Howler Monkey (Bolivian red Howler monkey) Alouatta seniculus sara

Order: Primates

Family: Cebidae

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.

Alouatta seniculus sara at San Diego Zoo.

2) 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.

3) Implantation

No early implantation stages have been described.

4) General Characterization of the Placenta

Mossman (1987) stated that only few placentas of South American primates had been evaluated and he then described the placenta of Alouatta as being "discoid", with other cebids having two disks (see the chapters on Spider monkey and Saki monkey). He also alluded to a trabecular structure of the villi. This is not so much the case for the howler monkey, I believe. Its structure is much more villous than that of the callithrichids, although the subchorial villi have a filiform appearance, similar to those of the saki monkey. The villi are extremely cellular in this immature placenta, the only one that was available to me, and there are no hematopoietic islands in the villi. There are, however, nucleated red cells in the fetal circulation, as behooves such an immature gestation. The floor of the placenta has a thick layer of extravillous trophoblast that is adjacent to the often degenerating decidua basalis without apparently invading it, however. The single immature placenta I have had available for histology had only a single disk. It weighed 30 g with an accompanying fetus weighing 90 g. The umbilical cord was 12 cm long.

Implantation of young gestation with immature villi above and extravillous trophoblast ("X-cells") in the middle layer. Degenerating decidua basalis below.

Higher magnification of "X-cells" that effect the implantation. Note binucleate cells and large nuclei that are the result of endoreduplication.

5) 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.

Slightly immature villi of Howler monkey with numerous fetal capillaries, occasional Hofbauer cells, and surface syncytiotrophoblast.

6) Umbilical cord

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.

Two cross sections of Howler monkey umbilical cord (Alouatta seniculus sara). A tiny remnant of allantoic duct can be seen in the cord section on the left; it is between the thicker arteries.

7) Uteroplacental circulation

No published studies are known to me.

8) Extraplacental membranes

I have only one section available of the membranes from the lateral aspect of the immature placenta described above. It is shown next and, in contrast to some other primates, villi extend to the edge, and they are found to atrophy there beneath the chorion. No allantoic sac is present and the amnion is lined by a very thin epithelium without metaplastic change. It is avascular.

Margin of immature placenta with origin of free membranes. There is a decidua capsularis, quite similar to human gestations and atrophying villi are found.

9) 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.

10) Endometrium

There is little endometrial decidual transformation at the base, where much necrosis occurs and where considerable superficial fibrinoid is found. Decidua capsularis forms as is shown above.

11) Various features

No subplacenta exists.

12) Endocrinology

Herrick et al. (2000) studied the estrous cycle by RIA of urinary unconjugated progesterone. The approximate length of the cycle was found to be 29 days. Glander (1980) had earlier reported a 16 day cycle in free-ranging animals. Fecal testosterone was measured by Moreland et al. (2001) who also gave specifics on methods and results of electroejaculation. Their study was undertaken in order to assist with the potential aid to an endangered group of animals. I am unable to find publications on gonadotropins or measurements of estrogens.

13) Genetics

The karyotypes of howler monkeys are complex, with chromosome numbers ranging from 42 to 53, different species having different numbers. It is possible that hybrids among species or subspecies occur, but they were not considered in the book by Gray (1972), nor are they mentioned in other publications. This group of species is also characterized by the occurrence of Y-autosome fusions, microchromosomes, and multiple sex chromosome systems occurring in a variety of species. Here follows a possibly incomplete list of chromosome numbers from various publications in chronological order:

Koiffman & 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. mportantly, Mudry et al. (2001) studied the meiotic paring of chromosomes in two howler monkey species, and demonstrated the breakpoint by chromosome painting.

Karyotype of male Alouatta seniculus sara, 2n=50 from San Diego Zoo.

14) Immunology

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.

15) Pathological features

As is true of many catarrhine and platyrrhine monkeys, Howler monkeys often have focal infarcts in their placenta. These are very similar to those found in human gestations where they are commonly due to pre-eclampsia with altered decidual blood vessels. No such blood vessel changes have been described in these monkeys, however.

In 1998 a yellow fever virus epidemic killed numerous howler monkeys in eastern Amazonia (Mondet et al., 2002). The frequency of toxoplasmosis in howler monkeys was assessed by a serologic survey of numerous animals in French Guiana (Carme et al., 2002). Howlers, as well as other tree-dwelling species, had a low prevalence of antibodies to toxoplasma. At the Audubon Park, New Orleans, a howler monkey died from eosinophilic meningitis due to Angiostrongylus cantonensis infection (Gardiner et al., 1990). Pope (1966) identified lice, pinworms and a tapeworm in black howler monkeys. Salmonella typhimurium was isolated from an abscess in a black howler monkey by Kourany & Rossan (1971). Maruffo et al. (1966) found lipofuscin liver pigmentation in nearly all of the 290 free-ranging howler monkeys, with occasional fatty infiltration and rarely attended by necrosis.

Experimental infection with Herpes saimiri virus caused death in howler monkeys (Rangan et al., 1977). Maruffo & Malinow (1966) reported on a seminoma in one of 314 black howler monkeys studied, and later, Maruffo (1967) identified adrenal adenomas and a renal adenoma in a howler monkey. Scott (1992) described a dissecting aortic aneurysm. Others have also published on cardiac and vascular disease in howlers. Thus, Maruffo & Malinow (1967) examined 280 free-ranging black howler monkeys and found pericarditis in 20, myocarditis in 19, and endocarditis in 2 animals. Malinow & Maruffo (1965) identified aortic sudanophilia, streaks and small atheromas in the same group of animals autopsied.

Spontaneous abortus in howler monkey with villi at left, endometrium at right. Only very superficial trophoblast infiltration of the decidua was found.

The same abortus (2 cm embryo) with villi at left and endometrial glands at right.

Old infarct of placental tissue at right.

16) Physiologic data

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.

17) Other resources

Various fibrous tissue cell lines are available from CRES at the San Diego Zoo by contacting Dr. Oliver Ryder (oryder@ucsd.edu). The names of species available are at the end of the list above.

18) Other remarks - What additional Information is needed?

Implantation needs to be studied and some mature placentas need to be described, specifically to rule out bilobation of the placental disks. The length of the umbilical cord is not firmly established. We also need information of trophoblast infiltration into decidua and maternal vessels.

Acknowledgement

The animal photograph in this chapter comes from the Zoological Society of San Diego.