strongly prehensile with a very strong tail, is a preferably arboreal species, and it is the most folivorous of the South American primates. But fruit and other substances (nuts, blossoms) are also consumed. Fig trees are an important resource. In a detailed study of food consumed by red-handed howler monkeys, de Souza et al. (2002) described geophagy as also occurring in the wild. Howler monkeys, of course, are characterized by their loud howl - penetrating noises in the jungle. Having (inadvertently) rested under a tree with a band of howlers beginning their morning chatter, I can attest to the fear they may elicit. Jones (1980) lists 12 years as the longevity for a specimen of Alouatta villosa palliata.
General Gestational Data
Usually a single young is born after a gestation lasting around 180 days, and having a weight between 275 and 400 g. Shoemaker (1979) reviewed the captive reproduction in his zoo of a group of black howler monkeys and suggested from his literature review a gestational length of 187 days (139 in another paper) and 180-186 days for Alouatta palliata. Later (1982) he indicated that first successful keeping of howler monkeys in zoos did not occur until 1975, when the diet and other factors were better understood.
No early implantation stages have been described.
General Characterization of the Placenta
Details of fetal/maternal barrier
This placenta has a typical hemochorial relationship, with the villi covered by syncytium and directly bathed in maternal intervillous blood. Cytotrophoblast is already quite inapparent at this stage, but isolated cells may be found beneath the syncytium. Occasional syncytial "knots" are present. The fetal capillaries are close to the trophoblast; Hofbauer cells (macrophages) are present in the villous cores.
The umbilical cord of howler monkeys has not been studied, so far as I can tell. Young (1972) when seeking to identify the different types of anastomoses between the umbilical arteries in the cord ("Hyrtl's anastomosis") did not have howler monkeys available and found different anastomotic features in various other cebids. Many of the latter, however, also had four vessels in their cord, 2 arteries and 2 veins, as is shown for the single Alouatta seniculus sara cord available to me. It is similar in that respect to the umbilical cord of spider monkeys (see chapter on Ateles), except that there is no patent allantoic duct. Only tiny discontinuous remnants of the duct are found in the center between the umbilical arteries, as is also common in humans. Spatz (1968) related the length of primate umbilical cords to the overall length of neonates in numerous species and had seven howler monkey umbilical cords available. He determined the relationship to be similar to that of rhesus monkeys. There is no squamous metaplasia on the umbilical cord surface of this 12 cm long cord from the abortus studied here. It had a counterclockwise (right) twist.
No published studies are known to me.
Trophoblast external to barrier
There is no apparent infiltration of trophoblast deep into the endometrium, let alone into the myometrium. Only a thin layer of superficial decidua is infiltrated by extravillous trophoblast. There is no knowledge as to possible maternal vascular infiltration by trophoblast.
& Saldanha (1974) suggested chromosomal fusion as the mechanism of arriving
at the karyotype of A. fusca clamitans from the 2n=52 of A. caraya.
They also had two animals, however, with 2n=49 but did not expect this to
be due to a loss of a Y chromosome. The variation (47, 48, 49) of chromosome
numbers in A. seniculus stramineus found by Lima & Seuanez (1991),
as well as that of A. seniculus macconnelli (47,48,49), was attributed by
the authors to be due to the presence or absence of the microchromosomes
they had identified. Several reports that are listed above show the importance
of a Y-autosome translocation in howler monkeys. The complexity of the howler
monkey chromosomes was further exemplified by the studies of Consigliere
et al. (1998). They hybridized human chromosome-specific probes to howler
monkey chromosomes and found them to be extraordinarily complexly rearranged.
Moreover, studies of several howler species indicated that they, in themselves,
show great rearrangements. De Oliveria et al. (2002) did further FISH analyses
of three howler species with three specific and different painting probes.
The two mechanisms of sex chromosomal systems were verified and they concluded
that, among Platyrrhini, howlers have the most extensive chromosomal rearrangements.
They suggested that fusion, fission, inversion and Y-translocation all were
involved in their evolution.
James et al. (1997) examined 36 allozyme loci and RFLP loci of mtDNA in a group of A. pigra and found surprisingly little genetic heterogeneity in this group. Bonvincino et al. (2001) also studied genes (cytochrome bDNA) in several species of howler monkeys. They concluded that the unusual sex chromosome constitution described earlier appeared independently three times during the radiation of this species. Importantly, Mudry et al. (2001) studied the meiotic paring of chromosomes in two howler monkey species, and demonstrated the breakpoint by chromosome painting.
Multiple autoantibodies (rheumatoid factor, antinuclear antibody, antithyroglobulin, heterophil agglutinins and false VDRL) were identified in eight howler monkeys studied by Persellin & Chang (1974). I know of no other specific studies, except for the serologic surveys listed below.
Anesthesia and its reversal have been described in detail by Vie et al. (1998b). The same group of investigators recorded the hematologic findings and serum chemistry of red howlers (Vie et al., 1998a). Clark et al. (1987) examined plasma lipoproteins and found them similar to humans, while fatty acids were very low. The blood groups of howler monkeys were studied by Froehlich et al. (1977), and the prevalence of blood group "B" of South American monkeys was upheld. Their serum contained anti-A, and the saliva had H and B antigens.
Other remarks - What additional Information is needed?
Bonvincino, C.R., Lemos, B. and Seuanez, H.N.: Molecular phylogenetics of howler monkeys (Alouatta, Platyrrhini). A comparison with karyotypic data. Chromosoma 110:241-246, 2001.
Carme, B., Aznar, C., Motard, A., Demar, M. and de Thoisy, B.: Serologic survey of Toxoplasma gondii in noncarnivorous free-ranging neotropical mammals in French Guiana. Vector Borne Zoonotic Dis. 2:11-17, 2002.
Clark, S.B., Tercyak, A.M. and Glander, K.E.: Plasma lipoproteins of free-ranging howling monkeys (Alouatta palliata). Comp. Biochem. Physiol. B 88:729-735, 1987.
Consigliere, S., Stanyon, R., Koehler, U., Agoramoorthy, G. and Wienberg, J.: Chromosome painting defines genomic rearrangements between red howler monkey subspecies. Chromosome Res. 4:264-270, 1996.
Consigliere, S., Stanyon, R., Koehler, U., Arnold, N. and Wienberg, J.: In situ hybridization (FISH) maps chromosomal homologies between Alouatta belzebul (Platyrrhini, Cebidae) and other primates and reveals extensive interchromosomal rearrangements between howler monkey genomes. Amer. J. Primatol. 46:119-133, 1998.
Cortes-Ortiz, L., Bermingham, E., Rico, C., Rodriguez-Luna, E., Sampaio, I. And Ruiz-Garcia, M.: Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Mol. Phylogenet. Evol. 26:64-81, 2003.
Egozcue, J. and de Egozcue M.W.: The chromosome complement of the howler monkey (Alouatta caraya, Humboldt 1812). Cytogenetics 5:20-27, 1966.
Froehlich, J.W., Socha, W.W., Wiener, A.S., Moor-Jankowski, J. and Thorington, R.W.: Blood groups of the mantled howler monkey (Alouatta palliata). J. Med. Primatol. 6:219-231, 1977.
Gardiner, C.H., Wells, S., Gutter, A.E., Fitzgerald, L., Anderson, D.C., Harris, R.K. and Nichols, D.K.: Eosinophilic meningoencephalitis due to Angiostrongylus cantonensis as the cause of death in captive non-human primates. Amer. J. Trop. Med. Hyg. 42:70-74, 1990.
Glander, K.E.: Reproduction and population growth in free-ranging mantled howling monkeys. Amer. J. Phys. Anthropol. 53:25-36, 1980.
Gotch, A.F.: Mammals - Their Latin Names Explained. Blandford Press, Poole, Dorset, 1979.
Groves, C.: Primate Taxonomy. Smithsonian Institution, Washington, D.C. 2001.
Harada, M.L., Schneider, H., Schneider, M.P., Sampaio, I., Czelusniak, J. and Goodman, M.: DNA evidence on the phylogenetic systematics of New World monkeys: support for the sister-grouping of Cebus and Saimiri from two unlinked nuclear genes. Mol. Phylogenet. Evol. 4:331-349, 1995.
Herrick, J.R., Agoramoorthy, G., Rudran, R. and Harder, J.D.: Urinary progesterone in free-ranging red howler monkeys (Alouatta seniculus): preliminary observations of the estrous cycle and gestation. Amer. J. Primatol. 51:257-263, 2000.
Hsu, T.C.: Cited by: de Boer, L.E.M.: Cytotaxonomic Studies in the Primate Suborders Prosimii and Platyrrhini.Drukkerij Bronder-Offset B.V., Rotterdam, 1974.
Hugot, J.P.: Phylogeny of neotropical monkeys: the interplay of morphological, molecular, and parasitological data. Mol. Phylogenet. Evol. 9:408-413, 1998.
R.A., Leberg, P.L., Quattro, J.M. and Vrijenhock, R.C.: Genetic diversity
in black howler monkeys (Alouatta pigra). Amer. J. Phys. Anthropol.
Jones, T.C., Thorington, R.W., Miller, A. and Morgan, L.: Y-autosome translocation in the howler monkey, Alouatta palliata. J. Med. Primatol. 4:299-307, 1975.
Koiffman, C.P. and Saldanha, P.H.: Cytogenetics of Brazilian monkeys. J. Hum. Evol.3:275-282, 1974
M. and Rossan, R.N.: A subcutaneous abscess associated with Salmonella
typhimurium in a black howler monkey (Alouatta villosa). Lab.
Anim. Sci. 21:412-414, 1971.
Ma, N.S.F., Jones, T.C., Thorington, R.W., Miller, A. and Morgan, L.: Y-autosome translocation in the howler monkey, Alouatta palliata. J. med. Primatol. 4:299-307, 1975.
Malinow, M.R. and Maruffo, C.A.: Aortic atherosclerosis in free-ranging howler monkeys (Alouatta caraya). Nature 205:948-949, 1965. (see also: Naturally occurring atherosclerosis in Howler monkeys (Alouatta caraya. J. Atheroscleros. Res. 8:368-380, 1966).
Maruffo, C.A.: Spontaneous tumours in howler monkeys. Nature 213:521, 1967.
Maruffo, C.A. and Malinow, M.R.: Seminoma in a howler monkey (Alouatta caraya). J. Pathol. Bacteriol. 91:280-282, 1966.
Maruffo, C.A. and Malinow, M.R.: Pathologic changes of the heart in free-ranging howler monkeys (Alouatta caraya, Humboldt, 1812). Amer. J. Vet. Res. 28:237-243, 1967.
Maruffo, C.A., Malinow, M.R., Depaoli, J.R. and Katz, S.: Pigmentary liver disease in howler monkeys. Amer. J. Path. 49:445-456, 1966.
Minezawa, M., Harada, M., Jordan, O.C. and Borda, C.J.V.: Cytogenetics of Bolivian endemic red howler monkeys (Alouatta seniculus sara): accessory chromosomes and Y-autosome translocation related numerical variations. Kyoto University Overseas Research Report on New World Monkeys. 5:7-16, 1985.
Mondet, B., Vasconcelos, P.F., Travassos da Rosa, A.P., Travassos da Rosa, E.S., Rodrigues, S.G., Travassos Rosa, J.F. and Bicout, D.J.: Isolation of yellow fever virus from nulliparous Haemagogus (Haemagogus) janthinomys in eastern Amazonia. Vector Borne Zoonotic Dis. 2:47-50, 2002.
Moreland, R.B., Richardson, M.E., Lamberski, N. and Long, J.A.: Characterizing the reproductive physiology of the male southern black howler monkey, Alouatta caraya. J. Androl. 22:395-403, 2001.
Mossman, H.W.: Vertebrate Fetal Membranes. MacMillan, Houndmills, 1987.
Mudry de Pargament, M.D., Brieux de Salum, S. and Collilas, G.J.: Estudio cyogenetico del mono aullador Alouatta caraya de la Republica Argentina. Physis (Buenos Aires), Secc. C. 40 (98):63-70, 1981.
M.D., Rahn, M., Gorostiaga, M., Hick, A., Merani, M.S. and Solari, A.J.:
Revised karyotypes of Alouatta caraya (Primates: Platyrrhini) based
on synaptonemal complex and banding analyses. Hereditas 128:9-16, 1998.
Nowak, R.M.: Walker's Mammals of the World. 6th ed. The Johns Hopkins Press, Baltimore, 1999.
De Oliveira, E.H., Neusser, M., Figueiredo, W.B., Nagamachi, C., Pieczarka, J.C., Sbalqueiro, I.J., Wienberg, J. and Mueller, S.: The phylogeny of howler monkeys (Alouatta, Platyrrhini): reconstruction by multicolor cross-species chromosome painting. Chromosome Res. 10:669-683, 2002.
Persellin, R.H. and Chang, R.J.: Multiple IgM autoantibodies in a nonhuman primate. Inter. Arch. Allergy 46:815-821, 1974.
Pope, B.L.: Some parasites of the howler monkey of northern Argentina. J. Parasitol. 52:166-169, 1966.
Rahn, M.I., Mudry, M., Merani, M.S. and Solari, A.J.: Meiotic behavior of the X1X2Y1Y2 quadrivalent of the primate Alouatta caraya. Chromosome res. 4:350-356, 1996.
Rangan, S.R., Martin, L.N., Enright, F.M. and Abee, C.R.: Herpesvirus saimiri-induced lymphoproliferative disease in howler monkeys. J. Natl. Cancer Inst. 59:165-171, 1977.
Scott, G.B.D.: Comparative Primate Pathology. Oxford University Press, 1992.
Shoemaker, A.H.: Reproduction and development of the black howler monkey Alouatta caraya at Columbia zoo. Internat. Zoo Yearbk. 19:150-155, 1979.
Shoemaker, A.H.: Fecundity in the captive howler monkey, Alouatta caraya. Zoo Biol. 1:149-156, 1982.
Smith, J.D.: The systematic status of the black howler monkey, Alouatta pigra Lawrence. J. Mammal. 51:358-369, 1970.
De Souza, L.L., Ferrari, S.F., da Costa, M.L. and Kern, D.C.: Geophagy as a correlate of folivory in red-handed howler monkeys (Alouatta belzebul) from eastern Brazilian Amazonia. J. Chem. Ecol. 28:1613-1621, 2002.
Spatz, W.B.: Nabelschnur-Längen bei Insektivoren und Primaten. Z. Säugetierk. 33:226-239, 1968.
Vie, J.C., Moreau, B., de Thoisy, B., Fournier, P. and Genty, C.: Hematology and serum biochemistry values of free-ranging red howler monkeys (Alouatta seniculus) from French Guiana. J. Zoo Wildl. Med. 29:142-149, 1998a.
Vie, J.C., De Thoisy, B., Fournier, P, Fournier-Chambrillon, C., Genty, C. and Keravec, J.: Anesthesia of wild red howler monkeys (Alouatta seniculus) with medetomidine/ketamine and reversal by atipamezole. Amer. J. Primatol. 45:399-410, 1998b.
Young, A.: The primate umbilical cord with special reference to the transverse communicating artery. J. Human Evol. 1:345-359, 1972.
Yunis, E.J., Torres de Caballero, O.M., Ramirez, C. and Ramirez Z.E.: Chromosomal variations in the primate Alouatta seniculus seniculus. Folia Primatol. 25:215-224, 1976.
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